With the rise of integrated pest management (IPM), practical applications of biological control agents releases have become increasingly complex to improve pest control with reduced used of chemical pesticides (Kogan 1998; Stiling & Cornelissen 2005; Desneux et al. 2007; Naranjo et al. 2015; Huang et al. 2020; Zang et al. 2021). Starting from simple pairs with one natural enemy species targeting one pest species, applications have been progressively improved in releasing combinations of multiple species of biocontrol agents to achieve sustainable control of multiple pest populations simultaneously and throughout the cropping season (Barbosa 1998; Heimpel & Mills 2008). Such efficacy is achieved notably through the precise monitoring of pest population dynamics in situ (Tan et al. 2016). Multi-species releases should also involve natural enemy species with limited niche competition (Liu et al. 2012; Chailleux et al. 2014b; Liang et al. 2021; Sanchez-Hernandez et al. 2021), but with complementary ecologies allowing the regulation of pest populations over different time periods and spatial scales (Hall 2011; Chailleux et al. 2017). Most often, a specialist natural enemy (e.g., a parasitoid wasp) is combined with a generalist natural enemy in multi-species releases (Tan et al. 2016; Perez-Valencia et al. 2019): this way the specialist, targeting the dominant pest species, prevents its outbreaks, while the generalist regulates pest populations of secondary pest species (Chailleux et al. 2013; 2017; Dainese et al. 2017; Aparicio et al. 2020).
Yet such systems are intrinsically complex to develop since many factors may influence species interactions and the efficacy of pest control, including biocontrol agent fitness, their relative proportion, introducing times and developmental stages (Huffaker et al. 1971). The successful colonization of crop systems, and the establishment of stable populations by released biocontrol agents is even more challenging and may heavily rely on means to support populations (Bianchi et al. 2006). This is especially true since biocontrol agents are most often released before pest populations reach high densities to prevent pest outbreak (Albajes et al. 2000). Therefore the development of strategies supporting biocontrol agent populations could be useful in extending the adoption of multi-species releases.
The use of banker plants has been increasingly investigated and developed in the context of conservation biological control (Frank 2010; Gurr et al. 2017). Banker plants are non-crop plants supporting populations of herbivorous species which do not attack adjacent crops (Parolin et al. 2012), and which may be used as alternative prey or hosts by natural enemies targeting the main pest species in cropping systems. Hence, banker plants can be used in combination with crops and serve as entry points for the inoculative release of biocontrol agents. By providing shelter and alternative prey / hosts, banker plants can enable the early colonization of adjacent crops by natural enemies (Li et al., 2013) and the establishment of their populations when main prey are scarce (Yano et al. 2018). Plant species supporting populations of alternative prey / hosts in the same family or functional group than the main pest species are well suited to be used as banker plants (Laurenz & Meyhofer 2021). For instance, the non-crop oat species Avena sativa supporting populations of the alternative aphid species Metopolophium dirhodum resulted in an increased suppression of the main pest Myzus persicae by its parasitoid Aphidoletes aphidimyza in chilly crop (Capsium annuum; Hansen 1983). Similarly, the non-crop papaya plant Carica papaya supporting populations of the alternative whitefly species Trialeurodes variabilis successfully increased the suppression of the main pest Bemisia tabaci by the ladybird Delphastus pusillus in many vegetable crops (Osborne et al. 1991). These non-crop plants and alternative prey could also supply sufficient food resources and space to help biocontrol agents maintain their populations after the suppression of the main pest species and thereby avoid their escape from the target agroecosystem, which is common in practical biological control application and may cause severe loss (Huang et al. 2011). Such effect could in turn increase the suppression of secondary outbreaks of pest populations (Zheng et al. 2017).
Unlike other functional plants providing alternative food (floral) resources or attracting natural enemies (Gurr et al. 2017; Zhao et al. 2017; Perović et al. 2018; Jaworski et al. 2019), one key aspect in assessing the suitability of a plant species as a banker plant is the high fitness of the alternative herbivorous prey / host developing on the banker plant, versus a low fitness on crop plants (Huang et al. 2011; Damien et al. 2020; Wang et al. 2020). Theoretically, the alternative prey / host on banker plants and the target prey / host on crops form an apparent competition system by sharing a natural enemy (van Veen et al. 2006; Chailleux et al. 2014b; Jaworski et al. 2015; Desneux et al. 2019; Monticelli et al. 2021). Hence, the density of banker plants and alternative host / prey could severely impact the balance between the target agroecosystem and the banker plant system (Orrock et al. 2010). Most studies investigating the suitability of species as banker plants focused on a single plant species supporting a single alternative herbivorous prey species (Andorno & Lopez, 2014). Conversely in practical applications relying on multi-species releases of biocontrol agents, many functional non-crop plants have been studied for their potential to provide alternative food resources and shelter to these multiple natural enemies, but they have seldom been evaluated as constituents of a banker plant system (Avery et al. 2014; Jandricic et al. 2014). The use of a single functional plant species providing alternative food resources is likely to support populations of natural enemy species with similar ecological niches (Xu et al. 2020). Still, some functional plants may jointly provide alternative food resources such as nectar and pollen resources (Wäckers & van Rijn 2012) and support alternative host / prey populations, thereby potentially targeting natural enemy species with very different ecologies. Alternatively, combining various banker plant species to enhance populations of multiple natural enemy species could help achieve long-term sustainable pest control in multi-pest cropping systems.
Tomato is a major vegetable greenhouse crop in China (Li et al. 2021), attacked by several major insect pest species including the whitefly Bemisia tabaci Gennadius, 1889 (Hemiptera: Aleyrodidae) and the aphid Myzus persicae Sulzer, 1777 (Hemiptera: Aphididae), often present simultaneously (Lange & Bronson 1981 ; Czosnek & Ghanim 2011; Li 2013; Hullé et al. 2020). Encarsia formosa Gahan, 1924 (Hymenoptera: Aphelinidae) is a parasitoid wasp specialized on whiteflies and commonly used as a biocontrol agent to suppress B. tabaci whitefly populations (Enkegaard 2011; Tao et al. 2018). In particular, E. formosa can prey and develop on Trialeurodes ricini Misra, 1924 (Hemiptera: Aleyrodidae), a whitefly mainly using the castor been host plant Ricinus communis Linnaeus, 1753 (Wang et al. 2016): it prefers R. communis over other host plants (Huang et al. 2014) and cannot survive on tomato (Shishehbor & Brennan 1996). Propylea japonica Thunberg, 1780 (Coleoptera: Coccinellidae) is a predatory ladybird attacking a variety of prey species and often used in biocontrol programmes especially to control aphids (Vuong et al. 2001; Kuroda & Miura 2003; Yang et al. 2014). In particular, P. japonica preys and develops on the aphid Megoura japonica Matsumura (Hemiptera: Aphididae) (Li et al. 2011). This aphid species develops well on soybean Glycines max Merr, 1917 or Vicia faba Linnaeus, 1753 (Wang et al. 2013) but has a reduced fitness on tomato crops (Liang Y, unpublished data). Besides, both R. communis – T. ricini and G. max – M. japonica have been used as banker plant systems in commercial greenhouses, most often introduced as infested potted plants between cropped plants (Liang Y, unpublished data). Predatory ladybirds often engage in intraguild predation (Michaud 2010; Ovchinnikov et al. 2019; Liang et al. 2021) and may especially prey on parasitoid wasps developing inside their host (Chacón & Heimpel 2010; Tan et al. 2016; Aparicio et al. 2020). Therefore, the use of distinct banker plant systems supporting E. formosa and P. japonica could reduce the risk for intraguild predation and help enhance the control of the B. tabaci – M. persicae pest complex in greenhouse tomato crops.
In the present study, we tested the role of combined banker plant applications in enhancing pest control in a multi-pest, multi-biocontrol agent system in a laboratory and a greenhouse experiments. Using tomato crops, we measured the abundance of the pest species B. tabaci as main tomato pest and M. persicae as secondary pest, and of the introduced biocontrol agents E. formosa and P. japonica. We evaluated the potential of the two banker plant systems in combination: (i) R. communis supporting populations of the whitefly T. ricini, itself parasitized by by E. formosa and (ii) G. max supporting populations of the aphid M. japonica, itself preyed upon by P. japonica (Table 1). We asked: How efficient is the long-term control of the two pest populations by the two natural enemies (1) In absence of banker plants ? (2) When one banker plant system is provided ? And (3) When two banker plant systems in combination are provided ?