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Article

Maize Under Pressure: Spread of Helicoverpa armigera into Romanian Agroecosystems

by
Emil Georgescu
1,
Maria Toader
2,*,
Ioan Sebastian Brumă
3,4,*,
Lidia Cană
1,
Luxița Rîșnoveanu
5,6,
Paula-Lucelia Pintilie
7,
Roxana-Georgiana Amarghioalei
7,
Alina Crețu
8,
Cristina Cionga
8,
Cristina Radu
8 and
Horhocea Daniela
1
1
Agricultural Engineering Laboratory, National Agricultural Research and Development Institute Fundulea, 915200 Fundulea, Romania
2
University of Agronomic Sciences and Veterinary Medicine of Bucharest, 011464 Bucharest, Romania
3
“Gh. Zane” Institute for Economic and Social Research, Romanian Academy, Iași Branch, 700481 Iași, Romania
4
Asociation Rural Development Research Platform, Lețcani, 700481 Iasi, Romania
5
Faculty of Agrifood and Environmental Economics, Bucharest University Economic Studies, 010374 Bucharest, Romania
6
Agricultural Research Development Station Brăila, 818008 Brăila, Romania
7
Agricultural Research Development Station Secuieni, 617415 Neamț, Romania
8
Association Forum of Agriculture and Professional Processors from Romania, Mihail Kogălniceanu, 920081 Ialomița, Romania
*
Authors to whom correspondence should be addressed.
Agronomy 2025, 15(6), 1306; https://doi.org/10.3390/agronomy15061306
Submission received: 2 May 2025 / Revised: 19 May 2025 / Accepted: 23 May 2025 / Published: 27 May 2025

Simple Summary

Cotton bollworm (Helicoverpa armigera) is a polyphagous pest that can produce high levels of damage to maize, soybean, and cotton, with significant impacts worldwide, except on the North American continent. Up until ten years ago, it was considered a minor pest in Romania. We monitored the population of this pest in southeast Romania using pheromonal traps from 2020 to 2024, and we studied the behavior of nine maize hybrids from three maturity groups in response to a cotton bollworm attack in 2024. We found an increase in corn earworm captures in the traps starting from 2022, more than 12 times higher compared to 2020–2021. There was a high population in 2024. In most of the years, we found two flight peaks in August and September; however, in 2022 and 2024, a peak occurred in July too. In September 2024, regarding all the maize hybrids in this study, the pest attack incidence on cobs was 100%. We analyzed the maize hybrids’ yield for total aflatoxin (B1 + B2 + G1 + G2) levels. Because of the high number of pest attacks in 2024, the aflatoxin levels were higher than the maximum limits (Reg. EC 1881/2006) for all hybrids in this study.

Abstract

This paper presents a five-year study monitoring cotton bollworm (Helicoverpa armigera) flight dynamics using pheromonal traps and a study relating to the behavior of nine maize hybrids from two maturity groups in response to a pest attack in 2024. The monitoring and field assessments were conducted in Southeast Romania, Călărași County, at the NARDI Fundulea. During the monitoring period, from 2020 to 2024, air temperature was higher than average in the summer months while rainfall was below average, except in June 2021. The total number of moths captured in the traps was 246 in 2020, 406 in 2021, 5064 in 2022, 1024 in 2023, and 4145 in 2024. In the middle of July 2022, the average captured moths per trap was 483.3; in the middle of September, it was 589.0 catches. In 2024, in the last 10 days of July, the average captured moths per trap was 311.7; in the last 10 days of August, it was 358.0, while in the middle of September, it was 362.3. In 2024, at the beginning of August, the attack incidence of corn earworm on maize hybrids ranged from 43.75 to 53.75%, and on 13 September, it was 100% for all hybrids. This is the first report from southeast Romania that mentions a higher population of cotton bollworm in the late summer and beginning of autumn and the first report to mention a large number of pest attacks on maize cobs in September.

1. Introduction

Cotton bollworm (CBW) (Hepicoverpa armigera Hübner, 1809, Lepidoptera: Noctuidae) is one of the most dangerous pests for agricultural and horticultural crops worldwide, except in the United States [1,2,3,4,5]. It is invasive in South America and was first reported in Brazil in 2013 [6]. Many authors considered this species a pest from the Old World [7,8]. In the USA, the CBW is a quarantine pest, detected only in Puerto Rico in 2014 [9,10]. However, in this country, it is Helicoverpa zea, a species closely related to H. armigera [11]. In Europe, it is considered a native pest, widespread in the central and southern parts of the continent, which occasionally have outbreaks [3,12,13,14]. Data from the literature reveal that CBW is a polyphagous pest with more than 100 plant species from different botanical families [15,16,17,18]. Recent studies have shown that CBWs have more than 200 host plants [4,19,20]. The most important crops for this pest are cotton, maize, sorghum, soybean, pigeon pea, chickpea, cowpea, and tomato [1]. In recent years, global economic losses caused by CBW were over USD 3 billion [4,21]. In a short period after the invasion of CBW in Brazil, financial losses caused by this pest were over USD 2 billion [22]. However, most of the economic losses caused by CBW are in tropical and subtropical areas and are less impactful in countries with temperate climates [7,23,24]. In the EU, this pest was introduced to the A2 list [25]. CBW has up to 12 generations per year in countries with tropical climates and from 3 to 5 generations per year in countries in subtropical and Mediterranean areas [1,25]. In regions with a temperate climate, this pest has 1 to 3 generations per year and can overwinter [26,27,28]. CBW is characterized by a high degree of prolificity; a single female can lay more than 1000 eggs during her life span, with a maximum of 2700 eggs [1]. Although early reports indicate that CBW does not exhibit migratory behavior [5], recent papers demonstrate that moths can fly more than 10 km, especially during egg laying, specifically between 10 and 500 km [13,29]. Other papers mentioned that CBW moths can migrate up to 2000 km, using wind currents [30]. Research conducted in China, using an entomological radar, revealed that the moths migrate up to 2000 m in altitude, when winds are favorable [31]. The same research shows that the moths’ speed reaches 30–33 km/hour during this migration. In Europe, CBW was considered a facultative migratory pest [24,32]. According to Pedgley [33], CBW moths can migrate long distances, borne by wind, from Southern Europe to the British Isles. Other studies have shown evidence of the migration of this pest from the northern regions of Europe to the south and the Mediterranean basin in autumn [1]. There have been many reports concerning CBW’s resistance to insecticides from different chemical classes [34,35,36,37,38,39,40], including newer active ingredients from the diamide class [41,42,43]. CBW develops resistance mechanisms to transgenic (Bt) cotton, soybean, and maize in countries where these crops are cultivated on a large scale [44,45,46,47,48,49]. Its high adaptability to different climates, overwintering capacity, high prolificity, and high resistance to insecticides and Bt crops make it very challenging to control this pest. The grain lesions caused by feeding CBW larvae on the maize cobs can be infected with fungi from the Aspergillus and Fusarium genera [50,51]. Mycotoxins are metabolic products of the fungus and can accumulate in the infected maize grains [52,53,54]. The aflatoxins were produced by the Aspergillus flavus and A. parasiticus fungi [55,56,57]. There are several types of aflatoxins, but the most dangerous for human consumption and animal feeding is aflatoxin B1, which can cause liver cancer [52,57,58,59]. The same authors mentioned that people exposed to aflatoxins and chronic infection with the hepatitis B virus have an increased risk of hepatocellular carcinoma. This danger occurs when infected maize grains are directly consumed [60,61]. If the livestock consumes the infected maize grains, the B and G type aflatoxins are metabolized into M type aflatoxins [62], found in milk and dairy products [63,64]. Drought and high temperatures favor Aspergillus flavus activity and can increase aflatoxin levels in the maize grains attacked by CBW larvae [52,65,66]. Because of climate change, the aflatoxins are not a problem only in tropical and subtropical areas, but there are also increasing cases in some European countries, including Hungary [67]. According to EU Commission Regulation (EC) No 1881/2006, the maximum level of total aflatoxins (B1 + B2 + G1 + G2) in maize grains is 10.00 μg/kg, while for B1 aflatoxins it is 5.00 μg/kg [68]. Farmers cannot use maize for livestock and human consumption if the maximum aflatoxin level exceeds this limit [69,70]. This fact can negatively affect local and national agriculture, with severe economic losses for the farmers and even bankruptcy [71,72]. In Romania, maize is one of the most important crops. Data from the Ministry of Agriculture and Rural Development show that in this country, from 2015 to 2023, the area cultivated with maize constituted over 2.5 million hectares in 2015, 2016, 2019, 2020, and 2021 [73]. Also, Romania has a higher area cultivated with maize compared to other EU27 countries [74]. However, in Romania, total production ranged from 8.037.134 tons in 2022 to 18.663.939 tons in 2018 [73]. In some years, maize production decreases due to drought, weeds, or pests [75,76,77]. The most dangerous pests for maize crops in Romania are maize leaf weevil (Tanymecus dilaticollis), wireworms (Agriotes spp.), European corn borer (Ostrinia nubilallis), and western corn rootworm (Diabrotica virgifera virgifera) [78,79,80,81]. Until the first decade of this century, CBW was considered a minor pest for the maize crops in Romania [82]. In 2009, a Romanian paper presented data confirming yield damages CBW produced to maize crops [83]. The author mentioned that in the counties south of Romania, the percentage of the attacked cobs by CBW larvae ranged from 0 to 34%, while maize yield losses ranged from 4.4 to 6.6%. This is the first reference from the Romanian literature, after the 2000s, about maize yield losses caused by this pest. More recent data reveal a higher CBW population in Central Moldavia (East Romania) from 2019 to 2024 [84]. In an article published in a journal for farmers, Cotună [85] presents evidence regarding a high CBW population in western Romania in 2022 and high aflatoxin levels in the maize grains in this area, exceeding the limit of 10.00 μg/kg. In recent years, information concerning CBW dynamics and attacks on maize cobs has been missing in southeast Romania. Also, there is no recent information concerning aflatoxin levels in maize grains. The last data from this region are from Smeu and Casian [86]. The authors mentioned that in 2019, only one sample of maize registered aflatoxin levels higher than the 10.00 μg/kg limit set by the Commission Regulation (EC) No 1881/2006. In southeast Romania, there are many areas cultivated with maize [87], and an increase in CBW attacks combined with high aflatoxin content can threaten farmers from this region, with economic consequences to national agriculture.
This study aimed to evaluate CBW flight dynamics, assess CBW attacks on maize cobs, and analyze maize grains for aflatoxin content in a maize field in southeast Romania.

2. Materials and Methods

2.1. Experimental Site

CBW flight was monitored from 2019 to 2024. Field assessments were conducted in 2024 at the maize field site at the Plant Protection Collective, Agricultural Engineering Laboratory at the National Agricultural Research and Development Institute (NARDI) Fundulea, Călărași County, southeast Romania (latitude: 44°46′ N; longitude: 26°32′ E, 68 m a.s.l). The normal climate for this area is temperate and continental, with a yearly average temperature of 10 °C and an average annual rainfall of 571 mm [88,89]. At the field site, the terrain is flat, and the soil type is clay loam (33% clay and 35% loam) with medium texture, a humus content of 2.8–3.2%, and a pH of 6.4–6.8 [88]. Table 1 presents average temperatures and rainfall amounts at the field site.
During the CBW flight monitoring period, from 2020 to 2024, the average monthly temperatures were higher than the 50-year average in most cases (Figure 1). In all summer months, the temperatures were higher than average. In September, except in 2021, the temperature exceeded the 50-year average. In June 2024, there was a positive deviation of 5.3 °C from the 50-year average, while in July 2024, there was a positive deviation of 5.0 °C from the 50-year average. In August 2024, there was a positive deviation of 4.1 °C from the 50-year average. The Supplementary Materials (Figure S2-1) present the yearly temperatures registered at the field site from 1960 to 2024. In the last two decades, the average annual temperatures registered at the station exceeded the average. In 2023 and 2024, the average temperature was higher than 14 °C. Data from the Romanian literature show that 2024 was the warmest year in Romania since the start of the meteorological recordings [90]. Meteorological data from the NARDI Fundulea field site reveal that during the CBW flight period, from 2020 to 2024, the rainfall amounts were lower (Figure 2) in most months.
In the summer months, except June 2021, the rainfall amounts were lower than the 50-year average. The lowest deviation from the average was in June 2024 (−59.3 mm). In Romania, June and July were the year’s wettest months [90]. However, in recent years, the amount of rain registered in the first two months of summer has been lower than the average. The Supplementary Materials (Figure S2-2) present the yearly rainfall registered at the field site from 1960 to 2024 at NARDI Fundulea. In recent years, the rainfall was close to or below average, with a minimum of 285.2 mm in 2022. The Supplementary Materials (S1) present daily meteorological data from 2020 to 2024 at NARDI Fundulea. This data reveal that in the years with total rainfall amounting close to the average, the rain distribution throughout the year was unequal. Overall, weather conditions during this study at the field site in southeast Romania were characterized by temperatures higher than the 50-year average and rainfall below the average.

2.2. CBW Flight Monitoring

From 2020 to 2024, the flight pattern of CBW was monitored at NARDI Fundulea. Three pheromonal funnel traps (VRAL+ type) from Csalomon were used [91]. The traps were placed in a maize field in a triangle system, 100 m from each other and 15 m from the field margins, covering an area of 2 hectares planted with maize.
The traps were placed in the field at the beginning of April, before the maize sowing, to register a possible early CBW flight, and maintained until the end of November to register a possible late flight of this pest. The traps were kept in the field after the harvest, which usually occurs in late September or October. The traps were checked twice weekly, and all CBW moths were counted. The pheromone was changed one time every 6 weeks in the spring and autumn months and one time every 4 weeks in the summer months when the maximum air temperature exceeded 30 °C. Table 2 shows maize sowing, plant emergence, and harvest data during the 5-year CBW flight monitoring period. In 2020 and 2021, the monitored field site used the F423 maize hybrid; in 2022 and 2023, it used the Iezer hybrid; and in 2024, it used the Felix hybrid. These hybrids were created at NARDI Fundulea and were from the same FAO 401–500 group [92,93]. In the experimental field, soil work, fertilization, and herbicide application were following standard technology for maize crops.

2.3. Field Trial

In 2024, we organized an experiment at the NARDI Fundulea field site to assess the attack of CBW larvae on maize cobs. For this study, it has nine maize hybrids from three maturity groups. These hybrids are presented in Table 3. The experiment was organized according to a randomized block scheme. Each variant (maize hybrid) was replicated four times. Each plot had a length of 10 m, a width of 4.2 m, and a total area of 42 square meters. The maize was sown with a manual planter on 15 May. The distance between rows was 0.7 m, and the density was 65,000 plants/ha. Maize emergence was registered on 24 May.
The assessments were conducted on 18 July, 23 July, and 2 August after the appearance of cobs and the grain-filling stage. Also, one evaluation was conducted on 13 September at the maturity stage, and the last on 4 October, before the harvest. At each plot, 20 maize plants were chosen randomly, and the cobs were analyzed. We recorded the CBW attack incidence (the number of attacked plants from the number of analyzed plants) and the number of CBW larvae/plant.

2.4. Aflatoxin Analysis

On 26 September, we sampled maize cobs from each plot. After being detached from the plants, they were taken to the laboratory, and the grains were separated from the cobs. From each plot, 250 g of grains were harvested, resulting in 1000 g per variant. The grains were deposited in paper bags and, on 3 October, sent to the Sanitary Veterinary and Food Safety Laboratory in Bucharest, part of the National Sanitary Veterinary and Food Safety Authority in Romania. The liquid chromatography-mass spectrometry method LC-MS/MS (PS-L-RM-15, Ed4, Rev0) determined the aflatoxin level from the maize grains. This method combines liquid chromatography’s physical separation capabilities with mass spectrometry’s mass analysis capabilities [94].

2.5. Statistical Analysis

Data were statistically analyzed using Tukey’s honestly significant difference test (HSD) at a significance level of p ≤ 0.05. For statistical analysis, the ARM 2022 software [95] was used. The results of CBW flight monitoring were presented as the total number of moths captured in all traps during one maize growing season and the mean values of the CBW moths captured per trap, per 10 days. The chart showing CBW flight dynamics at NARDI Fundulea, from 2020 to 2024, was made with Microsoft Excel 2007. The results of the field trial were presented as mean values for the CBW larva attack incidence (AI%), the CBW larva average number per plant, the standard deviation (SD) from the average values, and the coefficient of variation (CV).

3. Results

3.1. CBW Flight Dynamics

In 2020, at the maize field site at NARDI Fundulea, the total number of captured CBW moths in the traps was 206. The number of captures slightly increased in 2021. In 2022, the traps captured 5064 moths, more than 12 times the number of insects compared with the previous year. In 2023, 1024 CBW moths were registered in the traps, while 4145 CBW moths were captured one year later (Figure 3). This study reveals a high increase in the CBW population in a maize field in southeast Romania.
Table 4 and Table 5 and Figure 4 present the results concerning CBW flight dynamics at the maize field site at NARDI Fundulea, southeast Romania.
In 2020, there was reduced CBW flight; the first month’s moths were captured in the traps on 1 June. We registered two flight peaks in the middle of July (36.0 moths/trap) and the last days of August (17.0 moths/trap). The flight of CBW continued in September, while the last insects were captured in the traps on 13 October.
In 2021, the CBW flight dynamics were similar to those of the previous year. The first captured moth was on 26 May. We registered a flight peak in the middle of August. In the last 10 days of this month, the average captures/trap was 18.7. CBW was captured in the traps until 21 September.
In 2022, it was ascertained that there was high CBW migration in the maize field site at NARDI Fundulea. The first moths were captured on 7 April. In the middle of July, there was the first flight peak (483.3 moths/trap). The second flight peak was registered in the middle of September, with 589.9 moths/trap. It was the first time we registered high CBW activity in the maize field in September. Maize was harvested on 4 October. In the first 20 days of August, we registered many captured moths in the traps (288 and 140.3 moths/trap). The flight of this pest continues until the middle of October. However, on 13 November, two CBW moths were found in the traps. It was the first time we confirmed a CBW flight in November, at NARDI Fundulea.
In 2023, CBW activity was reduced compared with the previous year but higher than in 2020 and 2021. The flight started on 6 April. The first flight peak was registered in the first 10 days of August (76.0 moths/trap), while the second peak was in the last 10 days of the same month (68.0 moths/trap). The flight was continuous in the first 20 days of September, but the number of captured months was lower than the previous year. There were no CBW moths captured in the last 10 days of September, while this pest appeared in the traps in the first 20 days of October, but with low numbers. In the last 10 days of October, no CBW moths were captured, but one moth was found in the traps on 10 November.
In 2024, we captured more than 4100 moths in the traps, the second-highest number of CBW captures from the study period after 2022. The first adults were in the traps on 27 April. In May, CBW activity was reduced. The first flight peak was in the last 10 days of July (311.7 moths/trap). The second flight peak was registered in the last 10 days of August (358.0 moths/trap). In the first 10 days of September, a high number of CBW moths were caught in the traps, while the third flight peak was registered in the next 10 days of this month (362.3 moths/trap). This year, there was a continued and high CBW flight in the last 10 days of August into the first 20 days of September. CBW continued to fly in the maize field site in the next 20 days, with a few moths captured in the traps. The last moth was captured on 22 October.

3.2. CBW Attack Incidence

Data from Table 6 reveal that in the NARDI Fundulea maize field site trial, CBW larva attacks on maize cobs were not registered in the assessments conducted on 18 and 23 July. On 2 August, the maize hybrids from this trial had an attack incidence that ranged from 43.75% to 50.00%. In the following assessment, conducted on 13 September, when maize was at maturity, the attack incidence was at its maximum for all maize hybrids in this study.
There were no significant statistical differences among the maize hybrids in this study concerning CBW attack incidence or between the maize hybrids’ maturity groups. A possible explanation is higher pest activity in 2024, especially in August and September.

3.3. CBW Number of Larvae per Plant

Data from Table 7 reveal that the first two assessments conducted on 18 and 23 July did not reveal CBW larvae on the maize plants in this field trial. In the third assessment on 2 August, the number of CBW larvae varied from 0.34 to 0.39 larvae/plant. On 13 September, there was a higher number of larvae per plant. However, the variation among the maize hybrids from this trial was slight, from 0.93 to 1.01 CBW larvae/plant. In the last assessment, conducted on 4 October, there were no CBW larvae found in the maize plots, even though moths were captured in the traps in the last 10 days of September.
There were no significant statistical differences among the maize hybrids concerning the number of CBW larvae or their maturity group. This is the first study to reveal a high number of CBW larvae per plant close to the middle of September.

3.4. Aflatoxin Level in the Maize Grains

Table 8 and Table 9 present the total aflatoxin (B1 + B2 + G1 + G2) level analysis results for the nine maize hybrid grains in this field study.
In this field trial, the B1 and total aflatoxin levels in all maize hybrids from the three maturity groups exceeded the limits established by EC Regulation 1881/2006. Regarding B1 aflatoxin, however, it was ascertained that there were significant differences among variants. Lower aflatoxin content was found in the KWS Kashmir and KWS Inteligens hybrids, while higher B1 aflatoxin content was found in the Magnus hybrids. At the same time, G2 aflatoxin was not detected in the maize hybrids from this trial. Regarding the level of total aflatoxins (B1 + B2 + G1 + G2) in this trial, it was observed that there were significant differences among the maize hybrids in this trial. However, all variants were over the allowed limit of 10 µ/kg. High temperatures registered in August and September and drought combined with high pest pressure on the maize favored the Aspergillus spp. fungus and contributed to higher levels of aflatoxins in the maize grains in all variants from this field trial, located in southeast Romania.

4. Discussion

OVER five years of monitoring, at the NARDI Fundulea maize field site in Călărași County, southeast Romania, we found a high CBW population in 2022 and 2024 compared with 2020 and 2021. The population of this pest increased by more than 12 times compared with the first two years of this study. In September 2024, we found high pest pressure in all maize hybrids from the field trial. The analysis of aflatoxin levels using LC-MS/MS (PS-L-RM-15, Ed4, Rev0) reveals higher total and B1 aflatoxin levels in the maize grains of all hybrids from this field trial. Compared with a previous study conducted in 2008 in the south of Romania [82], we found an intense CBW flight in August and September and a 100% CBW larva attack incidence in September. In 2019, Smeu and Casian [86] reported that in only one maize sample did aflatoxin levels exceed the limits of 10 µ/kg in south Romania, while in our study, conducted in southeast Romania in 2024, the aflatoxin levels were higher than the limits in all nine samples. In the west of Romania, in 2022, Cotună [82] found high CBW attack incidence in eight maize hybrids, ranging from 56 to 100%. The same author showed high total aflatoxin content, exceeding the 10 µ/kg limit. In a 30-year monitoring study with a light trap, at ARDS Secuieni, located in Central Moldavia (East Romania), Pintilie et al. [84] showed an increasing CBW population from 2019 to 2024 compared with the past. Between 1994 and 1998, at ARDS Secuieni, there were only 9 CBW captures in the light trap, between 1999 and 2003, only 2 captures, between 2004 and 2008, 38 captures, and between 2009 and 2013, 4 captures. The number of CBW captures in the light trap increased to 544 between 2014 and 2018, while in the next five years it increased to 4520 moths. The results from NARDI Fundulea, southeast Romania, reported in this paper, the results reported at ARDS Secuieni, by Pintilie et al. [84], and the results reported by Cotună [82], in 2022, in the west of Romania, suggest a CBW outbreak in Romania in recent years. Possible reasons for this are climate change and global warming, which can affect crop pest populations and intensify their attacks [96,97]. Liu et al., 2024 [98] mentioned that when the temperature is in the optimal range, from 32 to 35 °C, the development of CBW accelerates, their life cycle shortens, and female prolificity increases. However, if temperatures exceed 35 °C, mortality increases and female prolificity decreases. This can be a possible explanation for the higher CBW captures in the trap, in our study, at the end of summer and beginning of autumn, when temperatures are optimal for this pest, and lower captures in the summer period when temperatures exceeded 35 °C. The increase in temperature in Romania in recent years, because of global warming, has led to the rise in the CBW population in areas where it had been a minor pest. Global warming can create a shift in lepidopteran pest migrations to northern latitudes [99]. At the same time, high temperatures and drought represent favorable conditions for Aspergillus spp. Fungus, which can consequently increase aflatoxin levels in maize grains [65]. Increasing European temperatures and drought can increase the pest attacks on maize and their aflatoxin content [67]. Research conducted in different parts of the world concluded that CBW is a facultative migratory pest [13,29], but in some cases can be highly migrant, up to 2000 km [30] using wind currents [33]. A European study reveals that in some conditions, CBW second-generation moths migrate from northern regions to southern areas of the Mediterranean basin [1]. We hypothesized that a possible explanation for the higher number of CBW registered in the traps in Romania, in recent years, is due to pest migration in the second part of the summer. Further studies are necessary to elucidate this phenomenon. Huang and Hao [100] analyzed the effects of climate change on the CBW population dynamics in south Xinjiang, China. The authors of this study revealed that in recent years, the CBW abundance in the first and second generation decreased while in the third generation it increased. A similar trend was observed during our 5-year monitoring of this pest at NARDI Fundulea, in the southeast of Romania.
This paper is the first report from the Romanian literature about high CBW activity in southeast Romania in September. It is also the first report of a significant CBW larva attack on maize cobs close to the middle of September. The high CBW pressure in this period makes protecting maize very challenging.

5. Conclusions

During the five years of monitoring, the average monthly temperatures at NARDI Fundulea, in the southeast of Romania, were generally higher than the 50-year average, while rainfall was below average.
The five-year monitoring study revealed a high increase in CBW population in the field site in southeast Romania starting in 2022.
In 2022 and 2024, during the maize growing season, the CBW maximum flight peak was in mid-September.
In mid-September 2024, the incidence of CBW larva attacks was 100% in all maize hybrids from the field trial.
In 2024, the total aflatoxin level of the maize grains belonging to nine hybrids from this study was higher than the limit of 10 µ/kg.
Under global warming conditions, the CBW pest can threaten the maize crops in southeastern Romania.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agronomy15061306/s1, S1. Daily meteorological data (temperature, precipitation, RH) recorded at the NARDI Fundulea field site, from 2020 to 2024. S2. Charts with yearly temperatures and rainfall registered at NARDI Fundulea between 1960 and 2024. S3. Pictures from the maize field site, NARDI Fundulea.

Author Contributions

Conceptualization, E.G. and M.T.; methodology, E.G.; software, E.G. and L.C.; validation, C.R., A.C. and L.R.; formal analysis, C.C.; investigation, E.G.; resources, E.G. and I.S.B.; data curation, P.-L.P.; writing—original draft preparation, E.G.; writing—review and editing, M.T. and I.S.B.; visualization, R.-G.A.; supervision, H.D.; project administration, L.C.; funding acquisition, I.S.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Ministry of Agriculture and Rural Development, Romania, through the ADER Program 2023–2026 within the project ADER 2.1.5 “Fly dynamics of the Ostrinia nubilalis and Helicoverpa armigera based on classical and automated traps in the South-East area of Romania and influence of those pests’ concerning contamination with mycotoxins” (contract nr. 2.1.5./4.04.2024).

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding authors.

Acknowledgments

The authors especially thank the field technicians Loghinescu Ioana, Stoian Silvia, Radu Daniela, Cenea Daniela, and Vasilescu Adrian, laboratory technician Putineanu Felicia, and tractor driver Gunică Daniel. They all work at the Plant Protection Collective, Agricultural Engineering Laboratory from the National Agricultural Research and Development Institute Fundulea, Romania.

Conflicts of Interest

The authors declare no conflicts of interest.

References

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Figure 1. Temperature deviation from 50-year average at NARDI Fundulea from 2020 to 2024.
Figure 1. Temperature deviation from 50-year average at NARDI Fundulea from 2020 to 2024.
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Figure 2. Rainfall deviation from 50-year average at NARDI Fundulea from 2020 to 2024.
Figure 2. Rainfall deviation from 50-year average at NARDI Fundulea from 2020 to 2024.
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Figure 3. The total number of cotton bollworm captures from the traps during one year in the maize field site, NARDI Fundulea.
Figure 3. The total number of cotton bollworm captures from the traps during one year in the maize field site, NARDI Fundulea.
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Figure 4. Cotton bollworm flight dynamics at field site at NARDI Fundulea, between 2020 and 2024.
Figure 4. Cotton bollworm flight dynamics at field site at NARDI Fundulea, between 2020 and 2024.
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Table 1. Temperature and rainfall multiyear averages at NARDI Fundulea field site from April to November.
Table 1. Temperature and rainfall multiyear averages at NARDI Fundulea field site from April to November.
YearMultiyear Average
(50 Years)
(°C)
Rainfall
50-Year Average
(mm)
April11.345.1
May17.062.5
June20.874.9
July22.771.1
August22.349.7
September17.548.5
October11.342.3
November5.442.0
Table 2. Data on maize sowing, emergence, and harvest at the field site where Helicoverpa armigera were monitored.
Table 2. Data on maize sowing, emergence, and harvest at the field site where Helicoverpa armigera were monitored.
YearSowingEmergenceHarvest
202014 April28 April17 September
20217 May15 May5 October
20223 May10 May4 October
20235 May12 May22 September
202414 May21 May31 October
Table 3. Experimental variants used in this study at NARDI Fundulea.
Table 3. Experimental variants used in this study at NARDI Fundulea.
VariantMaize
Hybrid Name
Company * FAO **
Group
1KWS AdonisioKWS300–349
2P9415Corteva300–349
3MagnusNARDI Fundulea350–399
4P9944Corteva350–399
5DKC 4031Dekalb350–399
6KWS KashmirKWS350–399
7KWS InteligensKWS400–449
8DKC 5110Dekalb400–449
9P0450Corteva400–449
* Company that produces the maize hybrid. ** Maize FAO classification group (FAO 300–349 with shorter vegetation period than FAO 400–449).
Table 4. Cotton bollworm flight dynamics at field site at NARDI Fundulea, between 2020 and 2024.
Table 4. Cotton bollworm flight dynamics at field site at NARDI Fundulea, between 2020 and 2024.
MonthYear
2020
Year
2021
Year
2022
Year
2023
Year
2024
Number of Captures/Trap
AprilI001.01.00
II000.500
III0000.52.3
MayI00001.3
II001.70.77.0
III04.03.78.360.0
JuneI1.01.01.342.318.0
II00.311.338.05.0
III00.702.71.0
JulyI0069.312.049.0
II36.03.3483.33.727.3
III2.01.748.044.3311.7
AugustI014.3288.076.0116.0
II4.038.3140.326.742.0
III17.018.714.368.0358.0
SeptemberI3.017.058.74.3296.7
II6.06.7589.019.0362.3
III4.04.327.7028.3
OctoberI1.0014.01.021.0
II8.004.30.70.7
III00000.3
NovemberI0000.30
II000.700
III00000
Table 5. Data of first and last captures of cotton bollworm in traps at field site at NARDI Fundulea, from 2020 to 2024.
Table 5. Data of first and last captures of cotton bollworm in traps at field site at NARDI Fundulea, from 2020 to 2024.
YearFirst
Capture
Last
Capture
20201 June13 October
202126 May21 September
20227 April13 November
20236 April10 November
202427 April22 October
Table 6. Attack incidence of cotton bollworm larvae on maize cobs, NARDI Fundulea field site.
Table 6. Attack incidence of cotton bollworm larvae on maize cobs, NARDI Fundulea field site.
VariantMaize
Hybrid Name
18 July23 July2 August13 September4 October
Attack Incidence (%)
1KWS Adonisio0 ± 0 a*0 ± 0 a48.75 ± 4.79 a100 ± 0 a100 ± 0 a
2P94150 ± 0 a0 ± 0 a53.75 ± 4.79 a100 ± 0 a100 ± 0 a
3Magnus0 ± 0 a0 ± 0 a53.75 ± 4.79 a100 ± 0 a100 ± 0 a
4P99440 ± 0 a0 ± 0 a50.00 ± 8.16 a100 ± 0 a100 ± 0 a
5DKC 40310 ± 0 a0 ± 0 a43.75 ± 6.29 a100 ± 0 a100 ± 0 a
6KWS Kashmir0 ± 0 a0 ± 0 a45.00 ± 4.08 a100 ± 0 a100 ± 0 a
7KWS Inteligens0 ± 0 a0 ± 0 a47.50 ± 6.45 a100 ± 0 a100 ± 0 a
8DKC 51100 ± 0 a0 ± 0 a43.75 ± 6.29 a100 ± 0 a100 ± 0 a
9P04500 ± 0 a0 ± 0 a50.00 ± 4.28 a100 ± 0 a100 ± 0 a
Tukey’s HSD (p = 0.05)0011.15200
Standard deviation (SD)004.64000
Variation coefficient (CV)009.5700
* Means followed by same letter do not significantly differ (p = 0.05, Tukey’s HSD).
Table 7. The number of cotton bollworm larvae on maize cobs, NARDI Fundulea field site.
Table 7. The number of cotton bollworm larvae on maize cobs, NARDI Fundulea field site.
VariantMaize
Hybrid Name
18 July23 July2 August13 September4 October
Larvae/Cob
1KWS Adonisio0 ± 0 a*0 ± 0 a0.34 ± 0.09 a0.99 ± 0.09 a0 ± 0 a
2P94150 ± 0 a0 ± 0 a0.38 ± 0.03 a0.96 ± 0.03 a0 ± 0 a
3Magnus0 ± 0 a0 ± 0 a0.38 ± 0.05 a1.01 ± 0.03 a0 ± 0 a
4P99440 ± 0 a0 ± 0 a0.35 ± 0.07 a0.95 ± 0.09 a0 ± 0 a
5DKC 40310 ± 0 a0 ± 0 a0.34 ± 0.05 a0.98 ± 0.06 a0 ± 0 a
6KWS Kashmir0 ± 0 a0 ± 0 a0.34 ± 0.03 a0.89 ± 0.03 a0 ± 0 a
7KWS Inteligens0 ± 0 a0 ± 0 a0.39 ± 0.05 a0.96 ± 0.06 a0 ± 0 a
8DKC 51100 ± 0 a0 ± 0 a0.34 ± 0.05 a0.99 ± 0.03 a0 ± 0 a
9P04500 ± 0 a0 ± 0 a0.39 ± 0.03 a0.93 ± 0.06 a0 ± 0 a
Tukey’s HSD (p = 0.05)000.1100.1360
Standard deviation (SD)000.0460.0570
Variation coefficient (CV)0012.795.890
* Means followed by same letter do not significantly differ (p = 0.05, Tukey’s HSD).
Table 8. The level of aflatoxins in the maize yield from this experiment.
Table 8. The level of aflatoxins in the maize yield from this experiment.
VariantMaize
Hybrid Name
Aflatoxins (µ/kg)
B1B2G1G2
1KWS Adonisio205.06 ± 56.43 *8.99 ± 1.1513.66 ± 2.800 ± 0
2P9415356.49 ± 98.1014.08 ± 1.805.17 ± 1.060 ± 0
3Magnus419.67 ± 115.4913.80 ± 1.7718.71 ± 3.830 ± 0
4P9944204.00 ± 56.146.06 ± 0.782.09 ± 0.430 ± 0
5DKC 4031198.54 ± 54.6411.01 ± 1.4132.80 ± 6.720 ± 0
6KWS Kashmir39.73 ± 10.843.08 ± 0.3930.01 ± 6.150 ± 0
7KWS Inteligens76.56 ± 21.073.66 ± 0.4715.70 ± 3.220 ± 0
8DKC 5110315.50 ± 86.8330.96 ± 3.9616.81 ± 3.440 ± 0
9P045081.17 ± 22.344.69 ± 0.5957.99 ± 11.880 ± 0
* Maximum limit for B1 aflatoxin is 5 µ/kg (Commission Regulation (EC) No 1881/2006).
Table 9. The level of total aflatoxins in the maize yield from this experiment.
Table 9. The level of total aflatoxins in the maize yield from this experiment.
VariantMaize
Hybrid Name
Total Aflatoxins (µ/kg)
(B1 + B2 + G1 + G2)
1KWS Adonisio229.87 ± 7.98 *
2P9415379.11 ± 117.05
3Magnus455.50 ± 140.66
4P9944213.60 ± 65.96
5DKC 4031245.00 ± 75.66
6KWS Kashmir73.20 ± 22.60
7KWS Inteligens96.80 ± 29.89
8DKC 5110370.66 ± 114.46
9P0450144.87 ± 44.74
* Maximum limit for total aflatoxins is 10 µ/kg (Commission Regulation (EC) No 1881/2006).
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Georgescu, E.; Toader, M.; Brumă, I.S.; Cană, L.; Rîșnoveanu, L.; Pintilie, P.-L.; Amarghioalei, R.-G.; Crețu, A.; Cionga, C.; Radu, C.; et al. Maize Under Pressure: Spread of Helicoverpa armigera into Romanian Agroecosystems. Agronomy 2025, 15, 1306. https://doi.org/10.3390/agronomy15061306

AMA Style

Georgescu E, Toader M, Brumă IS, Cană L, Rîșnoveanu L, Pintilie P-L, Amarghioalei R-G, Crețu A, Cionga C, Radu C, et al. Maize Under Pressure: Spread of Helicoverpa armigera into Romanian Agroecosystems. Agronomy. 2025; 15(6):1306. https://doi.org/10.3390/agronomy15061306

Chicago/Turabian Style

Georgescu, Emil, Maria Toader, Ioan Sebastian Brumă, Lidia Cană, Luxița Rîșnoveanu, Paula-Lucelia Pintilie, Roxana-Georgiana Amarghioalei, Alina Crețu, Cristina Cionga, Cristina Radu, and et al. 2025. "Maize Under Pressure: Spread of Helicoverpa armigera into Romanian Agroecosystems" Agronomy 15, no. 6: 1306. https://doi.org/10.3390/agronomy15061306

APA Style

Georgescu, E., Toader, M., Brumă, I. S., Cană, L., Rîșnoveanu, L., Pintilie, P.-L., Amarghioalei, R.-G., Crețu, A., Cionga, C., Radu, C., & Daniela, H. (2025). Maize Under Pressure: Spread of Helicoverpa armigera into Romanian Agroecosystems. Agronomy, 15(6), 1306. https://doi.org/10.3390/agronomy15061306

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