Companion crops alter olfactory responses of the fall armyworm (Spodoptera frugiperda), and its larval endoparasitoid (Cotesia icipe)

doi:10.21203/rs.3.rs-2535302/v1

Download PDF

Research Article

Companion crops alter olfactory responses of the fall armyworm (Spodoptera frugiperda), and its larval endoparasitoid (Cotesia icipe)

https://doi.org/10.21203/rs.3.rs-2535302/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

The fall armyworm (FAW), Spodoptera frugiperda, is a devastating invasive pest and a threat to food security in Africa, with yield losses of 20–50%. Recent studies highlighted the importance of cereal crops such as maize and sorghum as the most preferred host plants for FAW oviposition. In the current work, we investigated the olfactory responses of FAW and its larval endoparasitoid Cotesia icipe to odours from the preferred host (maize) in the presence of six potential companion crops including beans, groundnut, sweet potato, greenleaf- and silverleaf desmodium, and cassava. We hypothesized that odours released by companion crops in maize-based intercropping systems would alter host preferences of FAW for oviposition and its parasitoid responses. In dual choice bioassays, FAW laid significantly more eggs on maize than on the other plants; however, significantly fewer eggs were laid on maize when companion plants were present. Markedly, the presence of cassava did not affect the oviposition responses of FAW. While wind tunnel bioassays confirmed the differential behavioural responses of the FAW, we found that its larval endoparasitoid C. icipe was attracted to volatiles from both the individual companion plants and when they were combined with maize. Coupled gas chromatography-mass spectrometry (GC-MS) analysis detected several potential behaviour-modifying compounds including (Z)-3-hexenyl acetate, (E)-β-ocimene, (E)-4,8-dimethyl-1,3,7-nonatriene, (E)-β-caryophyllene, camphor, methyl salicylate and (E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene. Our findings provide evidence supporting diversified maize cropping system could reduce FAW damage by repelling the pest while recruiting its natural enemies and hence may serve as an ecologically sustainable FAW management strategy.

Bioassay

Companion plants

Fall armyworm

Natural enemies

Oviposition

Volatiles

Companion plant volatiles modify the behaviour of FAW and its parasitoid natural enemy
Companion plant odours deter FAW oviposition while attracting C. icipe
Crop diversification has potential for ecologically sustainable FAW management

The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a generalist and invasive noxious pest native to tropical and subtropical regions of the Americas (Harrison et al. 2019). The FAW has been recorded in over 350 host plants belonging to several plant families, although it prefers grasses (Montezano et al. 2018; Sisay et al. 2022). In 2016, the FAW was first reported in West and Central Africa (Goergen et al. 2016; FAO 2017), from where it spread very quickly to other regions of the continent (Day et al. 2017; Baudron et al. 2019). Currently, FAW is present in over 45 African countries (Guimapi et al. 2022), and has become a serious threat to food security in the continent due to its substantial damage on staple food crops especially maize (Zea mays L.). For example, estimates from 12 African countries showed that FAW can cause annually maize losses of 8.3–20.6 million metric tonnes, equivalent to $2.5–6.2 billion, and enough to feed 40 to 100 million people (Rwomushana et al. 2018). In Kenya, FAW causes yield loss of about a third of the annual maize production, estimated at 1 million tonnes (De Groote et al. 2020). Emergency responses to counter the rapid spread and damage by FAW rely on extensive application of chemical pesticides (Kumela et al. 2018; Rwomushana et al. 2018). However, such approaches may have several undesirable consequences such as development of insecticide resistance, environmental pollution and health-related risks (Tamiru et al. 2011; Day et al. 2017). Additionally, most smallholder maize farmers in Africa cannot afford the costs of repeated insecticide applications (Hruska 2019). Hence, there is an urgent need to develop ecologically sustainable and cost-effective FAW management strategies adapted to African smallholder farming systems.

Increasing vegetation diversity through intercropping has been shown to suppress insect pest infestation, enhance naturally occurring pest enemies and lessen crop damage (Letourneau et al. 2011; Lithourgidis et al. 2011). Moreover, intercropping influences the rate at which the insect pest immigrates into a crop field and its population dynamics within the field (Smith and McSorley 2000; Han-ming et al. 2019). Smallholder farmers in Africa commonly intercrop maize with other crop species to reduce insect pest damage while enhancing crop productivity (Rahman et al. 2020). Several studies have reported reduced FAW infestation in diversified cropping systems where maize fields are intercropped with cowpea, beans, soya bean, pigeon pea, groundnut, canavalia and desmodium (Murdoch 1975; Altieri 1980; Altieri and Letourneau 1982; Smith and McSorley 2000; Sekamatte et al. 2003; Thayamini and Brintha 2010; Hailu et al. 2018; Harrison et al. 2019; Tanyi et al. 2020; Udayakumar et al. 2021). A notable example is the push-pull cropping system, which involves use of pest repellent intercrop and an attractive trap plant (Khan et al. 2010). A recent study confirmed that a reduced FAW infestation in the push-pull cropping system was associated with insect pest repellent volatile organic compounds (VOCs) emitted by desmodium intercrops (Sobhy et al. 2022).

On the other hand, there have been cases of contrasting findings (Baudron et al. 2019; Nwanze et al. 2021). For example, Garcia Gonzalez et al. (2010) found maize fields intercropped with pumpkin had lower FAW infestations compared to fields with maize alone in Cuba. In contrast, a study conducted in Eastern Zimbabwe showed that intercropping maize with pumpkin increases FAW damage (Baudron et al. 2019). Different factors including natural enemy abundance, variation in the ecosystem, and agronomic practices employed by respective farmers could contribute to the contrasting results. However, several studies from FAW native region of tropical and subtropical America have shown that the combined use of diversified cropping system and natural enemies could maintain FAW populations at significantly low level for smallholder farmers (Wyckhuys et al. 2006). Thus, the effectiveness of diversified cropping systems in mitigating FAW damage could be enhanced by selecting appropriate crop mixtures as well as better understanding the kind of tritrophic interactions between crop, pest and its natural enemies. Moreover, better insight into the ecological interactions and the underpinning mechanisms are crucial for the success of adopting appropriate crop diversification as a pest management tool.

Recent studies from our laboratory demonstrated that FAW exhibited divergent ovipositional preferences when presented with different host plants (Sisay et al. 2022). Our current work extends that of our previous finding and investigates olfactory responses of FAW and its key larval endoparasitoid, Cotesia icipe Fernandez-Triana and Fiaboe (Hymenoptera: Braconidae), to diverse companion food crops commonly used in a maize-based intercropping system. We tested the hypothesis that odours released by companion crops in maize-based intercropping systems would alter FAW ovipositional responses and host finding in its larval endoparasitiod C. icipe. To achieve this, we: (i) compared the oviposition responses of FAW to maize and/or six potential companion plants including beans (Phaseolus vulgaris L.), groundnut (Arachis hypogaea L.), sweet potato (Ipomoea batatas (L.) Lam.), greenleaf desmodium (Desmodium intortum (Mill.) Urb.), silverleaf desmodium (Desmodium uncinatum (Jacq.) DC.),cassava (Manihot esculenta Crantz) and millet (Panicum miliaceum L.); (ii) assessed the role of olfaction in FAW responses and that of its endoparasitoid C. icipe; and (iii) used gas chromatography-mass spectrometry (GC-MS) to compare and identify the potential discriminant and behavior-modifying companion plant volatiles.

Plants

The experimental plants, including maize (Z. mays), variety “SC Duma 43”, millet (P. glaucum), bean (P. vulgaris), groundnut (A. hypogaea), sweet potato (I. batatas), cassava (M. esculenta), greenleaf desmodium (D. intortum),silverleaf desmodium (D. uncinatum) and millet (P. miliaceum L.) were obtained from Simlaw Seeds Company, Kenya and the nursery plots of the International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya [01º 13’ 25.6” S 036º 53’ 49.1” E, 1616 meters above sea level (masl)]. The experimental plants were grown individually in plastic pots (4 L) filled with soil and organic manure mixed at a 2: 1 ratio inside an insect-proof screen house. All plants were grown under natural conditions (25 ± 2°C, 65 ± 5% RH; 12 L: 12 D photoperiod), at icipe and were used in the experiments after 3–4 weeks from the date of planting.

Insects

FAW larvae used in our study were obtained from icipe’s Animal Rearing and Quarantine Unit (ARQU). The initial insect colony at ARQU was established with specimens collected from FAW infested maize fields in Mbeere (00º 42’ 25.1” S 037º 29’ 0.14” E, 1091 masl), Embu County, Kenya. The larvae were reared on a natural diet in ventilated sleeved transparent Perspex cages (60 × 60 × 60 cm). The bottom of the cage was lined with a paper towel to absorb excess moisture and provide an environment for pupation. The larvae were fed with young maize leaves which were changed and replaced with fresh ones every 2–3 days and allowed to pupate inside the same containers. Pupae were transferred into plastic containers (10 mm diameter × 50 mm height) lined with cotton wool inside ventilated Perspex cages (30 × 30 × 30 cm) until adult emergence. The adults were fed on a mixture of water and honey (9: 1) soaked in cotton wool. Butter papers were placed inside the cage as an oviposition substrate for females. Harvested eggs were placed in 8 L jars with ventilated lids till neonates emerged. At the 3rd instar stage, larvae were collected with a camel brush and were transferred into Perspex cages (60 × 60 × 60 cm) and fed with maize leaves until pupation. Pupae were transferred into Perspex cages as described above and the process was repeated. The laboratory-reared culture was infused with a field-collected insect population every 2–3 months to ensure colony vigour. C. icipe were reared on 2nd instar larvae of FAW. The insect cultures were maintained at 25 ± 2^oC, 50–70% RH, 12L: 12D photoperiod.

Oviposition bioassay

Two complementary experiments were conducted to investigate the oviposition responses of FAW moths towards test plants in dual and multiple-choice tests following previously described methods (Khan et al. (2007), with some modification.

In Experiment I (Fig. 1A), a dual choice test was carried out using two potted 3–4 weeks old seedlings. Each test plant was placed in the opposite corners of the oviposition cage (100 × 100 × 100 cm) covered with fine wire mesh netting. A wad of cotton wool (10 cm diameter) soaked with a 10% honey solution in a Petri dish (90 × 15 mm) was placed at the centre of each cage to nourish FAW moths. Thereafter, six gravid FAW females (2–3 days old) were released into each cage before nightfall and allowed to oviposit overnight under natural conditions. Seven plant combinations were tested (Table 1). The following day (15 h after release), the experimental plants were removed and the number of eggs and egg batches on each plant were counted under a light microscope (Leica EZ4HD, Leica Microsystems, Schweiz, Switzerland).

Table 1

Plant combinations used to test the preference of FAW in dual and multiple-choice oviposition assays
No.	Dual choice assay	multiple choice assay
1	Maize vs millet^a	Maize vs beans + maize
2	Maize vs cassava	Maize vs groundnut + maize
3	Maize vs sweet potato	Maize vs sweet potato + maize
4	Maize vs beans	Maize vs cassava + maize
5	Maize vs groundnut	Maize vs silverleaf desmodium + maize
6	Maize vs silverleaf desmodium	Maize vs greenleaf desmodium + maize
7	Maize vs greenleaf desmodium

^aMillet was included in the dual choice test as a positive control from the grass family.

In Experiment II (Fig. 1B), FAW oviposition behaviour was investigated by setting up assays for different crop combinations commonly used under maize-based multiple cropping systems. Potted plants with six different plant combinations (Table 1), were placed in the opposite corners of an oviposition cage (150 × 150 × 150 cm) covered with a fine wire mesh netting. Ten gravid FAW females (2–3 days old) were released into the cage to oviposit overnight, and a cotton ball saturated with 10% honey solution placed in the middle of the cage served as food source for the moths. The number of eggs and egg batches on each plant were collected and counted the following day as described above. All treatments were replicated 10 times.

Wind tunnel bioassay

Behavioural responses of female FAW to volatiles from maize, millet, cassava, sweet potato, beans, groundnut, silverleaf- and greenleaf desmodium and control (air) were tested individually and in a combination with maize in wind tunnel bioassay (122 × 32 × 32 cm, Analytical Research Systems, Gainesville, USA). The wind tunnel comprised a transparent glass on an aluminum frame, odour source ports and exhaust tubes (Sobhy et al. 2022). Bioassays were conducted using 2–3 days old gravid FAW moths. Newly emerged female moths were allowed to spend at least two nights in cages containing male FAW moths to ensure mating and females with enlarged abdomens carrying fully developed eggs were selected for the bioassay. Prior to running the wind tunnel assay, the moths were kept in the bioassay room for 1 h to acclimatize. Potted live plants were placed outside the wind tunnel as odour sources for the bioassay and avoid interference with visual cues. Volatiles from the experimental plants, enclosed with heat sterilized oven bags, were delivered into the wind tunnel chamber through the inlet ports at the upwind end of the wind tunnel at the rate of 300 mL min^− 1. Gravid FAW moths were gently introduced individually into the wind tunnel through a side panel at the downwind end of the tunnel, 100 cm away from the odour source. The following behavioural parameters were measured during a 5 min observation period: takeoff, wing fanning, walking, upwind flight (oriented flight to odour source), landing distance and the number of close visits to the odour source. Odour in the wind tunnel chamber was continuously exhausted (at 30 cm s^− 1) out of the bioassay room through polyvinyl chloride (PVC) pipes fitted to a suction pump (50/60 Hz, 10A). All bioassays were conducted between 18:00–22:00 with reduced lighting provided by a red-light bulb (40 watts), positioned at 30 cm above the wind tunnel to provide uniform illumination of the tunnel. All tests were replicated three times with 20 insects per replicate making a total of 60 insects per treatment and each female was tested only once.

Olfactometer bioassay

Two sets of bioassays were conducted to investigate the response of C. icipe to constitutive plant-derived volatiles from maize, cassava, sweet potato, beans, groundnut, silverleaf desmodium, greenleaf desmodium and solvent [Dichloromethane (DCM)] control in a Perspex four-arm olfactometer as described previously (Tamiru et al. 2011). In the first experiment, a choice test compared C. icipe responses to constitutive volatiles from individual plants with control (solvent only). In this set up, the choice test was carried out by placing the test stimuli (10 µL aliquots of headspace sample) in one arm, while the remaining three arms were the same volume of solvent (DCM) controls. The treatment stimulus was applied to a piece of filter paper (4 × 25 mm) using a micropipette (Drummond Scientific, Broomall, USA), and allowed to dry for 30 s, then the filter paper was placed in an inlet port at the end of each olfactometer arm. Thereafter, 2–3 days old mated and experienced female C. icipe, exposed to odours from maize leaves damaged by FAW larvae (Sobhy et al. 2022), were transferred individually into the central chamber of the olfactometer using a custom-made piece of glass tubing. Air was drawn through the four arms towards the centre at 260 mL min^− 1. Time spent and entries in different olfactometer regions were recorded and compared using Olfa software (F. Nazzi, Udine, Italy) for 12 min (Tamiru et al. 2015). The olfactometer was rotated clockwise by 90º every 3 min to avoid positional choice bias. In the second experiment, a choice test was carried out, using a similar set up as described above, to compare insect responses to a combination of volatiles from maize with greenleaf desmodium, sweet potato, beans, cassava, groundnut, silverleaf desmodium against maize alone and solvent control. The two opposite arms held the test stimuli: 10 µL of maize + 10 µL of companion plants headspace volatiles in one arm and 20 µL (i.e 10 µL × 2) of maize headspace sample in the opposite arm; with the remaining two arms being blank controls (solvent only). All tests were replicated 12 times and each female was tested in the olfactometer once only.

Collection of volatiles

Headspace volatiles from the experimental plants (3–4 weeks old) were collected using a headspace sampling technique as described by Tamiru et al. (2011). Volatiles were collected from the test plants and control for 24 h starting at the last 2 h of photophase with four replications. Leaves of the test plants were gently enclosed inside polyethylene terephthalate (PET) oven bags (volume 3.2 L, ⁓ 12.5 mm thickness), heated to 150℃ for 1 h before use, and fitted with Swagelock inlet and outlet ports. Charcoal-filtered air was passed through the inlet port at the rate of 500 mL min^− 1. Volatiles were trapped on Porapak Q (50 mg, 60 ⁄ 80 mesh; Supelco, Bellefonte, USA) packed in filters, preconditioned with dichloromethane before use, and inserted in the outlet port through which air was drawn at 300 mL min^− 1. After entrainment, trapped volatiles were eluted with 0.5 mL DCM (analytical grade, Sigma-Aldrich, USA) into 2 mL sample vials (Agilent Technologies, WarsawPoland) and stored in a freezer (-80^oC) until required for bioassay and analysis.

Analyses of volatiles

An aliquot (2 µL) of headspace samples from the experimental plants was analysed using an Agilent 7890A gas chromatograph (GC) directly coupled to a mass spectrometer (MS) (MSD 5975C triple-axis, Agilent Technologies, Palo Alto, USA). The GC-MS was equipped with a non-polar capillary column (HP5-MSI, 30m length × 0.25mm i.d. × 0.25µm film thickness) (J & W, Folsom, USA). Helium was used as a carrier gas at a flow rate of 1.2 mL min^− 1. The oven temperature was maintained at 35 ^oC for 5 min and then programmed to increase at 10 ^oC min^− 1 to a final temperature of 280 ^oC and held for 10.5 min. The mass selective detector was maintained at an ion source temperature of 230 ^oC. Spectra was recorded at an electron impact of 70 eV, and an MS quadrupole temperature was maintained at 150 ^oC. Compounds were identified by comparing their mass spectra data with those with authentic standards using reference databases (Adams2, Chemecol and NIST11) and retention indices of a mixture of n-alkanes (C8-C23). Tentative identification of compounds was confirmed by co-injection with commercially available authentic standards where available. Quantification of the amounts (in nanogram) of identified volatile compounds was achieved using external calibration curves made from 1,000 ng µL^− 1 stock solutions of the selected identified compounds (Z)-3-hexen-1-ol, α-pinene, (E)-β-caryophyllene with varying concentrations from 1 to 500 ng/µL. The concentration of compounds was computed by extrapolating the peak area of the unknown against those of the known concentration and expressed in ng/plant/h. All peaks detected in the control (oven bag) were considered contaminants and therefore not included in the volatile quantification. Data were analysed using MSD Chemstation software F.01.00.1903 (Agilent Technologies).

Chemicals

Authentic standards used for quantification and comparison of tentative GC-MS identification were (E)-2-hexenal, (Z)-3-hexen-1-ol, 2-heptanone, 2-heptanol, α-pinene, β-pinene, 1-octen-3-ol, β-myrcene, α-phellandrene, ρ-cymene, limonene, β-phellandrene, (E)-β-ocimene, terpinolene, linalool, methyl salicylate, β-elemene, (E)-β-caryophyllene, α-humulene (> 95% purity) were purchased from Sigma-Aldrich. Dichloromethane (99.9% purity) was purchased from Merck (Darmstadt, Germany).

Statistical analyses

All data analyses were performed using R statistical software (v 4.0.4; R Core Team 2021). The number of egg batches and eggs laid in both oviposition bioassays were not normally distributed (Shapiro-Wilk test: p < 0.05). Hence, we used the Mann-Witney-Wilcoxon test to analyse the data collected in our choice bioassays and subsequent bioassays to compare egg deposition between maize (alone) and maize combined with companion plants. Data on the behavioural response of female FAW to plant volatiles in the wind tunnel were analysed using a generalized linear model (GLM) with logistic regression and a Tukey post-hoc test. The parameters recorded were insect takeoff, wing fanning, walking and oriented flight to odour source. Kruskal-Wallis tests followed by Dunn’s post-hoc tests were used to analyse the data on the distance flown upwind and the number of visits to the odour source by the moths to the various treatments.

Cotesa icipe responses in the four-arm olfactometer choice tests were analysed using one-way ANOVA after converting the time spent data into proportions to address dependence of visiting time followed by log₁₀-ratio transformation to allow for the analysis of compositional data as described by Aitchison (1982) and Tamiru et al. (2011). Significant means were separated using Student-Newman-Keuls (SNK) post hoc test (P < 0.05). The concentrations of volatile compounds emitted from all the test plants were analysed using the non-parametric Mann-Whitney Wilcoxon (two treatments) and Kruskal-Wallis (multiple treatments) tests because the data were not normally distributed (Shapiro-Wilk test: p < 0.05), followed by Dunn’s post-hoc to separate means. To determine the relative contribution of different VOCs to the dissimilarity across the test plants, we subjected the peak areas of identified VOCs to similarity percentage analysis (SIMPER). The profile was visualised using the non-metric multidimensional scaling (NMDS) and the VOCs profiles of the eight test plants were compared using one-way ANOSIM with the Bray–Curtis dissimilarity matrix.

Responses of FAW in oviposition assays

In experiment I, female FAW deposited eggs on all crop species tested, but significantly more egg batches and eggs were deposited on maize than on companion plants (Fig. 2A, B). In the dual choice oviposition bioassay, significantly more eggs were deposited on maize than on silverleaf desmodium (W = 89.5, P = 0.002), beans (W = 11.5, P = 0.003), cassava (W = 10, P = 0.002), greenleaf desmodium (W = 23, P = 0.03), groundnut (W = 20.5, P = 0.025) and sweet potato (W = 94, P = 0.0007) (Fig. 2A). A similar trend was recorded in the number of egg batches deposited on maize compared to the companion plants (Fig. 2B). However, there were no significant differences in the number of eggs (W = 61, P = 0.42) and egg batches (W = 66, P = 0.23) deposited on maize and millet (Fig. 2A, B).

In experiment II, the number of eggs oviposited by gravid FAW moths on maize (alone) were significantly reduced when maize was combined with companion plants (Fig. 3). Significantly more eggs were laid on maize alone than on maize when combined with beans (W = 12, P = 0.004, Fig. 3A), sweet potato (W = 8, P = 0.001, Fig. 3B), groundnut (W = 16.5, P = 0.01, Fig. 3C), silverleaf desmodium (W = 9, P = 0.002, Fig. 3E) and greenleaf desmodium (W = 1.5, P = 0.003, Fig. 3F). However, the number of eggs deposited on maize alone were not significantly different when maize was combined with cassava (W = 31, P = 0.158, Fig. 3D).

Significantly more egg batches were deposited on maize alone than on maize combined with beans (W = 15, P = 0.007, Fig. 4A), sweet potato (W = 21, P = 0.03, Fig. 4B) groundnut (W = 22, P = 0.03, Fig. 4C) and silverleaf desmodium (W = 14.5, P = 0.006, Fig. 4E). However, the number of egg batches deposited on maize alone were not significantly different from maize combined with cassava (W = 28.5, P = 0.102, Fig. 4D).

Responses of FAW in wind tunnel assays

In experiment I, with individual plant odour sources including control (clean air), maize volatiles elicited significantly more oriented upwind flight (Fig. 5A) from female moths than volatiles from companion plants and control (GLM Likelihood Ratio (LR) χ² = 61.38, df = 8, P < 0.001). Significantly more female moths flew upwind closer to odours from maize than companion plant species and control (Kruskal-Wallis χ² = 39.81, df = 8, P < 0.001) (Fig. 5B). Furthermore, the moths landed significantly further up from the release point and closer to maize odour source (Fig. 5C) compared to greenleaf desmodium, sweet potato, beans, silverleaf desmodium, groundnut and control (Kruskal-Wallis χ² = 36.37, df = 8, P < 0.001). Odour sources from the various experimental plants elicited significantly different behavioural responses in the female FAW moths including wing fanning (LR χ² = 36.75, df = 8, P < 0.001, Fig. 5D), walking (LR χ² = 20.93, df = 8, P = 0.007, Fig. 5E) and take-off flight (LR χ² = 20.71, df = 8, P = 0.008, Fig. 5F).

In experiment II, maize odours elicited significantly less upwind oriented flights (Fig. 6A) from gravid FAW moths when presented with odours from beans, cassava, groundnut, sweet potato, groundnut and both Desmodium sp. compared to maize odour alone (LR χ² = 36.75, df = 6, P < 0.001). Similarly, combining maize with other companion plants odours significantly reduced female FAW moth attraction and led to fewer closer flights to the odour sources (Kruskal-Wallis χ² = 47.31, df = 6, P < 0.001, Fig. 6B). Furthermore, the forward landing distance of the moths from the release point (Fig. 6C) was significantly reduced when maize volatiles were presented in combination with companion plants compared to maize volatile alone (Kruskal-Wallis χ² = 49.07, df = 6, P < 0.001). However, no significant differences were observed in the proportion of female moths that exhibited wing fanning (LR χ² = 5.53, df = 6, P = 0.48, Fig. 6D), walking (LR χ² = 2.99, df = 6, P = 0.81, Fig. 6E) and take-off flight behaviours (LR χ² = 11.91, df = 6, P = 0.06, Fig. 6F) between treatments.

Responses of C. icipe in olfactometer assays

Behavioural responses of C. icipe to constitutive plant volatiles of test plants and solvent control (DCM) in a four-arm olfactometer are shown in Figs. 7 and 8. Female C. icipe spent significantly more time in the olfactometer region with volatiles from greenleaf desmodium (F _{(1, 46)} = 11.32, P = 0.002), sweet potato (F _{(1, 46)} = 25.70, P < 0.001), beans (F _{(1, 46)} = 7.393, P = 0.009), cassava (F _{(1, 46)} = 4.295, P = 0.044), groundnut (F _{(1, 46)} = 6.36, P = 0.015) and silverleaf desmodium (F _{(1, 46)} = 15.55, P < 0.001) volatiles than solvent control. However, no significant differences were observed in the time spent by C. icipe between maize volatiles and solvent control (F (1, 46) = 0.619, P = 0.435) (Fig. 7).

Interestingly, C. icipe was significantly attracted to odours from maize combined with companion plant species (greenleaf desmodium, sweet potato, beans, cassava, groundnut, silverleaf desmodium) than to volatiles from maize (alone) and solvent control (Fig. 8). Female C. icipe parasitoids spent significantly more time in the olfactometer arm containing volatiles from maize combined with greenleaf desmodium (F _{(2, 45)} = 10.84, P < 0.001), sweet potato (F _{(2, 45)} = 3.66, P = 0.03), beans (F _{(2, 45)} = 5.788, P = 0.005), groundnut (F _{(2, 45)} = 14.57, P < 0.001) and silverleaf desmodium (F _{(2, 45)} = 18.56, P < 0.001) than in the olfactometer arms with maize alone and solvent control. In contrast, there was no significant difference in C. icipe response to volatiles of maize combined with cassava, maize alone and solvent control (F _{(2, 45)} = 0.648, P = 0.528) (Fig. 8D).

Analyses of volatiles

GC-MS analysis of companion plant headspace volatiles detected a total of 48 components belonging to seven chemical classes namely, aldehyde (1), alcohols (3), ketones (2), monoterpenes (14), esters (3), homoterpenes (2), and sesquiterpenes (23) (Table 1 and Fig. 9). Heatmap clustering revealed quantitative and qualitative variations in volatile emissions from the test plants (Fig. 9A). The monoterpene (E)-β-ocimene was the most abundant VOC identified in silverleaf and greenleaf desmodium (Kruskal-Wallis χ² = 18.36, df = 5, P = 0.002) followed by (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) (Kruskal-Wallis χ² = 14.23, df = 5, P = 0.01) and (E)-β-caryophyllene (Kruskal-Wallis χ² = 14.56, df = 5, P = 0.01) (Table 1). The three compounds were also detected in other companion plant species, but in relatively lower amounts than in the volatiles released by desmodium spp. VOCs that were detected in companion plant volatiles but not detected or found in trace amounts in the main crop (maize) included (E)-2-hexenal, 1-octen-3-ol, 3-octanone, methyl salicylate (MeSA), β-selinene and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), and hence could be of potential biological relevance. Interestingly, these compounds including DMNT were not detected in cassava except for (E)-2-hexenal. The monoterpenoids camphor and limonene were the main VOCs identified in headspace collection from beans, with likely impact on FAW and C. icipe behaviour.

Mapping volatile organic compounds using non-metric multidimensional scaling plot (NMDS) clustering demonstrated significant variation in volatile composition between the test plants (ANOSIM: P = 0.0001, R = 0.85) (Fig. 9B). Based on analysis of similarities (ANOSIM) the following compounds, namely (E)-β-ocimene (21%), (E)-β-caryophyllene (15%), DMNT (10%), (Z)-3-hexenyl acetate (10%), TMTT (7%), camphor (7%), limonene (6%), (Z)-3-hexen-1-ol (4%), germacrene D (4%) and δ-cadinene (4%) contributed most of the differences between the test plants (Figs. 9C and 10).

Table 1

Mean amount (ng/plant/h) of volatile organic compounds (VOcs) identified in the headspace collections of intact test plants (n = 4)
No.	RT(Min)				Compound¹	RI_alk²		RI_L³		Maize		Millet		Sweet potato		Groundnut		Cassava		SLD		GLD		Beans		P value⁴
1	8.05				(E)-2-hexenal*	861		856		nd		Nd		nd		nd		21.84 ± 0.49^b		26.48 ± 0.32^a		nd		nd		0.02
2	8.12				(Z)-3-hexen-1-ol*	863		860		26.3 ± 1.28^bc		Nd		27.4 ± 4.24^bc		26.6 ± 2.1^bc		23.66 ± 1.07^c		57.62 ± 12.14^a		36.7 ± 3.12^ab		nd		0.01
3	8.93				2-heptanone*	894		895		24.99 ± 2.62		Nd		nd		nd		nd		nd		nd		nd		-
4	9.16				2-heptanol*	904		903		23.93 ± 1.44		Nd		nd		nd		nd		nd		nd		nd		-
5	9.82				α-pinene*	935		934		24.44 ± 2.44		26.98 ± 3.83		27.04 ± 1.69		23.09 ± 0.31		22.09 ± 0.41		27.22 ± 1.9		30.82 ± 9.03		19.88 ± 2.07		0.14
6	10.67				Sabinene	975		974		nd		22.18 ± 0.4		23.23 ± 1.82		22.06 ± 0.11		nd		nd		nd		nd		0.19
7	10.71				β-pinene*	977		978		nd		21.32 ± 0.15^ab		23.75 ± 0.85^a		21.17 ± 0.13^ab		nd		nd		nd		18.36 ± 1.57^b		0.005
8	10.82				1-octen-3-ol*	982		981		nd		nd		nd		25.29 ± 1.61		nd		37.43 ± 8.79		35.02 ± 9.97		nd		0.47
9	10.98				3-octanone	989		984		nd		nd		nd		nd		nd		nd		33.86 ± 8.74		nd		-
10	11.01				2,3-dehydro-1,8-cineole	991		986		nd		22.38 ± 0.84		nd		nd		nd		nd		nd		nd		-
11	11.03				β-myrcene*	992		992		22.81 ± 0.37		nd		23.47 ± 0.36		nd		nd		nd		nd		nd		0.11
12	11.29				α-phellandrene	1005		1005		nd		21.68 ± 0.3		nd		nd		nd		nd		nd		nd		-
13	11.36				(Z)-3-hexenyl acetate	1009		1007		26.67 ± 2.9		nd		nd		60.68 ± 8.87		nd		nd		32.54 ± 12.07		nd		0.08
14	11.66				ρ-cymene*	1026		1020		nd		nd		nd		24.19 ± 0.95		21.92 ± 0.38		nd		nd		nd		0.20
15	11.73				Limonene*	1029		1030		31.33 ± 6.6		21.38 ± 0.32		41.04 ± 5.66		25.06 ± 0.18		21.8 ± 0.32		nd		38.27 ± 16.09		27.66 ± 4.12		0.12
16	11.76				β-phellandrene*	1031		1032		nd		24.55 ± 2.92		nd		nd		nd		nd		nd		nd		-
17	11.78				1,8-cineole	1032		1036		nd		22.04 ± 0.34		nd		25.58 ± 1.27		nd		nd		nd		nd		0.20
18	12.09				(E)-β-ocimene*	1050		1050		nd		27.86 ± 6.43^b		23.9 ± 1.39^b		47.66 ± 3.62^ab		38.97 ± 9.81^ab		202.5 ± 35.81^a		153.08 ± 28.67^a		nd		0.002
19	12.80				Terpinolene*	1089		1090		nd		nd		21.08 ± 0.12		nd		nd		nd		nd		nd		-
20	12.99				Linalool*	1101		1101		30.01 ± 5.76		23.17 ± 1.51		nd		25.39 ± 2.76		nd		41.77 ± 4.23		nd		nd		0.06
21	13.26				DMNT	1117		1116		40.01 ± 8.06^ab		26.48 ± 2.21^b		36.91 ± 5.27^ab		68.24 ± 6.19^a		nd		97.8 ± 21.61^a		57.79 ± 7.25^a		nd		0.01
22	13.77				Camphor	1148		1146		nd		nd		nd		nd		nd		nd		nd		45.26 ± 8.37		-
23	14.62				Methyl salicylate*	1202		1199		nd		nd		nd		51.38 ± 10.79		nd		nd		23.2 ± 9.37		nd		0.11
24	15.93				Lavandulyl acetate	1293		1289		33.11 ± 4.58		nd		nd		nd		nd		nd		nd		nd		-
25	16.85				α-longipinene	1360		1352		nd		nd		nd		nd		21.81 ± 0.58		nd		nd		nd		-
26	17.07				Cyclosativene	1377		1369		55.25 ± 8.02		nd		nd		nd		nd		nd		nd		nd		-
27	17.15				Longicyclene	1382		1376		nd		nd		nd		nd		40.8 ± 5.4		nd		nd		nd		-
28	17.16				α-ylangene	1383		1382		nd		27.33 ± 1.51		23.61 ± 2.61		nd		nd		nd		17.73 ± 2.21		nd		0.14
			Table 1 (continued) Mean amount (ng/plant/h) of volatile compounds identified in the headspace collections of intact test plants (n = 4)
No.	RT(Min)				Compound¹	RI_alk²		RI_L³		Maize		Millet		Sweet potato		Groundnut		Cassava		SLD		GLD		Beans		P value⁴
29	17.17				α-copaene	1384		1384		67.27 ± 10.88^a		nd		22.77 ± 0.78^b		nd		nd		nd		nd		nd		0.02
30	17.37				β-elemene*	1398		1397		28.84 ± 5.63		nd		35.99 ± 2.89		nd		nd		nd		nd		nd		0.34
31		17.64		Longifolene			1419		1406		nd		nd		nd		nd		26.67 ± 0.95^a		nd	nd	16.87 ± 1.17^b		0.02
32		17 .73		α-cedrene			1426		1424		nd		nd		nd		nd		nd		nd	nd	15.93 ± 0.68		-
33		17.80		(E)-β-caryophyllene*			1432		1430		83.37 ± 4.68^a		25.29 ± 3.52^b		79.22 ± 26.07^a		nd		29.97 ± 2.92^b		81.34 ± 11.8^a	89.04 ± 10.01^a	nd		0.01
34		17.92		(E)-α-bergamotene			1442		1451		25.35 ± 2.22		nd		34.38 ± 2.44		28.96 ± 4.86		nd		nd	nd	nd		0.19
35		18.22		α-humulene*			1466		1465		32.04 ± 3.2		27.32 ± 6.24		30.78 ± 3.55		nd		22.47 ± 1.11		24.02 ± 1.44	21.81 ± 0.58	20.61 ± 2.93		0.10
36		18.31		β-chemigrene			1473		1476		nd		nd		22.67 ± 0.84		nd		nd		nd	nd	nd		-
37		18.34		β-selinene			1475		1475		nd		nd		nd		nd		nd		30.59 ± 7.45	nd	nd		-
38		18.39		γ-gurjunene			1479		1477		nd		nd		nd		nd		nd		nd	26.59 ± 4.82	nd		-
39		18.58		Germacrene D			1494		1490		39.91 ± 8.55		25.79 ± 4.55		48.35 ± 6.04		nd		26.37 ± 3.28		nd	nd	nd		0.07
40		18.62		α-selinene			1498		1498		nd		nd		34.81 ± 1.48		nd		nd		33.14 ± 9.79	nd	nd		0.34
41		18.79		Isodaucene			1512		1500		nd		nd		42.95 ± 8.09		nd		nd		nd	nd	nd		-
42		18.82		α-muurolene			1514		1502		25.22 ± 3.93		nd		nd		nd		nd		nd	nd	nd		-
43		18.96		γ-cadinene			1525		1513		23.21 ± 1.15^b		66.11 ± 4.61^a		nd		24.41 ± 0.82^b		nd		nd	nd	nd		0.02
44		19.09		δ-cadinene			1536		1525		46.66 ± 9.97		32.47 ± 11.07		33.19 ± 1.33		nd		nd		nd	nd	nd		0.27
45		19.52		unknown			1574		-		38.34 ± 7.28		24.75 ± 2.77		27.42 ± 2.55		35.43 ± 5.59		nd		nd	29.73 ± 5.48	nd		0.46
46		19.67		TMTT			1585		1584		nd		nd		58.54 ± 8.03^ab		35.51 ± 5.18^b		nd		nd	61.6 ± 2.58^a	nd		0.01
47		19.84		Caryophyllene oxide			1599		1588		nd		nd		39.34 ± 8.61		nd		nd		nd	nd	nd		-
48		20.12		Epi-cedrol			1623		1625		nd		nd		nd		nd		nd		nd	nd	17.91 ± 2.09		-

¹Tentative identification of volatile organic compounds (VOCs) was done by comparing their mass spectra with those from the authentic standards where available, mass spectra databases (Adams2, Chemecol and NIST11) and the online NIST Chemistry Webbook as well as retention index (KI). *Indicates compounds confirmed with authentic standards.

²Retention index relative to C₈-C₂₃ n-alkanes on HP-5MS capillary column

³ Retention index obtained from literature (Khan et al. 2012)

⁴P-value of non-parametric Kruskal-Wallis and two sample Wilcoxon tests for comparing amounts of volatile organic compounds between the test plants. Means (± SE) with different superscript letter(s) within the rows are significantly different (P < 0.05). nd = not detected, SLD = Silverleaf desmodum, GLD = Greenleaf desmodium, DMNT = (E)-4,8-Dimethyl-1,3,7-nonatriene, TMTT = (E, E)-4,8,12-Trimethyl-1,3,7,11-tridecatetraene.

Olfaction plays a crucial role in locating and discriminating between preferred host plant and non-host plants in phytophagous insects. Our results demonstrated that maize is a more preferred host plant for FAW oviposition than other tested crops confirming previous findings (Sisay et al. 2022). The presence of companion plants significantly reduced FAW oviposition on maize. This demonstrates the impact of the companion plants in disrupting olfactory cues mediating FAW oviposition leading to less egg deposition and reduced subsequent infestation and damage by the pest. Our findings support the results from previous studies which reported decreased FAW infestation in maize fields intercropped with companion plant species compared to sole maize cropping (Willey et al. 1983; Hailu et al. 2018; Tanyi et al. 2020). Intriguingly, the presence of cassava did not affect the egg laying responses of FAW, implying odours released by cassava plants may not influence oviposition behaviour of the pest. Our results corroborate the findings by Nwanze et al. (2021), who reported an extreme scenario where the presence of cassava in maize-cassava intercropping system encouraged FAW oviposition and subsequent feeding on maize plants in Niger Delta Region.

Significant upwind flight and closer landing by FAW moths to odour sources from maize plants compared to other plant species in the wind tunnel bioassay suggest attractiveness of maize volatiles. However, the attractiveness of maize volatiles was significantly reduced in the presence of companion plant volatiles resulting in decreased oriented (upwind) flight of FAW moths toward maize odour. These results confirm the presence of oviposition deterrents in the volatile chemistry of neighbouring companion plants since the experimental plants were positioned outside the wind tunnel to avoid influence of any visual and tactile cues. The FAW moths were subjected to only naturally emitted headspace volatiles delivered through the inlet ports in this bioassay set up. Moreover, the findings explain the significantly lower number of eggs deposited by gravid FAW females on maize when combined with the companion plants. Several studies reported the repellent and masking effects of companion plant odours in disrupting the host-seeking abilities of crop pest as shown in the current study (Renwick 1989; Cook et al. 2007; Bandara et al. 2009; Sujayanand et al. 2015; Webster and Carde 2017; Harrison et al. 2019; Hruska 2019; Ahissou et al. 2021). Our results contrast with an inconclusive report by Rojas et al. (2003) who claimed that FAW females do not rely on plant volatiles for orientation to host plants but also suggested a more precise experiments under natural conditions to verify their results. Our findings from complementary oviposition and wind tunnel experiments provide clear evidence on the vital role of plant volatiles in the host-selection process of the FAW. Moreover, our results corroborate with the findings from several studies that have established the chemical basis for host-location behaviour of lepidopterous insects (Rembold et al. 1991; Honda 1995; Hartlieb and Rembold 1996; Signoretti et al. 2012; Sobhy et al. 2022).

In contrast to their effects on FAW, constitutive volatiles from the companion test plants were attractive to the larval endoparasitoid C. icipe, one of the key biological control agents of FAW in the region. Furthermore, the parasitoids were more attracted to odours from maize mixed with sweet potato, beans, groundnut, greenleaf desmodium and silverleaf desmodium than volatiles from maize plant alone. The attraction of C. icipe is of interest as the parasitic wasp provides biological control against FAW (Mohamed et al. 2021). This is an additional ecological benefit of crop diversification system where plant damage and infestation are reduced through enhanced ecosystem service provided by natural enemies. Diversified maize fields have been shown to enhance foraging behaviour and abundance of natural enemies such as parasitoids that are reported to suppress pest population (Khan et al. 2010; Quispe et al. 2017). Activities of beneficial insects (parasitoids and predator) have been shown to increase in a diversified cropping system and suppress the number of arthropod pests under field conditions (Letourneau et al. 2011; Seni 2018; Rahman et al. 2020).

Chemical analysis of headspace samples revealed qualitative and quantitative variation in volatile profiles of companion plants. Some of the predominant volatiles identified include (Z)-3-hexenyl acetate, (E)-β-ocimene, DMNT, camphor, (E)-β-caryophyllene, and TMTT. A recent study by Sobhy et al. (2022) demonstrated that these compounds elicit electrophysiological and behavioural responses in FAW and its parasitoid (C. icipe). The same compounds have also been reported to be produced by maize plants when attacked by herbivores and shown to play a defence role by repelling pests and recruiting their natural enemies (Carroll et al. 2006; D’Alessandro and Turlings 2006; War et al. 2012; Pickett and Khan 2016; Pinto-zevallos et al. 2016; Tamiru et al. 2015). Therefore, it is rational to attribute the FAW repellence effects and attraction of C. icipe parasitoid to these compounds emitted by the companion plants. Previous studies by Khan et al. (1997, 2000) and Pickett et al. (2006) have documented the emission of herbivore-induced compounds such as (E)-β-ocimene, (E)-β-caryophyllene and (E)-4,8-Dimethyl-1,3,7-nonatriene (DMNT), by intact Melinis minutiflora and Desmodium sp. Moreover, intercropping these forage crops with maize, repelled insect pests while simultaneously recruiting more natural enemies (parasitoids) to the intercrop system compared to maize monocrop (Khan et al. 2010). In our study, the volatile compounds (E)-β-ocimene, DMNT and (E)-β-caryophyllene were emitted in relatively large amounts by companion plants silverleaf and greenleaf desmodium while in a relatively lower amount in other companion plant species. Lower volatile emissions could elicit a potent behavioural response in insects if the bioactive compounds are present in the right blend (Bruce et al. 2010). It was also interesting to note that most of the prominent bioactive compounds such as (E)-β-ocimene and DMNT were not detected in beans though similar behavioural effects were exhibited due to the crop. The defence responses in beans could be attributed to the relatively large emission of camphor, which has been reported to have a repellent effect on most insects (Chen et al. 2013). Other volatile compounds present in the test companion plants but were not detected or found in trace amounts in the main (maize) crop include (E)-2-hexenal, 1-octen-3-ol, 3-octanone, methyl salicylate, β-selinene and TMTT. These compounds have been reported to have ecological importance by mediating plant defence responses either as a repellent, or deterrent to herbivores and attraction of their natural enemies (Binder and Robbins 1996; Signoretti et al. 2012; Agbessenou et al. 2022; Sobhy et al. 2022).

In summary, our findings provided evidence supporting associational resistance conferred by companion plant volatiles. Constitutively emitted companion plant volatiles had a repellent effect and decreased host attractiveness to FAW moth oviposition leading to fewer egg depositions on maize when combined with companion plants. Moreover, the heterospecific plant association enhanced the attraction of the key pest’s natural enemy, C. icipe parasitoid. Our results agree with Letourneau et al. (2011) report which showed significantly stronger herbivore suppression, natural enemy enhancement and crop damage suppression effects of diversified cropping systems compared to mono-crop systems. Furthermore, our volatile analyses results coupled with complementary bioassays data clearly demonstrated the role of plant volatiles in modulating the FAW-plant-C. icipe interactions. There is an urgent need to design effective agroecological pest management strategies alternative to pesticide-intensive monoculture crop production (Isbell et al. 2011). This requires a better understanding of the ecological interactions between the crops, their pests, and the natural enemies of the pests. Our study provides insights not only into the chemical ecology of fall armyworm-plant-natural enemy interaction of the different edible plant species used in a maize-based intercropping system but also explains the underpinning mechanism for the control of the pest in the diversified cropping system. There is a great potential to improve sustainable pest management by designing effective crop diversification schemes which include selecting appropriate plants with repellent effects on herbivores' pests and possibly attracting pest’s natural enemies.

Acknowledgments

We also thank Wanyama Onesmus Kaye, Basilio Njiru, Collins Onjura, Moses Otieno and Jeremiah Nyongesa for their technical support.

Funding

This research was supported by the European Union (EU) grant number FOOD/2018/402-634 through the International Centre of Insect Physiology and Ecology (icipe). We gratefully acknowledge icipe core funding provided by the Swedish International Development Cooperation Agency (Sida); the Swiss Agency for Development and Cooperation (SDC); the Australian Centre for International Agricultural Research (ACIAR), the Federal Democratic Republic of Ethiopia, and the Government of the Republic of Kenya. E.P. was supported by the Deutscher Akademischer Austauschdienst (DAAD) In-Region Postgraduate Scholarship (Personal Grant No. 91789313).

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Ethical Approval

This study does not contain any experiments using any animal species that require ethical approval.

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Agbessenou A, Akutse KS, Yusuf AA, Khamis FM (2022) The endophyte Trichoderma asperellum M2RT4 induces the systemic release of Methyl Salicylate and (Z) -jasmone in tomato plant affecting host location and herbivory of Tuta absoluta. Front Plant Sci 13:860309. doi:10.3389/fpls.2022.860309.
Ahissou BR, Sawadogo WM, Bokonon-Ganta AH, Somda I, Verheggen F (2021) Integrated pest management options for the fall armyworm Spodoptera frugiperda in west Africa: challenges and opportunities. a review. Biotechnol Agron Soc Environ 25:192–207. https://doi.org/10.25518/1780-4507.19125.
Altieri MA (1980) Diversification of corn agroecosystems as a means of regulating fall armyworm populations. Fla Entomol 63:450–456.
Altieri MA, Letourneau DK (1982) Vegetation management and biological control in agroecosystem. Crop Prot 1:405–430.
Bandara KANP, Kumar V, Ninkovic V, Ahmed E, Pettersson J, Glinwood R (2009) Can leek interfere with bean plant-bean fly interaction? Test of ecological pest management in mixed cropping. J Econ Entomol 102:999–1008. https://doi.org/10.1603/029.102.0319.
Baudron F, Zaman-Allah MA, Chaipa I, Chari N, Chinwada P (2019) Understanding the factors influencing fall armyworm (Spodoptera frugiperda J.E. Smith) damage in African smallholder maize fields and quantifying its impact on yield. A case study in Eastern Zimbabwe. Crop Prot 120: 141–150. https://doi.org/10.1016/j.cropro.2019.01.028.
Binder BF, Robbins JC (1996) Age- and density-related oviposition behavior of the european corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). J Insect Behav 9:755–769. https://doi.org/10.1007/BF02213555.
Burnett CW, Jones Jr BS, Mabry TJ (1978) Influence of sesquiterpene lactones of vernonia (Compositae) on oviposition preferences of Lepidoptera. Am Midl Nat 100:242–246. URL: https://www.jstor.org/stable/2424798.
Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924. https://doi.org/10.1007/s10886-006-9117-9.
Chen W, Vermaak I, Viljoen A (2013) Camphor-a fumigant during the black death and a coveted fragrant wood in Ancient Egypt and Babylon-a review. Molecules 18:5434–5454. https://doi.org/10.3390/molecules18055434.
Cook SM, Khan ZR, Pickett JA (2006) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400. https://doi.org/10.1146/annurev.ento.52.110405.09140
Day R, Abrahams P, Bateman M, Beale T et al (2017) Fall armyworm: impacts and implications for Africa. Outlooks Pest Manag 17:96–201. https://doi.org/10.1564/v28.
D’Alessandro M, Turlings TCJ (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24–32. https://doi.org/10.1039/b507589k.
De Groote H, Kimenju SC, Munyua B, Palmas S, Kassie M, Bruce A (2020) Spread and impact of fall armyworm (Spodoptera frugiperda J.E. Smith) in maize production areas of Kenya. Agric Ecosyst Environ 292:1–9. https://doi.org/10.1016/j.agee.2019.106804
FAO (2017) FAO advisory note on fall armyworm (FAW) in Africa.
Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J.E. Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLOS ONE 11:1–9. https://doi.org/10.1371/journal.pone.0165632
Garcia González MT, Rojas JA, Castellanos Gonzalez L, Enjamio Jiménez D (2010) Policultivo (maíz-calabaza) en el control de Spodoptera frugiperda (Smith) en fomento, sancti spiritus. Cent Agríc 37(1):57–64.
Guimapi RA, Niassy S, Mudereri BT et al (2022) Harnessing data science to improve integrated management of invasive pest species across Africa: An application to fall armyworm (Spodoptera frugiperda) (J.E. Smith) (Lepidoptera: Noctuidae). Glob Ecol Conserv 35:e02056 https://doi.org/10.1016/j.gecco.2022.e02056
Hailu G, Niassy S, Zeyaur KR, Ochatum N, Subramanian S (2018) Maize–legume intercropping and push-pull for management of fall armyworm, stemborers, and striga in Uganda. Agron J 110: 2513–2522. https://doi.org/10.2134/agronj2018.02.0110.
Han-ming HE, Li-na L, Munir S, Bashir NH, Wang Y, Yang J, Li C (2019) Crop diversity and pest management in sustainable agriculture. J Integr Agric 18:1945–1952. https://doi.org/10.1016/S2095-3119(19)62689-4
Harrison RD, Thierfelder C, Baudron F, Chinwada P, Midega C, Scha U, Van Den Berg J (2019) Agro-ecological options for fall armyworm (Spodoptera frugiperda J.E. Smith) management: providing low-cost, smallholder friendly solutions to an invasive pest. J Environ Manage 243:318–330. https://doi.org/10.1016/j.jenvman.2019.05.011
Hartlieb E, Rembold H (1996) Behavioral response of female Helicoverpa (Heliothis) armigera HB. (Lepidoptera: Noctuidae) moths to synthetic pigeonpea (Cajanus cajan L.) kairomone. J Chem Ecol 22:821–837. https://doi.org/10.1007/BF02033589
Honda K (1995) Chemical basis of differential oviposition by lepidopterous insects. Arch Insect Biochem Physiol 30:1–23. https://doi.org/10.1002/arch.940300102
Hruska AJ (2019) Fall armyworm (Spodoptera frugiperda) management by smallholders. CAB Rev 14: 1–11. https://doi.org/10.1079/PAVSNNR201914043
Isbell F, Adler PR, Eisenhauer N et al (2017) Benefits of increasing plant diversity in sustainable agroecosystems. J Ecol 105:871–879.
Khan ZR, Ampong-Nyarko K, Chilishwa P, Hassanali A et al (1997) Intercropping increases parasitism of pests. Nature 388:631–632.
Khan ZR, Midega CAO, Wadhams LJ, Pickett JA, Mumuni A (2007) Evaluation of napier grass (Pennisetum purpureum) varieties for use as trap plants for the management of African stemborer (Busseola fusca) in a push-pull strategy. Entomol Exp Appl 124:201–211.
Khan ZR, Midega CAO, Bruce TJA, Hooper AM, Pickett JA (2010) Exploiting phytochemicals for developing a “push-pull” crop protection strategy for cereal farmers in Africa. J Exp Bot 61:4185–4196. https://doi.org/10.1093/jxb/erq229
Khan M, Mousa AA, Syamasundar KV, Alkhathlan HZ (2012) Determination of chemical constituents of leaf and stem essential oils of Artemisia monosperma from central Saudi Arabia. Nat Prod Commun 7:1079–1082. https://doi.org/10.1177/1934578x1200700829
Kumela T, Simiyu J, Sisay B, Likhayo P, Gohole L, Tefera T (2018) Farmers’ knowledge, perceptions and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. Int J Pest Manag 65:1–9, https://doi.org/10.1080/09670874.2017.1423129
Letourneau DK, Ambrecht I, Rivera BS et al (2011) Does plant diversity benefit agroecosystems? a synthetic review. Ecol Appl 21:9–21. https://doi.org/10.1890/09-202
Lithourgidis AS, Dordas CA, Damalas CA, Vlachostergios DN (2011) Annual intercrops: an alternative pathway for sustainable agriculture. Aust J Crop Sci 5:396–410.
Midega CAO, Pittchar JO, Pickett JA, Hailu GW, Khan ZR (2018) A climate-adapted push-pull system effectively controls fall armyworm, Spodoptera frugiperda (J.E. Smith), in maize in east Africa. Crop Prot 105:10–15. https://doi.org/0.1016/j.cropro.2017.11.003
Mohamed SA, Wamalwa M, Obala F, Tonnang HEZ, Tefera T, et al. (2021) A deadly encounter: alien invasive Spodoptera frugiperda in Africa and indigenous natural enemy, Cotesia icipe (Hymenoptera, Braconidae). PLOS ONE 16(7): e0253122. https://doi.org/10.1371/journal.pone. 0253122
Montezano DG, Specht A, Sosa-Gómez DR et al (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr Entomol 26:286–300. https://doi.org/10.4001/003.026.0286
Murdoch WW (1975) Diversity, complexity, stability and pest control. J Appl Ecol 12:795–807. URL: http://www.jstor.org/stable/2402091
Nwanze JAC, Bob-Manuel RB, Zakka U, Kingsley-Umana EB (2021) Population dynamics of fall armyworm [(Spodoptera frugiperda) J.E. Smith] (Lepidoptera: Nuctuidae) in maize-cassava intercrop using pheromone traps in niger delta region. Bull Natl Res Cent 45:44. https://doi.org/10.1186/s42269-021-00500-6
Penaflor MFGV, Erb M, Robert CAM et al (2011) Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234:207–215. https://doi.org/10.1007/s00425-011-1409-9.
Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: Perfumes for pollinator attraction and defense. Curr Opin Plant Biolo 5:237–243. https://doi.org/10.1016/S1369-5266(02) 00251–0.
Pickett JA, Khan ZR (2016) Plant volatile-mediated signalling and its application in agriculture: successes and challenges. New Phytol 212:856–870. https://doi.org/10.1111/nph.14274.
Pinto-zevallos, DM, Strapasson P, Zarbin PHG (2016) Herbivore-induced volatile organic compounds emitted by maize: electrophysiological responses in Spodoptera frugiperda females. Phytochem Lett 16:70–74. https://doi.org/10.1016/j.phytol.2016.03.005
Quispe R, Mazón M, Rodríguez-Berrío A (2017) Do refuge plants favour natural pest control in maize crops? Insects 8:71. doi: 10.3390/insects8030071
R Core Team (2019) R: a language and environment for statistical computing.Vienna: R foundation for statistical computing.
Rahman MM, Joaty JY, Islam MM (2020) Intercropping for insect pest management in sustainable agriculture: a review. Bull Inst Trop Agric Kyushu Univ 43:11–22. http://dx.doi.org/10.11189/bita.43.11
Rembold H, Köhne AC, Schroth A (1991) Behavioral response of Heliothis armigera Hb. (Lep., Noctuidae) moths on a synthetic chickpea (Cicer arietinum L.) kairomone. J Appl Entomol 112:254–262. https://doi.org/10.1111/J.1439-0418.1991.TB01055.X
Renwick JAA (1989) Chemical ecology of oviposition in phytophagous insects. Experientia, 45:223–228.
Rojas JC, Virgen A, Cruz-López L (2003) Chemical and tactile cues influencing oviposition of a generalist moth, Spodoptera frugiperda (Lepidoptera: Noctuidae). Environ Entomol 32:1386–1392. https://doi.org/10.1603/0046-225X-32.6.1386
Rwomushana I, Bateman M, Beale T et al (2018) Fall armyworm: impacts and implications for Africa evidence. OutLook Pest Manag 28:18–19. https://www.invasive-species.org/Uploads/Invasive-Species/FAW Evidence Note October 2018.
Saxena KN, Goyal S (1978) Host-plant relations of the citrus butterfly Papilio demoleus L.: orientational and ovipositional responses. Entomol Exp Appl 24:1–10. https://doi.org/10.1111/J.1570-7458.1978. TB02750.X.
Sekamatte BM, Ogenga-latigo M, Russell-smith A (2003) Effects of maize – legume intercrops on termite damage to maize, activity of predatory ants and maize yields in Uganda. Crop Prot 22:87–93. ttps://doi.org/10.1016/S0261-2194(02)00115-1
Seni A (2018) Role of intercropping practices in farming system for insect pest management. Acta Sci Agric 2:8–11.
Signoretti AGC, Peñaflor MFGV, Bento JMS (2012) Fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), female moths Respond to herbivore-induced corn volatiles. Neotrop Entomol 41:22–26. https://doi.org/10.1007/s13744-011-0003-y
Sisay B, Sevgan S, Weldon CW, Kruger K, Torto B, Tamiru A (2022) Responses of the fall armyworm (Spodoptera frugiperda) to different host plants: Implications for its management strategy. Pest Manag Sci. https://doi.org/10.1002/ps.7255. Epub ahead of print. PMID: 36301535
Smith HA, McSorley R (2000) Intercropping and pest management: a review of major concepts. Am Entomol 46:154–161. https://doi.org/10.1093/ae/46.3.154
Sobhy IS, Tamiru A, Morales CX et al (2022) Bioactive volatiles from push-pull companion crops repel fall armyworm and attract its parasitoids. Front Ecol Evol 10:1–16. https://doi.org/10.3389/fevo. 2022.883020
Sujayanand GK, Sharma RK, Shankarganesh K, Saha S, Tomar RS (2015) Crop diversification for sustainable insect pest management in eggplant (Solanales: Solanaceae). Fla Entomol 98:305–314. https://doi.org/10.1653/024.098.0149.
Tamiru A, Bruce TJA, Woodcock CM et al (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14: 1075–1083. https://doi.org/10.1111/j.1461-0248.2011.01674.x.
Tamiru A, Bruce TJA, Woodcock CM, Birkett MA, Midega CAO, Pickett JA & Khan ZR (2015). Chemical cues modulating electrophysiological and behavioral responses in the parasitic wasp Cotesia sesamiae. Can. J. Zool. 93: 281–287.
Tamiru A, Khan ZR (2017) Volatile semiochemical mediated plant Defense in cereals: a novel strategy for crop protection. Agronomy 7:1–8. https://doi.org/10.3390/agronomy7030058.
Tanyi CB, Nkongho NR, Okolle JN, Tening AS, Ngosong C (2020) Effect of intercropping beans with maize and botanicaleExtract on fall armyworm (Spodoptera frugiperda) infestation. Int J Agron 4618190:1–7. https://doi.org/10.1155/2020/4618190
Thayamini HS, Brintha I (2010) Review on maize based intercropping. J Agron 9:135–145.
Udayakumar A, Shivalingaswamy TM, Bakthavatsalam N (2021) Legume-based intercropping for the management of fall armyworm, Spodoptera frugiperda in maize. J Plant Dis Prot 128:775–779. https://doi.org/10.1007/s41348-020-00401-2.
War AR, Paulraj MG, Ahmad T et al (2012) Mechanisms of plant defense against insect herbivores. Plant signal behav 7:1306–1320. https://doi.org/10.4161/psb.21663.
Webster B, Cardé RT (2017) Use of habitat odour by host-seeking insects. Biol Rev 92:1241–1249. https://doi.org/10.1111/brv.12281.
Willey RW, Natarajan M, Reddy MS, Rao MR, Nambiar PTC, Kannaiyan, J Bhatnagar, VS (1983) Intercropping studies with annual crops. In: better crops for food, Ciba Foundation Symposium 97, 14–16, Pitman, London,UK.
Wyckhuys KAG, O’Neil RJ (2006) Population dynamics of Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) and associated arthropod natural enemies in Honduran subsistence maize. Crop Prot. 25:1180–90.
Xu H, Turlings TCJ (2018) Plant volatiles as mate-finding cues for insects. Trends Plant Sci 23:100–111. https://doi.org/10.1016/j.tplants.2017.11.004.

No competing interests reported.

Download PDF

Version 1

posted

You are reading this latest preprint version

Companion crops alter olfactory responses of the fall armyworm (Spodoptera frugiperda), and its larval endoparasitoid (Cotesia icipe)

Status:

Version 1

Abstract

Figures

Key Message

Introduction

Materials And Methods

Plants

Insects

Oviposition bioassay

Wind tunnel bioassay

Olfactometer bioassay

Collection of volatiles

Analyses of volatiles

Chemicals

Statistical analyses

Results

Responses of FAW in oviposition assays

Responses of FAW in wind tunnel assays

Analyses of volatiles

Discussion

Declarations

Ethical Approval

References

Additional Declarations

Status:

Version 1