High levels of nitrogen fertilization enhance the fitness of the vector of corn stunt disease, Dalbulus maidis
Abstract
Host plant quality is recognized to have a significant impact on the performance of herbivorous insects. Nitrogen, a fundamental element, plays a crucial role in plant life cycles, serving as a limiting resource for both plants and herbivores. Despite nitrogen-fertilized plants generally exhibiting enhanced nutritional content, responses to nitrogen variations remain non-uniform, depending on specific insect feeding guilds and the nature of herbivore–plant interactions. In the context of modern agriculture, fertilizers are essential for maintaining soil fertility and crop productivity. Focusing on corn, a fundamental crop in the American continent, heightened fertilizer input has significantly increased yields. However, the intricate relationship between pest behavior and fertilization practices necessitates elucidation. This study aimed to examine the effects of varying levels of nitrogen fertilization on the survivorship, developmental time, and performance of the corn leafhopper Dalbulus maidis (DeLong & Wolcott) (Hemiptera: Cicadellidae), a major maize pest and vector of the corn stunt disease. Bioassays were carried out under controlled conditions, and the vector was fed on maize plants subjected to three fertilization levels (100, 200, and 300 ppm). The results indicate that higher levels of nitrogen fertilization doubled the survival rate of nymphs and accelerated their development into adults. Additionally, adults that received high levels of nitrogen fertilization exhibited twice the longevity and fecundity. The reported findings could contribute to predicting the population dynamics of this crop pest and would enable rational decision-making when intervening for D. maidis control.
INTRODUCTION
The performance of herbivorous insects feeding on host plants is intricately shaped by the quality of plants (Awmack & Leather, 2002). This quality is determined by components, such as nutrients, amino acids, sugars, and defensive compounds. Nitrogen, in particular, holds significant importance as it plays a fundamental role in the life cycle and development of plants, serving as a limiting resource for both plants and herbivores, intervening in overall growth, metabolic processes, reproduction, and survival (Mattson, 1980; Subedi & Ma, 2009; Vankosky & Van Laerhoven, 2017; Wang et al., 2006). Nitrogen-fertilized plants are known to have higher nutritional content; nonetheless, the responses of plants to nitrogen variation are not uniform, as outcomes are influenced by the specific insect feeding guild and the nature of herbivore–plant interactions (Chen et al., 2010; Riedell et al., 1996). In this regard, there are reports on how high levels of fertilization decrease the synthesis of compounds in plants that are detrimental to herbivorous insects, making the plants more appealing to insects (Bentz et al., 1995; Hartvigsen et al., 1995). Furthermore, low nitrogen inputs can lead to reduced survival and development of other insect pests. This could be attributed to the enhanced accumulation of constitutive phenolics and glycoalkaloids in the leaves, alongside the low protein content (Han et al., 2019; White, 1993).
The utilization of fertilizers in modern agriculture plays a significant role in enhancing soil fertility and increasing crop productivity (Seleiman et al., 2020). Nevertheless, continuous cultivation and declining levels of soil organic matter pose substantial challenges, especially in tropical and subtropical production areas (Subedi & Ma, 2009). This issue is recognized as a major constraint on food production (Ayoub, 1999). To mitigate this problem and sustain soil fertility, it becomes crucial to increase nutrient doses, with a specific focus on nitrogen and phosphorus. Their availability stands as a primary limiting factor for crop yield (Huang et al., 2010; Miao et al., 2006; Wade et al., 2020; Yasin et al., 2012).
Corn is one of the most important crops in the Americas, with the USA, Brazil, and Argentina serving as its main producers (Ranum et al., 2014). For instance, during the 2021/2022 season, Argentina cultivated 8 million hectares, leading to a corn production of 60 million tons, an increase of more than a twofold compared with a decade ago. The United States, on the contrary, during this period had a cultivated area of 32 million hectares and a production of 348 million tons. In the case of Brazil, the cultivated area with corn was 18 million hectares, while the production was 88 million tons of this cereal (FAOSTAT, 2024). These countries have significantly increased fertilizer consumption, resulting in higher yields. According to FAOSTAT (2024), global fertilizer production reached 188 million tons in 2019. In Argentina, fertilizer consumption in agriculture increased significantly, rising from 300 000 tons in the 1990/91 season to nearly 5 million tons in 2021/2022, with maize being the crop that used the most, at 2 million tons. Considering that many insect pests benefit from higher fertilization levels in crops, it becomes imperative to expand the knowledge regarding the relationship between pest behavior and fertilization.
The corn leafhopper, Dalbulus maidis (DeLong & Wolcott) (Hemiptera: Cicadellidae), is an important maize pest distributed in the Americas, especially in countries like Argentina and Brazil (Carloni et al., 2013; Luft Albarracín et al., 2008; Melchert et al., 2023; Oliveira et al., 2013; Oliveira & Frizzas, 2022; Virla et al., 2013). This leafhopper causes significant economic losses (Carloni et al., 2013; Giménez Pecci et al., 2002; Virla et al., 2004). This is attributed to its ability to inflict physical damage on maize leaves and transmit pathogens persistently and propagatively, such as corn stunt spiroplasma (CSS), maize rayado fino virus, maize bushy stunt phytoplasma (Oliveira et al., 1998), and maize striate mosaic virus (MSMV: genus Mastrevirus) (Ruiz Posse et al., 2023; Vilanova et al., 2022, Virla et al. 2021).
Understanding the variations in the biology and performance of phytophagous insect pests resulting from different environmental factors is crucial for elucidating how vectors transmit phytopathogens (Eigenbrode et al., 2018). In this context, the availability of nitrogen in plants indirectly affects the insects that feed on them. Overall, plants with higher nitrogen levels tend to have greater nutritional quality, leading to increased growth and improved performance of phytophagous insects (Blake et al., 2011; Brodbeck et al., 1999; Cook & Denno, 1994). Several authors who conducted studies with hemipteran insects reported that changes in planting density and increased nitrogen fertilization can positively affect parameters, such as population density, growth rates, survival, fecundity, and even the spread of vector-borne diseases (Bi et al., 2005; Schetino Bastos et al., 2007; Sisterson et al., 2017). While numerous studies exist on how crop fertilization can create favorable conditions for the proliferation of pest populations (Brodbeck et al., 1999; Cook & Denno, 1994; Power, 1989; Schetino Bastos et al., 2007; Sisterson et al., 2015; Strauss, 1987), it is noteworthy that there are contrasting findings. Some studies have reported either negative effects or no discernible impact on insects that feed on crop plants subjected to fertilization (Bethke et al., 1998; Blua & Toscano, 1994; Casey & Raupp, 1999). The relationship between host plant nitrogen fertilization and performance of phytophagous insects has been extensively studied. However, there are limited contributions that specifically investigate the influence of nitrogen fertilization on the biology of D. maidis. Power (1989) reported that crops with low nitrogen levels exhibited a reduced abundance of D. maidis populations compared with those with higher nitrogen content. Furthermore, a recent field study (Virla et al., 2022) demonstrated an increase in the populations of this vector correlated with fertilizer concentration.
A fundamental understanding of a crop's nutritional status and its subsequent impact on the biology and performance of insect pests is crucial for effective pest management programs. This knowledge might enable targeted to manage these conditions effectively. This could potentially allow for optimal timing of control measures by understanding how nutritional status affects pest developmental stages. In light of this, the aim of this study was to assess the life cycle parameters of D. maidis feeding on maize plants under different fertilization treatments. Based on the results previously reported by Power (1989) and Virla et al. (2022), we hypothesize that the vector's performance on maize plants subjected to high nitrogen fertilization treatments will exhibit enhancements across various life cycle parameters.
MATERIALS AND METHODS
Dalbulus maidis laboratory rearing
The females of D. maidis used in the experimental assays were sourced from a pathogen-free colony, initially established using individuals collected from Los Nogales, Tucumán, Argentina (26°42′ S–65°13′ W; 588 m a.s.l.) (Melchert et al., 2023). The colony has been maintained for several years, and to minimize the risk of inbreeding, fresh individuals collected from the field that showed no evidence of disease symptoms were regularly introduced into the colony. To ensure that these were non-infective populations, PCR tests were conducted on a small sample (n = 20). Additionally, periodic PCR tests were performed to random individuals of the colony to ensure the absence of the pathogen. The insects were reared in custom-made cages constructed from polyvinyl chloride pipes (50 × 50 × 50 cm) and covered with white voile fabric. Potted maize plants of the landrace sweet white maize “maizón” were used as food and maintained under greenhouse conditions (25 ± 1°C and L14:D10 photoperiod) at the Biological Control Division Laboratory of PROIMI (Planta Piloto de Procesos Industriales Microbiológicos), Tucumán, Argentina (26°48′ S–65°14′ W; 465 m a.s.l.).
Plant treatments
Template hybrid maize seeds were used in the experimental assays. Seeds were planted in 240 mL expanded polystyrene pots (8.5 × 7.1 cm diameter) with a substrate composed of vermiculite and soil mix in a 50:50 ratio. Fertilization was applied after the first leaf was unfolded and fully expanded. Pots received fertilization three times per week during 4 weeks with a solution (Verdeagua hidroponia®, Buenos Aires, Argentina) containing 68 ppm P, 169 ppm K, plus 100 ppm N (low nitrogen treatment), 200 ppm N (medium nitrogen treatment), or 300 ppm N (high nitrogen treatment) from potassium nitrate (Hsu et al., 2009; Jauset et al., 2000; Wang et al., 2006). The fertilizer rates used in this study were selected based on the levels recommended by fertilizer suppliers to farmers in the northern region of Argentina and were already used in a previous field study with this pest (Virla et al., 2022). Additionally, plants were watered daily with 2 mL of water. They were grown under greenhouse conditions at 25 ± 1°C and L14:D10 photoperiod.
Life cycle of D. maidis at different nitrogen fertilization levels
Nymphs
Assays were performed using 20 gravid D. maidis females of known age (11–15 days old) per fertilization treatment, randomly collected from the colony previously described. Each group of 20 females was placed inside 20.5 cm long cylindrical PET cages covered with voile fabric on one side and closed on the other side with a cotton plug in which one plant from each fertilization treatment was previously placed. All plants used for laboratory assays had reached the V4 phenological stage. This stage was selected due to its size that is easily manipulated and because of previous reports showing D. maidis preference for the first growth stages in the field (García da Cunha et al., 2023). Females were allowed to oviposit for 24 h. At the end of this period, adults were removed, and plants were maintained inside the cages until nymphs emerged. The time of hatching was registered. Each nymph was individually placed inside glass test tubes (10 × 2 cm diameter) covered with a wetted cotton plug at the upper end. The curved end of each glass tube was pierced and covered with voile fabric to avoid water condensation. The nymphs were fed daily with fresh leaf pieces of maize from each treatment until nymphs reached adult stage (Van Nieuwenhove et al., 2016). Individual insects were checked daily to register ecdysis and survivorship. Nymph development time, mortality, and survival were recorded. One hundred nymphs per treatment were assessed. The assay was carried out in a rearing chamber under controlled conditions of temperature and photoperiod (25 ± 1°C and L14:D10 photoperiod).
Adults
For the construction of life tables, newly emerged adults reared on plants with low, medium, and high nitrogen fertilization were placed in couples (one female and one male) inside glass tubes (20 × 2 cm diameter). In total, 34 individuals (17 couples) were used for the low nitrogen treatment, 36 individuals (18 couples) for the medium nitrogen treatment, and 32 individuals (16 couples) for the high nitrogen treatment. Each couple was provided daily with a treated maize leaf at the respective fertilization level until all adults had died. The leaves were removed and dissected daily to count the number of eggs laid throughout each female's lifespan, as well as to record the longevity of both females and males. Longevity assessments were conducted on a total of 102 individuals across all treatments, comprising 51 females and 51 males.
Leaf chlorophyll content
To assess the effect of nitrogen fertilization, an evaluation of relative leaf chlorophyll content was carried out using an MC 100 chlorophyll concentration meter (Apogee Instruments™). Data were obtained by measuring 16 maize plants at the V4 stage (fourth leaf unfolded and fully expanded) for each fertilization treatment.
Statistical analysis
A GLM with a Gamma distribution and inverse link function was used to analyze the influence of fertilization treatment on egg and nymphal development, preoviposition period, and longevity of adults. Fecundity of D. maidis was analyzed using GLM with Poisson distribution and log link function. Sex ratio was analyzed using GLM with binomial distribution. Maize chlorophyll levels were analyzed using GLM with Gaussian distribution and identity function. Treatments were compared using likelihood ratio tests, and the Bonferroni test adjustment was used for multiple testing of these comparisons. A life table was constructed using age-specific survival rate (lx) and fecundity (mx) for each age interval per day. Using these data, we calculate the net reproductive rate (R0 = ∑lxmx), intrinsic rate of increase (Rm = ln(R0)/T), mean generation time (T = ∑xlxmx/R0) and population doubling time (DT = ln2/Rm).
A survival analysis was carried out in order to compare the effects of nitrogenated fertilization on the duration of the nymphal stage, using the non-parametric Kaplan–Meier survival analysis (Kaplan–Meier, 1958). We also performed Kaplan–Meier to analyze survivorship of adults. Survival curves from the different nitrogenated treatments [low nitrogen (100 ppm), medium nitrogen (200 ppm) and high nitrogen (300 ppm)] generated with this method were compared with Log-Rank tests.
All statistical analyses were performed using R Studio 2023.6.0.421 (Posit Team, 2023), with the packages “stats” v. 3.6.2 for GLM analysis and “survival” v. 3.8-3 for Kaplan–Meier survival analysis.
RESULTS
Influence of fertilization on nymph development and survival
Nitrogen fertilization significantly influenced the development time of the first, second, fourth, and fifth instars (χ2 = 718.47, df = 4, p < 0.05), while no effect was observed on the third instar. Concerning the total nymphal development time, a significantly shortened duration was observed (14.19 ± 0.18 days) when D. maidis fed on the high nitrogen fertilization treatment, compared with nymphs fed on low-fertilized maize (18.8 ± 0.36 days) (χ2 = 164.27, df = 2, p < 0.05). No significant differences were observed in the effect of nitrogen fertilization on egg development of D. maidis (Table 1).
| No. treatment (ppm) | Egg | First instar | Second instar | Third instar | Fourth instar | Fifth instar | Total nymphal development |
|---|---|---|---|---|---|---|---|
| Low nitrogen (100 ppm) | 7.30 ± 0.05a | 3.94 ± 0.09b | 2.47 ± 0.07a | 2.50 ± 0.09a | 3.47 ± 0.13b | 5.30 ± 0.43b | 18.2 ± 0.36b |
| Medium nitrogen (200 ppm) | 7.18 ± 0.04a | 3.28 ± 0.08b | 2.36 ± 0.07a | 2.57 ± 0.09a | 3.40 ± 0.10b | 4.97 ± 0.15b | 16.87 ± 0.18b |
| High nitrogen (300 ppm) | 7.27 ± 0.04a | 2.61 ± 0.07a | 2.28 ± 0.06a | 2.35 ± 0.06a | 2.67 ± 0.09a | 3.98 ± 0.16a | 14.19 ± 0.18a |
- Note: Within the same column, means followed by different letters are significantly different (α < 0.05).
Survival of nymphs varied among nymphal instars, with the highest mortality occurring during the first, third, and fourth nymphal instars for all treatments (41% deaths in the first and third instar, and 59% of deaths in the fourth instar). The development time from egg-laying to adult emergence was nearly 25, 24, and 21 days in low, medium, and high nitrogen treatments, respectively. Nymphs that successfully reached adulthood exhibited sex ratios of 2:1, 1.2:1, and 1.2:1 (female: male) for the low, medium, and high nitrogen fertilization treatments, respectively, which were not statistically different between treatments (χ2 = 1.74, df = 2, p = 0.41).
The analysis of survival via the Kaplan–Meier curves showed that nymphs from the medium and low treatments had a lower survival probability compared with nymphs from the high nitrogen treatment. Only 23% and 40% of the nymphs in the low and medium nitrogen treatments, respectively, reached the adult stage, while 56% of the nymphs in the high nitrogen treatment molted to adults. This difference was confirmed by the log-rank test (χ2 = 11.1, df = 2, p < 0.05; Figure 1).
Survivorship and longevity of D. maidis adults
The longevity of male and female individuals of D. maidis was significantly influenced by the application of nitrogen fertilizer. Males fed on plants treated with high nitrogen fertilizer treatment had a lifespan twice as long (59.2 ± 1.92) as those exposed to low fertilizer treatments (24.9 ± 1.21) (χ2 = 36.42, df = 2, p < 0.05). A comparison of female longevity revealed that those fed on high nitrogen treatment plants lived an average of 83.5 ± 2.28 days, while those fed on medium and low treatment plants lived 55.8 ± 1.76 and 52.8 ± 1.76 days, respectively (Table 2) (χ2 = 35.23, df = 2, p < 0.05). In all treatments, females exhibited a longer lifespan compared with males. Additionally, Kaplan–Meier survival curves demonstrate that adults exclusively fed on plants with high levels of fertilization throughout their lives had a greater probability of survival compared with those who consumed plants from medium and low fertilization treatments (χ2 = 31.7, df = 2, p < 0.05; Figure 2).
| No. treatment (ppm) | Male longevity (day) | N (range) | Female longevity (day) | N (range) | Preoviposition period (day) | Eggs per female | Eggs per day |
|---|---|---|---|---|---|---|---|
| Low nitrogen (100 ppm) | 24.9 ± 1.21a | 17 (7–43) | 52.8 ± 1.76a | 17 (20–76) | 4.53 ± 0.51a | 303 ± 4.22b | 6.05 ± 0.59a |
| Medium nitrogen (200 ppm) | 39.6 ± 1.48b | 18 (16–69) | 55.8 ± 1.76a | 18 (37–87) | 5.28 ± 0.54a | 342 ± 4.36a | 6.24 ± 0.58a |
| High nitrogen (300 ppm) | 59.2 ± 1.92c | 16 (23–102) | 83.5 ± 2.28b | 16 (66–102) | 5.28 ± 0.54a | 670 ± 6.47c | 8.06 ± 0.71a |
- Note: Means followed by different letters within the same column are significantly different (α < 0.05). Numbers in parenthesis represent the range of minimum and maximum values.
Fecundity and life table parameters of D. maidis females
No differences were observed when comparing the preoviposition period of D. maidis females (χ2 = 6.05, df = 2, p = 0.05), which range from 4 to 5 days. On the contrary, nitrogen fertilization had a remarkable positive effect on the fecundity of D. maidis. Females in the high nitrogen treatment group laid the most eggs on average, with a total of 670 eggs, compared with 303 and 342 eggs per female in the low and medium treatment groups, respectively. The mean number of eggs laid daily per D. maidis females was greater in the high nitrogen treatment compared with medium and low treatments (χ2 = 27.10, df = 2, p < 0.05; Table 2).
The life table for adult D. maidis in the various treatments reveals that the net reproductive rate (R0) and the intrinsic rate of increase (Rm) are higher among those fed with plants having the highest fertilizer concentration. This suggests a faster population growth rate in this treatment than at low and medium fertilization levels (Table 3).
| No. treatment (ppm) | R 0 | R m | T | DT |
|---|---|---|---|---|
| Low nitrogen (100 ppm) | 306.13 | 0.37 | 15.15 | 1.83 |
| Medium nitrogen (200 ppm) | 346.27 | 0.34 | 16.70 | 1.98 |
| High nitrogen (300 ppm) | 674.84 | 0.42 | 15.42 | 1.63 |
- Abbreviations: DT, doubling time (in days) for population; R0, net reproductive rate; Rm, intrinsic rate of increase; T, generation time (in day).
The likelihood of survival for D. maidis females that fed on plants subjected to high nitrogen fertilization begins to decline only on Day 69 (Figure 3C), whereas those subjected to low fertilization begin to decline on Day 21 (Figure 3A). Furthermore, female fertility under low fertilization peaks on Day 16, subsequently dropping significantly until they cease egg-laying and expire. It should be noted that in the high nitrogen treatment, fecundity (mx) remained relatively stable throughout the life of the females. Even the final surviving female individuals continued to lay eggs until a few days before their death, a phenomenon absent in the low fertilization treatment.
Leaf chlorophyll content
The readings showed a significant difference in the mean chlorophyll concentration between the three analyzed treatments (χ2 = 124.49, df = 2, p < 0.05) (Table 4).
| Nitrogen fertilization treatment | Chlorophyll content (μmol/m2) |
|---|---|
| High nitrogen (300 ppm) | 313.17 ± 6.70 a |
| Medium nitrogen (200 ppm) | 209.41 ± 4.46 b |
| Low nitrogen (100 ppm) | 150.93 ± 2.80 c |
- Note: Means followed by different letters within the same column are significantly different (α < 0.05).
DISCUSSION
In this study, we conducted the first evaluation of the effect of nitrogen fertilization on maize on the fitness and life cycle parameters of D. maidis. Our findings demonstrated that nitrogen fertilization applied to host plants significantly influences the performance of this leafhopper species, affecting nymphal development, survival, fecundity, and other relevant parameters. Previous research has shown the significance of host plant quality in the performance of various taxa of phytophagous insects (Awmack & Leather, 2002; Hunter & McNeil, 1997; Kuczyk et al., 2021; Mattson, 1980; Wang et al., 2006). The authors found that the survivorship of Homalodisca vitripennis (Say) (Hemiptera: Cicadellidae) nymphs was higher in plants fertilized with urea (Brodbeck et al., 1999). Similar results were reported by Bi et al. (2005), who found that nitrogen fertilization applied to cotton plants increased the density of the whitefly Bemisia argentifolii (Bellows & Perring) (Hemiptera: Aleyrodidae). Chlorophyll meter data herein reported indicated that plants receiving increased levels of nitrogen fertilizer exhibited elevated chlorophyll concentrations. This outcome is consistent with a study that reported a tight relationship between chlorophyll and nitrogen fertilization (Bojović & Marković, 2009). Measuring chlorophyll concentration proves to be a valuable and reliable method for assessing the nitrogen status of a maize plants, without damaging the leaves (Argenta et al., 2004).
In our study, we observed that nitrogen fertilization diminished the total nymphal development time, resulting in a shorter duration for nymphs to reach adulthood. Similar outcomes were reported for Halyomorpha halys (Stäl) (Hemiptera: Pentatomidae). They found that diet significantly influences nymphal development, affecting parameters like survival and development time (Acebes-Doria et al., 2016). The impact of different host plant species on the survival and nymphal development of certain hemipterans is illustrated in studies, such as Ishizaki et al. (2008) and Jiao et al. (2012). For instance, Jiao et al. (2012) found that the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) exhibits a higher survival probability on plants like tomato or cotton, which possess higher nutritional levels, compared with Poinsettia (Euphorbia pulcherrima [Euphorbiaceae]). Notably, these examples involve polyphagous insects, where variations in diet among species encompass not only nitrogen or carbohydrate content but also the presence or absence of defensive compounds (Behmer, 2009). In a study focused on Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae), a significant oligophagous insect pest of maize, authors demonstrated that nitrogen fertilization levels in maize affect population parameters, including nymphal development time (Wang et al., 2006). Our study aligns with these findings, demonstrating that D. maidis nymphs fed on maize with higher fertilization levels exhibit a faster nymphal development time compared with those fed on plants with suboptimal fertilization levels. Behmer (2009) proposes that nymphs growing on plants with lower nutrient quality require additional feeding time to attain the optimal nutrient requirement, such as protein and carbohydrates, essential for molting. When examining the time required for each nymphal instar, notable differences are observed in the duration of the first, fourth, and fifth instars. These differences may arise from the fact that these instars represent crucial stages with substantial changes, including body growth, wing bud development, and enlargement (Nault, 1998). However, Jansson and Smilowitz (1985) reported that nitrogen in plants minimally affected both population growth and requirements for larval development of Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Similar outcomes were reported on the impact of nitrogen fertilization on nymphs of the azalea lace bug Stephanitis pyrioides (Scott) (Hemiptera: Tingidae) (Casey & Raupp, 1999). Conversely, Jauset et al. (2000) found that neither nymphal survival nor development time of Trialeurodes vaporarium (Westwood) (Hemiptera: Aleyrodidae) were affected by nitrogen levels applied to host plants. Contrary to this, the survival curves in this study indicated that nymphs fed on maize with high levels of fertilization exhibit a greater likelihood of survival. Numerous studies have consistently shown that the quality of the host plant positively influences the fecundity and longevity of adult phytophagous insects (Du Plessis et al., 2012; Powell & Bellows, 1992; Rhodes et al., 2019; Silva et al., 2021). Rhodes et al. (2019) found that nitrogen fertilization had significant effects on fecundity and generation time in the madeira mealybug Phenacoccus madeirense Green (Hemiptera: Pseudococcidae). In this contribution, we present evidence that both the longevity and fecundity of D. maidis are markedly influenced by nitrogen fertilization. Females exposed to high nitrogen fertilization treatment exhibited a lifespan of up to 100 days, and their fecundity was twice as high as those in the low and medium nitrogen treatments. According to Awmack and Leather (2002) when a female insect encounters a poor-quality host plant, she may decrease the number of laid eggs, and in extreme scenarios, egg oosorption might occur in order to relocate their nutrient content. Similar responses have been observed in other insects, such as whiteflies (Jauset et al., 1998), the corn planthopper P. maidis (Wang et al., 2006), and Sogatella furcifera (Horvath) (Hemiptera: Delphacidae), a significant rice pest (Li et al., 2021). The results presented in this contribution align with the field experiments where it was found that the population density of D. maidis is higher in maize fields that received higher nitrogen doses (Virla et al., 2022).
According to Gripenberg et al. (2010), female herbivorous insects maximize their fitness by laying their eggs on plants that will promote the best development for their offspring. This principle is referred to as the “preference-performance hypothesis.” Given the variation in suitability of plants as food for insects, it is expected that female insects can differentiate between host plants with varying nutritional conditions for pre-imaginal development (Jaenike, 1978). Previous research has indicated that D. maidis can discriminate between plants with different fertilization levels using only olfactory cues, and thus lay more eggs in maize plants with higher nutritional quality (Melchert et al., 2023). In this context, the present study provides evidence that aligns with this hypothesis, demonstrating that nitrogen fertilization of corn plants has positive effects on the performance of D. maidis. While this study employed uninfected females, it is noteworthy that pathogens have the potential to influence insect behavior and performance. Future research should explore the impact of fertilization of corn in the plant-pathogen-vector system (Ingwell et al., 2012; Mauck et al., 2010; Rajabaskar et al., 2014). Since 2015, D. maidis has become a recurrent problem in Brazil, leading to this species being considered a key pest of the crop (Oliveira & Frizzas, 2022). In Argentina, the population of D. maidis has been growing in recent years, and it was during the last season of 2023/2024 that this pest experienced a population explosion, even in areas where its occurrence is occasional (Virla, 2024). According to this author, this seems to be the result of changes in the production system, such as the expansion of the planted area, increased planting dates, in addition to the occurrence of optimal environmental conditions for this to happen. According to FAOSTAT (2024), the agricultural use of nitrogen fertilizers in Brazil and Argentina has doubled in the last 10 years. The results presented in this work suggest that this increase in the use of nitrogen fertilizers is another important factor that enabled this population growth in Brazil and Argentina. It would be interesting in future studies to delve deeper into this topic with fieldwork and collect sufficient information to be able to contribute to designing integrated pest management strategies, where the nutritional status of crops becomes a variable to predict the population dynamics of this pest through predictive models (Rossini et al., 2021), ultimately aiding in reducing D. maidis populations.
AUTHOR CONTRIBUTIONS
Nicolás A. Melchert: Conceptualization; formal analysis; investigation; methodology; software; validation; writing – original draft; writing – review and editing. Carolina Manzano: Formal analysis; investigation; software; writing – review and editing. Eduardo G. Virla: Conceptualization; funding acquisition; investigation; methodology; writing – review and editing. Érica Luft-Albarracín: Conceptualization; funding acquisition; investigation; methodology; project administration; resources; supervision; writing – review and editing.
ACKNOWLEDGMENTS
The authors are grateful to the anonymous reviewers for their comments and suggestions, which have been greatly helpful for the improvement of this manuscript. This work was supported by PICT 2019 No. 1309 (FONCYT, Fondo para la Investigación Científica y Tecnológica) and PIP CONICET (Consejo Nacional de Ciencia y Técnica) No. 521. Nicolás A. Melchert thanks CONICET for the scholarship.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
