Introduction
Chickpeas (Cicer arietinum L.) are the second most consumed member of the Fabaceae family after soybeans (Glycine max) (Nascimento et al., Reference Nascimento, Silva, Artiaga, Suinaga and Nascimento2016). This crop is an important source of protein for humans, especially in developing countries of the Indian subcontinent, West Asia, North and East Africa, southwest Europe, and central America (Braga and Vieira, Reference Braga and Vieira1998; Kaur and Prasad, Reference Kaur and Prasad2021).
Although chickpeas are grown in more than 50 countries and cover 17.8 million hectares, the largest producers are India, Turkey, and Pakistan (FAO STAT, 2016). The planted area in Brazil is small, with yields of 2000 tons year−1; however, production is increasing significantly given favorable conditions such as the climate and its potential as an interim crop (safrinha) (Nascimento et al., Reference Nascimento, Silva, Artiaga, Suinaga and Nascimento2016).
Insects, especially their larvae, can significantly reduce chickpea yields. Crop damage occurs during the vegetative and reproductive phases. Average chickpea losses vary from 30 to 40% but may reach 100% of yield (Patanker et al., Reference Patanker, Giri, Harsulkar, Sainari, Deshpade, Ranjekar and Gupta2001; Wakil et al., Reference Wakil, Ashfaq, Ghazanfar, Afzal and Riasat2009). Spodoptera frugiperda (JE Smith) is a polyphagous species that is native to tropical regions of the Americas but that has been spreading rapidly to other areas such as various countries in Africa (Goergen et al., Reference Goergen, Kumar, Sankung, Togola and Tamo2016), India (Mallapur et al., Reference Mallapur, Naik, Hagari, Prabhu and Patil2018), and China (Jing et al., Reference Jing, Guo, Jiang, Zhao, Sethi, He and Wang2020).
In Brazil, this species is an important pest in corn and other crops such as soybeans, cotton, rice, and sorghum (Carvalho et al., Reference Carvalho, Omoto, Field, Williamson and Bass2013). Given rising demand and the expansion of cropland for chickpeas in Brazil, S. frugiperda could become an important economic pest with chickpeas serving as an effective host (Correa, Reference Correa2019).
S. frugiperda is usually controlled by synthetic pesticides, which, if used indiscriminately may lead to the selection of resistant individuals (Neri et al., Reference Neri, Moraes and Gavino2005). Tactics compatible with integrated pest management (IPM) have been used to reduce the use of synthetic insecticides and keep pest populations below economic damage levels. Insect-resistant plants are promising in this regard (Moreira et al., Reference Moreira, Silva, Carneiro, Picanço, Almeida-Vasconcelos and Pinto2018). In addition, there are no synthetic insecticides currently registered in Brazil for the control of S. frugiperda in chickpea crops (AGROFIT, 2020). Management programs for this pest are also lacking for this crop.
Plant resistance to insects (PRI) is an important part of IPM given its compatibility with other control tactics such as chemical and biological controls (Bueno et al., Reference Bueno, Batistela, Bueno, França-Neto, Nishikawa and Filho2011; Boiça Júnior et al., Reference Boiça Júnior, Bottega, Souza, Rodrigues and Michelin2015). PRI can be divided into three categories. The first of these is antixenosis, which is usually associated with plant morphological characteristics such as trichome density, leaf color, or chemical constituents such as volatile compounds that affect insect behavior regarding oviposition, feeding, and shelter (Smith, Reference Smith2005; Seife et al., Reference Seifi, Visser and Bai2013). The second category is antibiosis, which is manifested by plant chemical constituents that affect aspects of insect biology by prolonging life cycles, deforming insects, altering sex ratios, and reducing the weight of larvae and pupae (Sharma et al., Reference Sharma, Pampapathy, Lanka and Ridsdill-Smith2005; Souza et al., Reference Souza, Costa, Silva and Boiça Júnior2014; Almeida et al., Reference Almeida, Silva, Paiva, Araujo and Jesus2017). The third and final category is tolerance, which refers to a plant's ability to resist or recover from pest damage by producing new vegetative or reproductive structures (Smith, Reference Smith2005; Seife et al., Reference Seifi, Visser and Bai2013; Paiva et al., Reference Paiva, Resende, Silva, Almeida, Cunha and Jesus2018).
The main causes of resistance in chickpea plants have been associated with the presence or absence of glandular and non-glandular trichomes and chemical exudates containing organic acids (mainly malic and oxalic acid) (Narayanamma et al., Reference Narayanamma, Sharma, Vijay, Gowda and Sriramulu2013; Rachappa et al., Reference Rachappa, Teggelli, Yelshetty and Amaresh2019). Resistant chickpea genotypes have been screened to identify sources of antibiosis to significant pests. For example, the genotypes IG 70012, IG 70022, IG 70018, IG 70006, PI 599046, PI 599066 (Cicer bijugum), IG 69979 (C. cuneatum), PI 568217, PI 599077 (C. judaicum), and ICCW 17148 (C. microphyllum) have shown antibiosis to Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) (Golla et al., Reference Golla, Rajasekhar, Sharma, Hari Prasad and Sharma2018). The chickpea accessions ICC 17257, IG 70002, IG 70003, IG 70012, (C. bijugum), IG 69948 (C. pinnatifidum), IG 69979 (C. cuneatum), IG 70032, IG 70033, IG 70038, and IG 72931 (C. judaicum) showed drastic reductions in the larval weight of H. armigera (Sharma et al., Reference Sharma, Pampapathy, Lanka and Ridsdill-Smith2005).
In this study, we evaluated antibiosis to S. frugiperda in 12 chickpea genotypes by assessing larval growth and survival. We also analyzed the nutritional quality of the chickpea genotypes by larval consumption and correlated this with the expression of plant resistance.
Materials and methods
Plant material
The chickpea genotypes Jamu 96 and Blanco Sinaloa 92 (Mexico), Nacional 27 and Nacional 29 (Cuba), BG 1392 (Spain), BRS Kalifa, BRS Cristalino, BRS Toro, 004UP, 003UP, BRS Cícero, and BRS Aleppo (Brazil) were used in the biological study of S. frugiperda while Jamu 96, Blanco Sinaloa 92, Nacional 27, BRS Kalifa, BRS Cristalino, BRS Toro, 004UP, BRS Cícero, and BRS Aleppo were used in the nutritional quality tests. The chickpea genotypes were obtained from Embrapa Vegetables (Brasilia, Federal District, Brazil).
The seeds were sown in 5 liter pots containing a substrate (3:1:1 soil, sand, and organic compost) that was corrected and fertilized according to recommendations for chickpea cultivation (Nascimento et al., Reference Nascimento, Artiaga, Boiteux, Suinaga, Reis, Pinheiro and Spehar2014). The plants were kept in a greenhouse under natural light and temperature conditions (T: 30 ± 5°C, RH: 70 ± 10%, 12 h photoperiod) and irrigation was performed daily at field soil levels.
S. frugiperda colony
The experiments were conducted at the Integrated Pest Management Laboratory of the Goiano Federal Institute, Campus Urutaí (Urutaí, Goiás, Brazil). The S. frugiperda colony was established from larvae obtained from the Laboratory of Plant Resistance to Insects at UNESP, Jaboticabal, São Paulo, Brazil.
The pupae were sexed, separated into pairs (15 males and 15 females), and kept in polyvinyl chloride (PVC) cages (15 cm diameter × 20 cm height) for emergence and adult mating. The adults were fed with a 10% honey and vitamin solution, containing 1% methylparaben as an antifungal agent (Armes et al., Reference Armes, Bond and Cooter1992), and kept in the same PVC cages. The internal surfaces of these cages were covered with paper that functioned as an oviposition substrate.
S. frugiperda eggs were collected and transferred to plastic pots (14 cm diameter and 9 cm height), and the hatched larvae were fed with an artificial diet (Greene et al., Reference Greene, Leppla and Dickerson1976). The second-instar larvae were individually separated into the cells of a B16 PET tray (CM&CM Comercio de Plásticos, São Paulo, SP, Brazil) and fed with an artificial diet until reaching the pupal phase.
The insects were maintained under controlled conditions (25 ± 2°C, 70 ± 10% relative humidity, and a 12:12 h light/dark photoperiod) during all development phases.
Growth and survival of S. frugiperda
Newly hatched larvae from the F2 generation were individually separated into Petri dishes (9.0 cm diameter) that had been lined with moistened filter paper and sealed with polyethylene film. Leaves from the apical region of each chickpea genotype were placed and replaced inside the dishes as they were consumed (usually every 2 days). The insects remained in these containers until adult emergence. After emergence, the insects were transferred to plastic containers (150 ml) where they remained until the end of the cycle.
The following biological parameters were evaluated: (a) larval phase: period and viability of the larval stage and larval weight at 10 days old; (b) pre-pupal phase: period and viability; (c) pupal phase: period, weight at 24 h old and viability; (d) total cycle: period and viability; and (e) adult stage: longevity. The experiment used a completely randomized design with 12 treatments (genotypes) and 30 repetitions.
Nutritional indices of S. frugiperda
S. frugiperda larvae were fed with an artificial diet until the third larval instar, according to a methodology used in previous studies (Nogueira et al., Reference Nogueira, Costa, Di Bello, Diniz, Ribeiro and Boiça Júnior2019; Queiroz et al., Reference Queiroz, Miranda, Silva, Borella Júnior, Almeida, Hirose and Jesus2020). Ten larvae were weighed to obtain initial weights and later individually separated into Petri dishes (9.0 cm in diameter) and kept in an air-conditioned room (temperature: 25 ± 2°C, relative humidity: 60 ± 10%, and photophase 14 h) while feeding individually on each chickpea genotype.
The food (chickpea leaves) was weighed daily using an analytical scale (Model Adventurer AR2140, 2013; Ohaus Corporation, Florham, Park, NJ), accurate to 0.0001 g. Any leftover food and feces were removed and stored in separate Petri dishes at −20°C. After 5 days, the larvae were weighed, euthanized by freezing, and then dried in an oven with the leftover food (70°C for 48 h) until reaching a constant weight. The feces were kept at room temperature and weighed after 15 days.
The following variables were evaluated: initial weight of the third-instar larvae (g), final weight of larvae (g), weight of the food supplied (g), weight of feces (g), and feeding time (days). An aliquot of five larvae were weighed (fresh and dry weight) to obtain a correction factor for the initial dry weight, which was calculated using the average dry weight divided by the average fresh weight. The resulting value was then multiplied by the initial fresh weights of the larvae (Parra, Reference Parra, Panizzi and Parra1991). The same procedure was used to obtain a dry weight correction factor for the food supplied as a function of water loss. All weight values were transformed into dry weights for analysis.
The methodology proposed by Waldbauer (Reference Waldbauer1968) and modified by Scriber and Slansky Junior (Reference Scriber and Slansky Junior1981) was used to determine the quantitative nutrition indices of the larval phase. The indices were calculated using the following parameters: duration of the feeding period (days); Af: weight of the food supplied to the insect (g); Ar: weight of the leftover food provided to the insect (g), after T; F: weight of the feces (g) during T; B: larval weight gain (g) during T; B: average larval weight (g) during T; I: weight of ingested food (g) during T; I − F: food assimilated (g) during T; M = (I − F) − B: food metabolized during the feeding period.
Food consumption and food use rates were determined by the following formulas: relative consumption rate (RCR = I/B̅ × T), relative metabolism rate (RMR = M/B̅ × T), relative growth rate (RGR = B/B̅ × T), approximate digestibility (AD = ((I − F)/I) × 100), conversion efficiency of ingested food (ECI = (B/I) × 100), conversion efficiency of digested food (ECD = (B/(I − F)) × 100), metabolic cost (CM = 100 − ECD), and consumption index (IC = I/B̅).
The experiment was completely randomized with ten treatments (genotypes) and ten repetitions (individually separated larvae). The number of repetitions was based on previous studies (Freitas et al., Reference Freitas, Sousa, Nogueira, Di Bello and Boiça Júnior2018; Queiroz et al., Reference Queiroz, Miranda, Silva, Borella Júnior, Almeida, Hirose and Jesus2020).
Statistical analysis
Residual normality and homoskedasticity were checked by the Shapiro–Wilk and Bartle tests. When the data did not meet these assumptions, the Box–Cox method was used to find optimal transformations. The transformed data were then used to fit the analysis of variance models and the means were compared by the Scott–Knott test (α = 0.05). The means were then back transformed for presentation purposes. Hierarchical Cluster Analysis (UPGMA), based on the Euclidian generalized distance, was used to determine the degrees of resistance to S. frugiperda between the chickpea genotypes while canonical discriminant analysis (CDA), using a residual covariance matrix, was used to study the distance relationship between genotypes, and their relationships with the resistance variables at 5% of significance. All analyses were performed using R software, version 4.0.1 (www.rproject.org).
Results
The larval period, larval weight, and pupal period of S. frugiperda were statistically influenced by the chickpea genotypes (table 1). However, pupal weight (P = 0.90) and adult longevity (P = 1.03) were not influenced by the chickpea genotypes.
Table 1. Period length (±SE) larval, pupal, adult (days), and larval and pupal weight (g) of S. frugiperda fed on chickpea genotypes
SE, standard error.
Means followed by the same letter within a column do not differ by the Scott–Knot test at 5%.
The larval period (P = 0.0020) was lower in larvae fed on Nacional 29 and Nacional 27 genotypes, but longer in larvae fed on BG 1392, Blanco Sinaloa 92, Jamu 96, BRS Cristalino, 004UP, BRS Kalifa, BRS Cícero, BRS Toro, BRS Aleppo, and 003UP. Larval weight (P ⩽ 0.0001) was greater in larvae fed on Blanco Sinaloa 92, 004UP, BRS Cícero, BRS Toro, and Nacional 27.
The pupal period (P = 0.0013) was longer in larvae fed on Jamu 96, Nacional 29, BRS Cícero, BRS Aleppo, and 003UP, and shortest when fed on genotypes BG 1392, Blanco Sinaloa 92, BRS Cristalino, 004UP, BRS Kalifa, BRS Toro, and Nacional 27.
The chickpea genotypes influenced larval, pre-pupal and pupal viability and the total cycle of S. frugiperda (table 2). Larval viability (P ⩽ 0.0001) was higher in insects that fed on Jamu 96, BRS Cristalino, BRS Kalifa, BRS Toro, Nacional 27, and 003UP and lower in Nacional 29. Pre-pupal viability (P ⩽ 0.0001) was higher in BG 1392, Jamu 96, BRS Cristalino, BRS Kalifa, BRS Cícero, Nacional 27, BRS Aleppo, and 003UP. The Nacional 29 genotype showed the lowest pre-pupal viability values in S. frugiperda.
Table 2. Total cycle length (days) and viability (%) of S. frugiperda fed on chickpea genotypes
SE, standard error.
Means followed by the same letter within a column do not differ by the Scott–Knot test at 5%.
Pupal viability (P ⩽ 0.0001) was lower in Nacional 29 and higher in larvae fed on BG 1392, Jamu 96, BRS Cristalino, BRS Kalifa, BRS Cícero, Nacional 27, BRS Aleppo, and 003UP. The total cycle (P = 0.0055) of S. frugiperda was greater in insects fed on BG 1392, Jamu 96, BRS Cícero, BRS Aleppo, and 003UP. Blanco Sinaloa 92, BRS Cristalino, 004UP, Nacional 29, BRS Kalifa, BRS Toro, and Nacional 27 produced the lowest values.
The chickpea genotypes influenced the following nutritional indices: weight gain (mg), food intake (mg), RCR (mg mg−1 day−1), AD (%), ECI (%), ECD (%), and CM (%); however, RGR (mg mg−1 day−1) did not differ statistically between treatments (tables 3 and 4).
Table 3. Weight gain (mg), ingested food (mg), RGR (mg mg−1 day−1), and RCR (mg mg−1day−1) of S. frugiperda larvae fed on chickpea genotypes
SE, standard error.
Means followed by the same letter within a column do not differ by the Scott–Knot test at 5%.
Table 4. AD, conversion efficiency of ingested food (ECI) conversion efficiency of digested food (ECD), and metabolic cost (CM) (±SEM) of S. frugiperda larvae fed on chickpea genotypes
SE, standard error.
Means followed by the same letter within a column do not differ by the Scott–Knot test at 5%.
The lowest weight gain (P ⩽ 0.0001) in S. frugiperda resulted from Blanco Sinaloa 92 and Nacional 27, while Jamu 96, BRS Cristalino, 004UP, Kalifa, BRS Cícero, BRS Toro and BRS Aleppo produced the highest values. The lowest food intake levels were observed in Blanco Sinaloa 92, Jamu 96, BRS Cícero, and BRS Aleppo, resulting in lower RCR (P ⩽ 0.0001).
AD (P ⩽ 0.0001) was lowest in BRS Aleppo while ECI (P ⩽ 0.0001) was lowest in Nacional 27 and highest in BRS Aleppo. ECD (P = 0.0022) was highest in BRS Aleppo. S. frugiperda larvae showed the lowest metabolic cost (CM%) (P = 0.0022) when fed on BRS Aleppo.
UPGMA (based on Euclidian distance) showed that influence on the biological parameters of S. frugiperda depended on the level of resistance of a given chickpea genotype. Thus, the chickpea genotypes were grouped into four clusters according to the resistance level (fig. 1). The genotypes in group I (BRS Cristalino, BG 1392, BRS Toro, 004UP, and BRS Kalifa) were highly susceptible; group II (003UP), susceptible; group III, moderately resistant (Nacional 29, BRS Alepo, Jamu 96, and BRS Cícero); and group IV (Nacional 27 and Blanco Sinaloa 92), resistant. All biological parameters were used to group the genotypes.
Figure 1. Dendrogram based on biological variables of S. frugiperda larvae in different chickpea genotypes. Hierarchical cluster analysis was performed using the UPGMA method with Euclidean distance as the dissimilarity measure.
Both CDA and UPGMA appeared to cluster BRS Cícero, Jamu 96, and Nacional 29 into group III (moderately resistant), mostly due to longer pupal periods. BRS Aleppo was classified as moderately resistant and was influenced by the longest larval period and total cycle of S. frugiperda. The genotypes BG 1392, 004UP, BRS Toro, Blanco Sinaloa 92, and Nacional 27 BRS appeared to cluster into the highly susceptible group (according to CDA) given their higher larval weights and longevity (fig. 2).
Figure 2. Distribution of chickpea genotypes according to CDA of the biological parameters of S. frugiperda in different chickpea genotypes. LW (larval weight – mg), PW (pupal weight – mg), LP (larval period – days), PPP (pre pupal period – days), PP (pupal period – days), LO (longevity of adults – days), TC (total cycle – days).
Discussion
Characterizing the resistance of chickpea genotypes to S. frugiperda has not been widely studied. Most studies on chickpeas focus on pod bores, H. armigera (Narayanamma et al., Reference Narayanamma, Sharma, Vijay, Gowda and Sriramulu2013; Rachappa et al., Reference Rachappa, Teggelli, Yelshetty and Amaresh2019). However, recent reports on the distribution of S. frugiperda outside the Americas suggest a looming threat to global chickpea crops. S. frugiperda has already been reported across a significant area of chickpea cultivation. S. frugiperda was first confirmed in Africa in 2016 and has since spread throughout much of the African continent (Goergen et al., Reference Goergen, Kumar, Sankung, Togola and Tamo2016). Specimens of S. frugiperda were collected in Germany and the Netherlands in 2017 (CABI, 2017) and in India in 2018 (Mallapur et al., Reference Mallapur, Naik, Hagari, Prabhu and Patil2018). In the Americas, this polyphagous pest has been widely reported for many years (Montezano et al., Reference Montezano, Specht, Sosa-Gómez, Roque Specht, Sousa-Silva, Paula-Moraes, Peterson and Hunt2018). Thus, the selection of chickpea genotypes that are resistant to this insect has become an important component of IPM (Baldin et al., Reference Baldin, Vendramim and Lourenção2019).
Our results showed that the chickpea genotypes influenced the biological parameters of S. frugiperda through antibiosis and presented different degrees of resistance. Antibiosis occurs when normal plant feeding causes adverse biological effects that directly or indirectly affect insect development and/or reproductive potential (Carvalho et al., Reference Carvalho, Lima and Alves2011). The most significant effects of antibiosis are prolongation and mortality of immature insects and reductions in the size and weight of adult insects (Vendramim and Guzzo, Reference Vendramim, Guzzo, Panizzi and Parra2009).
The genotypes BG 1392, Blanco Sinaloa 92, Jamu 96, BRS Cristalino, 004UP, Kalifa, BRS Cícero, BRS Toro, BRS Aleppo, and 003UP prolonged the larval phase of S. frugiperda, while BRS Cristalino, 003UP, Nacional 29, BRS Kalifa, BRS Aleppo, BG 1392, and Jamu 96 produced the lowest larval weights. Prolongation of larval phases and reductions in larval weight can be associated with antibiosis.
Antibiosis is mainly caused by the presence of secondary metabolites or resistant physical tissues and structural barriers (trichomes). Compounds on the leaf surface determine host selection at the beginning of feeding while trichome density on the leaf surface can inhibit feeding by newborn larvae (Baldin et al., Reference Baldin, Vendramim and Lourenção2019).
Chickpea plants contain organic acids such as oxalic, malic, and citric acids. Oxalic and malic acids are associated with insect antibiosis in chickpeas (Narayanamma et al., Reference Narayanamma, Sharma, Vijay, Gowda and Sriramulu2013; Golla et al., Reference Golla, Rajasekhar, Sharma, Hari Prasad and Sharma2018).
Number of glandular and non-glandular trichomes is a resistance mechanism in chickpeas. The density of non-glandular trichomes has been negatively correlated with larval survival while oxalic and malic acids have been significantly negatively correlated with the survival of H. armigera larvae (Golla et al., Reference Golla, Rajasekhar, Sharma, Hari Prasad and Sharma2018). Thus, the genotypes IG 70012, IG 70022, IG 70018, IG 70006, PI 599046, PI 599066 (C. bijugum), IG 69979 (C. cuneatum), PI 568217, PI 599077 (C. judaicum), and ICCW 17148 (C. microphyllum) presented antibiosis to H. armigera.
The chickpea genotypes that affected the pupal period of S. frugiperda included Jamu 96, Nacional 29, BRS Cícero, BRS Aleppo, and 003UP, which produced the longest pupal periods. The larval and pupal parameters in the current study suggest that antibiosis is one component of resistance in these genotypes and may result from antifeedant or antibiosis resistance mechanisms such as the quantity of oxalic and malic acids or the density of glandular and non-glandular leaf trichomes (Golla et al., Reference Golla, Rajasekhar, Sharma, Hari Prasad and Sharma2018).
The viability of S. frugiperda in different periods was also affected by chickpea genotype, with the lowest viabilities in Nacional 29. Chronic antibiosis often causes larval and pupal mortality (Smith, Reference Smith2005). Larvae fed on BRS Aleppo, BG 1392, Jamu 96, BRS Cícero, and 003UP had longer life cycles. These genotypes probably were not able to adequately supply the nutritional demands of S. frugiperda. This characteristic is common in insects that have imbalanced feeding or that ingest inappropriate metabolites (Panizzi and Parra, Reference Panizzi, Parra, Panizzi and Parra2009). Prolonged life cycles are an aspect of plant resistance since they result in fewer generations of pests, lower population densities, and consequent reductions in crop damage (Lara, Reference Lara1991; Baldin et al., Reference Baldin, Vendramim and Lourenção2019).
Food quantity and quality affect growth rate, development time, body weight, and insect survival (Golizadeh et al., Reference Golizadeh, Kamali, Fathipour and Abbasipour2010; Cabezas et al., Reference Cabezas, Nava, Geissler, Melo, Garcia and Krüger2013). To analyze the influence of food on insect growth, it is necessary to determine the amount of food consumed, digested, excreted, metabolized, and converted into biomass (Bortoli et al., Reference Bortoli, Murata, Bortoli, Magalhães and Dibelli2011). The chickpea genotypes in the current study influenced the weight gain, food intake, RCR, AD, ECI, ECD, and CM of S. frugiperda.
The genotypes Blanco Sinaloa 92, Jamu 96, BRS Cícero, and BRS Aleppo were more suitable for S. frugiperda development and feeding since the larvae ingested less, while having lower metabolic costs and greater conversion efficiencies of the ingested and digested food. Nacional 29 was shown to be the worst food substrate since it was associated with the poorest performance of S. frugiperda. Nacional 29 may not provide adequate nutrients or may possess allelochemicals that affect S. frugiperda development.
Both hierarchical grouping and CVA separated the genotypes into different levels of resistance. These levels were classified as highly resistant, moderately resistant, susceptible, and highly susceptible (Lara, Reference Lara1991; Baldin et al., Reference Baldin, Vendramim and Lourenção2019). The antibiosis test suggested that BRS Cícero and Nacional 29 were the least suitable for S. frugiperda development. The prolonged larval period in BRS Cícero, the low larval viability in Nacional 29, and the short pupal periods in both genotypes may be attributed to the effect of secondary metabolites and confirm the presence of antibiosis. These resistant genotypes could be combined with other IPM strategies to control S. frugiperda in chickpea crops.
Prolongation and mortality during the immature phases and reduction in the size and weight of immature and adult S. frugiperda are the main consequences of ingesting food that causes antibiosis (Vendramim and Guzzo, Reference Vendramim, Guzzo, Panizzi and Parra2009). The pupal period of S. frugiperda was affected by the chickpea genotypes. The longest pupal period was found in Jamu 96, Nacional 29, BRS Cícero, BRS Aleppo, 003UP, and the lowest pupal viability in Nacional 29. Larval weight was lowest in the genotypes BG 1392, Jamu 96, BRS Cristalino, BRS Kalifa, Nacional 29, BRS Aleppo, and 003UP.
Nacional 29 possesses chemical and/or morphological characteristics that interfere with S. frugiperda biology. These characteristics caused high mortality in the larval and pupal phases and contributed to this genotype's classification as highly resistant (group V) in hierarchical grouping. Active chemical compounds that are metabolized by the plant become physiological toxins that cause antibiosis, or deterrent substances that prevent insects from feeding and reduce survival rates (Eigenbrode et al., Reference Eigenbrode, Shelton and Dickson1990; Chagas Filho et al., Reference Chagas Filho, Boiça Júnior and Alonso2010).
BRS Aleppo promoted the longest larval periods, lowest caterpillar weights, and longest pupal periods in S. frugiperda. Highly susceptible genotypes were classified into group II, according to hierarchical cluster analysis. The total life cycle was lengthened for larvae feeding on BG 1392, Jamu 96, BRS Cícero, BRS Aleppo, 003UP, and FLIP 02-23C.
We found that the chickpea genotypes Nacional 29, BRS Aleppo, Jamu 96, and BRS Cícero presented antixenosis to S. frugiperda. These results were obtained from detached leaves, and when working with plants. However, the results need to be checked and compared to evaluate if these responses can be repeated. Using insect-resistant cultivars is highly desirable, particularly in subsistence agriculture in developing countries. Furthermore, PRI is also compatible with other IPM strategies such as biological, natural insecticide and chemical controls. These resistant genotypes can also be used as donor sources in breeding programs for insect resistance or used directly by Brazilian farmers as a component of IPM in chickpea crops.
Acknowledgements
We are grateful to the Coordination for the Improvement of Personnel in Higher Education (CAPES) for scholarships for FC and the Goiano Federal Institute for financial support. We also thank Jeffrey Lee Wangen for English revision and valuable insights into this manuscript.
Author contributions
FC, CLTS, WMN, ACSA, and FGJ conceived and designed the experiments while FC and CLTS performed the experiments. FC, CLTS, and FGJ analyzed the data and FC, ACSA, WMN, and FGJ wrote the paper. All authors read and approved the final manuscript
Conflict of interest
The authors declare no conflict of interest in this research.
