Pest Management: Intercropping

Introduction

Until the past few hundred years, agricultural systems were based on large numbers of different crops, crop varieties, and landraces that were heterogeneous in their genetic make-up [1]. In addition, farming systems included both animals and plants further increasing diversity. As a result of increasing specialization, mechanization, and modern plant breeding, diversity on the farming system level and crop level has been drastically reduced worldwide at an ever-accelerating speed especially over the past 100 years. Fewer and fewer varieties that are genetically homogeneous are being grown in ever-larger fields [2]. The large-scale monoculture agricultural practices relying on pesticide and mineral fertilizer inputs have also led to a general decline in soil organic carbon and with this in soil microbial diversity and activity [3,4] with consequent effects on soil fertility and health [5].

Monoculture is usually understood to be the continuous use of a single crop species over a large area. However, with respect to plant pathogens and pests, it is important to differentiate between monoculture at the level of species, variety, or resistance genes (see Table 1) [1,6]. For example, within a species, there may be many different genotypes with different resistances to a specific pest or pathogen and great variation with respect to competitiveness with weeds and other crops. Depending on the breeding system, within a variety, diversity for resistance or morphological traits can be non-existent or high. Especially clonally reproduced or strictly inbreeding species may contain no diversity within a given

TABLE 1 Possibilities for Intercropping at Three Levels of Uniformity on Which Monocultures Are Commonly Practiced [1]

variety. Resistance gene monocultures can arise if different varieties all possess the same resistance (or susceptibility) gene(s). For example, in the late 1960s, virtually all hybrid maize cultivars in the southeastern United States possessed the cytoplasmically inherited Texas male sterility (Tms). Unfortunately, Tms is closely linked to susceptibility to certain strains of the pathogen Cochliobolus carbonum (syn. Helminthosporium maydis). The monoculture for susceptibility (while different varieties had been planted) led to selection for these strains and in 1970 the pathogen caused more than $1 billion (= 10⁹) losses [7]. Currently, Europe is experiencing the decline of the European ash (Fraxinus excelsior) due to the invasion of a novel pathogen (Hymenoscyphus fraxineus) for which there is almost no resistance present, that is, a monoculture of susceptibility [8].

Intercropping [9] can be practiced at the species, variety, and gene level (Table 1) with effects on pathogens [1,6,10], insect pests [11,12], and weeds [13-15] (Table 2). One of the most important considerations for the successful design of intercropping systems for pest control is the achievement of functional diversity, that is, diversity that limits pathogen and pest expansion and that is designed to make use of knowledge about host-pest/pathogen interactions to direct host and pathogen evolution [1,10]. Moreover, functional diversity is also a matter of complementary use of resource niches, for example, deep versus shallow rooting, legume versus non-legume crops. A famous example, not only in terms of functional diversity but also of human diet, is the successful intercropping of the “Three sisters”, namely maize, bean, and winter squash, in Central and North America since 3500 B.C. [16].

Protection Mechanisms Acting in Intercropped Systems

Pathogens, insect pests, and weeds differ fundamentally in their biology and their effects on crops, and different protection mechanisms act with respect to these organisms (Table 2).

Pathogens are mostly dispersed through wind, water splash, soil, and animals (vectors). In intercropped systems, the most important mechanisms for disease control are mechanical distance and barrier effects and changes in microclimatic conditions due to differences in plant architecture. In addition, resistance reactions induced by avirulent pathogen strains may prevent or delay infection by virulent strains. A large percentage of the reduction of airborne diseases such as the powdery mildews and rusts in cereal cultivar mixtures has been shown to be due to induced resistance [17,18]. The protection mechanisms are universal with respect to airborne, splashborne, and some soilborne, diseases and they may be enhanced by pathogen diversity that, in turn, is enhanced by plant diversity [19]. Mixtures of plants varying in reaction to a range of diseases will lead to a multitude of additional interactions and the overall response in such populations will tend to correlate with the disease levels of the components that are most resistant to these diseases. In addition, less affected plants may compensate for yield losses due to reduced competition from diseased neighbors [1].

In contrast to pathogens for which passive or vectored dispersal is the norm, insects often search actively for their hosts. Thus, behavioral, visual, and olfactory cues play an important role. While environmental factors and landing on a non-host is likely the most important mortality factor for pathogens, natural enemies are at least as important for insect population dynamics [11,12]. Host dilution may affect an insect’s ability to see and/or smell its hosts. Predators and parasitoids are dependent on the constant presence of prey and alternative food sources, such as pollen and nectar, in the absence of the hosts and for effective control of insect pests, the presence of sufficient numbers of natural enemies is critical. The importance of natural enemies was often only recognized after insecticide applications induced pest resurgence due to the destruction of natural enemy populations. Intercrops and weeds therefore can play an important role in regulating insect pests. Plant-insect communication also plays a role. For example, plants may signal their neighbors about insect attacks leading to the production of antinutritive compounds or attractants for natural enemies [20,21].

Weeds usually are early successional plants adapted to colonize open, nutrient-rich spaces. Intercrops, especially cover and mulch crops, directly compete with weeds for these spaces and also for light. As many weeds are adapted to certain crops and cropping patterns, changing these patterns (e.g., rotations)

TABLE 2 Mechanisms Affecting Pathogens, Insect Pests, and Weeds in Intercropped Systems and Selected Additional Interactions of Importance [1,13,19,29]

and management operations (e.g., sowing time) connected with different kinds of crops within the same field impede the adaptation and dominance of (problem) weeds. Also, filling the spaces that usually would be taken up by weeds with useful or more neutral plants will reduce weed habitat and help out- competing them [13,14,22]. An important consideration is that plants may be weeds only during certain phases of crop development. At other stages, the presence of the same “weeds” may be beneficial because they may provide food and habitat for beneficial insects and erosion control.

Besides the many positive effects of intercrops, it is important to keep in mind that weeds may serve as alternative hosts for insect pests and pathogens and that insects often are disease vectors, especially for viruses that may reside symptomless in certain weeds [1].

In order to understand the many interactions in intercropped systems, it is indispensable not only to consider plants, insects, and pathogens in the system but also the whole microbiome that interacts with them [23]. Plants not only take up nutrients from the soil, but they also actively release organic carbon-based chemicals such as organic acids and sugars into the soil. Roughly speaking about 30%-50% of the carbon that plants assimilate through photosynthesis is released into the soil [24]. These compounds provide the energy (carbon) and organic acids necessary for the microorganisms in order to function as well as for supporting the weathering of soil minerals making them available as plant nutrients. In addition, most plants live in symbiosis with root infecting mycorrhizal fungi that usually are very specific and genetically diverse [25]. The diversity of root exudates and in turn the diversity of the soil microbiome is greatly enhanced by plant diversity including intraspecific diversity (e.g., [26]), and by this, many of the interactive processes between crops, weeds, insects, and pathogens are influenced. For example, high microbial diversity and activity in the soil usually supports resistance induction and direct disease suppression [19,27]. Also, suppression of the production of certain secondary metabolites by plants can be triggered by certain rhizosphere bacteria. In turn, this may reduce their attractiveness to certain insects. In the case of cucumbers, this is helpful in suppressing the spotted and striped cucumber beetles (Diabrotica undecimpunctata and Acalymma vittata, respectively) that act as vectors (transmitting agents) of bacterial wilt of cucumber due to Erwinia tracheiphila [28].