Introduction

Salvinia molesta Mitchell, a free-floating fern, is among the most widespread and environmentally harmful of the invasive plant species (Schooler et al. 2011). It is distinguished by its explosive rate of multiplication and growth, which is perhaps the highest of all plants (Crites et al. 2006). Salvinia has invaded lakes, rivers, channels and other wetlands in tropical and subtropical habitats around the world (Room 1990), covering several of them from bank-to-bank, and elbowing out most other vegetation (Luque et al. 2014; Bhat 2016). After spreading horizontally, salvinia forms dense mats of up to 1 m thickness that cuts the sunlight off from the underlying water and makes the waterways unnavigable (Coetzee et al. 2011). This also hampers the photosynthesis in the water body and the aerial replenishment of oxygen in the water lying beneath the salvinia carpet is blocked (Hussain et al. 2016b). As a result, the dissolved oxygen levels fall and the neustans and benthos are severely stressed. The stagnation of water caused by the salvinia facilitates mosquito breeding, and there is a rapid and precipitous loss of biodiversity in the invaded water body (Abbasi and Nipaney 1993). Salvinia’s unabated spread is because of its ability and to regenerate vegetatively even from tiny pieces of its leaves and its propensity to double its number every 3–4 days (Schooler et al. 2011).

With huge tracts of wetlands colonized by salvinia in South America, Africa, South Asia, and Australia (Abbasi and Nipaney 1993; Bhat 2016), billions of tonnes of salvinia biomass is generated every year across the world. As no method exists to utilize any sizeable fraction of this biomass (Ganeshkumar et al. 2014; Bhat 2016), it remains unharvested, causing serious harm to the wetlands (Abbasi and Nipaney 1986; Abbasi 1997). On senescence, it decays aerobically and anaerobically—mostly latter—generating global warming gases carbon dioxide and methane (Abbasi et al. 2011). As anaerobic decomposition in the anoxic epilimnion is the predominant salvinia decay pathway, it becomes a major contributor of methane emissions. With methane having molecule to molecule, 34 times greater global warming potential than carbon dioxide (Shindell et al. 2009), the harm caused by salvinia decay is immense.

The extensive and rapid spread of salvinia has been halted and repelled by the use of a few biological agents (Room et al. 1981; Sullivan et al. 2011) but such successes have been few and far between. Worse, none has led to any enduring solution to the salvinia problem. Mechanical removal of salvinia and use of weedicide have recorded even lesser success in controlling its spread. Attempts to utilize salvinia for the generation of compost, green manure or mulch (Raju and Gangwar 2004; Arthur et al. 2007; Dorahy et al. 2009), as fodder (King et al. 2004; Leterme et al. 2010), as a source of biogas (Abbasi et al. 1990; Abbasi and Nipaney 1991; Abbasi et al. 1992a, b; Abbasi and Abbasi 2010; Ganesh et al. 2005), or for making drugs (Chantiratikul et al. 2009; Choudhary et al. 2008; Li et al. 2013; Tauseef et al. 2013), have all proved uneconomical. Thus, finding a sustainable, ecologically sound, and inexpensive way with which salvinia biomass can be utilized on the scales it is generated appears to be the only recourse which can make it profitable to regularly harvest the weed, thereby keeping a check on its alarming growth.

Vermicomposting is one such option, by which the weed can be regularly harvested and converted it into beneficial biofertilizer. Studies conducted across the world on manure-based vermicompost have shown that such vermicompost is a well stabilized, aesthetically pleasing, and finely divided peat-like material with excellent physicochemical and biological characteristics (Edwards et al. 2011) that one seeks in a good organic fertilizer. In a recent study, Ganeshkumar et al. (2014) have found that salvinia can be directly and quickly converted into vermicompost, following the concept of high-rate vermicomposting earlier developed by Abbasi and co-workers (Abbasi et al. 2009,  2015). But before the process is put to large-scale use, it must be ascertained whether salvinia vermicompost is as much, or at least nearly as much, soil friendly and plant friendly as manure-based vermicompost is known to be. This question is highly significant because salvinia plants contain unusually large concentrations of polyphenols and lignin. This feature makes salvinia strongly allelopathic and hardy (Leterme et al. 2010; Hussain et al. 2016a) and it becomes essential to rule out any adverse effect that the polyphenols and lignin content of salvinia might exert on the utility value of salvinia’s vermicompost. To alley this apprehension, the present field-scale study has been carried out to see how a common vegetable ladies finger (Abelmoschus esculentus) responds to the application of salvinia vermicompost during its germination growth, and fruit production phases.

Materials and methods

General

All analytical work was performed with analytical reagent grade chemicals, and alkali-resistant borosilicate glassware. The dilution water was deionized and double distilled before use. Dry weight determinations of all samples of soil, plants, and vermicompost were done by heating known quantities of samples at 105 °C to constant weights.

Vermicompost was generated from the whole plants of salvinia, collected from the ponds in the vicinity of Pondicherry University campus, employing earthworm species Eisenia foetida. Pulse-fed, high-rate, vermireactors were utilized for the purpose. The setting and operation of the vermireactors were as detailed earlier by Nayeem-shah et al. (2014) and Ganeshkumar et al. (2014). No pre-composting, manure supplementation or any other form of pre-treatment was done. The vermicompost was periodically assessed in the form of easily identifiable, separable, and quantifiable vermicast that was generated in each 20-days pulse (Abbasi et al. 2009, 2015). The total nitrogen, phosphorus and potassium (NPK) contents of the vermicompost were 17.9, 2.92 and 11.45 g/kg, respectively. The soil used in the present experiment was collected from an uncultivated area of Pondicherry University campus. This was done to prevent interference from any previous fertilizer application. The soil, which was characterized as sandy loam, had pH 6.35, and contained organic carbon, total nitrogen, phosphorus and potassium to the extent of 8.8, 2.71, 0.24, and 0.75 g/kg, respectively.

Planting of ladies finger

Germination and plant growth studies were carried out in 50-l plastic containers. In each treatment, 35 such bags were filled with soil and amended with four levels of salvinia vermicompost: V0 (control), V1-25 g, V2-37.5 g, and V3-50 g on dry weight basis. This corresponds to 0, 2.5, 3.75 and 5 t/ha VC, respectively. Five seeds of ladies finger (Abelmoschus esculentus) were sown in each container. The study was carried out during February–May which is the period considered ideal for growing ladies finger in the region where authors work (ICAR 2011).

Analysis

The fraction of seeds that germinated within 8 days of sowing was enumerated to determine the germination success. Thereafter, one of the healthy seedlings was retained in each bag while discarding the other four. The growth experiments were then carried out for 15 weeks, irrigating all the containers with tap water every day. 100 days after sowing, five plants from each treatment were randomly harvested. Their shoot length (cm), root length (cm), plant biomass (g), number of leaves, stem diameter (mm) and number of branches were determined. The speed and the extent of flowering were computed in terms of number of days taken by the plants to produce their first flower, and the total number of flowers produced per plant. The number of pods and the average length (cm), diameter (mm), and weight (g) of the pods per plant were recorded.

Fresh leaves of the ladies finger plants were collected for estimation of chlorophyll and carotenoids. These pigments were extracted from the leaves using N, N-dimethyl formamide (DMF) following a procedure of Moran and Porath (1980). The concentrations of the pigments were determined spectrophotometrically at 470, 647 and 664 nm as detailed by Wellburn (1994). The protein, carbohydrates, and mineral content of the ladies finger pods were estimated by Kjeldahl, Anthrone and dry washing methods, respectively (Nielsen 2010).

Disease incidence and pest infestation

Soon after the start of the experiments, the leaves of the ladies finger plants began getting infected by leaf miners and leaf spot diseases. It could be seen that the prevalence of infection was highly pronounced in the control plants but much lesser in the vermicompost-fertilized plants. The symptoms of the leaf miners infection, which is caused by Liriomyza spp, were feeding punctures and white speckles on the leaf surface (Ahmed 2000). The leaf spot disease, caused by the fungus Alternaria alternate, was manifested by light brown spots appearing on the leaves, which later turned into concentric dark brown spots (Tohyama et al. 2005; Hussain et al., 2017b). When the infection became particularly severe, it caused the infected leaves to turn brown and fall off (Antonijevic et al. 2007). Another form of infection, which affected only the fruits, was due to Earias vittella (Sharma et al. 2010; Halder et al. 2015; Hussain et al. 2017b) called ‘borer infection’. It was quantified as the fraction, by weight, of the infected fruits relative to the total fruits.

Tests of significance

These were performed by one-way analysis of variance and least significant difference (Alan and David 2001; Field 2009).

Results and discussion

Seed germination and plant growth

In vermicompost treatments, the germination success was significantly (P < 0.05) higher than in the controls. The maximum (97%) germination was observed in V3 treatment. It was followed by 96% and 87% success in V4 and V2 treatments (Fig. 1a). The controls had shown the least germination success. The augmentation of soil with salvinia vermicompost also enhanced the growth of ladies finger in terms of shoot and root length, plant biomass, number of leaves, and number of branches (Fig. 1b–h). The maximum shoot length (96.2 ± 9.4), root length (48.2 ± 4.8), shoot diameter (14.04 ± 0.7), shoot dry weight (23.31 ± 2.3), root dry weight (7.96 ± 0.6), number of leaves (26.8 ± 2.3), and number of branches (4.8 ± 0.5) were recorded in V4 treatment. The lowest growth was recorded in the controls. With the exception of root length, the improvement in growth even with the lowest (V1) level of vermicompost augmentation in comparison to controls was dramatic and highly significant.

Fig. 1
figure 1

Effect of salvinia vermicompost on a germination percentage; b shoot length; c root length; d stem diameter; e shoot dry weight; f root dry weight; g number of leaves; and h number of branches, of ladies finger plants. The standard deviation is indicated on the chart. The results shown in columns accompanied with an asterisk are significantly different from the controls at P ≤ 0.05

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Past studies on the effect of vermicompost derived from animal manure on plants have shown that such vermicomposts have major, medium, and micronutrients in more bioavailable form compared to their parent substrate (Hussain et al. 2016a). The vermicompost is also endowed with much richer and diverse microflora than the parent substrate (Hussain et al. 2015, 2016b). It appears that salvinia-based vermicompost also acquires similar plant-friendly and soil friendly attributes. Additionally, manure-based vermicomposts are known to contain fulvic acids, humic acids, and phytohormones (Atiyeh et al. 2002; Ievinsh 2011; Doan et al. 2015) which rejuvenate the soil and makes it plant-friendly. Recently, Hussain et al. (2016b) have reported that salvinia loses its reproductive ability after it is ingested by earthworms. The microbial and enzymatic degradation of salvinia during its passage through the earthworm gut leads to generation of several fatty acids, alcohols, alkanes, alkenes, and nitrogenous compounds. These compounds together with the presence of growth hormones and humic acids may have contributed to the better growth in VC-treated plants than in controls, as has been observed earlier in case of manure-based vermicomposts (Atiyeh et al. 2002; Doan et al. 2015; Kumar et al. 2015).

Humic acids are known to stimulate plant growth through increased cell division, enhancement of uptake of nutrients and water, and enhancement of the soil microbial population (Atiyeh et al. 2002; Chen et al. 2004; Delgado et al. 2002; García-Gil et al. 2004; Xu et al. 2014; Hussain et al. 2017a, b). It has been reported that humic acids derived from manure-based vermicompost facilitate elongation of roots and emergence of lateral roots—besides enhancing the root’s H+-ATPase activity in maize (Canellas et al. 2002). Both humic acids and plant growth hormones are probably produced by the diverse microbial population present in vermicompost (Frankenberger and Muhammad 1995). Improvement in the physical properties of the soil, especially enhancing its air and water holding capacity, have also been reported which increase the plant productivity in soil treated with manure-based vermicompost (Edwards 2004). Evidently, salvinia vermicompost possesses similar virtues to be able to generate similar effects.

Flowering and yield

Salvinia vermicompost not only induced early flowering in the ladies finger plants compared to the controls, but also resulted in the appearance of a significantly (p < 0.05) larger number of flowers. In all the vermicompost treatments, the yield was significantly higher than the controls. The fruit yield, reflected in the number and weight of pods per plant (10.90 ± 1.10, 105.23 ± 5.77), and the size (length and diameter) of the pods (12.35 ± 0.98; 16.17 ± 1.54), was significantly higher in VC treatments than in the controls (Fig. 2).

Fig. 2
figure 2

Effect of salvinia vermicompost on a early flowering; b number of flowers per plant; c number of pods per plant; d length of pods; e diameter of pods; and f weight of pods per plant, of ladies finger. The standard deviation is indicated on the chart. The results shown in columns accompanied with an asterisk are significantly different from the controls at P ≤ 0.05

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The findings are similar to the ones achieved with manure-based vermicompost by other authors earlier (Jouquet et al. 2011; Abduli et al. 2013; Joshi et al. 2015; Doan et al. 2015; Song et al. 2015), and indicate that the salvinia vermicompost also possesses similar virtues.

Biochemical aspects

Vermicompost application increased the concentration of photosynthetic pigments exemplified by the chlorophyll and carotenoid content in the leaves to a highly significant extent as compared to the controls (Fig. 3a–c). There was also an increase in the protein and carbohydrates content of the pods, but the increase was not statistically significant (Fig. 3f, g). On the other the total solids and ash (mineral) content of the pods grown in vermicompost-augmented soil was significantly higher than that of control soil (Fig. 3d, e). These findings indicate that salvinia-based vermicompost also has as much beneficial effect in terms of plant biochemistry as manure-based vermicomposts are known to cause (Abduli et al. 2013; Yadav et al. 2015).

Fig. 3
figure 3

Effect of salvinia vermicompost on a chlorophyll ‘a’; b chlorophyll ‘b’; c carotenoids content of ladies finger leaves and d total solids; e ash; f carbohydrates and g protein content, of ladies finger fruits. The standard deviation is indicated on the chart. The results shown in columns accompanied with an asterisk are significantly different from the controls at P ≤ 0.05

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Disease incidence

Vermicompost caused a reduction in the incidence of diseases in the leaves as well as the pods; the extent of this effect increased in proportion to the VC concentration (Fig. 4). At the early stages of growth, the seedlings were seen severely infested by leaf liner, but the infection subsided as the growth increased. In this respect, also, the salvinia vermicompost seems to possess beneficial effects similar to the ones known to be possessed by manure-based vermicomposts.

Fig. 4
figure 4

Disease incidence and percentage of infected fruits in ladies finger as affected by the salvinia vermicompost. The standard deviation is indicated on the chart. The results shown in columns accompanied with an asterisk are significantly different from the controls at P ≤ 0.05

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There is no definite knowledge on the mechanism governing the pesticidal properties of the vermicompost (Hussain 2016). A possible cause can be that vermicompost supplies highly bioavailable nutrients which enhance the vitality of the plants, empowering them to ward off infection. Another likely reason is the presence of pathogen-destroying microorganisms in the vermicompost (Yardim et al. 2006; Aghamohammadi et al. 2016; Datta et al. 2016; Xiao et al. 2016).

Past studies have reported that vermicompost derived from animal manure possesses both these virtues (Edwards 2004; Edwards et al. 2011) and, hence, induced the resistance in plants against several plant pathogens (Szczech 1999; Szczech and Smolinska 2001; Choudhary et al. 2010; Nath and Singh 2011). The present study indicates that salvinia vermicompost may also be acquiring similar virtues which enable it to induce resistance against pathogens in ladies finger plants.

Conclusion

The paper reports studies which have assessed the effect of the vermicompost of the aquatic weed salvinia on the germination, growth, yield, and quality of the fruits of a common food plant ladies finger (Abelmoschus esculentus). The role of the vermicompost in warding off the diseases of the ladies finger leaves and pods was also witnessed. In general, a positive effect was exerted by the vermicompost in increasing germination success, plant growth, yield, and pest resistance. The degree of benefit increased in proportion to the concentration of the applied vermicompost when it was varied in the range 2.5–5 tonnes/ha. In contrast to the toxic and allelopathic nature of salvinia, its vermicompost proved totally benign, and appeared to be highly plant friendly, with virtues of an organic fertilizer similar to the ones known to be possessed by the vermicomposts derived from animal manure.