Establishing suppressive conditions against soilborne potato diseases with low rates of fish emulsion applied serially as a pre-plant soil amendment

Abstract

Soil amendment with fish emulsion (FE) can suppress potato scab and verticillium wilt, but the effective broadcast rates (20 000 L ha⁻¹) may not be feasible for commercial use. The aim of this 4-year study was to establish suppressive conditions against soilborne potato diseases and increase tuber yield with economically feasible rates of FE. Diluted FE (1000 and 2000 L ha⁻¹ or 0.05 and 0.1%) was applied to field plots or micro-plots twice a year before planting and after harvesting potatoes starting in autumn of 2007 and ending in spring of 2010. In the micro-plots, FE (0.1%) added to an infested potato soil (site BL) consistently reduced scab severity by 44.9% (2008), 44.8% (2009) and 30.9% (2010) compared with the control. Scab severity on tubers harvested from these plots was also low in 2011 when no further FE was applied, but the effect was not significant. In the field, FE (2000 L ha⁻¹) consistently reduced scab severity by 45% (2008), 53% (2009), 44% (2010) and 38% (2011); reduced the percentage of tubers with deep-pitted scab by 48% (2008), 51% (2009), 66% (2010) and 77% (2011); and increased the percentage of marketable tubers by 37% (2008), 83% (2009), 20% (2010) and 8% (2011). These field plots also showed a low percentage of Verticillium dahliae-infected potato plants during the first 3 years of the field trial. Fish emulsion treatments increased total tuber yield by 7–20% in the first 3 years, but there was no effect in the fourth year when no FE was applied. Marketable tubers were consistently higher in the plots amended with FE (2000 L ha⁻¹). Fish emulsion soil treatments increased soil bacteria but the numbers dropped to the control level in the fourth year when no FE application was made. There was no change in total fungal numbers. The results suggest that economically feasible rates of FE can provide disease suppression and enhance tuber yield and the effect may last a year or more after the last FE application.

Résumé

Un amendement de sol à base d'émulsion de poissons (EP) peut enrayer la gale de la pomme de terre et la flétrissure verticilienne, mais le taux d'application (20 000 L ha⁻¹) n'est pas économiquement viable. Le but de cette étude de quatre ans était d'établir les conditions inhibitrices qui contraient les maladies terricoles de la pomme de terre et permettaient d'accroître le rendement en tubercules, et ce, en utilisant des taux d'application d'EP économiquement viables. De l'automne 2007 au printemps 2010, des solutions diluées d'EP (1000 et 2000 L ha⁻¹, ou 0.05 et 0.1%) ont été appliquées deux fois par année à des parcelles de terrain ou à des microparcelles, avant de semer et après avoir récolté les pommes de terre. Sur les microparcelles, de l'EP (0.1%) appliqué sur un sol infesté (site BL) a invariablement réduit la gravité de la gale de 44.9% (2008), de 44.8% (2009) et de 30.9% (2010), comparativement aux microparcelles témoins. La gravité de la gale observée sur les tubercules récoltés dans ces parcelles était également faible en 2011 quand les applications d'EP avaient cessé, mais l'effet n'était pas significatif. Sur les parcelles de terrain, l'EP (2 000 L ha⁻¹) a invariablement réduit la gravité de la gale de 45% (2008), de 53% (2009), de 44% (2010) et de 38% (2011), a réduit le pourcentage de tubercules affichant des lésions profondes de 48% (2008), de 51% (2009), de 66% (2010) et de 77% (2011) et a augmenté le pourcentage de tubercules de qualité marchande de 37% (2008), de 83% (2009), 20% (2010) et de 8% (2011). Au cours des trois premières années des essais en champ, les parcelles de terrain affichaient également un faible pourcentage de plants de pommes de terre infectés par Verticillium dahliae. Les traitements à l'EP ont accru le rendement en pommes de terre de 7 à 20% au cours des trois premières années, mais il n'y a pas eu d'effet marqué durant la quatrième année lorsqu'on n'a pas appliqué d'EP. Le taux de tubercules de qualité marchande était invariablement plus élevé dans les parcelles amendées avec l'EP (2000 L ha⁻¹). Les traitements à base d'EP ont accru l'abondance des populations de bactéries dans le sol, mais, au cours de la quatrième année, alors que les applications d'EP avaient cessé, l'abondance est retombée au niveau des parcelles témoins. Le nombre total de champignons est resté inchangé. Les résultats suggèrent que des taux économiquement viables d'EP peuvent enrayer la maladie et améliorer le rendement en tubercules. En outre, l'effet du traitement peut durer un an ou plus après la dernière application.

Keywords:

• disease management
• potato scab
• soil organic amendment
• verticillium wilt

Mots clés:

• amendements biologiques du sol
• flétrissure verticilienne
• gale de la pomme de terre
• gestion des maladies

Introduction

The potato has been used as a model system to investigate the effects of various soil amendments on plant diseases caused by soilborne plant pathogens (Lazarovits, 2001; Lazarovits et al., 2001, 2005). In particular, we have been examining the effect of soil amendments on common scab and verticillium wilt, two economically important soilborne diseases that often infect potatoes in the same field. Common scab or potato scab is caused by several Streptomyces spp. (Goyer et al., 1996; Loria et al., 1997) of which S. scabies (Thaxter) Waksman & Henrici, syn: S. scabiei (Trüper & de' Clari, 1997) is the predominant causal agent (Lambert & Loria, 1989; St-Onge et al., 2008). Depending on the Streptomyces strain and the soil environment, infection of newly developing young tubers can lead to shallow, raised or deep-pitted lesions (Goyer et al., 1996; Loria et al., 1997). Potato scab has become increasingly important in recent years due to the demand for a blemish-free, high-value product and low tolerances for pathogen presence in seed tubers. Verticillium wilt is caused by soilborne fungi Verticillium dahliae Klebahn and V. albo-atrum Reinke and Berthhold. Both species may be present in the same field or even on the same plant (Howard et al., 1994). Although V. albo-atrum is generally considered more pathogenic than V. dahlia (Howard et al., 1994), it is not the more widespread or predominant of the two species particularly in Canada (G. Lazarovits, unpublished data). The disease causes early dying of leaves and stems leading to severe yield reductions in a variety of important crops including potato and tomato worldwide (Powelson & Rowe, 1993; Rowe & Powelson, 2002).

Streptomyces spp. and V. dahliae can survive in soil for long periods in the absence of susceptible hosts and pose a long-term threat to potato production in infested soils (Mace et al., 1981; Kritzman & Grinstein, 1991).

There is no single effective strategy currently available to control potato scab or verticillium wilt. Fumigation of the infested fields with chemical sterilants such as methyl bromide, vapam, chloropicrin and other chemicals (Rowe & Powelson, 2002; Goicoechea, 2009) can reduce soil populations of these pathogens which may lead to disease suppression. These chemicals, however, are not always available, can be expensive, potentially dangerous to apply, and environmentally undesirable. Their application may also lower populations of non-target beneficial soil microorganisms, and that could lead to elimination of subsequent antagonism and competition. Various soil amendments have been shown to influence the severity of potato scab and verticillium wilt (Davis et al., 1996; Conn & Lazarovits, 1999; Lazarovits et al., 1999). In general, the rates of these organic amendments found effective in suppressing potato scab and verticillium wilt were very high and may not be economically feasible for commercial application. Unfortunately, long-term studies with low application rates of these and other soil organic amendments at the same field locations are rare. These specific studies are needed to establish disease suppressive conditions by exploiting the potential of natural biological control.

Fish emulsion or fish soluble nutrients are liquid by-products of the processing of fish into fish meal. They are made from whole fish or fish waste by cooking and acid processing. They have been used mainly as fertilizers (Ceci, 1975; Aung & Flick, 1980; Aung et al., 1984) although other uses, such as disease management, have been reported as well (Wyatt & McGourty, 1990; Abbasi et al., 2003, 2004; El-Tarabily et al., 2003). Foliar sprays of a mixture of FE and bacteria were used to control moths (Wyatt & McGourty, 1990) and Abbasi et al. (2003) demonstrated that diluted solutions of FE could control bacterial spot of tomato and pepper. Fish meal, the dried protein obtained from processed fish, has been used as a soil amendment with great success in vegetable production (Gagnon & Berrouard, 1994; Blatt & McRae, 1998). Fish solid waste has also been known to reduce the populations of plant-parasitic nematodes (Akhtar & Mahmood, 1995). Fish emulsion as a pre-planting amendment to potting substrates and organic soil has shown effectiveness for controlling damping-off diseases (Abbasi et al., 2004). Soil amendment of FE can enrich soil microbes and generate suppressive conditions against soilborne diseases, such as seedling damping-off, potato scab and verticillium wilt. However, the rates (20 000 L ha⁻¹) of FE that provided effective control of potato scab can be too costly for commercial use.

The objective of this 4-year study was to establish suppressive conditions against soilborne potato diseases with economically feasible rates of FE applied serially as a pre-plant amendment. The effects on common scab, verticillium wilt, and tuber yield of potato under micro-plot and field conditions are described.

Materials and methods

Potato seed, soil and fish emulsion

Disease-free seed potatoes (Solanum tuberosum L. ‘Snowden’ or ‘Yukon Gold’) of Elite II quality were obtained from a registered seed producer in Ontario. The cultivar ‘Snowden’ was not available in 2011. Both varieties are susceptible to common scab. A commercial potato field (site BL) in Ontario with a history of verticillium wilt and potato scab was used for field trials and soil from this field was brought to London, ON for micro-plot trials. Soil type from these field plots was a loamy-sand and it had organic matter content of 1.3% to 2.8% and pH of 6.6–6.9.

Fish emulsion (FE) samples made from whole menhaden fish [Brevoortia tyrannus (Latrobe)] in commercial operations were provided by Omega Protein, Houston, TX. Nutrient analysis by A&L Laboratories showed that various FE samples contained 50–54% dry matter content, 4–6% total nitrogen, 1.5–2% P₂O₅ and 1.2–2.7% K₂O. Fish emulsion has a C:N ratio of 4–6:1 and pH of 2.4–2.8. Fish emulsion is water-soluble and it can be sprayed onto or injected into field plots. According to information provided by Omega Protein, FE contains some heavy metals at nontoxic levels (e.g., chromium at < 4.0 ppm). Fish emulsion samples also contain volatile fatty acids (VFAs) and major VFAs in the FE are acetate (95 mM), formate (40 mM), n-butyrate (35 mM) and propionate (13 mM) (Abbasi et al., 2009).

Micro-plot trials

Micro-plots trials were set up at the Agriculture and Agri-Food Canada Research Farm, London, ON, in the autumn of 2007. These micro-plots actually consisted of plastic drainage tiles (25-cm diameter, 25-cm long) buried into a sandy loam soil. There were six replicate tiles per treatment. Soil for these trials was brought from a commercial potato field in Ontario (site BL) with a history of potato scab and verticillium wilt. Fish emulsion (0.05% and 0.1% mass/mass soil) was incorporated into 13 kg of the naturally infested soil in plastic bags and one bag of soil was transferred to each of six replicate micro-plots per treatment. Fish emulsion was applied to the micro-plots twice a year – before planting and after harvesting potatoes – starting in the autumn of 2007 and ending in the spring of 2010. One potato tuber of the susceptible variety ‘Snowden’ was planted in each micro-plot 7–10 days after the FE treatment during the first week of June each year from 2007 to 2010, and ‘Yukon Gold’ in 2011 (‘Snowden’ was not available in 2011). The application of FE was stopped in 2010 to see if its effect on disease suppression and yield could last more than one year. The control micro-plots were fertilized with inorganic fertilizer at the standard recommended fertilizer regime (200 kg N ha⁻¹, 150 kg P₂O₅ ha⁻¹ and 150 kg K₂O ha⁻¹), whereas the micro-plots receiving FE treatments were only partially supplemented with inorganic fertilizer to the same fertility regimes as control. Incidence of V. dahliae was determined by collecting two leaf petioles from the lower portion of each of the six replicate plants per treatment during mid-August every year (Conn & Lazarovits, 1999). The petioles were surface sterilized by placing them in 1.5% sodium hypochlorite for 2 min. Three sections from each petiole were plated onto soil-pectate-Tergitol (SPT) agar medium (Hawke & Lazarovits, 1994), the dishes incubated at 24 °C in the dark for 2 weeks, and the presence or absence of V. dahliae determined microscopically. A plant was scored as infected if a characteristic colony of V. dahliae was present in just one petiole section. A typical colony of V. dahliae also produces microsclerotia within a week. After 12 weeks, all tubers from each micro-plot were harvested and sorted. Only tubers with a diameter of 2 cm or greater were rated for scab severity using a rating scale of 0–6 where 0 = 0%, 1 = trace to 5%, 2 = 6–15%, 3 = 16–25%, 4 = 26–35%, 5 = 36–60% and 6 = 61–100% of tuber surface covered with scab lesions. The tubers were weighed to determine yield.

Field trials

Experimental plots were established in the spring of 2007 in a commercial potato field (site BL) in Ontario with a history of potato scab and verticillium wilt. Each plot was 15 m × 5.5 m in size with four blocks or replicates and six rows per treatment arranged in a randomized block design. The blocks were separated by a 15-m wide buffer zone or laneways. All plots received a total of 150 kg N ha⁻¹, 45 kg P₂O₅ ha⁻¹ and 120 kg K₂O ha⁻¹ from mineral fertilizer (Pre-plant incorporated (PPI) = 300 kg 5-15-40 ha⁻¹, Planter fertilizer (calcium ammonium nitrate) = 300 kg 27-0-0 ha⁻¹ banded on both side of tubers, and side dress before hilling = 300 kg 27-0-0 ha⁻¹). Plots did not receive any treatment until after harvesting potatoes. Fish emulsion treatments were applied as a soil amendment at a rate of 9 and 18 L plot⁻¹ or 1000 and 2000 L ha⁻¹ (giving a final concentration equivalent of 0.05% and 0.1% mass/mass soil). At this rate, FE was applied to the field plots twice a year – before planting and after harvesting potatoes – starting in the autumn of 2007 and ending in the spring of 2010. The concentrated FE is very thick so it was diluted 1:1 with water to assist in application. The diluted solution was poured into watering cans and manually applied to the surface of the plots. The plots were then rototilled or cultivated to a depth of 12–15 cm. Potato tubers ‘Snowden’ were planted 25 cm apart 1 week after the FE amendment during the first week of June each year from 2007 to 2010, and ‘Yukon Gold’ in 2011 (‘Snowden’ was not available in 2011). The application of FE was stopped in 2010 to see if its effect on disease suppression and yield lasted more than one year. Incidence of V. dahliae in the leaf petiole of 25 plants from the middle two rows (approximately half from each row) of each replicate plot was determined in mid-August in each year as described above. Each year, all tubers from the middle two rows of each plot were harvested mechanically, washed, sorted and graded. The tubers with a diameter of 5 cm or greater were weighed to determine total yield per plot and 100 randomly selected tubers were also rated for scab severity as described above. Yield data were converted to t ha⁻¹ by estimating yield in t/100-m rows and multiplying by 111 rows (0.9 m apart). Marketable yield of tubers was determined by multiplying tuber yield by the percentage of tubers with < 5% surface covered with scab lesions.

Soil samples (10 per plot) were collected in 2008, 2009, 2010 and 2011 with a core sampler to a depth of 22–30 cm from the field plots every year after harvesting potatoes to determine pH and population densities of total bacteria and fungi. The 2010 soil samples could not be analyzed for population densities of total bacteria and fungi. A 10 g soil sample was removed from the composite sample of each plot and added to 90 mL of sterile 0.1% water agar in plastic pouches (17 × 30 cm). The pouches were heat-sealed and shaken on an orbital shaker (200 rpm) for 2 h. The soil mixtures were then homogenized by placing the pouches in a Stomacher blender set on normal speed for 30 s. Serial 10-fold dilutions were prepared in saline solution (0.85% NaCl) and 100 μL of soil suspension was applied to each plate of 0.1% tryptic soy agar (TSA; pH 7.4) and rose bengal agar (rose bengal, dextrose, peptone, yeast extract, KH₂PO₄, MgSO₄*7H₂0, agar, pH 5.8) media, and plates were incubated at room temperature (22 °C). The number of bacteria that grew on 0.1% TSA medium was counted after 7 days and fungal numbers were determined on rose bengal medium after 4 days. Numbers of microorganisms were adjusted to represent colony forming units (CFU) g⁻¹ dry soil.

Statistical analyses

The field and micro-plot data from each year were analyzed separately and subjected to analysis of variance using MINITAB statistical software version 13.0 (Minitab Inc., State College, PA, USA), and if P values indicated a significant difference (P < 0.05), means were separated by Fisher's protected least significant difference (LSD) test. Bacterial and fungal population data from field plots was transformed to the logarithmic scale before subjecting to one-way analysis of variance. Disease severity data were analyzed using Jandel SigmaStat statistical software (Jandel Scientific, San Rafael, CA, USA). Data were subjected to one-way analysis of variance using Kruskal–Wallis non-parametric test statistics and means were separated according to Student–Newman–Keuls test.

Results

Effect of low rates of FE as soil amendment on scab, verticillium wilt and tuber yield of potato in micro-plots trials

There were no significant differences in the severity of potato scab on tubers produced in the untreated control soil or the soil amended with 0.05% rate of FE (Fig. 1). Soil amendment with 0.1% rate of FE consistently reduced scab severity by 44.9% in 2008, 44.8% in 2009 and 30.9% in 2010 compared with the control (Fig. 1). Scab severity on tubers harvested from plots receiving 0.1% rate of FE in prior 3 years was also low in 2011, but the effect was not statistically significant. There were no significant differences in total yield of tubers (> 2 cm diameter) harvested from single plants grown in untreated control plots or in plots treated with FE in any year (Fig. 1). Based on petiole analysis of each plant per micro-plot, the majority of potato plants were marked positive for infection of V. dahliae in all four years, and FE treatments did not reduce the number of V. dahliae-infected potato plants compared with the control (data not shown).

Fig. 1. Effect of serial applications of economically feasible rates of fish emulsion (FE) as a pre-plant soil amendment on scab severity and tuber yield in micro-plots. Tubers were harvested in the autumn of each year and rated for scab severity using a scale of 0–6 based on the percentage of tuber surface covered with scab lesions where 0 = 0%, 1 = trace to 5%, 2 = 6–15%, 3 = 16–25%, 4 = 26–35%, 5 = 36–60%, and 6 = 61–100%. Error bars represent standard error of the mean (n = 6). Treatments within a year with the same letter are not significantly different (P < 0.05).

Effect of low rates of FE as soil amendment on scab, verticillium wilt and tuber yield of potato in field trials

The severity of scab on tubers was low to moderate with an average severity rating of 0.9–1.5 during the four seasons from 2008 to 2011 (Fig. 2). In the first year of the trial, both rates (1000 and 2000 L ha⁻¹) of FE applied as pre-plant soil amendment reduced scab severity by 36–45% and reduced the percentage of tubers with deep-pitted lesions by 41–48% (Fig. 2). In the second year of the trial, the scab severity was slightly higher in all plots and only FE (2000 L ha⁻¹) reduced scab severity by 53% and reduced the percentage of tubers with deep-pitted lesions by 51% (Fig. 2). In the third year of the trial, both rates reduced scab severity by 33% to 44% and reduced the percentage of tubers with deep-pitted lesions by 66% (Fig. 2). In the fourth year of the trial, no FE was applied to any plots and scab was less severe in plots receiving FE (2000 L ha⁻¹) in prior years. In tubers harvested from such plots, scab severity was reduced by 38%, and the percentage of tubers with deep-pitted lesions was reduced by 77% (Fig. 2).

Fig. 2. Effect of serial applications of economically feasible rates of fish emulsion (FE) as a pre-plant soil amendment on scab severity and deep-pitted lesions on tubers in an Ontario commercial potato field. Tubers were harvested in the autumn of each year and rated for scab severity (see Fig. 1). Error bars represent standard error of the mean (n = 4). Treatments within a year with the same letter are not significantly different (P < 0.05).

Fish emulsion soil amendment also impacted the incidence of verticillium wilt based on petiole analysis of 25 plants per plot during mid-August of each year (Fig. 3). Soil amendment with FE (2000 L ha⁻¹) consistently reduced the percentage of V. dahliae-infected potato plants in all 3 years by 48% in 2008, 23% in 2009 and 42% in 2010 (Fig. 3). Fish emulsion (1000 L ha⁻¹) only reduced the percentage of V. dahliae-infected potato plants during the first year of the trial (Fig. 3). There was no effect of any treatment in the fourth year of the trial, when plots were not treated with FE (Fig. 3).

Fig. 3. Effect of serial applications of economically feasible rates of fish emulsion (FE) as a pre-plant soil amendment on Verticillium dahliae-infections of potato petioles in an Ontario commercial potato field. Error bars represent standard error of the mean (n = 4). Treatments within a year with the same letter are not significantly different (P < 0.05).

Both marketable tubers (with < 5% surface scab) and total tubers (> 5 cm diameter) were significantly higher in the FE-treated plots. Both rates (1000 and 2000 L ha⁻¹) of FE increased the marketable tubers by 34% and 37% in 2008, by 34% and 83% in 2009 and by 19% and 20% in 2010, respectively (Fig. 4). Total tuber yield was increased in the FE-treated plots by 16% to 19% in 2008, by 14% to 20% in 2009, and by 7% to 11% in 2010 (Fig. 4). Plots were not treated with FE in the fourth year of the trial and there was no effect on total tuber yield; however, the percentage of marketable tubers was still higher in the plots receiving FE (2000 L ha⁻¹) in the prior years (Fig. 4).

Fig. 4. Effect of serial applications of economically feasible rates of fish emulsion (FE) as a pre-plant soil amendment on total and marketable tubers (< 5% surface covered with lesions) in an Ontario commercial potato field. Error bars represent standard error of the mean (n = 4). Treatments within a year with the same letter are not significantly different (P < 0.05).

The pH and microbial populations of bacteria and fungi were determined in soil samples collected every year after harvesting tubers. The pH of the soil samples collected from the field plots treated with FE was slightly lower during the first 2 years of the trial, but pH in such FE-treated plots rose to comparable pH levels seen in the control during the last 2 years of the trial (Table 1). The total numbers of culturable bacteria was higher in soil samples collected from the field plots treated with FE soil amendment during the first 2 years, and no differences in bacterial counts were found in the fourth year of the trial when plots were not treated with FE (Table 2). In all years of testing, the fungal numbers remained the same in the untreated control plots and in the plots treated with FE (Table 2).

Table 1. Effect of fish emulsion (FE) pre-plant amendment on soil pH

	pH of soil after harvesting tubers
Treatments	2008	2009	2010	2011
Control	6.6 ± 0.1	6.4 ± 0.2	6.3 ± 0.1	6.1 ± 0.2
FE (1000 L ha^−1)	6.0 ± 0.1	5.4 ± 0.1	5.8 ± 0.1	5.8 ± 0.2
FE (2000 L ha^−1)	6.0 ± 0.4	5.4 ± 0.3	6.3 ± 0.5	5.9 ± 0.2
Note: Means ± SE (standard error) are average of four replicates. pH was determined from soil (8 g) – water (40 mL) mixtures shaken for 1 h.

Table 2. Effect of fish emulsion pre-plant soil amendment on total bacteria and fungi

	Population density in field plots at harvest ^a
Treatments	2008	2009	2011
Total bacteria (log CFU g^−1 soil)^b
Control	7.15 ± 0.05 a	7.07 ± 0.08 a	7.16 ± 0.08 a
FE (1000 L ha^−1)	7.24 ± 0.10 a	7.69 ± 0.06 b	7.20 ± 0.04 a
FE (2000 L ha^−1)	8.17 ± 0.05 b	7.50 ± 0.05 b	7.20 ± 0.02 a
Total fungi (log CFU g^−1 soil)^b
Control	4.94 ± 0.03 a	4.88 ± 0.06 a	4.96 ± 0.02 a
FE (1000 L ha^−1)	5.19 ± 0.08 a	4.88 ± 0.06 a	4.92 ± 0.05 a
FE (2000 L ha^−1)	4.80 ± 0.04 a	4.76 ± 0.02 a	5.02 ± 0.05 a
Note: Means ± SE (standard error) are average of four replicates. Values followed by a different letter within each year for bacteria and fungi are significantly different at P < 0.05 according to Fisher's protected LSD test.
^aSoil samples were not analyzed for population densities in 2010.
^bBacteria were determined on 0.1% tryptic soy agar and fungi on rose bengal medium.

Discussion

Incorporating or amending organic materials into agricultural soils can be a source of nutrients for crop plants and it can also provide suppression of certain soilborne diseases. However, the amending rates of organic material used in most cases for disease suppression are usually very high. This is because the high rates of some organic material may provide immediate relief of disease by directly suppressing pathogen populations depending on the product (Tenuta & Lazarovits, 2002; Mazzola et al., 2007). For example, high-N and organic acid-containing materials when used at high rates can cause an almost immediate reduction in pathogen populations via short-lived toxic metabolites (Tenuta et al., 2002; Conn et al., 2005; Lazarovits et al., 2005; Abbasi et al., 2009; Abbasi, 2011). However, very high amendment rates of these materials may not be practical for obvious economic reasons and phytotoxicity, and they can also have some negative consequences on the environment as not all nutrients may be taken up by the plants, and some may end up polluting water ways. In addition, organic materials can improve soil and plant health by increasing the organic matter content of the amended soil (Weil & Magdoff, 2004), and enhance the natural biological control potential of agricultural soil by increasing the activity and diversity of resident soil microbial communities (Mäder et al., 2002). In general, plant diseases caused by soilborne plant pathogens are less severe in soils receiving organic materials (Davis et al., 2001; van Bruggen & Temorshuizen, 2003), and such amended soils generally have higher biological activity and diversity (van Diepeningen et al., 2006). Indigenous soil microbial communities generally contribute to disease suppression by reducing and competing with pathogen populations. However, high loads of organic material may not be required to influence these communities and enhance their biological control effectiveness. Unfortunately, the long-term studies with low application rates of organic materials at the same field locations are lacking or somehow ignored.

This 4-year study was aimed at serially applying the economically feasible rates of FE as a soil amendment prior to planting to establish suppressing conditions against soilborne potato diseases such as common scab and verticillium wilt. The results indicated that a 10-fold lower amending rate of FE compared with that used in our previous study (Abbasi et al., 2006) to the field plots effectively suppressed potato diseases and improved marketable and total tuber yields. Potatoes harvested from field plots receiving FE (2000 L ha⁻¹) consistently showed significantly less scab severity and low percentage of deep-pitted scabby tubers compared with potatoes harvested from the non-amended control plots. Such field plots also showed a low percentage of V. dahliae-infected potato plants during the first 3 years of the field trial. Total tuber yield from FE plots (2000 L ha⁻¹) was higher during the first 3 years when FE was applied; however, the percentage of marketable tubers was consistently higher during all 4 years compared with the control plots. Potato tubers harvested from the micro-plots amended with 0.1% FE also had less scab severity, further confirming the suppressive effect of economically feasible rates of FE on potato scab. However, no effect on tuber yield was observed in the micro-plots. The micro-plot data were based on single plants restricted in a plastic drainage tile. Future studies will not include drainage tiles and the number of plants will be increased to at least 10 per replicate.

Fish emulsion is an organic material that can provide suppression of soilborne diseases by both direct toxicity to plant pathogens (Abbasi et al., 2009) and stimulation of biological control activity in the amended soil or substrates (Abbasi et al., 2004). Very high application rates of FE can be toxic to plant pathogens and the toxic effects may be due to presence of organic acids, such as acetic and formic acids in FE (Abbasi et al., 2009) and also due to generation of toxic compounds in the soil after adding high rates of FE. High rates of FE can be phytotoxic in dry weather if not applied well ahead of planting (Abbasi et al., 2006). The rates of FE used in the current study were very low and cannot be directly toxic to causal agents of common scab and verticillium wilt diseases; therefore, it is less likely that direct toxicity has played a role in disease suppression reported in this study. On the other hand, increased soil biological activity and stimulation of biological control after application of FE to soil may be the key mechanism of disease suppression. There can be other possible mechanisms of disease suppression such as an increase in plant tolerance or resistance in the FE-mediated suppression of soilborne plant pathogens.

Bacterial activity in the soil samples from the field plots amended with FE (2000 L ha⁻¹) was significantly higher and this corresponded with lower percentage of V. dahliae-infected potato plants and less scab severity on tubers harvested from such plots. Several bacteria isolated from these FE-treated plots may have potential biological control activity against soilborne pathogens (unpublished data). It is possible that FE-stimulated bacterial activity including antagonistic agents in the amended soils may have been partly responsible for this disease reduction. However, any direct or specific role of this increased bacterial activity in reduction of scab severity on tubers and V. dahliae infection of potato plants has yet to be determined. Biological control has been reported for both potato scab (Neeno-Eckwall et al., 2001; Hiltunen et al., 2009; Al-Mughrabi, 2010; St-Onge et al., 2011) and verticillium wilt (Davis et al., 1996; 2001).

The potato rhizosphere offers an ideal model to explore biocontrol strategies for disease management. Seed potato tubers also offer an ideal avenue in terms of surface area to introduce high densities of biocontrol agents. Bacterial species isolated from rhizospheres of potato or other plant species have shown antagonistic activity against soilborne potato pathogens (Berg et al., 2002, 2006; Krechel et al., 2002) and may play a role in soil suppressiveness. We are also characterizing bacteria isolated from the potato field plots for their potential role in biological control of soilborne potato diseases. Such information would assist in selecting and enriching suppressive microflora after addition of organic materials and possibly establishing them in the field for disease suppression. It is known that utilization of organic amendments, crop residues or green manures can affect soil microbial communities and dynamics (Garbeva et al., 2004; Mazzola, 2007; Larkin et al., 2011; Bernard et al., 2012) thereby serving as important components in establishing and maintaining soil suppressiveness. Fish emulsion may provide that ideal base to enrich suppressive microflora under both greenhouse and field settings. In fact, FE has been used as a substrate for plant growth promoting rhizobacteria (El-Tarabily et al., 2003).

We previously reported that a high rate (20 000 L ha⁻¹) of FE reduced potato scab and verticillium wilt in soils of different characteristics, organic matter content and pH (Abbasi et al., 2006) and the reduction was not site- or soil-specific, unlike other amendments which have been shown to be greatly influenced by organic matter content and soil pH (Conn & Lazarovits, 1999, 2000; Tenuta & Lazarovits, 2002). However, the level of potato scab disease on tubers in field soil had an impact on the efficacy of FE as a disease control product. Our previous study (Abbasi et al., 2006) indicated that FE may not provide disease suppression in soils showing very high scab severity on tubers. Soils with medium level of disease (scab index of 1–3 on tubers) are ideal to establish these long-term studies with soil organic amendments. In soils with high levels of disease (scab index of > 3.0 on tubers), it may take longer to establish disease suppression with low rates of organic amendments.

This study demonstrated the effectiveness of economically feasible rates of FE to suppress soilborne potato diseases and enhance marketable and total tuber yields. The FE amendment rate of 2000 L ha⁻¹ applied every year before planting tubers should be feasible since it will also provide fair amounts of N-P-K fertilizer (80–120 kg N, 30–40 kg P₂O₅ and 24–54 kg K₂O ha⁻¹). In the organic crop production systems, growers rely on organic residue management to manage diseases caused by soilborne plant pathogens as well as for crop fertility requirements. Fish emulsion can provide nutrients to crops and can be an ideal product to establish disease suppressing conditions by enriching suppressive microflora. We need to compare autumn vs spring applications of FE for disease suppression. Our preliminary results from a new field study indicate that autumn application may not be necessary and disease suppression can be achieved with a single spring application before planting.

Acknowledgements

Technical support was provided by Brian Weselowski, Igor Lalin, Bruce McPherson, Albert Asztalos, and several summer students during 2007–2011. Special thanks to George Lazarovits, Kenneth Conn, and Bruce Reynolds for collaborative work, and the participating potato grower for allocating the experimental plots on his farm. This research was funded by Agriculture and Agri-Food Canada.