DETERMINATION OF ANTIXENOSIS
Adult Preference
The analysis of variance applied to the adult preference data demonstrated that at least two treatments showed significant differences, as the obtained p-value (3.2x10-5) was less than 0.05. Among the 10 selected varieties, IAC AIRAN and Amarelo Astecão stood out, showing significant means compared to Pipoca Roxo Kika for adult preference for food/shelter on corn plants (Table 2). This variety exhibited characteristics of antixenosis resistance, as it was less preferred by adults compared to IAC AIRAN and Amarelo Astecão, which had higher attractiveness and, therefore, may be susceptible to D. maidis.
Table 2
Means of adult D. maidis insects that preferred different corn varieties
VARIETIES | MEANS |
IAC AIRAN | 3.75a* |
AMARELO ASTECÃO | 3.35a |
AMARELO LALESKA | 2.95ab |
BRANCO PEDRO 2 | 2.75abc |
NS 90 PRO 2 | 2.75abc |
PIPOCA PEDRO | 2.75abc |
AL BANDEIRANTE | 2.1bc |
BRANCO PEDRO 1 | 2.1bc |
VERMELHO PEDRO | 1.85bc |
PIPOCA ROXO KIKA | 1.7c |
*means followed by the same letter in the column do not differ from each other using the Tukey test (p < 0.05) |
Non-preference refers to an effect on the insect's behavior in relation to the plant. Antixenotic allelochemicals are compounds that induce repellent reactions in emitters, guiding the insect away from the plant. They also hinder initial penetration, potentially interfering with the insect's continued feeding or oviposition (Lara 1991).
Diaz-Montano et al. (2006) assessed the resistance of soybean genotypes to the soybean aphid (Aphis glycines) (Hemiptera: Aphididae) and found that the varieties K1639 and Pioneer 95B97 exhibited antixenotic resistance, as they had fewer adults on soybean plants. When there is little attractiveness or a low level of colonization of an insect on a genotype, the existence of factors hindering feeding and/or oviposition is suggested, typically occurring in plants with antixenotic characteristics (Smith 2005). Additionally, Panda and Krush (1995) state that antixenotic resistance occurs due to the presence of morphological factors such as trichomes and tissue hardness, deficiency and/or chemical compounds, or a combination of any of these factors.
Trichomes are the first structures that insects come into contact with upon landing on plants. Numerous examples confirm the role of trichomes in indicating resistance through antixenosis or antibiosis in different plant species, and depending on the types of trichomes, different reactions can occur in insects (Bastos et al. 2015).
War et al. (2012), in a literature review describing plant defense mechanisms against insects, pointed out that trichomes on plants can affect insects either positively or negatively. In this experiment, it cannot be stated whether trichomes positively or negatively influenced the preference of adults for feeding on the 10 selected varieties, as it was not possible to quantify the trichomes of these selected varieties due to their absence in these plants.
Oviposition with choice
According to the Kruskal-Wallis test, the means did not show a statistically significant difference, as the obtained p-value (0.907) was higher than 0.05. Although there was no statistical difference, numerically, D. maidis females laid fewer eggs on the Branco Pedro 1 variety (2.7 eggs) and laid more on Amarelo Astecão plants (28.15 eggs). However, one cannot conclusively state a preference for oviposition for this variety.
Peeters (2002) asserts that the antixenotic characteristics of plants can hinder or prevent feeding and oviposition due to the presence of repellents and/or the absence of attractants. In other words, when insect females are placed on resistant plants, they deposit fewer eggs than females on susceptible variety plants.
Oviposition without choice
As for the oviposition data without the chance of choice, there were statistically significant differences between at least two of the evaluated varieties, as the obtained p-value (0.009) was lower than 0.05. Among the evaluated varieties, D. maidis oviposition (Table 3) on Al Bandeirante plants showed a significant difference compared to oviposition on Amarelo Astecão plants.
Table 3
Data from the no-choice oviposition test (considering the number of nymphs to determine the total number of D. maidis eggs) in different corn varieties
VARIETIES | MEANS |
AL BANDEIRANTE | 6.5a* |
AMARELO LALESKA | 5.3ab |
PIPOCA PEDRO | 4.8ab |
BRANCO PEDRO 1 | 4.7ab |
BRANCO PEDRO 2 | 3.9ab |
NS 90 PRO 2 | 3.6ab |
IAC AIRAN | 2.6ab |
PIPOCA ROXO KIKA | 2.5ab |
VERMELHO PEDRO | 2.4ab |
AMARELO ASTECÃO | 2.1b |
*means followed by the same letter in the column do not differ from each other using the Tukey test (p < 0.05) |
Among the selected varieties, Al Bandeirante stood out by having a higher mean compared to Amarelo Astecão. Therefore, it is likely that Al Bandeirante plants exhibit susceptibility factors for D. maidis oviposition, while Amarelo Astecão plants, in this no-choice oviposition assay, show antixenotic characteristics for oviposition.
Despite Amarelo Astecão having one of the lowest egg means in this assay, for adult preference for food and/or shelter, this variety is among the highest means compared to other varieties. Lara (1991) states that it is more likely for the opposite to occur in no-choice tests, meaning a variety may demonstrate resistance characteristics in a choice test but not maintain that characteristic when grown alone in the absence of other varieties. However, this fact may apply to Al Bandeirante plants; for choice tests, it did not show as much susceptibility, but for no-choice assays, it was one of the varieties that exhibited higher susceptibility to oviposition.
Lima and Lara (2004) evaluated the resistance of soybean genotypes to the silverleaf whitefly Bemisia tabaci (Genn.) Biotype B (Hemiptera: Aleyrodidae) and found that in a no-choice test, the genotype BR-8212547 was less preferred, showing non-preference resistance for oviposition to B. tabaci.
Baldin et al. (2019) affirm that antixenotic resistance is related to plant attributes with the presence of plant structures that can prevent or affect the insect's action on the host, preventing the pest insect from preferring the host for feeding, oviposition, or reproduction.
DETERMINATION OF ANTIBIOSIS
Regarding the parameters evaluated to verify resistance through antibiosis, it can be stated that there were statistical differences in the nymphal period, development period (Egg-Adult), and longevity, but nymphal mortality data did not show significant differences.
Duration of the nymphal period
The nymphs of D. maidis evaluated on the 10 varieties went through the five instars, similar to Zurita et al. (2000). For the time in days of the nymphal period (Table 4), nymphs on NS 90 PRO 2 variety plants had the longest period (20.29 days) compared to nymphs on Branco Pedro 2 variety plants (17.7 days), which had a shorter nymphal period at a temperature of 25 ± 1°C.
Table 4
Duration of the nymphal period in days of D. maidis on corn plants
VARIETIES | MEANS |
NS 90 PRO 2 | 20.29a* |
PIPOCA ROXO KIKA | 19.52ab |
AMARELO ASTECÃO | 19.46ab |
VERMELHO PEDRO | 19.24ab |
AMARELO LALESKA | 19.18ab |
IAC AIRAN | 19.04ab |
AL BANDEIRANTE | 18.38ab |
PIPOCA PEDRO | 18.13ab |
BRANCO PEDRO 1 | 17.93ab |
BRANCO PEDRO 2 | 17.17b |
*means followed by the same letter in the column do not differ from each other using the Tukey test (p < 0.05) |
The two means were lower than the 24.8 days reported by Zurita et al. (2000) at 26°C and close to Tsai (1988), who reported 20 days at 26.7°C. However, at temperatures between 23 and 27°C, the range was about 12 to 16 days (Marín 1987; Waquil et al. 1999). The duration of the nymphal period in days presented in this study may be related to the characteristics of each evaluated variety, such as the prevalence of antibiosis resistance characteristics in NS 90 PRO 2 plants and susceptibility characteristics in Branco Pedro 2. All plants were under the same temperature conditions (25°C), so this factor should not have influenced the respective nymphal periods.
According to Smith (2005) and Baldin et al. (2019), the extension of nymphal phases may be related to the presence of plant characteristics, such as chemical compounds that can have deleterious effects on the insect's biology or inhibit its feeding. Thus, the insect will need more time to obtain the necessary energy to molt.
Nymphal Mortality
Regarding nymphal mortality, although the data did not show statistically significant differences, there was a variation from 10–50%. NS 90 PRO 2 had a 50% mortality rate for nymphs, while in Branco Pedro 2 plants, only 10% of the total died. Faria et al. (2021) evaluated corn genotypes for D. maidis and found that 60XB14, 90XB06, IAC 8046, XB8018, and IAC 8390 had a high nymphal mortality rate with viabilities between 16.67% and 25.00%, confirming the expression of antibiosis and/or antixenosis against D. maidis.
Lara (1991) considers that antibiosis resistance is related to the insect feeding normally on the plant and subsequently experiencing adverse effects on its biology, such as mortality during the insect's younger stage.
Development Period
For the development time from egg to adult in days (Table 5), insects on Pipoca Roxo Kika plants had the longest period (31.92), compared to insects on Branco Pedro 2 plants (28.58), which had a shorter development time.
Table 5
Development period from eggs to adults of D. maidis on corn plants
VARIETIES | | MEANS |
PIPOCA ROXO KIKA | | 31.92a* |
NS 90 PRO 2 | | 31.7ab |
AMARELO LALESKA | | 30.84abc |
AMARELO ASTECÃO | | 30.54abcd |
VERMELHO PEDRO | | 29.91abcd |
IAC AIRAN | | 29.82abcd |
PIPOCA PEDRO | | 29.62bcd |
BRANCO PEDRO 1 | | 29.59bcd |
AL BANDEIRANTE | | 29.42cd |
BRANCO PEDRO 2 | | 28.58d |
*means followed by the same letter in the column do not differ from each other using the Tukey test (p < 0.05) |
The two means were higher than that presented by Waquil et al. (1999), where the egg-to-adult cycle was 26.3 days at 26.5°C. According to Davis (1966), the development time averaged 27 days at 21.1°C, 22.5 days at 23.8°C, 14 days at 26.6°C, and 32.2°C. The corn varieties evaluated in this research were kept under similar environmental conditions of temperature (25.8°C), yet the insects exhibited different development times.
Baldin et al. (2005) assessed the types of resistance in tomato genotypes concerning B. tabaci. The authors found that the mean development period (egg-adult) of genotypes PI-127826, PI-134418, PI134417, and LA-444-1 differed significantly from the mean of PI-126931, prolonging the insect's cycle, indicating the occurrence of non-preference for feeding and/or antibiosis.
When the insect requires more time to complete its immature stage due to inadequate nutrition in the host, it is attributed to the expression of non-preference and/or antibiosis presented by the plant (Lara 1991; Panda and Khush 1995).
Adult Longevity
Regarding the adult longevity of D. maidis on corn plants (Table 6), the insects on Al Bandeirante plants (31.94 days) stood out among the highest means compared to those on Amarelo Laleska, Amarelo Astecão, NS 90 PRO 2, Pipoca Roxo Kika, and Vermelho Pedro. These periods were shorter than the 51.4 days reported by Waquil et al. (1999).
Table 6
Mean adult longevity of D. maidis in different maize varieties
VARIETIES | | MEANS |
AL BANDEIRANTE | | 31.94a* |
PIPOCA PEDRO | | 17.95ab |
IAC AIRAN | | 17.25ab |
BRANCO PEDRO 1 | | 17.21ab |
BRANCO PEDRO 2 | | 17.01ab |
AMARELO LALESKA | | 14.14b |
AMARELO ASTECÃO | | 13.56b |
NS 90 PRO 2 | | 12.82b |
PIPOCA ROXO KIKA | | 10.86b |
VERMELHO PEDRO | | 9.36b |
*means followed by the same letter in the column do not differ from each other using the Tukey test (p < 0.05) |
The fact that the means are lower what was reported by Waquil et al. (1999) may be due to 61% of the sampled emerged adults being males, which on mean have a shorter lifespan than females. The average longevity for males is 16.3 days, and for females, it is 42.1 days (Oliveira 1996).
Among the insects with the shortest longevity, those on Vermelho Pedro plants had a longevity of 9.36 days. This longevity is close to the 9.93 days reported by Tsai (1988) at a temperature of 32.2°C, where the lowest survival means of adults were obtained at a higher temperature. This was not the case in this study, where all adults were kept in an environment at 25°C, indicating that other factors may have influenced longevity, such as possible resistance characteristics in Vermelho Pedro plants compared to Al Bandeirante plants.
In a study conducted by Oleszczuk et al. (2020), the authors found that the corn hybrid DK72-10 exhibited antibiosis resistance factors by reducing the survival of D. maidis compared to other hybrids studied in their research. However, this antibiosis was not sufficient to interfere with the inoculation of S. kunkelii.
Antibiosis resistance is generally characterized by the deleterious effects that the plant causes in the biology of insects trying to consume it (Smith 2005), such as a reduction in insect survival, prolonged development period, reduced weight, size, and fertility (Morais and Pinheiro 2012).
DETERMINATION OF TOLERANCE
According to the Kruskal-Wallis test, the data from these experiments did not show statistically significant differences, as the obtained p-values (0.79 and 0.55) for the two parameters were greater than 5%. Despite the means not showing statistically significant differences, corn plants exhibited a percentage growth ranging from 52.1–99.4% compared to control plants.
Among the 10 varieties evaluated, IAC AIRAN plants demonstrated growth (99.4%), while Amarelo Astecão plants showed growth (52.1%) compared to control plants after contact with D. maidis, but due to the absence of statistically significant differences, it cannot be stated whether there is a trend for IAC AIRAN regarding growth.
In tolerance, the plant does not cause any biological or behavioral changes to the insect, but the plant has the ability to resist or recover from the insect's attack, maintaining its productive capacity (Smith 2005). In other words, due to its genetic characteristics, this plant is less damaged than another (Almeida et al. 2021).
As for the visual damage scale data, the mean scores also did not show statistical differences among the evaluated varieties. On a scale from 0 for plants without symptoms to 6 for dead plants, the means ranged from 1.6 to 3.4. The variety Amarelo Astecão scored 3.4, while NS 90 PRO 2 and Pipoca Pedro plants scored 1.6 for both.
These data may indicate that Amarelo Astecão plants were more damaged, and NS 90 PRO 2 and Pipoca Pedro varieties were less damaged by D. maidis compared to others, demonstrating that there may be a small degree of resistance for this parameter. However, a trend towards this characteristic cannot be asserted due to the absence of statistically significant differences between the varieties.
Lara (1991) states that although damaged leaf areas do not proportionally equate to production damage, if plants under the same conditions show one with a slightly injured leaf area compared to others, it may mean that this plant has resistance characteristics to the insect.
Clustering of Resistant and Susceptible Varieties
The analyses represented by the dendrogram (Fig. 1) indicated that at the greatest Euclidean distance, two large distinct groups were formed.
Figure 1 Dendrogram demonstrating cluster analysis of the 10 corn varieties tested for resistance to D. maidis. Group 1 – Susceptible and Group 2 – Resistant
In Group 1, the varieties showing similarity were Al Bandeirante, IAC AIRAN, Branco Pedro 1, Branco Pedro 2, and Pipoca Pedro. Regarding Group 2, the varieties demonstrating similarity were Amarelo Astecão, Pipoca Roxo Kika, Vermelho Pedro, Amarelo Laleska, and NS 90 PRO 2. The clustering analysis successfully represented varieties exhibiting susceptibility in one group and those showing resistance in another.
Within the susceptible group, Al Bandeirante showed greater distance from the others, likely indicating it as the most susceptible among this group. This conclusion is supported by its susceptibility in the tests for oviposition without choice and longevity of D. maidis. Additionally, within this group, Branco Pedro 2 and Pipoca Pedro showed higher similarity. Branco Pedro 2 demonstrated susceptibility to D. maidis due to its quick nymphal period and egg-to-adult development, as observed in the insect feeding on these plants. The indicated similarity might be associated with other tests where Pipoca Pedro and Branco Pedro showed similar values, such as in adult preference and longevity.
In Group 2, representing varieties with resistance characteristics, the included varieties were Amarelo Astecão, Pipoca Roxo Kika, Vermelho Pedro, Amarelo Laleska, and NS 90 PRO 2. Amarelo Astecão stood out with a greater similarity distance, possibly due to its susceptibility in the no-choice oviposition test. Pipoca Roxo Kika and Vermelho Pedro shared a similar fusion point, likely linked to their comparable means in the no-choice oviposition test, nymphal period, and longevity. These varieties stood out for demonstrating resistance due to the short adult lifespan when the insect fed on these plants.
In Group 2, Amarelo Laleska and NS 90 PRO 2 also demonstrated similar means in the no-choice oviposition test and longevity. Moreover, NS 90 PRO 2 stood out for its extended nymphal period compared to the means of other varieties, showing a resistance characteristic.
According to Metz (2006), in hierarchical clustering, examples within the same cluster exhibit high similarity, while those in different clusters show low similarity. Additionally, greater distance implies lower similarity, while shorter distance indicates higher similarity among examples.
The results of this study suggest potential sources of resistance in corn plants that may assist in managing D. maidis. Certain varieties stood out for characteristics directly affecting the reproduction and development of the pest insect. These findings can contribute to better variety selection for cultivation, as well as to genetic improvement programs aiming to develop corn plants resistant to D. maidis, serving as important components for resistance in the development of new cultivars targeted for corn production in areas with high infestations of this significant pest.