Occurrence of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East–Asia Minor 1 (MEAM1) and Mediterranean (MED) in Commercial Fields of Solanum lycopersicum in Brazil
by
, , , , , and
Daniel de Lima Alvarez
1
,
Daniel Mariano Santos
1,
Pedro Hiroshi Passos Ikuno
1,*,
Caroline da Cruz Martines
1,
Sérgio Roberto Benvenga
2,
Cristiane Müller
3,
Renate Krause-Sakate
1 and
Regiane Cristina de Oliveira
1 1
Faculdade de Ciências Agronômicas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Fazenda Experimental Lageado, Avenida Universitária, n° 3780, Altos do Paraíso, Botucatu 18610-034, SP, Brazil
2
Inspecta—Research, Consulting and Training Ltd., Vicinal Guilherme Scatena Road, Km 06, Descalvado 13690-000, SP, Brazil
3
Corteva Agriscience, Engenheiro João Tosello Highway, 71, Mogi Mirim 13814-000, SP, Brazil
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(11), 2516; https://doi.org/10.3390/agronomy14112516
Submission received: 9 September 2024
/
Revised: 15 October 2024
/
Accepted: 23 October 2024
/
Published: 26 October 2024
(This article belongs to the Special Issue Ecological Aspects as a Basis for Future Pest Integrated Management)
Abstract
:The tomato (Solanum lycopersicum) is an important crop to the economy of Brazil, and the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is one of the limiting factors responsible for reducing its yields. These insects are part of a cryptic species group present across almost the entire globe. The most relevant cryptic species in the world are B. tabaci MEAM1 and MED due to their capability to adapt and cause damage to vegetables, grain, and ornamental crops. The arrival of MED in Brazil through the state of São Paulo represents risks to farmers in the region due to the difficulty in managing these insects. This study assessed the occurrence of both species in tomato crops in the southeastern region of Brazil in 2020 and 2021. An amount of 79 samples containing 767 insects were collected throughout the study period, and in the cities of Sumaré (SP) and Monte Mor (SP), several samples were collected from the same location throughout the year. The insects were stored and sent for molecular analysis. The results showed an increase in MED compared to MEAM1. The presence of MED in the Minas Gerais samples was not recorded. However, a higher percentage of MED was observed in the state of São Paulo, which was detected in the municipalities of Sumaré and Monte Mor. These results possibly indicate that MED could be starting to stabilize in open tomato fields in Brazil.
1. Introduction
The cultivation of the tomato crop Solanum tomato lycopersicum L. (Solanaceae) is crucial for the production of industrialized products and fresh consumption around the world. In Brazil, the growing area of this crop has remained permanent since 1990. In 2021, Brazil had a planted area of 54,885 ha with an average production of 3,932,814 tons [1].
The main type of tomato grown in the state of Goiás is industrial tomatoes with a focus on manufactured tomato products, which represents approximately 60% of the national production, followed by São Paulo and Minas Gerais [2]. The main states that produce tomatoes for fresh consumption are São Paulo, Minas Gerais, Goiás, Bahia, Paraná, and Santa Catarina [1].
Several factors are responsible for the decrease in tomato yields in the country, including phytosanitary problems [3], such as infestations of the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae).
Whiteflies are classified as pests with great destructive potential for crops worldwide, causing damage by feeding, the excretion of honeydew, and the transmission of different types of viruses [4,5,6]. Furthermore, this species has a wide geographic distribution, present across almost the entire globe, except in polar zones [7,8]. Among the main genera of transmitted viruses, Begomoviruses are mostly transmitted by Bemisia spp. with more than 400 species reported [9,10,11,12,13,14].
Viral transmission by whitefly is important in the Solanaceae family. Although the Begomoviruses are the most common, the list of whitefly-transmitted viruses is growing over time, and this insect can contribute to it by inoculating different viruses in the same plant, increasing the possibility of recombination and rearrangements and the appearance of new strains or species. In contrast, the viral infection can favor whitefly development by reducing plant defenses or can make the host more attractive by altering its physiological characteristics [13].
Currently, B. tabaci is classified as part of a complex of cryptic species that are morphologically indistinguishable but that have distinct biological, genetic, and ecological characteristics [8,15,16,17]. This species is capable of feeding on different hosts. It is estimated that there are approximately 700 monocotyledonous and dicotyledonous species that, in Brazil, are responsible for losses that can reach up to 100% in crops such as cucumbers, cabbage, peppers, tomatoes, and jiló [18].
Whiteflies were initially reported in Brazil in 1923 in Bahia [19] and, four decades later, in the states of São Paulo and Santa Catarina [20] and in Paraná on cotton plants [21]. In Brazil, the most important cryptic species are Bemisia tamaci Middle East–Asia Minor 1 (MEAM1) (Hemiptera: Aleyrodidae), which was reported in 1991 in São Paulo state (probably having arrived by the international ornamental plant trading market and the migration of insects [22,23]) and Bemisia tabaci Mediterranean (MED) (Hemiptera: Aleyrodidae), which was reported in Brazil for the first time in Barra do Quaraí in 2013. Another invasion was identified in São Paulo state in 2015, also related to ornamental plants [24,25].
Known for their colonization and destructive capacity, B. tabaci MED and B. tabaci MEAM1 [15] are the main threats to several crops found in Brazil. Despite the recent arrival and increase in distribution of B. tabaci MED in Brazil [22,25], B. tabaci MEAM1 continues to be the main cryptic species in the country [26].
As previously mentioned, B. tabaci MEAM1 is predominant in Brazil. However, in the southeastern region of the country, mainly in the state of São Paulo, where one of the B. tabaci MED entries occurred in the country [25], it was observed that the B. tabaci MED species is predominant when compared to B. tabaci MEAM1 in pepper, cucumber, and tomato crops, especially in greenhouses [27].
Due to the necessity to understand whether B. tabaci MED is starting to migrate to crops beyond greenhouses, the objective of this study was to evaluate the occurrence of B. tabaci MED and MEAM1 in open-field tomato crops in southeastern Brazil.
2. Materials and Methods
2.1. Insect Collection
Samples of B. tabaci were collected from commercial tomato fields in different regions of the states of São Paulo and Minas Gerais (Brazil) in 2020 and 2021 (Figure 1A,B). All samples were collected in an open field, and only one sample was collected in the greenhouse. In the state of São Paulo, samples were collected from regions closer to large commercial centers and at lower altitudes, except for the municipality of Capão Bonito. In Minas Gerais, the collection regions were further away from the large centers and at higher altitudes (Table 1 and Table 2). Adult insects were collected with an aspirator composed of a glass Pasteur pipette, a plastic pipe with a diameter of 0.5 cm, and a “voile” fabric sealing the pipe. The adults were placed in tubes containing 100% alcohol and were subsequently stored at −4 °C for further analysis.
2.2. Identification of the Cryptic Species of B. tabaci
A mitochondrial cytochrome oxidase I (mtCOI) gene analysis was performed. DNA was extracted from 10 individuals from each sample using the Chelex protocol [28]. The samples were subjected to PCR using the genetic primers C1-J-2195 and TL2-N-3014 [29]. The PCR reaction was carried out with a final volume of 50 µL (final concentrations of MgCL2 at 50 mM, dNTP at 2.5 mN, and oligonocleotides at 1 µM) with 0.5 units of Taq polymerase. The reaction took place in 1 cycle of 5 min at 94 °C and 35 cycles of 30 s at 94 °C, 45 s at 45 °C, and 1 min at 72 °C, with a final 10 min extension at 72 °C. Subsequently, a polymorphism analysis was performed using RFLP (restriction fragment length polymorphisms) of the amplicons [30] to differentiate B. tabaci MEAM1 from MED. From each PCR, 5 µL was used and digested with one unit of TaqI at 65 °C for 2 h in a final volume of 15 µL. The digested DNA was evaluated on a 1% electrophoresis gel stained with ethidium bromide.
3. Results
Forty-four samples were collected in 2020, and 417 insects were evaluated. In 2021, 35 samples from 350 insects were collected (Table 1).
From the samples collected in both 2020 (Table 3 and Table S1) and 2021 (Table 4 and Table S2), all of the B. tabaci MED individuals were from the state of São Paulo.
The samples collected from the municipality of Sumaré in 2020 showed population fluctuation, with B. tabaci MED being the dominant cryptic species, except in February (Figure 2A). The same trend continued in 2021 in all samples collected (Figure 2B).
When summarizing the data collected in both years analyzed for the municipality of Sumaré, it was noticed that a difference of approximately 40% was observed in the population of B. tabaci MED as compared to that of B. tabaci MEAM1. By 2021, this difference increased to 70%.
The results for the municipality of Monte Mor were similar to the others, in which, of the samples collected in 2020, only those taken in August presented B. tabaci MEAM1 as the dominant species (Figure 3A). In 2021, B. tabaci MED remained the dominant cryptic species in all of the samples collected (Figure 3B).
When summarizing the data for the municipality of Monte Mor, a difference of approximately 36% in B. tabaci MED individuals was observed when compared to B. tabaci MEAM1 in 2020, which increased to approximately 76% for the year 2021.
Overall, it was observed that the occurrence of B. tabaci MEAM1 was approximately 10% higher than B. tabaci MED in 2020. In 2021, there was a reversal in this percentage, with B. tabaci MED being approximately 18% higher than that of B. tabaci MEAM1, and, in the samples from Minas Gerais, B. tabaci MED was not collected.
4. Discussion
From the data obtained, it was observed that for the regions in which the samples were collected, the presence of B. tabaci MED was the highest only in some of the municipalities in the state of São Paulo and was not detected in Minas Gerais. Therefore, these results may relate to different hypotheses.
The cryptic species B. tabaci MEAM1 is known to be generally dominant in Brazil [26]. Despite this, since its arrival in Brazil, B. tabaci MED has also been increasing in some agricultural systems in the country, especially in ornamental and vegetable crops, such as peppers and cucumbers [24,25,27].
Since B. tabaci MED is an exotic cryptic species that was recently reported in the country, it is necessary to understand the process of establishment of this species in other countries where it is not native. It is evident that each country has different characteristics such as climate, altitude, relief, types of crops, natural enemies, and agronomic management. Nevertheless, examples obtained from other regions of the world can help us understand how this scenario will evolve in our study region.
The cryptic species B. tabaci MED and MEAM1 are considered the most abundant globally and are distributed in 44 and 42 countries, respectively [18], highlighting their importance for Brazil, where both species are found and where little is known about their dynamics. In other countries, such as China, the cryptic invasive species B. tabaci MED has suppressed MEAM1 in several regions [31].
Furthermore, when chemical pesticides are used to manage B. tabaci, the B. tabaci MED species population may have an advantage due to its lower susceptibility to insecticides [32,33,34]. In this study, the management of all crop fields was similar, and farmers sprayed insecticide molecules such as sulfoxaflor, piriproxyfen, pyridabem, acetamiprid, flupyradifurone, pymetrozine, and cinantraniliprole. The use of these molecules may also be related to the suppression of B. tabaci MEAM1, noting that, in Brazil, the labeled doses of insecticides are only registered for B. tabaci MEAM1. However, as observed in the results (Table 1 and Table 2), this phenomenon only occurred in some regions, indicating that other factors may also be involved in these events.
Coincidentally, in the municipalities where B. tabaci MED was observed in abundance when compared to B. tabaci MEAM1, the altitudes were close to 600 m, whereas in other locations, the altitude was higher (Table 3 and Table 4). In regions of higher altitudes, thermal amplitudes tend to be greater with lower average temperatures. The B. tabaci MED populations tend to tolerate higher temperatures, whereas B. tabaci MEAM1 does not, which can explain the difference in the areas of occurrence between them [35,36,37]. Therefore, this factor may play an important role in the suppression of B. tabaci MEAM1 in open tomato fields.
Another hypothesis is that both municipalities in which samples with a higher amount of B. tabaci MED were collected are physically close to where the B. tabaci MED was first reported in the state of São Paulo, which was probably introduced through ornamental plants [25]. This region represents the largest commercial center for ornamental plants in the country. This supports the hypothesis that there is a greater migratory flow of different B. tabaci MED populations in this region of the state.
Another factor to be considered is the host—although studies conducted in Brazil have shown that in a scenario without the spraying of insecticides, tomatoes have more favorable characteristics for the development of B. tabaci MEAM1 [38,39]. In a scenario where insecticides are sprayed, this dynamic can change and B. tabaci MED becomes the dominant cryptic species [40].
5. Conclusions
In the state of São Paulo, the cryptic species B. tabaci MED has been established in commercial tomato crops in open fields. The cryptic species B. tabaci MED was not found in Minas Gerais.
It is still not possible to determine the main factors that influence its presence in open tomato fields. Perhaps there are more variables responsible for its establishment.
Therefore, constant monitoring studies of this pest in Brazil are increasingly necessary as the dynamics of these insects change rapidly, and focusing on these dynamic changes can be the key to the successful control of this insect from the perspective of integrated pest management.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14112516/s1, Table S1: Data referring to the cryptic species MEAM1 and MED collected in an open tomato field in the states of São Paulo and Minas Gerais in 2020; Table S2: Data referring to the cryptic species MEAM1 and MED collected in an open tomato field in the states of São Paulo and Minas Gerais in 2021.
Author Contributions
Conceptualization, D.d.L.A. and R.C.d.O.; formal analysis, C.d.C.M. and R.K.-S.; investigation, D.d.L.A. and D.M.S.; data curation, D.d.L.A.; writing—original draft preparation, D.d.L.A.; writing—review and editing, P.H.P.I.; supervision, R.C.d.O., S.R.B., C.M. and R.K.-S. All authors have read and agreed to the published version of the manuscript.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—finance code 001; Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP (processes number 2017/21588-7, 2018/02317-5, 2019/10736-0 and 2018/19782-2); Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (304126/2019-5) Regiane C. de Oliveira holds a CNPq fellowship. This research received no external funding. The APC was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (304126/2019-5) Regiane C. de Oliveira holds a CNPq fellowship.
Data Availability Statement
The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.
Acknowledgments
Thanks to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP, Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq, and Faculdade de Ciências Agronômicas (FCA) of Universidade Estadual Paulista “Júlio de Mesquita Filho”—Botucatu.
Conflicts of Interest
Author Sérgio Roberto Benvenga was employed by the company Inspecta—Pesquisa, Consultoria e Treinamento Ltda. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Figure 1.
(A) Locations of cities where the insects were collected in 2020. (B) Locations of cities where the insects were collected in 2021. Red area and gray points represent São Paulo state and cities, respectively. Yellow area and blue points represent Minas Gerais state and cities, respectively.
Figure 1.
(A) Locations of cities where the insects were collected in 2020. (B) Locations of cities where the insects were collected in 2021. Red area and gray points represent São Paulo state and cities, respectively. Yellow area and blue points represent Minas Gerais state and cities, respectively.
Figure 2.
(A) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2020 in Sumaré—SP. (B) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2021 in Sumaré—SP.
Figure 2.
(A) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2020 in Sumaré—SP. (B) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2021 in Sumaré—SP.
Figure 3.
(A) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2020 in Monte Mor—SP. (B) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2021 in Monte Mor—SP.
Figure 3.
(A) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2020 in Monte Mor—SP. (B) Percentage of Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in commercial tomato production fields in 2021 in Monte Mor—SP.
Table 1.
Location, coordinates, and altitude of samples collected in 2020.
| Local | Geographic Coordinates | ||
|---|---|---|---|
| Latitude | Longitude | Altitude (m) | |
| Apiaí—SP | S 24°20′59.5″ | W 49°01′15.4″ | 980.00 |
| Araras—SP | S 22°24′46.5″ | W 47°11′02.0″ | 637.00 |
| Araras—SP | S 22°21′39.7″ | W 47°07′27.2″ | 644.00 |
| Araras—SP | S 22°24′29.1″ | W 47°12′36.5″ | 655.00 |
| Capão Bonito—SP | S 24°04′47.1″ | W 48°12′32.1″ | 702.00 |
| Capão Bonito—SP | S 24°03′16.0″ | W 48°12′48.2″ | 745.00 |
| Capão Bonito—SP | S 24°03′27.5″ | W 48°13′22.6″ | 747.00 |
| Capão Bonito—SP | S 24°05′00.0″ | W 48°13′41.5″ | 789.00 |
| Mogi Guaçu—SP | S 22°22′15″ | W 46°56′16″ | 587.00 |
| Mogi Mirim—SP | S 22°19′50.8″ | W 47°04′21.5″ | 629.00 |
| Monte Mor—SP | S 22°53′53.9″ | W 47°20′53.9″ | 655.00 |
| Monte Mor—SP | S 22°53′52.7″ | W 47°20′31.2″ | 663.00 |
| Sumare—SP | S 22°53′24.9″ | W 47°16′23.6″ | 594.00 |
| Sumare—SP | S 22°53′09.5″ | W 47°16′07.1″ | 611.00 |
| Sumare—SP | S 22°53′37.0″ | W 47°16′37.5″ | 612.00 |
| Sumare—SP | S 22°53′52.6″ | W 47°15′44.2″ | 622.00 |
| Sumare—SP | S 22°53′30.5″ | W 47°15′51.0″ | 626.00 |
| Sumare—SP | S 22°53′49.1″ | W 47°16′42.4″ | 626.00 |
| Boa Esperança—MG | S 21°02′03.0″ | W 45°37′34.9″ | 808.00 |
| Campo do Meio—MG | S 21°04′50.8″ | W 45°51′19.4″ | 790.00 |
| Campo do Meio—MG | S 21°10′09.7″ | W 45°54′22.7″ | 794.00 |
| Campo do Meio—MG | S 21°09′14.9″ | W 45°56′11.8″ | 796.00 |
| Campo do Meio—MG | S 21°04′52.3″ | W 45°49′31.0″ | 800.00 |
| Campo do Meio—MG | S 21°04′22.4″ | W 45°51′46.0″ | 805.00 |
| Campos Gerais—MG | S 21°10′38.6″ | W 45°35′46.1″ | 855.00 |
| Campos Gerais—MG | S 21°09′20.7″ | W 45°36′37.5″ | 890.00 |
Latitude and longitude are expressed in degrees (°), minutes (′), and seconds (″). Altitude is expressed in meters (m). SP—state of São Paulo. MG—state of Minas Gerais.
Table 2.
Location, coordinates, and altitude of samples collected in 2021.
| Local | Geographic Coordinates | ||
|---|---|---|---|
| Latitude | Longitude | Altitude (m) | |
| Araras—SP | S 22°25′05.4″ | W 47°11′04.0″ | 640.00 |
| Araras—SP | S 22°21′41.3″ | W 47°07′27.8″ | 643.00 |
| Araras—SP | S 22°24′29.2″ | W 47°12′36.4″ | 657.00 |
| Mogi Mirim—SP | S 22°19′10.8″ | W 47°03′32.7″ | 606.00 |
| Monte Mor—SP | S 22°54′24.3″ | W 47°21′14.4″ | 622.00 |
| Sumare—SP | S 22°53′32.7″ | W 47°17′12.3″ | 607.00 |
| Sumare—SP | S 22°53′53.8″ | W 47°16′12.3″ | 621.00 |
| Sumare—SP | S 22°53′49.2″ | W 47°15′36.8″ | 635.00 |
| Andrelândia—MG | S 21°41′36.7″ | W 44°11′08.8″ | 1149.00 |
| Campo do Meio—MG | S 21°10′09.7″ | W 45°54′22.7″ | 794.00 |
| Campos Gerais—MG | S 21°09′51.2″ | W 45°35′52.1″ | 852.00 |
| Campos Gerais—MG | S 21°10′01.5″ | W 45°35′46.4″ | 860.00 |
| Campos Gerais—MG | S 21°09′20.7″ | W 45°36′37.5″ | 890.00 |
| Sacramento—MG | S 19°39′03.1″ | W 47°33′21.8″ | 1038.00 |
| Sacramento—MG | S 19°38′47.3″ | W 47°33′04.7″ | 1041.00 |
Latitude and longitude are expressed in degrees (°), minutes (′), and seconds (″). Altitude is expressed in meters (m). SP—state of São Paulo. MG—state of Minas Gerais.
Table 3.
Data referring to the cryptic species Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in open tomato fields in the states of São Paulo and Minas Gerais in 2020.
Table 3.
Data referring to the cryptic species Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in open tomato fields in the states of São Paulo and Minas Gerais in 2020.
| Local | Geographic Coordinates | Collection Days | Results (%) | |||
|---|---|---|---|---|---|---|
| Latitude | Longitude | Altitude (m) | MEAM1 | MED | ||
| Apiaí—SP * | S 24°20′59.5″ | W 49°01′15.4″ | 980.00 | 27 Nov 20 | 30 | 0 |
| Araras—SP | S 22°24′46.5″ | W 47°11′02.0″ | 637.00 | 30 Jul 20 | 100 | 0 |
| Araras—SP | S 22°21′39.7″ | W 47°07′27.2″ | 644.00 | 04 Jun 20 | 100 | 0 |
| Araras—SP | S 22°24′29.1″ | W 47°12′36.5″ | 655.00 | 13 Apr 20 | 100 | 0 |
| Capão Bonito—SP | S 24°04′47.1″ | W 48°12′32.1″ | 702.00 | 06 Feb 20 | 90 | 10 |
| Capão Bonito—SP | S 24°03′27.5″ | W 48°13′22.6″ | 747.00 | 07 Feb 20 | 80 | 20 |
| Capão Bonito—SP * | S 24°03′16.0″ | W 48°12′48.2″ | 745.00 | 08 Sep 20 | 20 | 0 |
| Capão Bonito—SP * | S 24°05′00.0″ | W 48°13′41.5″ | 789.00 | 08 Sep 20 | 50 | 10 |
| Mogi Guaçu—SP ** | S 22°22′15″ | W 46°56′16″ | 587.00 | 04 Feb 20 | 100 | 0 |
| Mogi Mirim—SP | S 22°19′50.8″ | W 47°04′21.5″ | 629.00 | 15 Apr 20 | 100 | 0 |
| Monte Mor—SP | S 22°53′53.9″ | W 47°20′53.9″ | 655.00 | 15 Aug 20 | 60 | 40 |
| 15 Sep 20 | 40 | 60 | ||||
| 15 Oct 20 | 30 | 70 | ||||
| 15 Nov 20 | 20 | 80 | ||||
| 15 Dec 20 | 10 | 90 | ||||
| Monte Mor—SP | S 22°53′52.7″ | W 47°20′31.2″ | 663.00 | 18 Apr 20 | 30 | 70 |
| Sumare—SP | S 22°53′24.9″ | W 47°16′23.6″ | 594.00 | 15 Aug 20 | 20 | 80 |
| 15 Sep 20 | 10 | 90 | ||||
| 15 Oct 20 | 30 | 70 | ||||
| 15 Nov 20 | 60 | 40 | ||||
| 15 Dec 20 | 0 | 100 | ||||
| Sumare—SP | S 22°53′09.5″ | W 47°16′07.1″ | 611.00 | 15 Aug 20 | 62.5 | 37.5 |
| 15 Sep 20 | 90 | 10 | ||||
| 15 Oct 20 | 30 | 70 | ||||
| 15 Nov 20 | 20 | 80 | ||||
| 15 Dec 20 | 0 | 100 | ||||
| Sumare—SP | S 22°53′37.0″ | W 47°16′37.5″ | 612.00 | 06 Jun 20 | 10 | 90 |
| Sumare—SP | S 22°53′52.6″ | W 47°15′44.2″ | 622.00 | 24 Feb 20 | 80 | 20 |
| 16 Apr 20 | 20 | 80 | ||||
| 07 May 20 | 40 | 60 | ||||
| Sumare—SP | S 22°53′30.5″ | W 47°15′51.0″ | 626.00 | 16 Apr 20 | 10 | 90 |
| Sumare—SP | S 22°53′49.1″ | W 47°16′42.4″ | 626.00 | 15 Aug 20 | 50 | 50 |
| 15 Sep 20 | 10 | 90 | ||||
| 15 Oct 20 | 10 | 90 | ||||
| 15 Nov 20 | 20 | 80 | ||||
| 15 Dec 20 | 10 | 90 | ||||
| Boa Esperança—MG | S 21°02′03.0″ | W 45°37′34.9″ | 808.00 | 27 Jul 20 | 100 | 0 |
| Campo do Meio—MG | S 21°04′50.8″ | W 45°51′19.4″ | 790.00 | 06 Jul 20 | 100 | 0 |
| Campo do Meio—MG | S 21°10′09.7″ | W 45°54′22.7″ | 794.00 | 05 Mar 20 | 100 | 0 |
| Campo do Meio—MG | S 21°09′14.9″ | W 45°56′11.8″ | 796.00 | 27 Oct 20 | 100 | 0 |
| Campo do Meio—MG | S 21°04′52.3″ | W 45°49′31.0″ | 800.00 | 29 Aug 20 | 100 | 0 |
| Campo do Meio—MG | S 21°04′22.4″ | W 45°51′46.0″ | 805.00 | 30 Jan 20 | 100 | 0 |
| Campos Gerais—MG | S 21°10′38.6″ | W 45°35′46.1″ | 855.00 | 29 Jan 20 | 100 | 0 |
| Campos Gerais—MG | S 21°09′20.7″ | W 45°36′37.5″ | 890.00 | 31 Jan 20 | 100 | 0 |
* Other insects were collected in the sample (Thrips spp.); ** sample collected in a greenhouse.
Table 4.
Data referring to the cryptic species Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in open tomato fields in the states of São Paulo and Minas Gerais in 2021.
Table 4.
Data referring to the cryptic species Bemisia tabaci MEAM1 and Bemisia tabaci MED collected in open tomato fields in the states of São Paulo and Minas Gerais in 2021.
| Local | Geographic Coordinates | Collection Days | Results (%) | |||
|---|---|---|---|---|---|---|
| Latitude | Longitude | Altitude (m) | MEAM1 | MED | ||
| Araras—SP | S 22°25′05.4″ | W 47°11′04.0″ | 640.00 | 21 Jun 21 | 100 | 0 |
| Araras—SP | S 22°21′41.3″ | W 47°07′27.8″ | 643.00 | 28 Apr 21 | 100 | 0 |
| Araras—SP | S 22°24′29.2″ | W 47°12′36.4″ | 657.00 | 15 Mar 21 | 100 | 0 |
| Mogi Mirim—SP | S 22°19′10.8″ | W 47°03′32.7″ | 606.00 | 30 Mar 21 | 100 | 0 |
| Monte Mor—SP | S 22°54′24.3″ | W 47°21′14.4″ | 622.00 | 15 Feb 21 | 20 | 80 |
| 15 Mar 21 | 20 | 80 | ||||
| 15 Apr 21 | 20 | 80 | ||||
| 15 May 21 | 0 | 100 | ||||
| 15 Jun 21 | 10 | 90 | ||||
| 15 Jul 21 | 0 | 100 | ||||
| Sumare—SP | S 22°53′32.7″ | W 47°17′12.3″ | 607.00 | 15 Feb 21 | 10 | 90 |
| 15 Mar 21 | 10 | 90 | ||||
| 15 Apr 21 | 0 | 100 | ||||
| 15 May 21 | 0 | 100 | ||||
| 15 Jun 21 | 0 | 100 | ||||
| 15 Jul 21 | 0 | 100 | ||||
| Sumare—SP | S 22°53′53.8″ | W 47°16′12.3″ | 621.00 | 15 Feb 21 | 30 | 70 |
| 15 Mar 21 | 10 | 90 | ||||
| 15 Apr 21 | 0 | 100 | ||||
| 15 May 21 | 0 | 100 | ||||
| 15 Jun 21 | 0 | 100 | ||||
| 15 Jul 21 | 0 | 100 | ||||
| Sumare—SP | S 22°53′49.2″ | W 47°15′36.8″ | 635.00 | 15 Feb 21 | 100 | 0 |
| 15 Mar 21 | 40 | 60 | ||||
| 15 Apr 21 | 30 | 70 | ||||
| 15 May 21 | 10 | 90 | ||||
| 15 Jun 21 | 30 | 70 | ||||
| 15 Jul 21 | 0 | 100 | ||||
| Andrelândia—MG | S 21°41′36.7″ | W 44°11′08.8″ | 1149.00 | 25 Feb 21 | 100 | 0 |
| Campo do Meio—MG | S 21°10′09.7″ | W 45°54′22.7″ | 794.00 | 29 Mar 21 | 100 | 0 |
| Campos Gerais—MG | S 21°09′51.2″ | W 45°35′52.1″ | 852.00 | 25 Jan 21 | 100 | 0 |
| Campos Gerais—MG | S 21°10′01.5″ | W 45°35′46.4″ | 860.00 | 01 Feb 21 | 100 | 0 |
| Campos Gerais—MG | S 21°09′20.7″ | W 45°36′37.5″ | 890.00 | 22 Jan 21 | 100 | 0 |
| Sacramento—MG | S 19°39′03.1″ | W 47°33′21.8″ | 1038.00 | 18 Jan 21 | 100 | 0 |
| Sacramento—MG | S 19°38′47.3″ | W 47°33′04.7″ | 1041.00 | 24 Aug 20 | 100 | 0 |
Latitude and longitude are expressed in degrees (°), minutes (′), and seconds (″). Altitude is expressed in meters (m). SP—state of São Paulo. MG—state of Minas Gerais.
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de Lima Alvarez, D.; Santos, D.M.; Ikuno, P.H.P.; da Cruz Martines, C.; Benvenga, S.R.; Müller, C.; Krause-Sakate, R.; de Oliveira, R.C. Occurrence of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East–Asia Minor 1 (MEAM1) and Mediterranean (MED) in Commercial Fields of Solanum lycopersicum in Brazil. Agronomy 2024, 14, 2516. https://doi.org/10.3390/agronomy14112516
AMA Style
de Lima Alvarez D, Santos DM, Ikuno PHP, da Cruz Martines C, Benvenga SR, Müller C, Krause-Sakate R, de Oliveira RC. Occurrence of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East–Asia Minor 1 (MEAM1) and Mediterranean (MED) in Commercial Fields of Solanum lycopersicum in Brazil. Agronomy. 2024; 14(11):2516. https://doi.org/10.3390/agronomy14112516
Chicago/Turabian Stylede Lima Alvarez, Daniel, Daniel Mariano Santos, Pedro Hiroshi Passos Ikuno, Caroline da Cruz Martines, Sérgio Roberto Benvenga, Cristiane Müller, Renate Krause-Sakate, and Regiane Cristina de Oliveira. 2024. "Occurrence of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East–Asia Minor 1 (MEAM1) and Mediterranean (MED) in Commercial Fields of Solanum lycopersicum in Brazil" Agronomy 14, no. 11: 2516. https://doi.org/10.3390/agronomy14112516
APA Stylede Lima Alvarez, D., Santos, D. M., Ikuno, P. H. P., da Cruz Martines, C., Benvenga, S. R., Müller, C., Krause-Sakate, R., & de Oliveira, R. C. (2024). Occurrence of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East–Asia Minor 1 (MEAM1) and Mediterranean (MED) in Commercial Fields of Solanum lycopersicum in Brazil. Agronomy, 14(11), 2516. https://doi.org/10.3390/agronomy14112516
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