Spatial distribution of Bemisia tabaci MEAM1 nymphs and adults in soybean crops: An Analysis of Dispersions and Population FrequenciesABSTRACT
Bemisia tabaci MEAM1 (Hemiptera: Aleyrodidae) is a polyphagous insect with high dispersion ability, enabling it to easily establish itself on various hosts. In soybeans, its incidence has been increasing over the years. This study aimed to investigate the spatial distribution of B. tabaci nymphs and adults in different soybean canopy strata under field conditions. The study was conducted in four soybean fields during two growing seasons. Each field was composed of 50 plots of 10 x 10 m, distributed in five blocks of 10 plots each. Weekly samplings were performed to collect B. tabaci adults and nymphs. Aggregation indices were used to assess the degree of aggregation of B. tabaci, including the variance-to-mean ratio, Morisita’s index, and the k exponent. In addition, the occurrence data recorded in the fields were fitted to Poisson and negative binomial distributions. The results indicated that the distribution of B. tabaci was aggregated, both for nymphs and adults, throughout the crop development. The negative binomial distribution best described the distribution of B. tabaci in soybean crops. These findings suggest that monitoring of B. tabaci should be conducted throughout the crop season, as efficient pest management is closely related to the timing of decision-making for control measures. The information obtained in this study provides valuable insights into the aggregation behavior of B. tabaci in soybean crops, contributing to the development of more effective pest management strategies. These strategies, when well-implemented, can reduce the use of insecticides, lower pest control costs, and preserve beneficial insects in the crop.
Keywords:
Whitefly; Aggregation indices; Theoretical frequency distributions; Sampling scheme; Monitoring
Introduction
Soybean (Glycine max (L.) Merr.) is the world's leading oilseed crop, with global production of 401.325 million tons (Lemos et al., 2017). Brazil contributed 154.605 million tons, representing 38.5% of the worldwide output (CONAB, 2023). This oilseed plays a crucial role in various production chains, including those related to animal and human food, biofuels, textiles, paints, and plastics (Cunha and Espíndola, 2015). However, soybean cultivation faces the attack of several insect pests. Among them, the whitefly Bemisia tabaci MEAM1 (Gennadius) (Hemiptera: Aleyrodidae) is considered a key pest in this production context (Arcanjo et al., 2023).
Whiteflies wreak havoc on crops in multiple ways. Adults and nymphs directly damage plants by sucking sap from the phloem (Gangwar and Charu, 2018). Furthermore, they can cause indirect damage due to the excretion of a sugary secretion called honeydew, which fuels the growth of a sooty mold (Capnodium) that blocks sunlight and saps photosynthetic capacity (Lima et al., 2018). Their prolific breeding, short life cycle, diverse diet, migratory habits, and global reach solidify their reputation as a major pest (Cruz and Baldin, 2017).
Although B. tabaci has been associated with soybeans for several years, it was considered a secondary pest. However, considerable damage began to be reported due to high infestations in the 1990s (Czepak et al., 2018). Currently, it is widespread in agricultural areas, causing losses in various cultivated crops such as cotton, cucurbits, beans, tomatoes, vegetables, and soybeans (Silva et al., 2017).
Given the increasing importance of this insect for soybean cultivation in Brazil, sampling techniques are still being established and tested to facilitate field monitoring. Effective sampling of pest population density is essential for pest control decision-making (Czepak et al., 2018; Pozebon et al., 2019). Determining the spatial distribution of B. tabaci is the first step in establishing efficient sampling plans, aiming to reduce sampling time and increase result reliability (Grigolli et al., 2012). Furthermore, it provides an accurate representation of the insect's virus aggregation indices and theoretical frequency distribution, yielding comparable results (Fernandes et al., 2018).
Pinpointing an insect's distribution within a field depends on two key things: sampling the relevant ecosystem (Suekane et al., 2018) and having an ecosystem that allows for proper sampling. These samplings then reveal whether the insects have an aggregated, uniform, or random distribution. Confirming the exact distribution pattern, however, requires comparing the observed data to theoretical frequency distributions for the specific insect and crop (Barbosa and Perecin, 1982).
In light of the above, this study aimed to provide an in-depth understanding of the horizontal distribution of B. tabaci across various stages of soybean growth to understand its population dynamics better and help develop more effective pest management strategies.
Materials and methods
This study was conducted under field conditions in four commercial production areas each year, over two agricultural years, with two areas located in the municipality of Dourados-MS (latitude 22°15'S, longitude 54°24'W), and the other two in the municipality of Anaurilândia-MS (latitude 22°16'S, longitude 52°53'W), during the agricultural years of 2020/21 and 2021/22.
The experimental areas were cultivated with the M 5947 IPRO soybean variety in both agricultural years, with a spacing of 0.5 meters between rows. Crop, disease and weed management were carried out following the crop's recommendations to avoid interference with the whitefly population (Sediyama et al., 2015).
A total of 12 evaluations were conducted in the agricultural year 2020/21, and 11 evaluations in the agricultural year 2021/22, in each sample field. The characterization of soybean plant development stages followed the methodology proposed by Sediyama et al. (2015), dividing the crop into vegetative stages (V1 to Vn) and reproductive stages (R1 to R8).
Within their respective municipality, areas were spaced 2000 meters from each other. These areas consisted of 50 plots measuring 10 x 10 meters (100m2), distributed in five blocks of 10 plots each. The spatial distribution of B. tabaci nymphs was determined through weekly sampling, using the methodology proposed by Czepak et al. (2018). The adults were counted using a vacuum-type suction device coupled to an acrylic structure measuring 0.70 m wide and 0.50 m long (Figure 1) for 30 seconds of suction per plot.
Front view of the assembled device for collection and sampling adults of Bemisia tabaci, exemplifying its use in the soybean crop field.
Figure 2 shows the various parts that make up the system, in which component (a) is a combustion engine with 0.7 kW. Component (b) is an adapter that can be fitted to the motor, and a simple tube on the other side. Component (c) is a 12-inch corrugated hose, which is clamped to component (b). Component (d) is a rim covered with a voile fabric, which is accommodated in component (c), forming a kind of removable basket. Item (e) is a steel funnel with support for loading, and item (d) is attached to the smaller base of the funnel. The larger base of the funnel is then fitted to item (f), which is made of acrylic and zinc.
Front view of the assembled device for collection and sampling adults of Bemisia tabaci and its respective disassembled parts (a) combustion engine, (b) adapter, (c) corrugated hose, (d) rim covered with a voile fabric, (e) steel funnel, (f) isolation dome.
The engine (Figure 2A), when turned on, creates a vacuum inside component (f), which sucks the insects along component (e) and traps them in component (d). Component (d) is removed from component (e) for insect counting, allowing the insects retained in the basket to be counted on the voile fabric.
The infestation of B. tabaci occurred naturally, and the number of nymphs and adults counted was grouped according to soybean phenology and used to determine the mathematical description of the B. tabaci population distribution. This was done through the calculation of the mean, variance, aggregation indices, and theoretical frequency distributions.
The degree of B. tabaci aggregation was assessed through the following indices: variance-to-mean ratio, Morisita Index, and k exponent of the negative binomial distribution (Fernandes et al., 2018). Furthermore, theoretical frequency distributions (Poisson distribution and negative binomial distribution) were employed to fit the occurrence data of the insects observed in the fields, as described by Fonseca et al. (2017). Statistical analysis was performed using the chi-squared test (χ2) at 1% and 5% probability levels.
Results
A total of 28,324 nymphs and 15,448 adults were counted in the sample areas in the 2020/21 growing season, and 7,683 nymphs and 6,729 adults in the 2021/22 growing season. Evaluations were conducted from emergence to maturity. Adults were observed from V2 (second trifoliate leaf opened), and nymphs from V4 (fourth trifoliate leaf opened), with the highest occurrence of nymphs and adults during pod formation and grain filling.
Dispersion Indices:Table 1 shows the mean, variance, and aggregation indices (variance-to-mean ratio (I), Morisita's Index (I), and k exponent). Based on the variance-to-mean ratio (I) and Morisita's (I) indices, the distribution of B. tabaci nymphs in the upper canopy stratum was random at V4 and R1, but aggregated in all other evaluations, regardless of the evaluation location (upper, middle third, and lower canopy strata). Conversely, based on the k exponent of the negative binomial (Table 1), nymph infestation occurred in an aggregated manner in almost all evaluations, except for the upper canopy at R1 (uniform). For B. tabaci adults (Table 1), the aggregation indices variance-to-mean ratio (I) and Morisita's Index (I) indicated randomness at V2, V4, and R1. However, subsequent evaluations indicated an aggregated distribution type. According to the k exponent of the negative binomial, except for V2 (uniform), adult distribution was aggregated throughout the crop cycle.
Evaluation timing (in days after emergence: DAE), plant phenology, average infestation, and dispersion indices of Bemisia tabaci nymphs and adults in soybean cultivation under field conditions.
Frequency Distribution:Table 2 displays the chi-squared values obtained for B. tabaci nymphs fit to both theoretical frequency distribution models. Nymphs in the upper canopy fit the Poisson distribution seven times (V6, R3, R5, R5.4, R6, R7, and R8), and the negative binomial distribution three times (V6, R6, and R7). Nymphs in the middle third of the canopy fit the Poisson distribution nine times (R1, R2, R3, R4, R5, R5.4, R6, R7, and R8), and the negative binomial distribution four times (R1, R2, R7, and R8). Nymphs in the lower canopy fit the Poisson distribution six times (R2, R3, R4, R5, R5.4, and R6), and the negative binomial distribution three times (R2, R3, and R5). The total number of nymphs fit the Poisson distribution ten times (V6, R1, R2, R3, R4, R5, R5.4, R6, R7, and R8), and the negative binomial distribution seven times (V6, R2, R5, R5.4, R6, R7, and R8). Adults (Table 2) fit the Poisson distribution nine times (R1, R2, R3, R4, R5, R5.4, R6, R7, and R8), and the negative binomial distribution six times (R1, R3, R4, R5, R6, and R8). In ecological statistics, the best fit occurs for frequency distributions that have the lowest chi-squared value.
Chi-squared goodness-of-fit test for observed frequencies to expected frequencies under the negative binomial and Poisson distributions for the number of Bemisia tabaci nymphs and adults in soybean cultivation under field conditions.
The number of B. tabaci class frequencies (Table 2) was insufficient to detect nymph distribution in the upper canopy at V4, R1, and R4, and for adults at V2 and V4. This outcome is due to the low occurrence of the species during these periods. Based on this, Table 2 highlights a distribution pattern for the pest. Nymphs, regardless of the occurrence location, fit better to the negative binomial distribution, showing that nymph distribution in soybean crops occurs in an aggregated way (S2 > ṁ). Regarding adults (Table 2), a better fit to the Poisson distribution is observed until V6; however, in subsequent evaluations, the best fit was achieved for the negative binomial distribution. Therefore, based on the theoretical frequency distribution, adults at the beginning of infestation exhibit a random distribution. Nonetheless, as infestation increases, the distribution becomes aggregated.
Discussion
When analyzing distribution, nymphs showed different patterns throughout canopy thirds and plant development stages. However, they tended to be aggregated along the developmental stages of soybeans. Czepak et al. (2018) observed similar behavior for distinct whitefly stages (egg, nymph, and pupal) in all thirds of soybean plants.
Regarding adult whitefly distribution, most evaluations, similar to the nymphal stage, showed them aggregating together. However, Suekane et al. (2018) observed this aggregation pattern only at the beginning of soybean development, with a uniform distribution when the whitefly population peaks. Conversely, other research supports an aggregated distribution for both nymphal and adult whiteflies in soybeans (Rodrigues et al., 2022). This pest has also shown the same distribution in other crops like cotton (Rodrigues et al., 2010) and cucumber (Moura et al., 2003).
Pozebon et al. (2019) analyzed whitefly distribution on soybean leaflets in both greenhouse and field settings. They observed that the pest also tends to aggregate in the middle and lower regions of leaflets under the greenhouse and the middle third in the field (Pozebon et al., 2019). This further reinforces that whiteflies tend to exhibit this pattern of aggregated behavior in infested crops, as was the case with soybeans.
Whiteflies are typically present in soybean crops throughout almost all stages of their development, reaching their peak population during the reproductive phase (Padilha et al., 2021). In this stage, an aggregative behavior is more evident, showing the pest is well established in the crop. Additionally, during this period, the crop is more vulnerable to the pest's attack, mainly due to the occurrence of sooty mold, which compromises the plant's photosynthetic capacity and, consequently, its productivity (Vieira et al., 2011).
This aggregative behavior of whiteflies, especially during the reproductive stages, can be supported by the fact that this insect has a fixed nymphal stage. While mobile in its first instar, during which the insect seeks the best location to feed, it becomes fixed upon molting until the emergence of the adult (Sani et al., 2020). This favors the whitefly to exhibit this pattern of aggregated distribution in its infestations.
Understanding the infestation patterns of whiteflies during crop development, as well as within distinct parts of the plant, is of utmost importance. The infestation pattern in various parts of the plant can vary depending on the plant's developmental stage, as identified by Czepak et al. (2018), especially for nymphs. Therefore, monitoring efforts for whiteflies should be intensified at the end of the vegetative stage and the beginning of the reproductive stage, as it is during these periods that whiteflies start to establish themselves in the crop, and both nymphs and adults can be observed (Rodrigues et al., 2022).
However, pest monitoring should be conducted throughout the entire period of the pest's development in the crop. Effective management of whiteflies is closely related to the timing of decision-making for the implementation of control measures. In this sense, sampling plans are a crucial factor in Integrated Pest Management (Pozebon et al., 2019).
Our findings contribute to understanding the distribution patterns of whitefly nymphs and adults in soybean crops. They emphasize the need for monitoring distinct stages of the pest, as well as different plant strata during its nymphal stage. This information can be used in sampling plans and, when effectively applied, reduce the use of insecticides and pest control costs, while also preserving beneficial insects in the crop (Rodrigues et al., 2010).
In summary, our study provides valuable insights into the behavior of whiteflies in soybean cultivation, which can be useful for more effective management strategies.
Conclusions
Whiteflies (Bemisia tabaci MEAM1) exhibit an aggregative behavior in soybean cultivation, both for nymphs and adults. This behavior is more evident during the reproductive stages of the plant.
Whitefly infestation pattern may vary with the plant's developmental stage and the stratum at which it is found.
Whitefly monitoring must be carried out throughout the pest's development period in the crop.
Acknowledgments
We wish to thank IFMS for financial support for the translation of this article. We are also grateful to DMA AGROPECUÁRIA for logistical support and aid in cultural management.
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Edited by
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Associate Editor:
Takumasa Kondo
