Streamlining Agroecological Management of Invasive Plant Species: The Case of Solanum elaeagnifolium Cav

Abstract

The increased demand for the adoption of sustainable practices to protect agroecosystems is challenged by the introduction and dominance of invasive plant species (IPS). The management of IPS requires a direct response from farmers and policy makers and is often associated with the adoption of practices that have negative ecological impacts. Solanum elaeagnifolium Cav. (silverleaf nightshade) is a noxious IPS posing a serious threat to agriculture and the environment. The increased resistance to the biotic and abiotic stress factors caused by high phenotypic plasticity, dense trichomes, and spines allow the weed to adapt to many habitats, rendering several herbicides ineffective. If an early detection and eradication fails, multiple management strategies should be adopted to mitigate a further dispersal. Herbicides should be applied before or during flowering to prevent the formation of berries and the production of seeds. Precision agriculture tools, such as decision support systems, can be exploited to reduce the herbicide input. Soil tillage should be avoided to prevent clonal reproduction. Mowing is an effective tool to prevent the setting of seeds. Biological agents should be carefully released as a part of an agroecological weed management framework. Future research should focus on the development of cross-boundary protocols and actions to monitor the introduction pathways for the early detection and agroecological management of S. elaeagnifolium.

1. Introduction

Modern agriculture is being severely affected by climate change, with the management of weeds becoming a greater challenge and the number of invasive plant species (IPS) increasing [1,2]. The successful eradication of an IPS is followed by a series of risks, mainly faced by farmers, concerning the decisions they have to take to avoid a recurrence of the problem. In particular, complacency, an underestimation of the risks, and disorientation from the real needs for monitoring a successful eradication of an IPS are the most important factors that lead to wrong decisions, the spread of invasive species and the economic and environmental degradation of farms and habitats. The lack of sufficient knowledge and awareness of those directly involved in mitigating the impact of weeds, namely farmers, leads to delayed actions that give an IPS a head start in the battle for dominance, and compounded by the lack of funds and subsidies, create a context that favors the failure to monitor the IPS. Otherwise, if the eradication of weeds fails from the outset, then it is likely to be extremely difficult to control the IPS, and comprehensive management frameworks need to be pursued. In this case, as well, a series of bad decisions lead to the intensification of the problem, high management costs, the further spread of an IPS or the emergence of new ones, all culminating in the continued application of inappropriate agricultural practices that have a negative ecological footprint. A conceptual framework for the decision-making process for the response to IPS outbreaks is summarized in Figure 1.

The management of common weeds has been thoroughly investigated for many different crops, different habitats, diverse farming systems, and the available tools and equipment, under changing conditions or hypothetical scenarios, creating an arsenal for farmers and policy makers to mitigate their impact on agricultural production, biodiversity, and the environment. However, it should be noted that the response against the spread of an IPS has some specific characteristics that require attention and the redesign of weed management frameworks. Indicatively, IPS: (a) are usually identified late, having already established and dominated the invaded environment; (b) are only barely investigated by research, knowledge from the literature, and from monitoring and management protocols; (c) often their risk is underestimated and thus not taken seriously, leading to misguided management practices that favor their dominance and magnify their impact; and (d) they display special morphological and physiological traits that render many common weed management practices ineffective, resulting in the adoption of other practices that have a negative ecological impact.

The modern market demands more safe, equitable, and green production and consumption has led to the reduction in pesticides and the adoption of sustainable practices that protect pollinators, animals, non-target organisms, and the user, while improving the soil’s health, biodiversity indicators, and the resilience of agricultural systems to climate change and energy and disruptions in the pesticide market. Particularly in Europe, the legislation to reduce the use of pesticides by 50% in the coming years and the farm to fork and biodiversity strategies have led to a dramatic reduction in the available solutions for the management of weeds. However, the successful management of weeds is assisted by a range of old and new tools including non-chemical methods, new technologies, innovative cultural practices, and competitive plant material. All these techniques are summarized in the papers of Tataridas et al. [3] and Cordeau [4] can be integrated into a framework of the agroecological management of weeds and agroecological crop production. Although many of these techniques are simple, affordable, and effective, farmers still face significant dilemmas. Some of these (such as the range of applicability, cost-effectiveness of the applications, impact on non-target organisms, etc.) are being intensively investigated in recent years for common weeds in many countries. However, the situation remains more difficult for IPS for the reasons mentioned above [3]. A list of common dilemmas for farmers is illustrated in Figure 2.

This review aims to suggest a novel framework for the holistic and efficient agroecological management of an important IPS, Solanum elaeagnifolium Cavanilles, that is often managed with practices with negative implications, to serve as a paradigm for the sustainable management of an IPS in general.

2. The Case of Silverleaf Nightshade

2.1. Solanum elaeagnifolium

Solanum elaeagnifolium (or commonly silverleaf nightshade) is a summer perennial noxious invasive plant species that belongs to the Solanaceae family. It is native to the South-West USA and North Mexico, and probably to Argentina. Solanum elaeagnifolium is considered to be a cosmopolitan invasive plant species which is highly aggressive as it is acclimatized to many different pedoclimatic conditions and invades a vast number of different habitats, including agricultural and livestock regions, urban areas, roadsides and disturbed areas, ruderal environments and abandoned places, irrigation channels, and forest margins [2,5,6]. The negative impacts deriving from its presence include the yield losses of various crops (e.g., cotton, soybean, maize, wheat, sorghum, and vegetables), the decline in biodiversity, the intoxication of animals, the hosting of harmful insects, fungi, bacteria, and viruses, the blockage of irrigation channels, the increase in the production costs for farmers, and the reduction in the value of land. Indicatively, it has invaded all five continents and in the last few years, new records have been made in many countries [7], which unexpectedly are located to the North of the typical latitude growth range of the species. This movement to the North is beyond doubt linked with climate change and the rise in temperatures, factors that favor the dispersal and establishment of S. elaeagnifolium in new suitable habitats. Solanum elaeagnifolium is commonly known as silverleaf nightshade due to the silver colors of its leaves. However, it should not be overlooked that its common name in South Africa, a severely infected country from S. elaeagnifolium, is ‘Satansbos’, or the bush of Satan, and in some locations of Northern Greece, it is known as ‘Lernaean Hydra’ due to the ability to regenerate extensively [8,9].

A series of key biological and ecological traits hinder the management of S. elaeagnifolium and set this species on several lists of quarantine pests. Silverleaf nightshade propagates both sexually through seeds and asexually through rhizomes and rootstocks. A single plant is capable of producing more than 120 berries; each one of them can occasionally bear more than 60 seeds. The rhizomes extend in a wide network in the soil, reaching even 2.80 m at depth and up to 3 m horizontally. The shoots and leaves are covered with a dense layer of stellate trichomes and frequently with orange to brown-colored prickles. The presence of trichomes reduces the uptake, absorption, and translocation of herbicides to the root system. Silverleaf nightshade regrows shortly after mowing or tillage from buds that are found on rhizomes or in the stems. Root fragments of a 0.5 cm length produce new shoots, raising awareness on the control treatments that focus on the root system. Moreover, the herbicides have been reported to have a low efficacy against S. elaeagnifolium because the translocation to the root system is not always guaranteed even for effective systemic herbicides such as glyphosate.

2.2. Chemical Control

To achieve the exhaustion of the weed’s growth potential, the application of effective systemic herbicides, such as glyphosate, had been adopted. The application of glyphosate at the rate of 3600 g a.e. ha⁻¹ in summer or autumn can significantly reduce the new shoots of S. elaeagnifolium the following spring [10]. Gitsopoulos et al. observed that the application of glyphosate in the form of isopropylamine salt at a dose of 3600 g a.e. ha⁻¹ and provided a high weed control five weeks after application, while the efficacy was close to 90% when the herbicide was applied at a young vegetative stage or at the beginning of flowering [11]. Glyphosate at the rate of 2150 g a.e. ha⁻¹ at the green immature fruit stage with the addition of 5% ammonium sulphate provided more than 90% of the control of S. elaeagnifolium the following year [12]. Remarkably, the application of glyphosate in Morocco at doses of either 1440 g a.e. ha⁻¹ or 2160 g a.e. ha⁻¹ and either under the addition of surfactant or not, resulted in a 71–93% reduction in the seed viability when the herbicide was applied at full flowering [13]. In contrast, when glyphosate was applied at the immature green fruit stage slightly reduced seed viability, which accounted to 2–12%. The reduced rates of glyphosate applied in the fall (from 800 g formulation ha⁻¹) have been shown to provide an almost similar control (>93%) to higher rates (up to 1700 g formulation ha⁻¹) and at least a 77% reduction in the shoots the following season, indicating that in the long term, it is feasible to reduce the weed density without requiring high inputs [14], such as in the case of the clonal invasive species Asclepias syriaca L. [15]. Multiple applications of glyphosate or other systemic herbicides significantly reduce the shoot density both during one growing season and in the subsequent years. However, a single application of glyphosate was sufficient to significantly reduce the density of S. elaeagnifolium and increase the cotton fiber yield in a three-year study, maintaining similar yields to double and triple the applications of glyphosate, thus reducing the weed control costs [16]. Specifically, the shoot density after three years of applications was reduced by 12% with a single glyphosate application at the 4–6 leaf stage of cotton, by 50% when the herbicide was applied at the 4–6 leaf stage and again three weeks later, by 70% when applied early in the growing season and again at the stage where 20% of the bolls had opened, and reduced by 89% when three glyphosate applications were made at all three stages of the cotton’s growth. In a field experiment conducted in Greece on the efficacy of different glyphosate salts against S. elaeagnifolium plants that were either at the vegetative, flowering, or fruit stage, it was shown that the selection of the formulation salt has a significant effect on the glyphosate efficacy [17]. In detail, potassium and isopropylamine salts, the mixture of isopropylamine salt with ammonium, and the mixture of isopropylamine salt and 2,4-D provided 92–97% weed control on the plants in vegetative growth (5–10 cm). At the flowering stage, the control rate varied widely among the treatments (37–91%), while at the fruiting stage, the control was high (77–100%). Potassium salts had the lowest efficacy at the flowering stage, while the glyphosate mixture in the form of isopropylamine salt with 2,4-D provided the highest control (91%), indicating that it is an effective choice for the control of S. elaeagnifolium. However, in field experiments in Australia, it was observed that the combination of glyphosate with 2,4-D did not provide a consistent control in two fields because in one field, the number of shoots decreased by 61% over 3 years, while in the other field it remained stable [18]. Revegetation following a 2,4-D application was found to be more rapid after successive applications in pastures in Australia than with glyphosate, where the effect on the underground propagules was probably greater [19]. In Morocco, the herbicides glyphosate, sulfosate, and aminotriazole are proposed in the perennial crops (such as olive groves and citrus orchards) or after the harvest of the annual crops, and only in the case where heavy infestations are observed [20].

For the long-term control of new shoots, a repeated application of glyphosate or another residual herbicide, such as picloram, later in the growing season or in autumn is recommended for the long-term control of new shoots [21]. According to the same authors, the optimal stage for a herbicide application is the flowering stage, in order to avoid the production of seeds to a satisfactory level. In Australia, the flowering stage or being early at fruiting is also recommended for spraying post-emergence herbicides such as 2,4-D, picloram, and glyphosate [22]. The flowering and fruiting stage is, of course, not optimal for controlling S. elaeagnifolium rhizomes [21]. However, spraying with the residual picloram in the fall (for the Southern hemisphere) to target rhizomes is recommended [18]. Spraying with glyphosate at the flowering stage of the weed at rates between 2160 and 2880 g a.e. ha⁻¹ significantly reduced the dry weight of the shoots and fruits when followed by a second spraying targeting resprouts [23]. In the same study, it was shown that the synthetic 2,4-D auxin and oxyfluorfen diphenyl ether provided a moderate to adequate control of S. elaeagnifolium, although resprouts were observed. 2,4-D at the pre-flowering rate of 2240 g a.e. ha⁻¹ is considered to be an effective application for suppressing the growth of weeds [24]. 2,4-D at the rate of 720 g a.e. ha⁻¹ yielded a 90% control of S. elaeagnifolium 30 days after application, while the herbicides bromoxynil and prosulfuron were not effective [25]. An application with triclopyr, a highly effective herbicide widely used against the weed, at the dose of 1380 g a.i. ha⁻¹ provided a long-term absolute control during the three years of experimentation. In a study in Texas (USA), triclopyr at the rate of 1750 mL formulation ha⁻¹ resulted in a more than 80% weed control six weeks after the application [26]. The small leaf area of S. elaeagnifolium exposed to the absorption of the active substance is a major obstacle to the application of systemic herbicides against the weed by preventing the herbicide from being translocated to the extensive rhizome network and preventing a high efficacy [27]. Kidston et al. suggest that the efficacy of a herbicide is increased when applied after a period of rainfall when S. elaeagnifolium has a high metabolic activity [28]. The same is evidenced by a large-scale experimentation carried out in Morocco, where glyphosate at the dose of 2160 g a.e. ha⁻¹ was more effective in fields where they had previously received irrigation or rain [20]. The application of the post-emergence herbicide tembotrione at the rate of 148.5 g a.i. ha⁻¹ provided an acceptable control >80% six weeks after the application on plants in the young vegetative stage [11]. However, mixing tembotrione with the contact herbicide bentazone resulted in a reduced control of S. elaeagnifolium. The application of the ALS inhibitors, imazapyr, and imazethapyr provided no more than 65% and 57%, respectively, in a study conducted in Texas, the USA [29]. The use and mixture of herbicides having different mechanisms of action has been suggested for the control of weeds. The mixture of 2,4-D+dicamba+triclopyr+pyraflufen herbicides resulted in 91% control 40 days after application during flowering [30]. An application at the onset of the flowering of the mixture of 2,4-D, picloram, and metsulfuron methyl provided 90% weed control [21]. In the same study, however, it was shown that a long-term control was achieved when picloram was used. The application of the herbicide mixture triclopyr+picloram+aminopyralid, and picloram alone, in summer and autumn were found to be highly effective against S. elaeagnifolium, but their high cost compared to other known herbicides and the residual activity of picloram are barriers to the widespread use of similar residual herbicides [18]. Aminopyralid provided 97–100% weed control in the year of the application [31]. The contact herbicide glufosinate, which is a glutamine synthase inhibitor, at the dose of 1500 g a.i. ha⁻¹ provided 95% weed control and resulted in a significant reduction in the fresh plant weight one week after the application was applied when the plants were in the young vegetative stage or at the beginning of flowering [11]. However, the monitoring of the efficacy should be carried out in the following year in order to control the dynamics of the weeds. For example, the herbicide aminocyclopyrachlor was tested in 2009–2010 in the USA and was found to provide 45–87% control one year after its application (between doses of 35 and 140 g a.i. ha⁻¹, respectively), although the control was total up to 4 months after the application [32]. The mixture of herbicides bromacil and tebuthiuron, which has a residual activity in the soil and is not easily washed away by rainwater due to the physicochemical properties of the molecules, was found to provide the long-term control of S. elaeagnifolium in a study conducted in South Africa, while the herbicides imazapyr and hexazinone did not result in the long-term control of the weed [27]. In Morocco, bromacil is not recommended for large areas due to its high cost, but it can be applied to heavily infested fields with citrus trees older than four years [20]. The use of pre-emergence herbicides is not recommended for the control of S. elaeagnifolium as they have been found to have a low to moderate efficacy. In particular, pre-emergence applications of the herbicides pendimethalin at 670 g a.i. ha⁻¹, metolachlor at 2130 g a.i. ha⁻¹, prodiamine at 1680 g a.i. ha⁻¹, and dithiopyr at 560 g a.i. ha⁻¹ did not exceed 70% weed control eight weeks after the application [33]. In a cotton crop in Syria, trifluralin was only able to reduce germination but had no effect on the regrowth [34]. To reduce the amount of herbicide applied, it has been reported that mechanical tillage a few weeks before spraying can reduce the weed population so that lower herbicide doses can be applied [35].

2.3. Agroecological Weed Management Strategies

2.3.1. Bio-Based Herbicides

The use of natural or bio-herbicides is a promising strategy for the control of weeds, which is also in line with the European Union’s requirements to reduce chemical pesticides by 50% by 2030 [36]. The efficacy of essential oils and natural and biological herbicides has been thoroughly researched in recent years, and there are significant reviews of the existing literature worldwide [37,38]. The use of plant extracts from Eucalyptus plants has been shown to have phytotoxic properties and can inhibit seed germination and inhibit the growth of S. elaeagnifolium seedlings during the early growth stages [39], inhibiting up to 91% of the root growth [40]. In particular, essential oil from the leaf extract of Eucalyptus salubris F. Muell. containing a high content of the 1,8-cineole molecule had a high inhibitory effect on the seed germination (73%) and on the shoot and root length of the weed, of 75.7% and 82%, respectively. Seed germination was strongly inhibited due to allelopathy induced by the leaf extracts of the forest species Quercus pubescens Willd., Pinus brutia Ten., Cupressus semprevirens L., and Quercus coccifera L. [41]. Specifically, P. brutia leaf extracts led to the onset of the germination of S. elaeagnifolium seeds only on day 18 of the experiment, while the untreated control seeds started to germinate from day 8. This result is particularly important for the management of the new shoots of the weed and their early management. The extracts significantly reduced the root regrowth (6.67%), while the root regrowth of the untreated control exceeded 50%.

The addition of adjuvants such as specific surfactants increased the efficacy of the herbicides. The addition of ammonium sulfate to glyphosate at the rate of 2160 g a.e. ha⁻¹ resulted in an increase in the control of S. elaeagnifolium [13]. The addition of 2% ammonium sulfate and 0.5% non-ionic surfactant to glyphosate resulted in a very high weed control and a reduction in the subsequent season’s shoots [14]. The addition of 5% tallow amine ethoxylate or 5% ammonium thioate to glyphosate at the 1150 g a.e. ha⁻¹ rate resulted in an almost similar control to glyphosate at the 2310 g a.e. ha⁻¹ rate without the addition of a surfactant, suggesting that the addition of adjuvants can reduce herbicide inputs while maintaining the adequate control of S. elaeagnifolium [42].

2.3.2. Cultural and Novel Practices

Targeted burning increases the weed density as it leads to the sprouting of new shoots [23] and has been considered ineffective for the control of weeds since the mid-20th century [43]. Selective goat grazing is another tool to reduce the risk of the spread of weeds in dryland and grassland areas [44]. In Australia, it was observed that in isolated cases, the shoot density was reduced by up to 75% after continuous grazing or under a combination of grazing and herbicide sprays [45]. Ground squirrels feed with all parts of S. elaeagnifolium and could be further evaluated for the management of the weed, as revealed by Rammou et al. [46].

Research has been carried out on the use of cover or residual crops to inhibit the growth of S. elaeagnifolium. Digitaria eriantha Steud. and Digitaria milanjiana (Rendle) Stapf strongly compete with S. elaeagnifolium and significantly reduce the weed density [18]. Viljoen and Wassermann studied a potential weed inhibition using cover crops under dry conditions for four years, namely perennials (Medicago sativa L. and D. eriantha) and annual (Avena sativa L.) [8]. All three species competed strongly with the weed, but only D. eriantha provided the partial inhibition of the weed growth under water deficit conditions. Recognizing the potential of alfalfa to effectively compete with the weed, FAO (2011) suggests rotating crops where feasible with alfalfa [47]. The same conclusion was reached by Travlos et al., who observed that the selection of a competitive alfalfa variety is particularly important for the successful establishment of the crop in the first year [48]. In Morocco, growers knew that alfalfa and mint could reduce weed dynamics before scientific research on the management of weeds was initiated [35]. The frequent cutting of alfalfa is considered to be an effective means for reducing the density of weeds. Ground cover with plastics seems to not be an effective measure to control the weed, as it has been reported that it can easily puncture them and grow [23].

2.3.3. Precision Agriculture Tools

Farmers need support in terms of the actions they need to take to manage weeds. The only research conducted to date on the use of a decision support system for the management of S. elaeagnifolium was conducted in the USA in cotton [49]. A triple universal application with glyphosate at 840 g a.e. ha⁻¹ during the growing season resulted in an almost complete weed control (98%) compared to applying variable doses between rows. However, in the second year of experimentation, both treatments showed a similar control with no difference between them (65–85%) when evaluated 120 days after sowing. This result leads to the conclusion that an experimentation with decision support systems for the management of S. elaeagnifolium should last for several years and take into account the potential for the reproduction of the weed through both seeds and rhizomes.

The selection of the appropriate growth stage of the weed, as well as the weather conditions before, during, and after spraying, are also important parameters to be taken into account when deciding on spraying. For example, S. elaeagnifolium is adequately controlled with herbicide applications when it is before or during flowering and cotton is at the 4–6 leaf stage [16]. However, if the application is made at the stage where 20% of the cotton bolls have opened, the weed is woody and has entered berry formation stage, leading to a poor control. The same authors concluded that although herbicide sprays can control the weed population, summer rainfall can trigger the germination of seeds and the formation of new shoots.

2.3.4. Mechanical Weeding

Mechanical weeding, meaning involving tillage, has been widely criticized for its efficacy against S. elaeagnifolium. Repeated tillage leads to the clonal reproduction of the weed as its rhizomes are cut and multiple new shorter fragments are produced which spread quite easily and have the potential to produce multiple new shoots [50,51]. For this reason, the application of no-tillage has been proposed to avoid the reproduction and dispersal of weeds [21]. The rhizomes are capable of resprouting even at a depth of more than 5 cm, as demonstrated by a pot experiment conducted in a greenhouse [52]. However, there are also reports of new shoots from rhizomes being buried even 50 cm in the soil [48,50]. Therefore, the extensive fragmentation of the roots should be avoided. In the study by Stanton et al., it was shown that rhizomes with a long length (>5 cm) have a higher shoot and root biomass than shorter ones [52]. After three years of experimentation to control S. elaeagnifolium in a cotton crop in the USA, it was observed that the weed density increased 14-fold after two applications of the soil treatment for three years [16]. The use of a ripper in dry soil in the summer has been suggested as a means of reducing shoots by up to 95% the following year [24]. Mowing is another technique that requires a considerable cost and man-hours for the control of weeds that is mainly used in urban environments (parks and roadsides) and orchards. However, mowing on S. elaeagnifolium has been reported to increase specific adaptation and defense traits against pests [53]. Specifically, the first generation of seeds and seedlings from populations that received mowing for at least three consecutive years were shown to bear a higher seed weight, a faster germination rate, and a greater specific root length than the seeds and seedlings from populations that were not mowed. The first trait indicates that heavier seeds will germinate earlier and better, the second trait that the germination rate is an indication of the weed’s invasion potential, and the third trait that the weed can more efficiently take up the soil’s nutrients.

2.3.5. Biological Control

Based on the previous strategies for the management of S. elaeagnifolium, it turns out that the effectiveness of the different methods varies, and several applications have been reported as ineffective or too expensive. For this reason, the introduction of biological agents to be released was investigated and carried out. Various natural enemies such as insects and nematodes have been found to feed on the foliage, flowers, or seeds of the weed. However, in the weed’s native zone in Mexico, there is no natural enemy that targets the rhizomes, maintaining effectiveness only against the aboveground vegetation [54]. A successful insect for the control of S. elaeagnifolium is Leptinotarsa texana Schaeffer of the family Chrysomelidae, which was introduced into South Africa from the USA in 1992 [55] through multiple releases in five regions and, according to Olckers et al., [56] is the first attempt worldwide to establish the insect against a plant of the family Solanaceae. South Africa was one of the first countries to use natural enemies against the weed in the mid-1970s [51], while Australia listed S. elaeagnifolium as a plant that can receive a biological control in 1985 [57] and is considered to be a good target for biological control based on a recent list that rated the impact and need for the control of various invasive plants in the country [58]. According to Sheppard et al. [59], S. elaeagnifolium is among the list of the top twenty weeds that can receive a biological control in Europe. Research conducted in South Africa on the suitability of natural enemies for the control of S. elaeagnifolium indicated that native insect species are not sufficient for control, hence there is a need to import enemies from other environments [60]. Hoffmann et al. studied the damage to the leaf surface of S. elaeagnifolium caused by various insect species and suggested that the insect L. texana could significantly reduce the germination potential of the weed despite not feeding on the seeds, suggesting that a long-term use is necessary to deplete the underground reserves of propagules for the regrowth [61]. Leptinotarsa texana feeds only on the leaf surface of the weed and not on its berries or root system, however, plants that defoliate rapidly produce fewer berries and seeds [62]. The release of L. texana provided a similar efficacy to the chemical methods in a field experiment on sunflower in South Africa, while maintaining lower costs to the grower [63], and reports from the same country indicate that the complete defoliation of the weed has been observed on occasion on several dozen hectares [62]. In Australia, no systematic attempts have been made to eradicate the insect due to the insect’s lack of adaptation to the southern zones of the country where cereals are grown, although a more recent study on the climatic adaptation of L. texana using the CLIMEX model suggests that the insect could adapt to the areas invaded by S. elaeagnifolium [64].

The introduction of the insect Frumenta nephelomicta Meyrick into South Africa did not fare as well as L. texana as it failed to establish, probably due to the dry conditions [59,65]. The same was the case with the insect Leptinotarsa defecta Stal, whose presence is rare and whose impact on the weed is imperceptible [56]. The insect Gratiana lutescens (Boheman) was introduced in 1973 in South Africa but was shown to feed on the plant parts of other plants of the Solanaceae family, such as eggplant (Solanum melongena L.), and was therefore discarded [56]. Some cage tests showed that both L. texana and L. defecta could cause damage to eggplant, but reports from the USA, specifically Texas, cited by Olckers and Zimmermann say that eggplant is not affected by L. texana despite large populations of the insect and the presence of S. elaeagnifolium [51]. Of course, Olckers and Hulley consider that L. texana and L. defecta could not be important pests for the eggplant as it is not extensively grown in this country, crop rotations limit the spread of the insects, and they do not seem to attack the crop in its natural germination zone, i.e., the Americas [66]. For this reason, a thorough survey should be conducted for plants (both cultivated and native) that are potential carriers of the insects. For example, Lefoe et al. tested the selectivity of L. texana in Australia by ranking the plants as potential targets based on whether (1) they are economically important, i.e., they are cultivated plants on a small or large scale, (2) they are native but their products are used for some use, (3) they are part of the culture or history of a place, (4) they have a biogeographic and ecological similarity to S. elaeagnifolium, (5) they are known hosts, and (6) they are already under conservation [55]. Within the Solanacae family, S. elaeagnifolium appears as the primary host of L. texana, while S. melongena, Solanum rostratum, Solanum carolinense, and Solanum dulcamara appear as secondary hosts [67].

The efficacy of some herbivorous insects targeting solanaceous plants is not always assured as the weed reproduces largely by asexual propagules [51]. For this reason, it is necessary to introduce natural seed-feeding weed enemies beyond the foliage [60]. Kwong et al. prioritize the criteria by which a natural enemy is commonly selected, describing that the use of biological agents is appropriate where the available means of the management of weeds are ineffective or carry high costs and the weed causes a negative impact on agricultural production and/or the environment and does not carry potential uses, while the natural enemy is selective to the weed and can acclimatize to the environment to be released [68].

The nematode Orrina phyllobia (Thorne 1934) Brzeski, 1981 or Nothanguina phyllobia (Thorner) has been recorded as a natural enemy of S. elaeagnifolium and its presence has been documented in the USA, Mexico, and India [69]. This nematode is an obligate parasite that feeds on the leaf surface, shoots, and flowers of the weed [70] and especially on young developing leaves [71], leading to a very high reduction in the foliar biomass [72]. Robinson et al. [73] concluded that the symptoms are more severe after wetting the foliage with water because the nematodes are mobilized, suggesting that the combination of irrigation with the release of nematode would be an ideal biological tool for the control of weeds. In the region of Guanajuato, Mexico, an S. elaeagnifolium infestation and damage to the leaf area by the nematode was confirmed by molecular techniques [74]. However, the release of natural enemies should be done with special care in the case where there are nearby cultivated species of the genus Solanum sp., such as tomato (Solanum lycopersicum L.), eggplant, and potato (Solanum tuberosum L.), belonging to the family Solanaceae. According to Field et al. [57] the nematode Ditylenchus phyllobius (Thorne) Filip’ev or O. phyllobia is not suitable for release in Australia as it has a reduced selectivity by attacking many species of the genus Solanum. An evaluation of the selectivity of O. phyllobia found that in addition to S. elaeagnifolium and S. melongena, the nematode’s hosts were also Solanum coccineum, Solanum burchellii, and Solanum panduriforme [75].

Control is also required in areas where the weed is native, such as in Texas, the USA [76]. To select the most suitable S. elaeagnifolium enemies that could be introduced and released in a country, it is necessary to fully understand what the similarities and differences in the climate and genotypes of the weed are between the country of introduction and the natural zone of the enemy. For example, an analysis of the suitability of 30 enemies to be released against the weed in Australia indicated that potential biological factors can be sought in the central regions of Chile and Argentina because the climate in these regions is similar to that of Australia, potentially favoring enemy activity [68]. Climatic factors (such as summer rainfall) are another factor limiting the use of biological agents (such as the nematode O. phyllobia and the insects Gargaphia spp., L. texana, L. defecta, Gratiana pallidula, Trichobaris texana, Frumenta nephalomicta, and Zonosemeta vittigera) in Australia [54]. Similarly, areas bordering the Mediterranean basin and areas of central and southern Africa show a high similarity to the Brownsville area in the USA, where it is located in the natural weed vegetation zone [69]. Notably, South Africa contains one of the five Mediterranean climate types, indicating that natural enemies could also be unleashed in countries around the Mediterranean [69]. The same authors have published the most detailed report to date on natural enemies that can be used for the biological control of S. elaeagnifolium. According to Hill et al. [60] in their study in South Africa, it was found that more oligophagous insects attack S. elaeagnifolium than polyphagous ones. Selectivity studies of insects known to be used on other plant species (mainly of the Solanaceae family), such as the coleopteran Metriona elatior [77] and the coleopteran Platyphora semiviridis [78], should be carried out in the future. A detailed list of the insects found on S. elaeagnifolium in the 1960s in the USA is described by Goeden [79].

3. A Holistic Framework for Silverleaf Nightshade Management

Solanum elaeagnifolium is correctly considered to be one of the most noxious weeds worldwide due to specific key biological and ecological traits that have been presented previously, hence the adoption of multiple strategies are needed for the management of its invasion [2]. A conceptual framework is presented in Figure 3, aiming at presenting the necessary actions needed to mitigate the impact of this species, and be the model for the development of frameworks for the sustainable management of IPS based on agroecological approaches.

At a first glance, the early detection of the plant’s propagules (both the seeds and root fragments) is crucial to prevent the introduction of the weed in new regions. For this purpose, the thorough inspection of cargo and trade commodities, including soil and seed lots, is the very first action that must be carried out at the transboundary level. The successful detection of S. elaeagnifolium seeds is reinforced by new inspection technologies that are of a low-cost and highly accurate. Following the proper identification of S. elaeagnifolium¸ molecular and genetic tests should be implemented to trace the origin of the introduced population and attempt synergies with other countries for the embracing of common management protocols. Distinguishing between seed-derived plants and rhizomes-derived plants is recommended for the first time after an extensive literature review. The early established seedlings coming from seeds are morphologically distinctive from the shoots coming from rhizomes and this is justified on the one hand by the increased density of the trichomes and curliness of the leaves in root-derived plants, and on the other hand by the late growth of seed-derived plants and, apparently, the restricted root system.

The invasion of S. elaeagnifolium should not be limited to site-specific treatments and eradication attempts, as the weed has been reported to be easily transferred in hundreds of kilometers and is capable of multiplying its populations within a few years [80,81]. Therefore, farmers should adopt and revive cultural practices that may mitigate the impact of the weed and give a competitive advantage to the crops. The literature indicates that the adjustment of row spacing, the use of allelopathic cover crops (such as alfalfa), and the reduced tillage are all effective tactics to potentially temper the weed dynamics. Indicatively, the increased shade of the crop canopy reduces the dynamics and the chlorophyll content of S. elaeagnifolium [82]. This trait would benefit crops presenting a slow early growth such as cotton and soybean, thus, narrow row spacing accelerate this beneficial effect of the shade. As described previously, the frequent cutting of alfalfa and the use of allelopathic crops may reduce the growth dynamics and the competitiveness ability of S. elaeagnifolium at a great extent [48,83]. The use of winter legumes could deliver in soil important nutrients and raise nitrogen at a level which would promote the growth of early sown spring crops, such as maize, especially if the early sowing is combined with narrow row spacing. An ideal threefold scenario of effective cultural practices could be completed with the adoption of reduced tillage in order to avoid the clonal propagation of the weed. However, reduced tillage systems are not universally adopted globally due to biases, different approaches, and a lack of equipment and knowledge. For this reason, an occasional soil tillage every 3–4 years with deep ploughing might be effective to achieve a seed burial below 10 cm and, at the same time, expose rhizomes to sunlight. The berries burial at great depths may reduce the germination rate of the seeds and the generation of new shoots from root fragments might be reduced, respectively.

Nevertheless, S. elaeagnifolium invasions are considered to be detrimental for agricultural production, soil and ecosystems preservation, native flora, and biodiversity. Therefore, the adoption of integrated weed management strategies and the early control of the weed populations remains important. This is even more necessary in the European Union, where the reduction in the input of herbicides and the identification of effective chemical alternatives are highly required within the coming years [84]. This review summarizes all the available strategies for the integrated management of silverleaf nightshade. The most important highlight refers to the time of the application. Herbicides at reduced rates, natural herbicides, and mowing should be applied before or during the flowering stage to reduce the seed production of S. elaeagnifolium and prevent the vegetative reproduction.

The management of an invasive plant species is not only a spatial challenge but also includes the prevention of the future dispersal, the monitoring of an ongoing invasion, and the long-term sustainable management of the invaded sites. Climate change and the increase in temperatures will favor the invasion of S. elaeagnifolium in northern latitudes toward the poles [85]. The prediction of future silverleaf nightshades should be accompanied by distribution models and the definition of the pathways for introduction. As a result, regulations and preventative measures will be forced into action. On the other hand, the mapping of infested sites is a valuable tool to track the transfer of the weed in new fields, especially in agricultural areas where a non-proper crop rotation might allow for the establishment and dominance of S. elaeagnifolium. The eradication of isolated patches is labor intensive, expensive, and sometimes ineffective. However, scattered spots could be managed efficiently if the plants are not allowed to format berries and produce seeds. As a consequence, the eradication attempts will focus on the root bank which can limit the dispersal of the weed. To sum up, the release of biological agents and the use of decision support systems are two important strategies to make possible the reduction in the herbicide input and reduce the distribution of the dynamics of S. elaeagnifolium [86,87].

An overview of the feasible and reliable management practices for S. elaeagnifolium is associated with the growth stages of the weed and is presented in

Table 1. Recommended methods for the management of Solanum elaeagnifolium in different habitats.

Habitat	Method	S. elaeagnifolium Growth Stage	Season	Targets
Field crops (maize, cotton, soybean, peanut, vegetables)	Narrow row spacing Cover crops Competitive cultivars/hybrids Crop rotation Site-specific herbicide applications	Dormancy Seedling	Early in spring	Reduce weed pressure Diminish the soil seedbank Increase canopy coverage and shade Facilitate harvest Reduce yield losses
Perennial crops (olive groves, citrus orchards, vineyards)	Mowing (Allelopathic) cover crops as living mulch or residues Broadcast herbicide applications	Before flowering or during flowering	Late spring and early to mid-summer	Prevent berry formation and seed production Deplete root reserves Facilitate agricultural practices
Roadsides (highways and road network)	Mowing Broadcast herbicide applications Release of biological agents Broadcast sowing of desired plants	Before flowering or during flowering for mowing Seedling to flowering for defoliators biological agents	Early spring to late summer	Prevent berry formation and seed production Deplete root reserves Limit the reservoir for further dispersal
Grasslands	Selective grazing Release of biological agents	Seedling to flowering	Early spring to mid-summer	Prevent berry formation and seed production Deplete root reserves Give advantage to native flora
Urban areas (parks, flower beds, roadsides)	Hand weeding Site-specific natural herbicide applications	Seedling to berry	Early spring to autumn	Eradicate isolated patches
Abandoned places	Broadcast herbicide applications Selective grazing Release of biological agents	Seedling to berry	Early spring to autumn	Reduce soil seedbank Give advantage to native flora

. The literature reveals that glyphosate, picloram, triclopyr, aminopyralid, fluroxypyr, florpyrauxifen, 2,4-D, MCPA, glufosinate, tembotrione, and pyraflufen-ethyl are effective herbicides for the control of the weed. Leptinotarsa texana and O. phyllobia are two biological agents which could be released in invaded areas. A mechanical control should focus only on the cut of the stems and not on the root system to prevent a root fragmentation. Alfalfa and some allelopathic cover crops could be sown in winter or early in spring to reduce the pressure of S. elaeagnifolium.

4. Conclusions

Solanum elaeagnifolium could be characterized as the modern ‘Lernaean Hydra’, referring to the mythological monster that generated two heads after the cutting of a head. The frequent stem cuttings stimulate the regrowth of silverleaf nightshade and the single tactics for its management are ineffective, costly, and sustainable incompatible. The early detection of seeds and rhizomes is crucial to prepare the ground for the adoption of sustainable agricultural practices, such as the utilization of cover crops and the reduced tillage, and to adopt novel techniques for the long-term management of the weed. The application of reduced herbicide rates, mowing, and natural herbicides are all integral components of an effective integrated management framework, aimed at providing realistic and optimized solutions when these are applied in combination with new technologies, such as decision support systems and remote sensing. The circle is brought to completion with the systematic monitoring of invaded sites for the presence of silverleaf nightshade, the public and scientific education on its invasiveness dynamics, the cutting-edge development of new technologies, and the release of beneficial biological agents to prevent the growth of new ‘heads’ and to eventually ‘kill the beast’.