Damage caused by Diceraeus (= Dichelops) melacanthus in maize plants subjected to combinations: bioinoculation and imidacloprid seed treatment

ABSTRACT

The aim of this study was to evaluate the damages caused by Diceraeus (=Dichelops) melacanthus in maize plants subjected to bioinoculation with or without imidacloprid seed treatment. In this study, five different combinations of bioinoculants and imidacloprid seed treatment were applied to maize seeds in a completely randomized design. The bioinoculants used were Azospirillum brasilense and Bradyrhizobium japonicum. From emergence, the plants were subjected to infestation with the stink bug D. melacanthus (one stink bug/plant), with permanence up to 21 days after emergence. After this period, the phytotechnical parameters (shoot and root) of the corn plants were evaluated. In general, plant height was higher when imidacloprid was applied, suggesting compatibility with bioinoculants. The chlorophyll a content was higher when bioinoculants were applied, regardless of whether imidacloprid was present. Finally, the results indicate that the bacteria A. brasilense and B. japonicum do not induce resistance to the level of D. melacanthus infestation used in the present study. Therefore, these bacteria can be used in combination with imidacloprid, allowing for greater plant height, higher chlorophyll a content, and reduced damage caused by D. melacanthus.

Keywords
resistance induction; rhizobacteria; corn pests; sucking pests; neonicotinoids

INTRODUCTION

Maize is the second most important crop in Brazil, second only to soybeans (Sidra, 2021). In the 2019/2020 harvest, Brazilian production of maize amounted to approximately 100 million tons (Sidra, 2021). Within the corn production system, new technologies have been developed to increase production and reduce costs. Recent studies have shown that the use of bioinoculants (rhizobacteria), such as Azospirillum, can reduce the demand for nitrogen fertilizers (Picazevic et al., 2017; Caires et al., 2021) and increase maize development (Hafez et al., 2021; Moreno et al., 2021; Skonieski et al., 2019).

Researchers have shown that the use of bioinoculants, in addition to replacing synthetic nitrogen, can contribute to maize defense against herbivory (Amutha et al., 2007; Prischmann-Voldseth et al., 2020; Anandh et al., 2010). For example, the inoculation of maize plants with rhizobacteria can harm the development of Diabrotica speciosa (Coleoptera: Chrysomelidae) (Santos et al., 2014) and Mythimna separata (Lepidoptera: Noctuidae) (Li et al., 2019) on maize plants. This can be attributed to the fact that the bioinoculants and stimulate the production of secondary metabolites associated with defense (Santos et al., 2014).

Currently, one of the main maize crop pests in Brazil is the stink bug Diceraeus (= Dichelops) melacanthus (Hemiptera: Pentatomidae), which causes crop losses of 20% (Cruz et al., 2016) to approximately 100% (Silva et al., 2019; 2021). The use of insecticides for seed treatment has been essential to mitigate crop damage. One class of insecticides, neonicotinoids, are effective because of their systemic translocation in plants (Silva et al., 2019), meaning they can protect maize plants shortly after emergence (usually between the first five to 10 days). Common neonicotinoids in Brazil include clothianidin, thiamethoxam, and imidacloprid (Silva et al., 2021).

In this sense, the knowledge of the compatibility between seed treatment with insecticides and bioinoculants is essential for the successful establishment of field crops. For example, it has been demonstrated that the insecticide fipronil is incompatible with Azospirillum brasilense because it negatively affects the development of the bacterial population (Santos et al., 2021). In contrast, thiamethoxam has been reported to be associated with Azospirillum in a synergic effect, showing better results of growth in roots and shoots (Battistus et al., 2014). These contrasting results highlight the need for further research to allow for a better understanding of treatment compatibility.

Finally, although there are some published studies, research that assesses the development of plants subjected to insect infestation is still scarce. Thus, to better understand the relationships in maize pest management, this study aims to evaluate the damages caused by D. melacanthus in maize plants subjected to bioinoculation with or without imidacloprid seed treatment.

MATERIAL AND METHODS

Study location

The study was conducted in a greenhouse in the municipality of Guarapuava, Paraná, Brazil. The research was conducted for a period of 21 days after emergence (DAE), which comprises the period of greatest susceptibility of corn by D. melacanthus (Silva et al., 2021). During the study period, the average, maximum, and minimum temperatures in the study environment were 25.9 °C, 37.4 °C, and 17.5 °C, respectively. The average relative humidity (RH) was 41%.

Treatments used and growing practices

The variety of maize used for the study was hybrid IPS 1706, obtained from the Division of Research in Genetic Improvement of the Instituto de Desenvolvimento Rural do Paraná (IDR-PR), located in Londrina, Paraná. Maize seeds were subjected to five treatments: A. brasilense (0.15 mL/100 seeds); coinoculation of A. brasilense (0.15 mL/100 seeds) + Bradyrhizobium japonicum (0.16 mL/100 seeds); imidacloprid seed treatment (ST; 0.07 mL /100 seeds); A. brasilense (0.15 mL/100 seeds) + ST; and coinoculation + ST. The control consisted of seeds with neither bioinoculant nor ST.

The maize was sown on March 8, 2019, in 3 L pots filled with Latosol Bruno dystrophic soil. Five seeds were planted in each pot; however, after emergence, only two plants per pot were kept. To avoid water stress, the soil moisture was checked daily, and the plants were watered when necessary. During the study, no phytosanitary management was performed on the plants.

Stink bug origin and plant infestation details

The insects were obtained from the Entomology Laboratory of the IDR-PR, where they had been raised under controlled temperature (25 ± 2 °C), and moisture (60 ± 20%) conditions. The stink bugs were fed peanuts, snap beans, soybeans, and privet.

The infestation of corn plants occurred at development stage V1 (first expanded leaf) (Magalhães & Durães, 2006), and lasted 15 days (adapted from Bridi et al., 2016). This time interval is when maize is higly susceptive to stink bug damage (Silva et al., 2019). For the plant infestation, two unsexed adult insects were used per sample unit (pot), corresponding to one insect/plant.

To prevent the insects from escaping, the pots were adapted to be in the form of “cages” (40 x 20 cm in height and width, respectively) and covered with voile. The insects were monitored daily, and dead individuals were replaced (Bridi et al., 2016).

Evaluation of leaf damage

The damage to the maize plants was evaluated by adapting the scale described by Roza-Gomes et al. (2011): 1) no damage; 2) leaves with small punctuations, plants with no size reduction; 3) injured whorl (partially twisted), plant with size reduction; 4) twisted whorl or “suckering” plants (plants with tillers from the base); and 5) dead whorl.

Evaluation of plant phytotechnical parameters

After subjecting the plants to D. melacanthus infestation, the following phytechnical parameters were measured: plant height, chlorophyll a and b content, fresh weight (shoot and root), and dry mass (shoot and root). All evaluations took place at 21 DAE, except for plant height, which was assessed six days prior (15 DAE).

Plant height was measured with a ruler positioned vertically at the base of the maize stalk. Chlorophyll a and b contents were measured using an electronic chlorophyll meter (Falker ClorofiLog®, Model CFL1030). The readings were taken on the two plants grown in each pot (n = 20) by placing the device in the middle third of the expanded leaf.

The fresh mass of the aerial parts of all plants (n = 20) were evaluated. Immediately thereafter, the plants were removed from the pot. The aerial parts were sectioned and placed in a paper bag. The material was then sent to the laboratory, where it was weighed using an analytical scale.

All seedlings were harvested at the end of the treatment and were separated into aerial part and roots. In laboratory, the samples were weighed for the determination of fresh weight. Then, the sample was oven-dried to a constant weight at 80 °C, and the dry weight was then measured.

Statistical analysis

The data were initially subjected to normality (Shapiro & Wilk, 1965) and homogeneity of variance (Burr & Foster, 1972) tests to verify whether they met the assumptions of parametric statistics. An analysis of variance (ANOVA) was performed, followed by Tukey's test. The difference was considered significant when p ≤ 0.05 (SAS Institute, 2001).

RESULTS

Leaf damage

In general, less leaf damage was observed in the maize plants that had been treated with imidacloprid, demonstrating compatibility with bioinoculants (Figure 1). Leaf damage similar to that of the control was observed in maize plants that had been treated with bioinoculants but without imidacloprid (Figure 1).

Figure 1
Leaf damage (mean ± SE) caused by Diceraeus melacanthus on maize plants (at 21 DAE) submitted to different treatments. Damage score adapted from Roza-Gomes et al. (2011).

Plant height and chlorophyll content

Imidacloprid seed treatment, both with and without bioinoculants, resulted in higher plant height, especially at 21 DAE (Table 1). In general, the lowest chlorophyll a content was observed in the control plants. The plants with imidacloprid seed treatment and the control plants had similar chlorophyll b levels, which were lower than those of the plants with bioinoculant treatment (Table 1).

Table 1
Development parameters of corn seedlings (mean ± SE) subjected to infestation (n = 1 stink bug/plant) of Diceraeus melacanthus in a greenhouse.

Treatment	Phytotechnical parameters
	Plant height (15 DAE)	Plant height (21 DAE)	Chlorophyll a	Chlorophyll b
Control	12.9 ± 0.32 b	20.66 ± 0.76 b	13.81 ± 1.01 b	2.98 ± 0.14 b
Azospirillum	13.42 ± 0.63 b	19.92 ± 1.03 b	16.63 ± 0.63 a	3.27 ± 0.11 ab
Coinoculation	13.57 ± 0.68 b	23.31 ± 1.18 ab	15.11 ± 0.66 a	3.26 ± 0.06 ab
ST	15.87 ± 0.49 a	26.86 ± 0.41 a	14.74 ± 0.81 ab	2.875 ± 0.16 b
ST + Azospirillum	14.85 ± 0.42 ab	25.67 ± 0.44 a	15.96 ± 0.75 a	3.16 ± 0.10 ab
ST + coinoculation	14.32 ± 0.39 ab	26.56 ± 0.69 a	16.66 ± 0.71 a	3.52 ± 0.11 a
CV (%)	11.96	11.29	16.7	12.62
F	4.12	12.6	1.91	3.28
DF error	54	54	54	54
P	< 0.01	< 0.01	n.s	< 0.05

• Means ± SEM followed by the same letter in the column do not differ by Tukey test (5% probability). ns = non significant P. ST = seed treatment with imidacloprid; Coinoculation = Azospirillum + Bradyrhizobium.

Mass (fresh and dry) of the aerial part and root system

In general, the data did not show a clear relationship between plant mass (both fresh and dry) with seed treatment or bioinoculation (alone or combined) (Table 2). Neither the imidacloprid seed treatment nor the bioinoculation appeared to affect the root system (Table 2). For example, though the combination of seed treatment with coinoculation resulted in a greater fresh mass, the highest dry mass was observed for imidacloprid treatment with or without A. brasiliense (Table 2).

Table 2
Mass evaluation (mean ± SE) of shoot and root system of maize plants subjected to infestation (n = 1 bug/plant) of Diceraeus melacanthus in a greenhouse.

Treatment	Phytotechnical parameters
	Fresh aerial mass	Dry mass of aerial part	Fresh root mass	Dry root mass
Control	0.80 ± 0.05 ab	0.12 ± 0.01 ab	1.22 ± 0.1 b	0.30 ± 0.0 c
Azospirillum	0.71 ± 0.03 b	0.11 ± 0.01 b	1.27 ± 0.1 b	0.32 ± 0.0 bc
Coinoculation	0.79 ± 0.05 ab	0.13 ± 0.01 ab	1.25 ± 0.1 b	0.26 ± 0.0 c
ST	0.89 ± 0.04 ab	0.14 ± 0.0 ab	1.17 ± 0.1 b	0.40 ± 0.0 a
ST + Azospirillum	0.80 ± 0.04 ab	0.15 ± 0.01 a	1.06 ± 0.0 b	0.38 ± 0.0 ab
ST + coinoculation	0.95 ± 0.05 a	0.13 ± 0.01 ab	1.64 ± 0.1 a	0.35 ± 0.0 b
CV (%)	18.9	18.52	21.17	17.23
F	3.26	3.09	5.46	9.35
DF error	54	54	54	54
P	< 0.05	< 0.05	< 0.01	< 0.01

• Means ± SEM followed by the same letter in the column do not differ by Tukey test (5% probability). ST = seed treatment with imidacloprid; Coinoculation = Azospirillum + Bradyrhizobium.

DISCUSSION

In general, bioinoculation with A. brasiliensis and B. japonicum and imidacloprid seed treatment improved the chlorophyll a content in maize plants, even under pest infestation conditions. This result suggests that the bioinoculation increased the photosynthetic capacity of plants even under stress conditions, demonstrating the potential importance of bioinoculants in the physiology of corn. Interestingly, the same was observed for bioinoculated seeds treated with imidacloprid, suggesting the compatibility of nitrogen-fixing bacteria with the insecticide.

Leaf damage

It has been previously reported that bioinoculants can promote resistance induction against some pests. For example, incorporation of Azospirillum in soil has been shown to repel Antigastra catalaunalis (Lepidoptera: Crambidae) in sesame (Sesamum indicum) (Anandh et al., 2010). Interestingly, Azospirillum can also harm the development of some corn pests, such as the caterpillar Mythimna sequax (Li et al., 2019) and the D. speciosa (Coleoptera: Chrysomelidae) (Santos et al., 2014). The bioinoculation of the maize in this study does not appear to have had a harmful effect on stink bugs (longevity around 6 d), which explains the greater damage to plants in the absence of seed treatment. However, laboratory studies that assess insect biology may provide a better understanding of the relationship between bioinoculants and pests.

These results demonstrate that the relationship between bioinoculants and pests is still unknown; however, to date, this is the first study of bioinoculants carried out in association with D. melacanthus. Additionally, the pest population density used in the present study (one stink bug/plant) was high (Silva et al., 2021), which probably impaired the development of the plants. Thus, the use of a lower D. melacanthus population density could result in different outcomes.

Finally, the importance of studies examining other insecticides should be considered to gain a greater understanding of the relationship among bacteria, plants, and insects. For example, maize seeds inoculated with Bacillus subtilis show increased protection against sucking pests because the bacteria increase the absorption of the neonicotinoid thiamethoxam (Myresiotis et al., 2015). Similarly, Azospirillum can be recommended in association with a lower dose of thiamethoxam (Battistus et al., 2014). Conversely, A. brasilense is incompatible with the insecticide fipronil (Santos et al., 2020), which reduces the bacterial population and impairs biological nitrogen fixation. Thus, it is important to know the relationship between the bioinoculant and the insecticide to avoid decreased bioinoculant efficiency. In addition, further field studies are needed to explore the impact of bioinoculants and insecticides on plant development and pest damage to ultimately be able to provide recommendations to farmers.

Plant height and chlorophyll content

The seed bioinoculation combined with imidacloprid resulted in greater plant height. This observation suggests the compatibility of rhizobacteria with the insecticide, as both can help support better initial plant development. The relationship between neonicotinoids and increased initial plant growth has previously been reported in the literature (Preetha & Stanley, 2012). Additionally, the low amount of damage caused to the plants that received the imidacloprid seed treatment probably allowed for better initial development of the aerial parts of the plants. The plants that received the imidacloprid seed treatment, whether alone or in combination with bioinoculants, were observed to have 100% stink bug mortality within 48 h after infestation (data not shown), indicating the efficiency of the insecticide. This suggests that these bioinoculants and imidacloprid can be combined for D. melacanthus management without loss of insecticide efficiency. An important observation was the higher content of chlorophyll a, indicating greater photosynthetic capacity, in the plants that received bioinoculation. Chlorophyll content can be an indication of plant resistance to pest infestation (Melo et al., 2018), as feeding insects generally reduce this component (Golan et al., 2015; Joseph & Jespersen, 2021). Thus, this study demonstrates for the first time that bioinoculation of maize with A. brasilense and B. japonicum, whether combined with imidacloprid or not, can help to mitigate photosynthetic damage caused by pests. In contrast, those plants treated with imidacloprid alone had a chlorophyll content similar to that of the control plants, indicating two possibilities: 1) neonicotinoids do not directly influence chlorophyll content (Preetha & Stanley, 2012); or 2) there is compatibility between rhizobacteria and imidacloprid (with the dose used in the present study).

Mass (fresh and dry) of the aerial part and root system

The results for fresh and dry masses of the maize plants were variable. This inconsistency has already been observed in other studies on corn (Marques et al., 2020) and may be explained by the genetic material (hybrid) used (Muller et al., 2021). Additionally, Bashan and Dubrovsky (1996) observed that bioinoculants have a greater influence on shoot parameters than on the root system. Thus, two hypotheses can be considered: 1) the hybrid used in this study does not benefit from its root system, and 2) the high stink bug population density did not allow for better root development in plants inoculated without the insecticide. Further research is needed for both hypotheses.

The present study demonstrates that bioinoculants can be used concurrently with imidacloprid maize seed treatment. In Brazil, there is a growing use of rhizobacteria by farmers in maize crops (Santos et al., 2021), highlighting the importance of research on the subject. This study demonstrates that the use of imidacloprid seed treatment does not negatively affect the action of the bioinoculants. Thus, maize farmers will be able to use both treatments in combination to improve plant performance and protect against D. melacanthus.

Additional research should be conducted to better understand the compatibility of different doses and strains of bioinoculants and insecticides. This research could include compatibility studies, for example, laboratory observation of the survival rate of the maize rhizobacteria with different insecticides.

CONCLUSIONS

Maize seeds bioinoculated with A. brasilense and B. japonicum, either with or without imidacloprid, did not allow decrease the chlorophyll a content of plants subjected to infestation of D. melacanthus. In addition, we conclude that the use of rhizobacteria combined with imidacloprid seed treatment can improve maize plant development and reduce the damage caused by D. melacanthus.

ACKNOWLEDGEMENTS, FINANCIAL SUPPORT, AND FULL DISCLOSURE

The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support. The authors declare that there are no conflicts of interest regarding the publication of this work.

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Publication Dates

• Publication in this collection
  09 Jan 2023
• Date of issue
  Nov-Dec 2022

History

• Received
  14 Sept 2021
• Accepted
  24 Feb 2022