Introduction

Agriculture globally is facing many challenges including climate change, biodiversity loss and rising demands for food production (Deutsch et al. 2018; Rockstrom et al. 2009; Tilman et al. 2011). In response to these challenges, a growing volume of research is contributing towards a redesign of agricultural systems that provide nutritious food for all healthy and resilient ecosystems (Bommarco et al. 2013; Pretty et al. 2018; Struik and Kuyper 2017; Tilman et al. 2011). Evidence is growing that a sustainable intensification of agriculture can be achieved by combining scientific and farmer knowledge to develop ecologically and agronomically compatible practices (Pretty et al. 2018). Integrated pest management (IPM) is an example of redesigning intensive agricultural systems. Instead of relying principally on synthetic pesticides, IPM uses non-chemical or botanical insecticide measures to suppress pest population increase and a range of curative management tactics with synthetic pesticide use as last resort (Barzman et al. 2015). The declining availability of many pesticides due to resistance and deregistration, reflecting increasing awareness of their environmental and human health consequences, has driven changes towards ecologically based practices (Barzman et al. 2015; Borel 2017; Chagnon et al. 2015; Li et al. 2017; Sumon et al. 2018).

A central part of IPM is biological control in which natural enemies including parasitoids, predators and pathogens are introduced and/or promoted (Bale et al. 2008; Gurr et al. 2000a, 2018). Conservation biological control focuses on natural enemies already present in an agroecosystem and aims to maximize their impact on target pests by, for example, reducing the adverse effects of insecticide use (Begg et al. 2017; Ehler 1998). Habitat manipulation works in conjunction with conservation biological control and is used to provide conditions that promote natural enemies and suppress pest populations (Fiedler et al. 2008; Gurr et al. 2000b, 2017). This can include field level interventions such as establishing plants to provide floral resources, refuges and alternate hosts for natural enemies (Griffiths et al. 2008; Gurr et al. 2017). Plants that are selected for habitat manipulation have usually been studied for morphological and physiological floral characteristics that provide optimum benefits to natural enemies (Baggen et al. 1999; Balzan et al. 2014). Habitat manipulation tactics can extend beyond the field to include landscape features including riparian areas and treelines, although the effect of landscape features on crop pests is variable (Karp et al. 2018; Tscharntke et al. 2007).

Ecologically based pest management tactics such as conservation biological control have been shown to reduce the use of synthetic insecticides in a variety of cropping systems whilst maintaining or increasing crop yields and efforts are being made to up scale the practice globally (Pretty et al. 2018; Wyckhuys et al. 2013; Xu et al. 2017). Despite these advantages, however, uptake of conservation biological control on a wide scale is limited (Gurr et al. 2016). In cases where uptake has been strong, the vegetation used in habitat manipulation provides multiple ecosystem services rather than suppressing pests alone (Khan et al. 2006, 2012). To date, however, there is a major gap in knowledge about the possibility of habitat manipulation plants providing botanical insecticides. This is important because synthetic insecticides present significant risks to human health. Agricultural workers and consumers are at risk of being negatively affected by insecticide products, tank mixes, drift, residues and breakdown products, especially as a consequence of poor registration, storage and misuse (Eddleston et al. 2002). In agricultural areas where there are high illiteracy rates, and poor training and equipment, the impacts are especially high (Amoabeng et al. 2017; Williamson et al. 2008).

Many plants possess secondary metabolites such as alkaloids, phenols and terpenoids that can have insecticidal activity such as toxicity, repellency, feeding deterrence against insect pests (Koul 2004). Botanical insecticides, including extracts and essential oils of these plant species, have been used to protect crops against insect herbivory for many years (Belmain et al. 2012; Isman 2000, 2008). Synthetic insecticides often have lethal and sub-lethal effects on natural enemies (Desneux et al. 2007). Biopesticides are considered relatively benign to non-target species owing to their rapid breakdown, selectivity nature and reduced risk of insecticide resistance as plant extract, particularly crude extracts have multiple modes of action other than toxicity, such as repellency (Amoabeng et al. 2013; Dubey et al. 2011; Isman 2006; Koul et al. 2008; Tembo et al. 2018). Another important benefit of botanicals is that they tend to depend on “suites” of closely related active constituents rather than a single active ingredient; this diversity may delay or mitigate the development of resistance in pest populations to most botanicals (Koul 2004). Biopesticides have been used for centuries as means of managing pests until synthetic insecticides replaced plant extracts (Isman 1997). The interest in botanical insecticides is increasing but still accounts for less than 1% of crop protectants used globally (Isman 2008, 2017). In developing countries, plant extracts are often prepared from common weed species that grow around the field and obtained freely, with labour as the only cost, resulting in cheaper pest management option when compared with synthetic insecticides (Amoabeng et al. 2014; Isman 2017).

The field of botanical pesticides is highly active [see reviews by Boulogne et al. (2012), Isman and Grieneisen (2014), Isman (2017), Yang and Tang (1988)] but this review considers two novel aspects. First, we assess the extent to which the plant species used in conservation biological control studies have been the subject of research to determine if they have potentially useful biopesticidal properties. Second, we consider the practicalities of using plants that have dual use in promoting biological control and as sources of botanical pesticides (Fig. 1).

Fig. 1
figure 1

A secondary plant species (such as buckwheat in this example) can potentially provide dual benefits for pest management, promoting biological control and providing insecticidal compounds to treat the crop

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Conservation biological control plant species

The identification of plant species studied for habitat manipulation purposes began with the published review by Fiedler et al. (2008) and was followed by a search on the online ISI Web of Science database to from 1989 to 2018 using search terms: flower* AND “conservation biological control”, flower* AND “natural enemy”,and “habitat management” AND “conservation biological control”. Between 1989 and 2006, 165 plant species belonging to 35 plant families were used in habitat manipulation studies. The criteria that were applied to the Fiedler et al. (2008) plant species included their effectiveness in previous habitat manipulation studies, frequency of natural enemy visitation, long flowering duration, availability of seeds, ease of establishment, agronomic suitability and the value of the plant as cover or alternative crop (Fiedler et al. 2008). The same search criteria were applied to conduct a follow-up database search (Table 1). Each plant species is listed once irrespective of the number of studies in which it was used. Where a plant was involved in more than one study, only one example reference is given.

Table 1 “Gap identification” of plants researched for conservation biological control and that have yet to be the subject of work to identify scope as sources of botanical insecticides (denoted by ‘o’) and plants that constitute “proof of concept” in having insecticidal properties as well as utility in conservation biological control (denoted by ‘+’; or more tentatively by a ‘x’ denoting a plant in the same genus showed insecticidal activity)
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Habitat manipulation studies from 1989 to 2006 involved 165 plant species belonging to 35 families and 188 new species from 29 families were the subject of work published between 2007 and 2018. The number of publications per year between 2007 and 2018 ranges from three (2009 and 2010) to ten in the first half of 2018 (Fig. 2). Conservation biological control studies are dominated by research from developed countries in North America and Europe as well as Australia, New Zealand and Japan (Wyckhuys et al. 2013). Tropical regions have more flowering species than temperate areas so there remains great potential of identifying additional plant species for use in habitat manipulation (Christenhusz and Byng 2016).

Fig. 2
figure 2

Temporal trend in published papers on habitat manipulation between 2007 and July 2018. Previously published papers on habitat manipulation (1989 to July 2006 were the subject of Fiedler et al. (2008))

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Plant families used in habitat manipulation with insecticidal activity

A search in Google, Google Scholar and Scopus using both the scientific and common names of each of the 283 plant species named in papers on conservation for the terms ‘’botanical insecticide”, “plant extracts”, biopesticides, “insecticidal activity” OR “pesticidal activity’’ revealed 15 (33.3%) (Apiaceae, Apocynaceae, Asteraceae, Boraginaceae, Brassicaceae, Campanulaceae, Fabaceae, Lamiaceae, Myrtaceae, Papaveraceae, Polygonaceae, Primulaceae, Proteaceae, Rosaceae, Rubiaceae and Scrophulariaceae) out of 44 plant families that have been involved in habitat manipulation studies, had at least one plant genus or species with insecticidal activity. Proteaceae had one plant used in habitat manipulation in the same genus as another plant used as a biopesticide. All other plant families had at least one plant species tried for its insecticidal activity and tested in habitat manipulation studies.

Three families, Apiaceae, Asteraceae and Lamiaceae, had more than ten species with insecticidal activity and accounted for more than 70% of plant species studied. These families also had the highest number of species used in habitat manipulation studies. Of the 18 plant species in Apiaceae involved in habitat manipulation studies, 13 (72.2%) have been tested and showed insecticidal activity. In the Asteraceae, 19 (25.7%) out of the 74 plant species involved in habitat manipulation studies have been tested for their insecticidal activity. In addition, five more plants species in the same genus as some of the species for habitat manipulation studies have been used for their insecticidal activity. Lamiaceae had 11 (39.3%) out of the 28 plants involved in habitat manipulation studies having insecticidal activity. Two families, Brassicaceae and Fabaceae, had several species involved in habitat manipulation studies but not many species in the families have been known to have insecticidal properties. Among the 14 species in the Brassicaceae family, five were identified to have activity against insects whilst two out of the 23 species in Fabaceae were identified to have activity against insects. Fagopyrum esculentum is one of the most studied species in habitat manipulation programs (Fiedler et al. 2008; Lavandero et al. 2006; Vattala et al. 2006) and was the only species with insecticidal activity among 12 species in Polygonaceae. At 2,500 ppm, a methanol extract of the grains of buckwheat was potent against the green peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphidiade) (Lee and Rasmussen 2000).

Boulogne et al. (2012) reviewed plant families and species with insecticidal activity and found that 656 plant species belonging to 110 families are known to have insecticidal activity in which Lamiaceae alone had 181 (28%) followed by Fabaceae, Asteraceae and Apiaceae. In all, 30 (66.8%) out of the 44 plant families in this review do not have insecticidal activity. It is, however, possible that plant species in these families have not yet been studied enough for their activity against insects.

The Apiaceae

The Apiaceae (umbellifers) is the 16th largest angiosperm family with 442 genera and 3575 species in which most of the aromatic flowering plants are found (Christenhusz and Byng 2016). It has a global distribution and many species with both habitat manipulation and insecticidal activity traits (Christenhusz and Byng 2016). Apiaceae species are annual, biennial or perennial herbs and woody shrubs and small trees that produce colorful inflorescences that secrete nectar attracting pollinators including bees, moths and beetles (Heywood et al. 2007). Their growth habit makes them agronomically suitable as habitat manipulation species (Fiedler et al. 2008). The flat headed morphology of their inflorescence provides easy landing and access to nectaries for natural enemies encouraging visitation (Heywood et al. 2007).

Plants in the Apiaceae produce secondary metabolites including coumarins, monoterpenes and sesquiterpenes (Lee and Rasmussen 2000). Essential oils have been tested as being acaricidal (Attia et al. 2011), bactericidal (Glisic et al. 2007; Matasyoh et al. 2009) and for medicinal purposes (Lee and Rasmussen 2000; Maulidiani et al. 2014). Essential oils from Apiaceae species have been used against stored product pests including the bean weevil Acanthoscelides obtectus Say (Coleoptera: Bruchidae) (Regnault-Roger et al. 1993), the cigarette beetle Lasioderma serricorne (F.) (Coleoptera: Anobiidae) and wheat flour beetle Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) (Kim et al. 2003). Insecticidal activity against turnip aphids, Lipaphis pseudobrassicae (Davis) (Hemiptera: Aphididae), pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) and the green peach aphid, M. persicae has been reported (Dancewicz et al. 2012; Sampson et al. 2005).

The Asteraceae (Compositae) family

The Asteraceae (daisy) is the second largest plant family after Orchidaceae (Stevens and Davis 2001) with 24,700 species in 1623 genera and a worldwide distribution (Christenhusz and Byng 2016). Asteraceae species have clusters of inflorescence that appears to be a single flower often referred to as head (Schmid 2004). The entire flower head moves towards the direction of the sun and that maximizing reflectivity which may enhance the attraction of pollinators and other beneficial insects (Schmid 2004), which along with their growth habit makes them largely acceptable for habitat manipulation (Altieri et al. 2005). A larger number of plants in the family are herbaceous, with shrubs and trees rare (Okunade 2002). Species in the Asteraceae have been exploited for their insecticidal activity against crop and storage pests (Gbolade et al. 2011) and also against several pathogenic organisms with success (Del-Vechio-Vieira et al. 2009; Senatore et al. 2004). The chemical composition of some species including Ageratum conyzoides L. (Asteraceae) has been well described (Chu et al. 2010; de Souza et al. 2009; Nenaah et al. 2015; Okunade 2002). The insecticidal activity of an aqueous extract of A. conyzoides has shown success rates comparable to chemical insecticides against diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae) (Amoabeng et al. 2013; Bhathal et al. 1994).

The Lamiaceae

The Lamiaceae (mints and deadnettles) is characterised by many aromatic species (Heywood et al. 2007).The family is composed of 7530 species in 241 genera and globally distributed (Christenhusz and Byng 2016).The Lamiaceae includes trees, shrubs, subshrubs and herbs that are annuals or perennials (Harley et al. 2004). The Lamiaceae has a large variety of species composed of plants that may bloom early in the season (annuals) and those that would bloom late but will continue in bloom for longer periods (perennials).

Lamiaceae have been used for the provision of ecosystem services such as herbs and spices that provide antioxidants, flavours and food preservatives (Demo et al. 1998; Hossain et al. 2008; Vallverdu-Queralt et al. 2014). Secondary metabolites from the Lamiaceae have activity against human pathogenic organisms (Baydar et al. 2004; Karanika et al. 2001) and have been used for their insecticidal activity against domestic, storage and field crop pests. Extracts of Origanum vulgare L. demonstrated efficacy against P. xylostella and Trichoplusia ni Hübner (Lepidoptera: Noctuidae) in a laboratory bioassay (Akhtar and Isman 2004). Ocimum gratissimum L. oil and its constituents have fumigant and repellent activity against a number of storage pests (Kim et al. 2003; Ogendo et al. 2008) as well as malaria vectors Aedes aegypti L. (Diptera: Culicidae) and Culex quinquefasciatus Say (Diptera) (Diptera: Culicidae) (Kamaraj et al. 2008).

Outlook and conclusions

The current review has shown that the most popular habitat manipulation plant families are among the top plant families that have also been exploited for their insecticidal activity. Accordingly, many of the species that have shown benefit in habitat manipulation have unrecognized additional value; they could be exploited for the secondary use of harvesting plant parts to produce botanical insecticides. Habitat manipulation and plant extracts make a potentially effective combination due to the largely benign nature of both tactics on natural enemies. It is widely acknowledged that tactics that can provide multiple ecosystem services may prove effective and most likely to be adopted than are tactics that provide single benefits in isolation (Gentz et al. 2010). The tractability of combining two tactics depends on the effect of each individual tactic on natural enemy populations. For example, an inherent toxicity to natural enemies by a biopesticide would be antagonistic towards conservation biological control. However, a combination in which both botanicals and habitat management do not have negative effects on natural enemies will likely result in additive or synergistic effect. A current study using six non-crop plants including A. conyzoides and Tridax procumbens (Asteraceae) with the same plant for habitat manipulation and plant extracts was successful and cost-effective in managing pests of cabbage (Amoabeng et al. unpublished data).

Much is currently not known about why some plant families have many species useful for both habitat manipulation (pollen and nectar producing) and botanical insecticides. However, there could possibly be link between plants with insecticidal activity being attractive to predators and parasitoids. Secondary metabolites occur in the pollen and nectar and, at optimum concentration, benefit pollinators, parasitoids and predators for example in mediating plant–pollinator interaction, protecting nectar from robbery and other microbial functions such as preserving nutrients in nectar from degradation and reducing diseases in pollen and nectar beneficiaries (Stevenson et al. 2017). It is possible that some plant species in the families producing nectar and with insecticidal activity have common ecological characteristics. According to Campbell (2015), plant defence against herbivores and reproduction do not evolve separately but may have reciprocal and interactive effects on each other. Our hope is that this review will constitute the first step in uniting the separate fields of botanical insecticides and nectar plants for biocontrol enhancement. Future experimental and meta-analysis papers will be required to identify mechanistic patterns that underpin dual utility.”

Realising dual or multiple ecosystem services from habitat manipulation is an ambitious call to rapidly restore some lost ecosystem services, but there are other precedents that suggest it is possible, e.g., Davis et al. (2012). Finney et al. (2017) studied the delivery of eight ecosystem services including pests suppression, nitrogen supply, weed suppression among others from ten cover crops. The study showed that where all the plant species supplied biomass, suppressed weeds and retained nitrogen, there were trade-offs between other ecosystem services among some species. This underscores the need to develop clear understanding of the intended services to be delivered and selection of plant species (Gurr et al. 2017). Ultimately, however, the present review suggests that further research is justified to fully explore scope for using habitat manipulation plants as a source of botanical insecticides. Among the research priorities is field work to assess the phenological and practical issues around duals use. For example, habitat manipulation plants normally need to be established early in the crop calender so they are blooming early in the season, providing resources to natural enemies and thereby prevent pest population build-up. This may be compatible with dual use because harvesting plant parts such as foliage or seed pods for botanical insecticide production could be later in the season on a “needs basis” to deal with uncontrolled pest build-up, should biological control falter. On a wider time scale, habitat manipulation plants could be harvested at the end of the growing season and stored for later processing into botanical insecticides for use in a subsequent crop. In addition, ‘non-crop’ species may be cultivated on any spare land and harvested for the preparation of botanical insecticides. This would avoid potential disruption of the conservation biological control aspect of the program and might further generate income to individuals who would cultivate plants for the extraction of botanical insecticides. Such low-tech approaches are particularly appropriate for developing country agriculture.