1. Introduction
The snap bean (
Phaseolus vulgaris L.) belongs to the
Fabaceae legume family, and
Phaseolus vulgaris L. is the only species that has distinct subspecies that are grown for snap beans. It is a unique vegetable that is enriched with protein content and is highly palatable [
1]. In parallel, it also plays a synergistic role in organic farming systems due to its deep root system, and the ability to fix nitrogen from air, which makes it an ideal crop to consider for crop rotation [
2,
3].
A myriad of factors could affect snap bean growth and yield in organic systems. Undoubtedly pests and disease occurrences are of paramount importance as they could reduce the yield significantly and deteriorate the quality. Usually, it is seed transmitted diseases that mostly attack snap bean. Notably, bacterial blight
Xanthomonas axanopodis pv.
phaseoli [
4] (Xap), halo blight
Pseudomonas savastanoi pv.
phaseolicola (Psp) and anthracnose
Colletotrichum lindemuthianum [
5,
6,
7] have been seen as the most harmful. These pathogens can persist in seeds for several years and reduce seed germination, cause rotting and seedlings death, as well reduce yield and quality [
8]. Snap bean varieties developed at Maritsa Vegetable Crops Research Institute (MVCRI), Bulgaria, possess high productivity, good taste and relative tolerance to major diseases when grown conventionally from disinfected seeds [
9]. Since seed disinfection is prohibited in organic systems, there is a need of effective alternative selection [
10].
Aphids (Hemiptera: Aphididae) are a major pest group not only due to their ability of direct host damage, but also as a vector of several viruses [
11]. Polyphagous black bean aphid (
Aphis fabae Scopoli) damages different parts of the plant [
12] and can cause significant yield loss estimated to be about 37% [
13]. Bean weevil (
Acanthoscelides obtectus Say) is another important pest especially for bean seed production. The relatively short window of oviposition in the field is considered to be critical time for bean weevil control [
14]. Since biological production is becoming more widespread in many countries, efforts have been directed towards the use of natural plant protection products such as phytopesticides. Many plants have insecticidal properties due to the presence of natural alkaloids, esters and other compounds [
15]. Azadirachtin-based insecticides (
Azadirachta indica A. Juss) are characterized as limonoids that act as antifeedant and deterrent [
16,
17,
18,
19]. Pyrethrins are extracted from flowers and seeds of the
Asteraceae pyrethrum plant (
Chrysanthemum cinerariaefolium Vis.). Worldwide, pyrethrum has been used as a safe and effective as pesticide for several years. Pyrethrum flowers contain pyrethrins that are synthesized from a mixture of esters. Pyrethrins have a broad-spectrum activity on most pests, causing quick knockdown effect as a contact and stomach poison. Simultaneously, they break down rapidly in the sunlight and, hence, do not cause harm to the environment and provide residue-free food [
20,
21,
22]. Due to these unique properties of affecting only target pests, being highly effective when applied in a very small quantity, and demonstrating quick decomposition, pyrethrins and other botanical products have steered an interest among scientific community [
23].
Besides plant derived insecticides, biological control using different predators, parasites and pathogens is another approach have been effective in organic systems. Entomopathogenic fungi produce metabolic compounds that may be toxic to insects and can be used to control pests as they are seen to be not detrimental against other non-target organisms [
24]. For example, the fungal culture or culture filtrate of
Beauveria bassiana (Bals.-Criv.) Vuill has potential for development as a mycopesticide to control the aphids [
25].
Organic cultivation relies entirely on ecological practices such as bio-control and enhancement of plant health and soil fertility through natural processes. Maintaining good soil health by combining the use of naturally derived products to control pests and diseases is a key to obtaining high quality residue free snap bean production when grown on organic farms. In this respect, the aim of the current study was to determine the impact of organic production practices on snap bean pests and diseases infestation, soil fertility and yield.
3. Results
3.1. Diseases
During the three experimental years, bacterial blight was reported as the main bacterial disease affecting snap beans. First symptoms usually occurred after plant emergence of and developed massively during flowering. Observed infection appeared as water-soaked spots on the lower leaf surface and lesions were usually surrounded by a narrow yellow halo those, turned brown. Over time, the lesions enlarged and ran together resulting in extensive necrotic areas. Leaves often appeared burned when the infection was severe. Meanwhile, leaves became ragged and sparsely dropped prematurely. Disease symptoms on pods were observed with variable size lesions that appeared circular, sunken and reddish-brown. Infected seeds shriveled, discolored and exhibited poor germination and vigor.
Anthracnose Colletotrichum lindemuthianum is the most common fungal disease that occurred throughout the experimental years. Anthracnose symptoms appeared on leaves, stems, pods and seeds. The most easily recognized anthracnose symptom were seen on the pods. Small, reddish-brown elongated spots were formed initially. During wet weather, a mass of pinkish colored spores was seen on the lesions. Infection started with the pod end up infecting developing seeds. Infected seeds had dark, sunken lesions of various sizes, which extended through the seed coat. When infected seeds were planted, the fungus multiplied and formed lesions on the cotyledons, and eventually spread to other plant parts throughout the season.
Other bean diseases observed during the growing seasons were of varying importance and frequently occurred diseases were Bean common mosaic virus (BCMV) that caused damage almost every year, while fusarium root rot (Fusarium solani f. faseoli) showed significant damage in some years.
The choice of plant protection products depends on their biological effectiveness, stability and its impact on key economic indicators. Considering these indicators, a first step in the plant protection program was to assess the efficacy of several fungicides (
Table 1).
As a result, the effect of double application of Bordeaux Mix 20 WP 3000 g/ha and Funguran ON 50 WP 3000 g/ha against bacterial blight and anthracnose was 65% and 66%, respectively. Against anthracnose, a comparison with two synthetic fungicides Ortiva Top 1000 mL/ha (a.i., azoxystrobin + difenoconazole) and Topaz 100 EC 500 mL/ha (a.i., penconazole), applied at flowering to pod formation in conventional field, showed 77.2% and 50.8% effectiveness, respectively. These results suggest that the Cu-containing products Bordeaux Mix 20 WP and Funguran ON 50 WP were equally effective to chemical fungicides against the main seed-borne diseases and, hence, can be used to control blight and anthracnose in snap bean production in organic system (
Figure 1).
The relatively lower effect of the applied plant protection products during the growing season was likely because the used seeds were non-treated before sowing. Hidden asymptomatic form of the infection resulted in a sustained increase in disease incidence in the crop over the years. The rate of seed infection increased over the years of the experimental period (
Figure 2).
3.2. Pests
Biological activity assessment of two products against
A. fabae showed that the product Krisant EC (750 mL/ha) had very good effectiveness (85.8%) within days of treatment, which was probably due to its good contact action inherent in pyrethrins. Naturalis (1000 mL/ha) also demonstrated good effectiveness against this pest, with maximum value recorded after the 7th day of the treatment (E = 83.5%). With Naturalis, no elevated initial activity was reported, but a good effectiveness of over 74% was observed in the interval 5–10 days after treatment. This is due to the mechanism of action of microbial products (
Table 2). Against the bean weevil, phytopesticide Krisant EC showed relatively better biological activity in both varieties studied here, with an overall effectiveness of 75% (
Table 3).
In recent years, unpredictable weather events caused by climatic changes seem to have increased the occurrence of the two-spotted spider mite (
Tetranychus urticae Koch.) in bean crops. The highest population density was found in the period from the second ten days of July to the second ten days of August, when average daily temperatures were highest [
31]. In our experiments, we observed good biological activity of Neem Azal against the two-spotted spider mite. The maximum value of effectiveness against the mobile forms of
T. urticae was 84% and was reported on the fifth day after treatment (
Table 4).
3.3. Monitoring Soil Nutrients
The experiment trial was initiated at a low level of soluble soil nutrients, and this deficiency remained constant during whole growing season irrespective of vermicompost application (
Table 5).
Before sowing (sample from mid-April), electrical conductivity (EC) of soil solution was very low (0.05 mS/cm), which corresponded to the low macronutrients content for all tested macronutrients, except P. Nutrient analysis of soil samples collected after ten days of sowing (end of April), which showed that the nutrients in soil were also low in both tested varieties. Right after the first application of vermicompost (beginning of June), the amounts of N, K and Mg, as well as pH, became lower, while Ca content and EC had not changed. After the second application of vermicompost (end of June), a slight increase in tested soil parameters was observed, generally N and EC, which was retained until the end of experiment.
3.4. Plant Growth and Productivity
The highest plants were produced by the Tangra variety in both plant development stages with height of 50.4 cm and 47.4 cm (
Figure 3 and
Table 6). At technological maturity, plant weight was highest in the Evros variety (111.3 g), while at botanical maturity, Tangra had heaviest plants (9.1 g). At technological maturity, the Evros variety formed the highest number and the heaviest green pods (15.8 and 71.9 g, respectively), which were significantly different from the Tangra variety. At botanical maturity, no differences between the varieties were observed for both traits.
The number of seeds per plant significantly differed between the two varieties—41.6 for Evros versus 29.0 for Tangra. Both varieties had statistically similar values for seed weight per plant and seed yield (
Table 6). For most plant growth and productivity traits, higher values were recorded in treated with organic pesticides plants, suggesting that the applied plant protection measures can limit pest attacks and therefore can reduce the risk of yield losses.
4. Discussion
Plant protection in organic fields entirely depends on adoption of preventive measures and techniques encouraging natural pest control. Often, an outbreak of pests imposes direct regulatory measures including application of approved biopesticides. Bordeaux mixture, containing copper sulfate, calcium hydroxide and water, is one of the first fungicides. It is commonly used in organic systems pest management and it is highly effective against bacterial and fungal diseases and used to manage several plant diseases [
32]. The current study examined two Cu-containing substances (Bordeaux mixture and Copper hydroxide), both are authorized to be used in organic fields under specific conditions and limits. Similar biological effectiveness of the two products against bacterial blight and anthracnose observed in this study suggests that they can be successfully used to control seed-borne diseases in organic cultivation of snap bean. Similarly, other authors observe good performance of copper-containing products in controlling anthracnose and blight diseases and increasing yield of bean and other crops [
33,
34]. In this study, use of non-pre-treated seeds resulted in a continued increase in diseases incidence over three years. This suggests that preventive control measures might be most important in organic snap bean growing and these measures are: use of disease-free seeds, crop rotation and weed control. Fungicide treatments should be applied if disease is present and if weather conditions would favor its development.
Pest management includes the use of plant insecticides as a suitable alternative for plant protection [
16,
35], since they have minimal residual effects and no pest resistance has been established against them. Most widely distributed and used commercial botanical pesticides include pyrethrum and neem products [
36]. Botanical pesticides are subject to many tests, performed mainly in laboratories [
37], but very few studies have shown their practical usefulness. Moreover, there is a lack of comparisons of biological effectiveness of a product on different pests’ species. The current study presents the biological activity of two commercial formulations of plant insecticides against the widespread pests of bean grown in organic field. Our findings showed a very good effectiveness of 85.8%, three days after treatment of the product with active ingredient pyrethrins against black bean aphid. These results are in agreement with Pavela [
38], who reported that extracts obtained from
Chrysanthemum cinerariifolium caused 98.3% mortality against
Myzus persicae Sulzer after two days of treatment. This was due to the rapid contact action that pyrethrins have, exerting their insecticidal effect by modulating the activity of voltage-gated sodium channels in the insect’s nervous system [
39].
Entomopathogenic fungus
Beauveria bassiana is a biocontrol agent that infects insect body by contact and is widely distributed in nature with wide range of hosts. It is safe for non-target organisms such as predators and parasitoids [
40]. After invading the insect host,
B. bassiana, produces many different secondary metabolites, such as beauvericin, bassianin, bassianolide, beauverolides, tenellin, oosporein and oxalic acid. These toxins induce a range of symptoms in the host, including severe dehydration, abnormal behavior, lack of coordination, convulsions, hindered feeding and metabolic disorders that eventually cause insect death [
41]. Our data showed that the product Naturalis, containing
B. bassiana, exhibited 83.46% effectiveness against
Aphis fabae after seven days of treatment. Similarly, Omar and co-authors [
42] investigated three different concentrations (1 × 10
2; 1 × 10
4; and 1 × 10
8 spores/mL) of
B. bassiana on adults of black bean aphid and reported 80% mortality on third day at the highest concentration (10
8 spores/mL).
Azadirachtin, a triterpenoid found in seeds of neem trees is one of most successful botanical pesticides, effective against a broad range of insect pest species. Azadirachtin- and neem-based products have also been evaluated against the spider mite [
43] and considered as valuable tool to control it [
44]. Azadirachtin causes several negative effects on arthropods, such as repellency, feeding inhibition, decreased oviposition, reduced fertility and fecundity, changes in behavior and increased mortality [
15,
45,
46]. In the current study, the maximum
T. urticae population reduction was observed five days after treatment. Normally, the highest peaks of neem-derived products that translocate in the plant occur on the fifth day after treatment and are stored in the roots, stems and leaves of plants up to a maximum of eight days. Afterwards, the effectiveness of the products declines [
47].
In organic fields, the only way to add more nutrients to the soil is the application of composts or vermicomposts as soil amendments. Vermicompost is considered a better alternative to the conventional compost due to better physical properties, higher microbial and enzymatic activity, and higher content of available nutrients [
48,
49]. In the current study, the application of 2850 L/ha vermicompost assured normal plant growth and satisfactory yield, despite of the low content of soluble soil nutrients throughout the experiment. As suggested by other authors, nutrients in vermicompost are not the sole factor that influence plant growth. It is well known that it can improve soil physical properties, nutrient turnover and increase the diversity and activity of soil microorganisms [
49].
The current study describes several techniques that can be successfully applied for organic growing of snap bean in open fields. They are in accordance with the current legislation adapted in Bulgaria, proved to be effective in a certified organic field and can contribute to increase the profitability of organic production. Hence, more research is needed to examine the long-term effect as well as the integration of other practices that can increase further benefits.