Transition challenge to organic agriculture: A course for advancing belowground insect pest management

Applied Soil Ecology 148 (2020) 103476

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Transition challenge to organic agriculture: A course for advancing belowground insect pest management

T

Innocent Nyamwasaa,b,c,1, Shuai Zhanga,1, Xiulian Sunb, Jiao Yina, Xiaofeng Lia, Jinhui Qina, ⁎ Jin-qiao Lia, Kebin Lia, a

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China c University of Chinese Academy of Sciences, Beijing 100049, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Soil insect pests Decomposing organic matter Interaction Soil organic volatiles

The global movement towards organic agriculture has aroused much criticism about its production performance. Despite efforts to prevent risks of food shortage, the negative role of soil insect pests has been marginalized, although these pests cause unmanageable crop losses. The aim of this study, therefore, is to corroborate the role played by organic inputs in soil pest attraction under field crop conditions and to identify the potential factors involved for potential use as bait for trapping soil pests. Laboratory experiments, field-cage tests and field investigations were undertaken in this study in addition to olfactory bioassay tests of the dominant soil, leaf litter, crop residue and cow dung manure volatiles likely to be involved in ovipositional site selection or shelter. The results showed that decomposing cow dung manure attracts more Holotrichia oblita during oviposition than the other treatments considered, and the associated volatile p-cresol was the best attractant. The results draw attention to the negative effect resulting from the application of decomposing organic matter and suggest a mixture including p-cresol, butanoic acid and indole as a promising alternative approach for soil insect pest control.

1. Introduction With the current boom in organic agriculture around the world (Lernoud and Wille, 2018) and limited areas occupied by agriculture globally (38%), there is a need to optimize agricultural productivity given the escalating global population pressure (Reganold and Wachter, 2016). A number of studies have indicated that organic farming offers a promising hope to address the aftermath of the agricultural green revolution by ensuring agriculture sustainability (Lamine and Bellon, 2009; Batáry et al., 2017). However, organic practices have suffered from low productivity, with the vested interest of a few agricultural corporations controlling the fate of food and farming (Agropoly, 2013; Schram et al., 2018 and references therein). Despite such examples of divided opinions regarding the pros and cons of the new farming system, the possible detrimental side effects resulting from interactions between organic inputs and ecosystem problems, such as soil insect crop pests, remain poorly studied, particularly due to difficulties in belowground soil insect pest sampling and monitoring (Nyamwasa et al., 2017, 2018). For instance, Potter et al. (1996) reported a higher

infestation of grubs of the green June beetle, Cotinis nitida, in plots treated with cow dung manure than in controls in a study with three tested pests. A similar result could occur among organic field crops as a result of the negative interaction between root crop insect pests and organic inputs (Mulder, 2015). For example, throughout 2014 and 2015, we recorded crop damage caused by soil insect pest (white grub) outbreaks at a high population density (60 grubs/m2) in various vegetable crop fields, resulting in near-total yield losses, and found that piles of cow dung manure scattered in rural areas as well as a heavy reliance on applying cow dung manure were two of the anecdotal reasons behind the outbreak (Nyamwasa et al., 2017). This may hold true because throughout our investigation, most white grubs were collected from organic-rich soils (Nyamwasa, pers. comm.), typically reported as a suitable location for Anomala sp. (Nyamwasa et al., 2018). Furthermore, mulching with organic matter is speculated to promote soil insect pest proliferation among crops requiring such practices, such as bananas in plantations (Viswanath, 1976; Gold et al., 2001), and it has been observed that mulch hosts larvae of the green June beetle (Merchant et al., 2016). Unlike the limited research regarding soil

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Corresponding author. E-mail address: [email protected] (K. Li). 1 These authors contributed equally to this work and are co-first authors. https://doi.org/10.1016/j.apsoil.2019.103476 Received 12 August 2019; Received in revised form 12 December 2019; Accepted 22 December 2019 Available online 13 January 2020 0929-1393/ © 2019 Elsevier B.V. All rights reserved.

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literature and those emitted from plant roots and rhizomes, such as the CO2 product of root respiration believed to facilitate larvae during the location of plant roots, were also included.

insect crop losses (Nyamwasa et al., 2018), loss data have prompted large-scale investigations regarding the proliferation of soil-borne diseases under organic farming. For instance, a survey conducted in seven European countries revealed that soil crop diseases such as late blight and black scurf inflict severe crop yield loss in organic agriculture (Finckh et al., 2006). The paucity of studies regarding soil insect pests is equally reflected in the studies of ecological cues mediating soil-dwelling pests, crops and organic matter inputs. Throughout different developmental stages, insects use a spectrum of ecological cues to locate their mates, food sources and oviposition sites (Field et al., 2000). Such oviposition cues are crucial for females in selecting suitable sites for later offspring development (Zsofia and Rufus, 2005). In this respect, soil volatiles and plant root exudates are often viewed through the lens of factors that likely facilitate this selection process, given that female soil-dwelling insects lay eggs in the soil. For example, various studies have shown that soil volatile organic compounds (VOCs) are important in the communication among diverse types of organisms inhabiting the soil, such as bacteria, plants and plant roots (Blom et al., 2011; Hung et al., 2013). All these reports suggest that soil VOCs are of great ecological and agronomic interest and call for advancing our knowledge, particularly with regard to the soil of agroecosystems. Although studies have identified key volatiles dominating belowground VOCs (Potard et al., 2017; Gray et al., 2010) emitted from the soil and their components, including volatiles emitted from decomposing organic matter, we still have poor insight into the interaction between soil VOCs and belowground insect crop pests. Such insight into mediating factors could likely be used for oviposition interference to achieve soil insect pest control. The gap to fill may be aggravated by the fact that VOC evaporation from plant litter/crop residues or soil solutions (Warneke et al., 1999; Gray et al., 2010; Greenberg et al., 2012) may synchronically intensify with the onset of soil insect pest emergence through the typical burst of VOCs from dry soils after rain (Greenberg et al., 2012; Peñuelas et al., 2014). In cold-temperate climates, for instance, the emergence of major crop-devastating soil pests, such as Holotrichia oblita, Holotrichia parallela, and Anomala corpulenta (Toepfer et al., 2014), is synchronized with the beginning of the rainy season and the crop growing period, which are characterized by the alternation of rainfall and sunlight, stimulating volatile emissions. Similar patterns have been observed in tropical countries. Belowground insect crop pest emergence and damage in Rwanda, for instance, have been observed throughout both short and long rainy seasons (Nyamwasa et al., 2017), which occur after crops have been planted. With this in mind, therefore, the present study seeks to explore the relative attractiveness of organic inputs and possible mediating factors (organic volatiles) involved during the oviposition of crop insect pests, and crop preference tests were also included to determine crop contribution to attractiveness given the importance of pest host specificity. The study also attempts to test the best attractants under field settings for the purpose of belowground pest control. H. oblita, a devastating pest of peanut crops whose larvae cause yield reductions of between 20 and 30% (Guo et al., 2016), was used in this study.

2.2. Insect collection and rearing Specimens of H. oblita beetles were collected from Cangzhou, Hebei Province, and Hefei, Anhui Province, China, in late April through midMay in 2018 and 2019. According to daily nocturnal monitoring beginning in early April, the beetles were collected before mating in this area between 19:00 and 22:00. Adults were reared in plastic boxes (45 cm × 26 cm) with leaves of Chinese Ulmus pumila L. at approximately 20% RH with light watering before the oviposition experiments. 2.3. Crop and organic manure preference tests in Plexiglas arenas The aim of these tests was to determine the possible attractiveness of partly decomposed and fully decomposed organic inputs and whether crops may have some influence on this attractiveness. The bioassays were conducted in an improved version of the Plexiglas arenas developed by Zsofia and Rufus (2005) (internal size 80 cm × 80 cm × 60 cm, with a circular window of 20 cm diameter). The crop bioassay comprised pots (height 12 cm, diameter 20 cm) planted with peanut, soybean, and potato plants four weeks after planting and included controls. The soil used was collected from the top 5 cm of the soil profile in cultivable fields without organic input for 2 years. Sixteen replicates, with each Plexiglas arena considered a replicate, were applied in the crop test. Four treatment pots of similar size were inserted into 4 holes in Styrofoam, flush with the surface of the Styrofoam. At approximately 19:00, 25 beetle pairs were released in the centre of the arenas containing randomized treatments (peanuts, soybean and maize) and fed on a daily basis with elm tree leaves. The organic input-based test was a three-choice oviposition bioassay in which animal-derived and plant-derived inputs were evaluated separately. The treatments included decomposing organic matter (a mixture of maize residues and shrub leaf litter (Platanus acerifolia), a common source of organic input in rural areas of China), completely decomposed plant-based organic fertilizers purchased from a local company (Chinese Academy of Agricultural Sciences and Peking Qigao Biotechnology Co. Ltd.), and a control (a pot with bare soil), whereas the animal-derived treatments comprised completely decomposed cow manure purchased at Chunfang Co. Ltd. (Hebei Province), cow manure partly decomposed for 3 months under conditions requiring 5 months for complete decomposition, and bare soil as a control. Overall, the experiment included 26 replicates, for a total of 78 pots, and each Plexiglas arena represented a replicate. All organic inputs were applied by top-dressing at a rate equivalent to 10 t/ha (Adediran et al., 2005) except for the decomposing mixture of crop residues and leaf litter, which was applied with uniform soil surface coverage (78.5 g = ~1.5 cm of thickness). Before application, the organic inputs were dried and later watered to stimulate the release of VOCs. The aim of the ultimate application rate was to reflect the possible influence of soil pest attraction resulting from the complete coverage of the soil with mulch, which is commonly applied in tomato fields, in banana and coffee plantations and for weed management (FAO, 2014a, 2014b; Schonbeck, 2012). The bioassay was performed for a period of 10 days in an environmental chamber at 25 °C, with hand watering of all treatments to maintain a similar moisture level; thereafter, the pots were removed to record the number of eggs per treatment and to measure the soil moisture contents and temperature. Moreover, fifteen replicates were implemented to evaluate the effect of the difference in soil moisture in the upper region (two-thirds of the pot height from the soil surface) and lower region (one-third of the pot height from the bottom) of the pot on the vertical distribution of females, males and eggs.

2. Materials and methods 2.1. Literature review An extensive literature review was conducted by exclusively searching for the most often-cited key soil volatiles. A total of 47 VOCs (Table 1) were considered for testing of their possible influences on soil insect pest attraction. These include VOCs from leaf litter, fertilized fields, crop residues, and animal organic inputs. Moreover, given the limited number of studies exploring volatiles emitted from crop residue inputs, we deliberately included some potential VOCs trapped in our laboratory with solid-phase microextraction (SPME) (Nyamwasa, unpublished data). Volatiles considered as standards (Table 1) in the 2

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Table. 1 Key volatiles emitted from different sources, including soil, plants and animal manures. Compound

Origin

Type of plant/animal/soil/volatile

References

Geosmin n-Hexane p-Cymene 3-Carene Hexanal Ethanol beta-Phellandrene Camphene alpha-Pinene Methanol

Soil Plant Plant Plant Plant Plant/soil Plant Plant Plant Plant/soil

Characteristic soil odour Leaf litter from various plants Leaf litter from various plants Needle litter Barley roots Wheat straw, soil and pig manure Needle litter Soil and litter samples from a diverse array of ecosystem types Litter from a wide range of plant species bare agricultural soil

Acetaldehyde

Leaf litter from various plants, pig manure and soil

Acetone Formaldehyde

Plant/soil/ animal Soil/animal Soil

Squalene

Soil

2- Methyl isoborneol CO2 1-Hexanol Acetic acid Formic acid Humulene Limonene Myrcene Caryophyllene o-Xylene or p-Xylene Methyl salicylate Estragole Linalool Hexanoic acid

Soil Plant Plant/soil Soil Soil/animal Plant roots Plant/soil Plant roots Plant/soil Plant/soil Plant Plant Plant Plant

Decanal 2-Butanone Butanoic acid Undecane 3-Methylindole Indole p-Cresol Dodecane Geraniol (z)-3-Hexen-1-ol Heptane Octane Eugenol Decane Skatole Nonanal Tridecane Hexadecanoic acid cis-3-Hexenyl acetate

Plant Animal Animal Plant Animal Animal Animal Plant Plant Plant Plant Plant Plant Plant Animal Plant Plant Plant/Animal Plant

Long-term application of organic, inorganic and organic-inorganic mixed fertilizers Soil/soil amended with cow dung manure Plant root respiration Plant litter/soil/wheat and maize residues Organically amended soil Plant litter, pig manure and soil Pinus roots, pine and spruce leaf litter Soil and litter samples from a diverse array of ecosystem types Pinus roots, pine and spruce leaf litter Maize root exudate Soil and litter samples from a diverse array of ecosystem types Plant roots and rhizomes Wheat, maize crop residues and elm tree litter Wheat, maize crop residues and elm tree litter Wheat, maize crop residues, elm tree litter and main component of D. flava and E. montana flower smell Wheat, maize crop residues and elm tree litter Cow dung Various animal manures Various types of plant leaf litter Pig manure Cow dung manure Cow dung and poultry manure Various types of plant leaf litter Standard plant volatile Standard leaf alcohol volatile Leaf litter from various plants Leaf litter from various plants Standard plant volatile Leaf litter from various plants Cow dung and poultry manure Wheat, maize crop residues and elm tree litter Leaf litter from various plants Organic, inorganic fertilizers Various plants/standard

Schulz & Dickschat, 2007; Peñuelas et al., 2014 Isidorov and Jdanova, 2002 Greenberg et al., 2012; Isidorov and Jdanova, 2002 Greenberg et al., 2012 Gfeller et al., 2013 Zhao et al., 2016; Potard et al., 2017 Greenberg et al., 2012 Greenberg et al., 2012; Leff and Fierer, 2008 Greenberg et al., 2012; Isidorov and Jdanova, 2002 Greenberg et al., 2012; Potard et al., 2017; Gray et al., 2010 and Bachy et al., 2018 Greenberg et al., 2012; Bachy et al., 2018 and Zhao et al., 2016 Greenberg et al., 2012; Potard et al., 2017; Zhao et al., 2016 Gray et al., 2010; Potard et al., 2017; Veres et al., 2014; Mancuso et al., 2015 Raza et al., 2017

Plant litter, pig manure and soil Plant litter, pig manure and soil

2.4. Crop and organic manure field-cage experiments and field investigation

Nyamwasa, unpublished data, Schulz & Dickschat, 2007 Johnson and Gregory, 2006 Nyamwasa, unpublished; Potard et al., 2017 Potard et al., 2017 Potard et al., 2017 Lin et al., 2007 and Isidorov et al., 2010 Leff and Fierer, 2008 and Lin et al., 2007; Lin et al., 2007 and Isidorov et al., 2010 Rasmann et al., 2005 Leff and Fierer, 2008 Van Schie et al., 2007 Nyamwasa, unpublished data Nyamwasa, unpublished data Nyamwasa, unpublished data; Jürgens et al., 2006 Nyamwasa, unpublished data Wurmitzer et al., 2017 Wurmitzer et al., 2017; Yasuhara, 1987 Isidorov and Jdanova, 2002 Powers et al., 1999 Wurmitzer et al., 2017 Aii et al., 1980; Yasuhara, 1987 Isidorov and Jdanova, 2002 Metzeger, 1934; Ruther and Mayer, 2005 Ruther and Mayer, 2005 Isidorov and Jdanova, 2002 Isidorov and Jdanova, 2002 Metzeger, 1934; Ruther and Mayer, 2005 Isidorov and Jdanova, 2002 Yasuhara, 1987, Wurmitzer et al., 2017 Nyamwasa, unpublished data Isidorov and Jdanova, 2002 Raza et al., 2017 Wang et al., 2009

introduced to the cages. The plastic boxes representing the different treatments were randomly placed in holes in the ground flush with the soil surface in each of the six field cages. The holes were the same size as the boxes, and the remaining ground space was thoroughly covered with a transparent plastic cover to prevent insects from laying eggs in other areas. Fifty male and 60 female beetles were released in the centre of the boxes, and elm tree leaves were supplied on a daily basis for feeding. The females were allowed to oviposit for 10 days. Data collection followed similar procedures to those previously described. Because of the interference of the typical heavy rainfall experienced during spring and summer of 2018, which sometimes submerged the treatment boxes and rendered it difficult to record data, the trial was supplemented with a night investigation in farming areas of Hebei Province (Guangyang district) based on available empirical knowledge of H. oblita emergence. A mulched field (10 m × 48 m) with leaf litter and maize residues was investigated from 5th May to 12th May in 2018 and 24th April to 8th May in 2019. Moreover, the resulting data were

Both crop- and manure-based choice tests were conducted in eight 2 m × 2 m white square field cages to examine oviposition site preferences in H. oblita. The experiments in both settings (Plexiglas and field cages) were carried out between May and August of 2017 and 2018. Six plastic boxes (43 cm × 20 cm × 15 cm) representing various treatments similar to the Plexiglas treatments were replicated twice separately for both bioassays within each field cage. The organic fertilizer treatments were applied to the top of the soil, and the control pots contained no fertilizer. The treatments were applied at a rate similar to that in the previous setting, with the exception of the mixture of decomposing crop residues and litter, which was applied by spreading the mixture on top of the soil surface at 215 g, which covered the entire plastic box surface with equal thickness, as previously stated. The crops in the planted boxes (peanut, soybean and maize) were grown under field conditions and regularly watered before being 3

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1-hexanol, (Z)-3-hexen-1-ol and methyl salicylate at a proportion of 1:1:1) and a mixture of animal-derived volatiles (P-cresol, butanoic acid and indole at a proportion of 2:2:1). A control (unbaited trap) was set up for comparison. Butanoic acid was included because it was found to be the best attractant for H. parallela during the screening stage (Li, unpublished data). Rubber containing 200 μL of each compound was fixed horizontally, and fifteen replications were performed for each treatment. The traps were emptied daily, and captured insects were counted and sexed.

compared with data from an analysis of national soil insect pest investigations carried out in 2018. 2.5. Volatile trapping and GCMS analysis Volatile trapping exclusively targeted the presence of p-cresol and indole in the decomposing and decomposed cow manure. A 20 mL headspace vial was half-filled with each treatment before SPME. For the analysis, SPME fibres PA (white) and 50/30 μm DVB/CAR/PDMS, 85 μm CAR/PDMS, 65 μm PDMS/DVB (pink), and DVB/CAR/PDMS (gray), purchased from Supelco Co., Ltd., were connected to a GCMS autosampler (GCMS-QP2010 Plus, Shimadzu Corporation, Kyoto, Japan) and exposed to volatiles emitted from the fertilizers. The extracts were analysed as follows: through splitless injection mode, the oven temperature was held at 60 °C for 5 min, increased at 5 °C/min to 260 °C, and then held at this temperature for 3 min. The ion temperature was 250 °C, and the scanning m/z was 50–650. The resulting compounds were identified by comparison with MS libraries (NIST14 and NIST14s).

3. Data analysis Differences in organic and crop preferences were analysed using one-way analysis of variance (ANOVA), and Pearson correlations were used to detect the relationships between soil moisture and ovipositional preferences and between soil moisture and the vertical distribution of the beetles in the soil. Differences in the means of the EAG responses were evaluated with Duncan's post hoc multiple range test, whereas Student's t-test was used to detect significant differences between the control and selected volatiles in the olfactometer tests. The data analyses were performed with both SPSS (version 17.0) and R software.

2.6. Bioassay of the behavioural response of H. oblita to volatiles

4. Results

The behavioural response of H. oblita to volatiles was studied in a Ytube olfactometer (made of a main tube of 30 cm in length and 3 cm in interior diameter and two branch tubes with a length of 20 cm and positioned at 70° to each other). The bioassay included both males and females and involved the best electroantennogram (EAG) respondents, compounds bearing six carbons, and volatiles reported at high concentrations in leaf litter, crop residues or animal-derived fertilizers. A total of 25 μL of the target attractant and paraffin oil as a control were tested against each other in the two arms of the Y-tube. Corresponding amounts of the synthetic compounds were loaded in rubber placed inside the test adaptor of the Y-tube with the head turned to the source of the charcoal-filtered air (2.5 L/min). Seventy-two insects of each sex released at the base of the Y-tube were tested in two replicates for every volatile between 19:00–21:00 in a dark room.

4.1. Organic input bioassay In both of the considered settings, H. oblita oviposited in all treatments, including bare soil. While this cannot be considered a general rule, the pest displayed a preference for organic matter, particularly in field cages, in comparison to the control (Fig. 2), and there was a significant difference between all pairs of treatments (Plexiglas arena (cow manure bioassay): F2:42 = 7.75, p < .05; field cage: F4:25 = 16.1, p < .05) except between plant-based organic inputs and the control in the Plexiglas arenas (mixture of crop residues and leaf litter: F2:32 = 0.018, p > .05). Oviposition was highest in partly decomposed cow dung in both settings (Fig. 1 and Fig. 2a). In the field cages, the number of eggs in the partly decomposed cow dung was 21 times that in the control, 1.85 times that in the partly decomposed residues, double that in the completely decomposed cow dung, and approximately triple that in the completely decomposed plant-based organic fertilizer. The results from the Plexiglas setting contrasted with those from the outdoor experiment. After adjusting for the difference in egg number according to the stage of decomposition of the organic inputs, 61.6% of oviposition occurred in the decomposing organic matter, 36.41% in the decomposed organic matter and 1.95% in control pots in the field cages, whereas in the Plexiglas arenas, 40% occurred in the decomposing organic matter, 32.76% in the completely decomposed organic matter and 27.1% in the bare soil. The distribution of eggs and adults appeared to be affected by the soil moisture content (Fig. 3a, b and c). A positive correlation was detected between the number of eggs and soil moisture content (Plexiglas setting: r = 0.58, p < .01; Field-cage setting: r = 0.49, p < .01). However, adult presence was negatively correlated with moisture content (r = − 0.278, p < .01). Adults preferred less moisture content than eggs (Fig. 3c and Supplementary material Fig. A.1), with a decrease in the number of beetles as the moisture content increased. As a result, the number of adults peaked at 14 RH, whereas the number of eggs reached a maximum at 33.5 RH in the outdoor conditions and 29 RH in the Plexiglas arenas. While this pattern was not straightforward across all replicates, more than half of the replicates with decomposing plant residues had higher moisture content than those with decomposing cow manure. The beetles were generally found close to the soil surface, and approximately 90% of the eggs were found in the lower region of the pots, usually below the root zone, while 10% were found in the upper 2/3 of the pots, and the beetles rarely laid eggs near the soil line. A high number of beetles preferred to hide in either partly

2.7. Antennal response to different volatiles An EAG analysis was performed using an EAG Micromanipulator MP-15 (Syntech, Kirchzarten, Germany) following the description by Alagarmalai et al. (2009). The test included 47 VOCs, 2 mixtures of the best attractants for each sex, and 2 mixtures of the major VOCs from the leaf litter and crop residues (Mix1: methanol, acetic acid, acetone, acetaldehyde, formaldehyde, ethanol and formic acid; Mix2: acetaldehyde, acetic acid and ethanol). All of the chemicals were purchased at Sigma-Aldrich and diluted to a final concentration of 1 μg/μL. The compound that exhibited the highest responses (p-cresol) was further subjected to a dilution series in paraffin oil as follows: 1:10, 1:10−2, 1:10−3 and 1:10−4 dilution. The antennae were dissected from the head and attached to electrode holders. The EAG responses of the antennae to each chemical were recorded in triplicate, with paraffin oil as a control. After the test solution was loaded, the EAG responses were monitored and analysed with EAG-Pro software (Syntech, Kirchzarten, Germany). 2.8. Field experiment: attractiveness of animal-derived and plant-derived organic volatiles Field tests were carried out within one week of the flight peak of H. parallela in early July 2019 in Henan province (China). At this time, the target pest H. oblita had already become less active, and the critical time for oviposition under field conditions had passed (Nyamwasa, personal communication) once we obtained the preliminary screening bioassay results. A water pan trap was used in this experiment, and the treatments included the best plant-derived volatiles (a mixture composed of 4

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Fig. 1. a–b. Ovipositional preference responses of H. oblita in Plexiglas arenas. CPD: cow dung, partly decomposed; CFD: cow dung, completely decomposed; DCRL: mixture of decaying crop residues and leaf litter; DDCRL: mixture of crop residue and leaf litter, completely decomposed; CK: control. The letters above the columns indicate significance. Bars topped with the same letter are not significantly different (p < .05) according to Duncan's test.

much higher attraction towards p-cresol and indole, whose mixture also evoked higher responses (Fig. 6d). While H. oblita males showed triple the response to p-cresol in comparison to the response to the other bestperforming plant-derived volatiles towards females, H. oblita consistently showed a higher response as the concentration of p-cresol increased (Fig. 8a). Despite this discrepancy, there was a tendency for females to respond better than males across a range of chemical plantderived volatiles. Females showed a significant response to 16 volatiles, while males showed a greater preference for 3 animal-derived volatiles than females (Fig. 6). Out of the 52 volatiles tested, the ranking by Duncan's test showed that the compounds bearing six carbons and their derivatives (cis-3-hexen-1-ol, 1-hexanol, cis-hexenyl acetate and methyl salicylate) were the most attractive to females. The GCMS analysis did not show p-cresol or indole in the completely decomposed cow dung manure; these compounds were only trapped in cow dung during decomposition (Fig. 8b).

decomposed cow dung manure or completely decomposed cow dung manure (Supplementary material Fig. A.1). Across all replicates, it was found that the moisture content was higher in Plexiglas than in the field cages (Fig. 4a). The soil temperature fluctuated slightly and did not affect egg location (Fig. 4c: the lower region temperature varied between 23.5 °C and 26.1 °C, and the upper region temperature varied between 24 °C and 26.8 °C). The nocturnal investigation (Table 2) showed the presence of H. oblita and Sympiezomias velatus in the mulched field, with no presence of either of these species in nearby fields. H. oblita appears to emerge shortly after S. velatus. In total, we collected 190H. oblita and 717 S. velatus, and the abundance of the latter was 3.7 times that of H. oblita. 4.2. Crop bioassay The analysis of host-plant association with oviposition indicated that all hosts attracted H. oblita but to different extents (Plexiglas arena: F3:61 = 18.537, p < .05; field cage: F3:33 = 9.955, p < .05). Peanut was the most attractive across the different settings (Fig. 5a and b). Maize and soybean were characterized by a low association with egg presence, but there was no significant difference for either crop (Fig. 5a and b). Changing the experimental environment had little effect on the H. oblita preferences in regard to maize, soybean and the control, which validates the use of the Plexiglas setting. Clearly, the beetle produced more eggs per female under Plexiglas in the shortest time. Oviposition averaged 15 eggs/female/10 days under Plexiglas, whereas in the field cages, it averaged 5 eggs/female/10 days. Overall, peanut was the most vulnerable crop to soil insect pests (H. oblita).

4.4. Y-tube olfactometer bioassay and attractiveness of synthetic plant volatiles in field setting There were statistically significant differences among the 25 volatiles further analysed with the Y-tube olfactometer (male: F24, 25 = 5.4, p < .01; female: F24, 25 = 4.8, p < .01). Among them, H. oblita consistently showed a higher preference (t(2): 5.6, p < .05) for pcresol, whereas there was no significant difference between the remaining compounds and the control (Fig. 7). However, seven compounds significantly attracted females when they were compared to the control (1-hexanol: t(2) = 6.934, p < .05; indole t(2) = 15, p < .05; hexanal: t(2) = 8.5, p < .05; formic acid: t(2) = 8.48, p < .05; cis-3hexen-1-ol: t(2) = 11.314, p < .05; methyl salicylate: t(2) = 24, p < .05; hexanoic acid: t(2) = 5.6, p < .05), and females were marginally significantly attracted to Mix1 (t(2) = 4.24, p = .05). Sexual differences were also observed for compounds such as hexanoic acid (t(2) = −13.864, p < .05), hexanal (t(2) = −7.6, p < .05) and 1hexanol (t(2) = −9, p < .05). The field trap results are summarized in Table 3. There were

4.3. EAG responses and GCMS results The EAG responses of both sexes of H. oblita to the prominent animal manure and plant-based organic fertilizer volatiles are displayed in Fig. 6. Overall, there were significant differences in EAG responses among treatments (male: F50, 102 = 43.945, p < .05; female: treatment (F50, 102 = 26.082, p < .05). Of the 51 volatiles tested, males exhibited 5

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significant differences between treatments at α = 0.01 (F2, 42 = 21.4, p < .01). Of the two combinations tested, the mixture of animal-derived organic volatiles attracted a higher number of H. parallela than the plant-derived organic volatiles. 5. Discussion The organic matter stage of decomposition and soil moisture content were important factors during ovipositional site selection. Decomposing organic cow manure consistently received more eggs than any other stage of decomposition, and more beetles were collected from cow manure than the other treatments in both settings. This observation suggests that the strong preference was not based on random encounters with hosts. Instead, decomposing cow manure was either more easily located or accepted at a higher level than the rest of the treatments, although the moisture content played a crucial role in acceptance for oviposition (Fig. 3). The effects of soil moisture changes shown here are consistent with the findings of other studies stressing the importance of moist soil during the development and survival of the larval stages of several beetles, including Japanese beetle (Popillia japonica) Newman and the African black beetle (Heteronychus arator), whose prevalence of larvae at optimum soil moisture suggests a maternal critical requirement for oviposition (Frew et al., 2016; Abdallah et al., 2016; and Shanovich et al., 2019). The critical need for a particular level of moisture was equally underscored by Knisley et al. (2018) in a study on tiger beetles (Cicindela albissima Rumpp). In the words of the authors, tiger beetle larvae developed faster with higher survival in watered plots than in unwatered plots. In our study, we also noticed that H. oblita is strongly hygrotropic, and searches for the highest available air humidity and for liquid water were obviously related to survival in both settings. Most beetles that failed to find shelter or hide in the soil were found dead above the experimental platform after one day in the outdoor environment and after nearly 3 days in the Plexiglas arenas or alive in the liquid water that had fallen unintentionally above the platform during watering or rain. In addition to moisture content, in our study, the effect of decomposing plant-derived organic matter was not clear; however, partly decomposed organic input has been recognized elsewhere as a breeding site and source of food for other soil insect pests. Examples include the high abundance of the notorious African black beetle reported in farmyard manure (Abdallah et al., 2016), reliance on decaying organic matter by larvae of the rhinoceros beetle (Trypoxylus dichotomus)

Fig. 2. Ovipositional preference responses of H. oblita under field cage conditions.

Fig. 3. a) Correlation between ovipositional preference and soil moisture content in the outdoor setting. b) Correlation between ovipositional preference and soil moisture content in Plexiglas arenas. c) Correlation between the beetle soil location and soil moisture content in Plexiglas arenas. 6

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Fig. 4. (a) Box-and-whisker plot of the soil moisture content variability in different settings (Plexiglas and field cages). The endpoints of the whiskers represent the minimum and maximum values. (b) Box-and-whisker plot of the soil moisture in Plexiglas arenas at different soil depths. Circles indicate observations that can be considered outliers. (4) Box-and-whisker plot of the variation in soil temperature across different soil depths. The endpoints of the whiskers indicate minimum and maximum values.

(Jouquet et al., 2018). Presumably, the high pest infestation under mulched fields could be equally associated with the buffering effects of mulching against extreme soil temperatures and the ability to decrease moisture loss rates from the soil surface (Mutsamba et al., 2016), which create ideal conditions for soil insect pest proliferation. However, our results suggest that decomposing organic matter may also conserve high moisture beyond H. oblita's tolerance, thereby resulting in a lack of a significant difference between eggs oviposited in decomposing and decomposed plant-derived matter. Clearly, it is difficult to control soil insect pests because factors that promote crop development, such as soil moisture and organic input, are the same factors that facilitate the survival of soil insect pests, which is worrying given the large amounts of crop residues applied (Scheunemann et al., 2015) for soil fertility improvement. The crop bioassay clearly shows that soil insect crop preference is not random and validates the “mother knows best” theory (Johnson and Gregory, 2006; Griese et al., 2019). This is reflected by the consistently higher number of eggs laid in the peanut treatments than in the other treatments. While such preferences may vary across different species or feeding behaviours (monophagous vs. polyphagous, Hewavithana et al., 2016 and Jurenka et al., 2017), the association of the highest number of eggs with peanuts could be explained by the fact that the vulnerable harvestable crop parts (nuts) are located in the soil underground, i.e., offspring occur in the vicinity of the source of food since the females prefer to lay high numbers of eggs near the crop root system. This is more likely in some species lacking parental care (Mayhew, 2018; Gilbert and Manica, 2015), where the mother should ensure that eggs are placed in an environment in which their progeny will not only easily and readily find an adequate food supply but also feel safe. A similar oviposition pattern has been previously observed in the number of masked chafer grubs (Gyawaly et al., 2016) and banana weevils (Abera et al., 1999), while the selective tendency of H. oblita towards a particular host crop found here is highlighted at a large scale by the recent national investigation (2018) report identifying peanut as the crop mostly infested by soil insects, from which the highest loss is most likely caused by white grubs (Supplementary material Fig. A. 2). The investigation of the interactive role played by VOCs in the location of organic inputs indicated interesting H. oblita sexual differences in the context of attraction. The stronger attraction of males to animal-

Table 2 Soil insect pest infestation in the mulched field with leaf litter (Platanus acerifolia) and maize residues. Duration

5th May to 12th May 2018

24th April to 8th May 2019

Total

Collected species Holotrichia oblita

Sympiezomias velatus

64 28 10 11 13 11 11 11 – – – – – – 1 1 7 5 8 – 2 – 4 190

– – – – – – – – 97 7 9 0 67 46 8 46 86 166 120 6 16 15 28 717

(Kojima, 2015), and current claims by farmers that organic mulch applied to tomato fields for soil moisture conservation has become a safe haven for white grub crop pests (Nyamwasa, pers. comm.), which also holds true for termite-infested areas as well (Mutsamba et al., 2016). According to the author, the majority of smallholder farmers are reluctant to apply soil cover containing organic matter, believing that the negative effects of attracting termites far outweigh the benefit that may result from organic mulching. Termite are typically known to damage crops that have reached senescence without timely harvesting (Nyamwasa et al., 2018), although specialist litter feeder termites also consume applied organic matter prior to its incorporation into the soil 7

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Fig. 5. Ovipositional crop preference responses of H. oblita in field-cages (a) and plexiglas arena (b). Treatment indicated by the same letter are not significantly different at the 0.05 probability level by the Duncan's test.

which have been consistently found at the highest concentrations in different soil types (Mancuso et al., 2015), including organically amended soil, crop residue, cropland and bare soil (Zhao et al., 2016; Potard et al., 2017; Bachy et al., 2018), and ethanol and formaldehyde at moderate concentrations in soil. Compounds such as methanol elicited minor effects, yet it has not only been reported in a number of studies (Mancuso et al., 2015; Bachy et al., 2018; Potard et al., 2017) as key dead organic matter volatiles but also represents a large share of total emissions (up to 99%; Gray et al., 2010). Hexadecanoic acid and squalene exhibited the highest abundance in a field fertilized with organic and inorganic inputs (Raza et al., 2017), while among the terpenes reported by Greenberg et al. (2012), alpha and beta-pinene were the most abundant leaf litter volatiles; unfortunately, none of these evoked a substantial response in the EAG test or olfactometer screening methods. However, 1-hexanol, a compound trapped from the crop residues, evoked a high response. These results are consistent with our previous study indicating the highest binding affinity of olfactory binding proteins (HoblOBP40) for 1-hexanol (Wang et al., 2013). Moreover, the production of CO2 through root emissions has also been at the centre of many studies as a soil pest-mediating factor for various soil arthropods and nematodes (Johnson and Rasmann, 2015; Kojima, 2015; Eilersa et al., 2016; Webster and Cardé, 2017; Rondon et al., 2017 and Cooper et al., 2019), but in our study, CO2 did not elicit a significant response with the olfactometer. Nevertheless, based on the fact that it was significantly more attractive to females than males, we suggest that it may play some role in ovipositional site selection. Other VOCs suspected to be involved in suitable site selection among soil insect pests are geosmin and 2-methylisoborneol, which are characteristic sources of the musty and earthy smell emitted by cyanobacteria, myxobacteria and actinomycetes (Oh et al., 2017; Veselova et al., 2019), but neither of them significantly provoked a reaction by H. oblita.

derived volatiles than plant-derived volatiles and vice versa, such as pcresol, indole and their mixtures, could be explained by the co-evolutionary relationship between scarab beetles and the long-term use of organic manures. The naissance of organic farming in Asian countries, such as China (Reddy, 2017), where farming activities have been the mainstay of citizens for nearly 5000 years, has increased the proliferation of scarab beetles. A typical example within this family is dung beetles, which still rely on animal wastes for survival (Nyamwasa et al., 2017). The study suggests that p-cresol and indole are potential control alternatives for disruption of the mating of H. oblita with bait traps given their outperformance of cis-3-hexen-1-ol and geraniol, which are thus far considered reference attractants for some soil insect pests (Table 1). Although we did not test their attractiveness towards H. oblita under field conditions, the mixture containing p-cresol, indole and butanoic acid may be useful for H. parallela management. To the best of our knowledge, this is the first study exploring the potential utility of animal manure-derived organic volatiles for soil insect pest management. Related previous attempts have mainly focused on plant-derived organic volatiles (Table 1, Mofikoya et al., 2019). In our study, plantderived volatiles exhibited higher attractiveness towards females than males, probably because females must first locate host food plants prior to searching for suitable places for oviposition. Other genera of scarab beetles, such as Anomala sp. and Protaetia sp., were less abundant. Whether their relatively small number could be associated with the small population size available in the investigated area, the poor attractiveness of the tested volatiles or traps set up prior to their peak emergence remains an open question; however, both species are notoriously documented in China as key crop pests (Roques et al., 2015; Suo et al., 2015). The most surprising part of the results was the relatively poor responses of H. oblita to the most dominant VOC emissions from diverse sources (leaf litter, organic field crops, crop residues and soil). These include compounds such as acetaldehyde, acetone, and acetic acid,

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Fig. 6. Electroantennogram (EAG) responses of male and female H. oblita to plant volatiles. Mean ± SE (N = 47) after correction of the EAG, with paraffin oil used as the control. Significant differences among different plant volatiles were analysed with one-way analysis of variance (ANOVA) at p < .05, and multiple comparisons were performed with Duncan's test. Significant differences are marked with different letters: green letters or letter intervals for females and black letters or letter intervals for males. Stars indicate statistically significant differences between females and males (Student's t-test): p < .05. “d”: EAG responses to p-cresol and indole blend. “c”: EAG responses to the 4 best plant-derived attractants mixture (methyl salicylate, cis-3-hexenyl acetate, 1-hexanol and cis-3-hexen-1-ol). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

6. Conclusion and recommendation

CO2 in host-plant location and selection by root-feeding insects, the current study suggests that several factors are involved in host location and acceptance (edaphic abiotic factors, organic inputs and their associated volatiles). In addition, while the discrimination of host crops during oviposition offers insight regarding suitable crops to rotate, knowledge about the exact soil location for egg deposition provides insight regarding the optimization of soil pest control. Moreover, as the timing of oviposition with respect to the host phonological stage has

Clearly, the negative impact of organic inputs in regard to attracting soil-dwelling insects has been overlooked, and the current findings reveal a close association between soil-dwelling pests and decomposing organic matter for the purposes of searching for food and shelter and selecting oviposition sites. Although most studies have stressed the role of root exudates and 9

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Fig. 7. Y-tube olfactometer responses of male and female Holotrichia oblita to plant volatiles. Mean ± SE (N = 25). Significant differences among the different plant volatiles were analysed with one-way analysis of variance (ANOVA) at a significance level of p < .05 against the control. Significant differences are marked with different letters. Asterisks indicate statistically significant differences between females and males (Student's t-test): * p < .05.

manures is required to avoid unnecessary loss. Last but not least, we encourage the exploration of the identified VOCs for use in belowground pest control, particularly the newly tested animal manure volatiles.

implications for understanding yield loss (e.g., possible critical periods of attack, Nyamwasa et al., 2018), the application of organic matter should be performed bearing in mind its detrimental effects. Therefore, strategies for the proper management of crop residues left in fields should be developed, and applying completely decomposed animal

Fig. 8. Illustration of the EAG dose-dependent response of H. oblita to p-cresol (a) coupled with the GCMS chromatograph peaks illustrating the best attractants (b). 10

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Table. 3 Total number of H. parallela individuals captured in a baited trap containing animal-derived volatiles and plant-derived volatiles in a water pan. Treatment

Number of captured H. parallela

Sex

Other insects captured

A P CK

738 a 689 a 379 b

346 males and 392 females 278 males and 411 females 190 males and 189 females

10 Anomala sp., 7 Lepidoptera sp. and 3 Protaetia sp. 18 Anomala sp. and 5 Lepidoptera sp. 2 Anomala sp. and 4 Lepidoptera sp.

The “A” treatment represents the P-cresol, butanoic acid and indole mixture, whereas the “P” treatment represents the mixture containing 1-hexanol, (Z)-3-hexen-1-ol and methyl salicylate. Different lowercase letters indicate significant differences between treatments at P < .01.

Declaration of competing interest

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