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Article

Diversity of Thrips Species Associated with Soybean Grown in Different Plant Arrangements at Various Phenological Stages

by
Jacek Twardowski
1,*,
Iwona Gruss
1,
Marcin Cierpisz
1,
Kamila Twardowska
1,
Joanna Magiera-Dulewicz
1 and
Marcin Kozak
2
1
Department of Plant Protection, Wrocław University of Environmental and Life Sciences, Grunwaldzki Square 24a, 50-363 Wrocław, Poland
2
Institute of Agroecology and Plant Production, Wrocław University of Environmental and Life Sciences, Grunwaldzki Square 24a, 50-363 Wrocław, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(9), 1501; https://doi.org/10.3390/agriculture14091501
Submission received: 27 June 2024 / Revised: 19 August 2024 / Accepted: 21 August 2024 / Published: 2 September 2024
(This article belongs to the Section Crop Protection, Diseases, Pests and Weeds)
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Abstract

:
Changes in crop seeding density may affect the presence of phytophagous organisms, whose development is closely associated with host plants. The main objective of this study was to evaluate the abundance and species composition of thrips (Thysanoptera) collected in soybean plants of two different varieties cultivated in different plant arrangements (row spacing, seed density) at different phenological stages. The research was carried out at two locations in southwest Poland between 2015 and 2018. The herbivores that inhabited the plants were caught using an entomological net. The experiments were conducted using a complete block design with four replications. A total of 20 species of thrips were identified and their dietary specialization was determined with an emphasis on the possibility of feeding on Fabaceae plants. Thrips tabaci, Aeolothrips intermedius, and T. fuscipes were the dominant species within the collected material. The general linear model revealed no significant changes in the number of thrips caused by the row spacing, seed density or soybean variety. The significant factor was the phenological stage. The number of thrips increased significantly during the flowering period and shortly after flowering, making them an important threat to the plants. Therefore, it is crucial to develop innovative pest management strategies tailored to effective soybean cultivation to mitigate potential pest-related challenges.

1. Introduction

Soybean is one of the most important crops in many parts of the world, along with wheat, rice and maize. Most of the production is located in the United States, Brazil and Argentina [1]. The seeds of this crop contain approximately 40% protein and 20% oil, making it a high-quality food for humans and animals. According to FAOSTAT data [2], the area under soybean in the world exceeds 132 million hectares, of which about 4% is placed in the European Union. The area of soybean cultivation has also increased in Poland, and the demand for its seeds is increasing every year. New varieties are being developed that can adapt to European climatic conditions and the length of the day. There are currently 40 varieties in the National Register of Agricultural Crops in Poland, and the number of varieties has increased significantly in recent years. In 2024, the soybean area was estimated at 79.8 thousand hectares (compared to around 48.2 thousand hectares in 2022) [3]. However, this crop is still considered a minor crop due to low and unstable yields [4].
Both plant spacing and density can significantly impact environmental conditions in the field, directly affecting the presence of entomofauna [5]. A higher plant density prevents the soil from heating up and keeps the air humidity relatively constant. The microclimate of a given field affects not only the size and quality of the crop, but also the presence and development of insects [6]. When considering the effect of plant density on the presence of harmful and beneficial entomofauna, it must also be taken into account that density affects not only the amount of food available in the form of host plants, but also the quality of this food, because sufficiently high density causes excessive competition for light and microelements contained in the soil, a change in the nutrient content of the plant and consequently a change in the attractiveness of plants to herbivores [7].
Thrips (Thysanoptera) are important herbivores that feed on soybean plants and are also responsible for virus transmission. Neves et al. [8] found for these reasons that soybean yield losses can reach 17%. More than 6500 thrips species have been identified worldwide, of which about 60 are considered crop pests and only about a dozen are capable of transmitting viruses [9,10]. The Thysanoptera fauna in Poland contains 226 species. The very uneven knowledge of these insects throughout the country makes it difficult to determine the level of threat to the species, which also affects agricultural crops. They have piercing sucking mouthparts, but unlike Hemiptera, the mouthparts of Thysanoptera are asymmetrical (with the right lower mandibles strongly reduced) [11]. These insects, which undergo incomplete metamorphosis, damage various parts of the plant (leaves, flowers, and rarely fruits), suck the contents of mesophyll cells, and inject toxins into the plants, causing typical discoloration in the form of silver-white spots and visible pieces of dark feces. Later feeding causes deformation and death of young leaves, premature leaf fall, and the death of healthy plants. Thrips appear to be particularly dangerous during flowering when soybean is often attacked. They spend most of their time hiding under leaves, which is made possible by their small size (most species reach 1–2 mm in body size) [12,13]. Their cryptic lifestyle makes them difficult to control with insecticides [14].
One of the most common pests in the order Thysanoptera is tobacco thrips (Thrips tabaci) [15]. It is a polyphagous species that is widespread in field and greenhouse crops throughout the world, including Poland. Its relatively short developmental cycle and its ability to undergo parthenogenesis make it an extremely dangerous pest of many crops [16]. In agricultural and horticultural practice, thrips play a major negative role in cereals (Haplothrips aculeatus, H. tritici, Limothrips cerealium, L. denticornis), legumes (Thrips major, T. fuscipennis, T. flavus, Frankliniella intosa, Taeniothrips atratus, Odontothrips loti), vegetables (Kakothrips robustus, T. tabaci), and greenhouse plants (F. occidentalis, T. tabaci) [16,17,18,19,20]. Crops also often contain beneficial Thysanoptera species. A common species in Poland is Aeolothrips intermedius, which is mainly a natural enemy of other thrips and mites (both adults and larvae of these species are predators) [21]. To date, no specific studies have been conducted on thrips that occur in soybean plants in Eastern Europe. The main objective of this study was to analyze the abundance and species composition of thrips in soybean crops with different plant arrangements at various phenological stages.

2. Materials and Methods

2.1. Study Area

Field research was carried out in 2015–2018 in two locations in southwest Poland: Agricultural Experimental Station in Wrocław-Pawłowice (51°10′36.5 N, 17°06′24.9 E) (Location 1), which is part of the Wroclaw University of Environmental and Life Sciences (Lower Silesia), and the experimental fields of the Opole Agricultural Advisory Centre (OODR) in Łosiów (50°80′14 N, 17°55′22 E) (Location 2) (Opole Voivodeship).
At Location 1, the experiment was conducted from 2015 to 2017 in a soybean plantation of the Merlin variety (Saatbau Linz, Austria). It was grown on typical brown Luvisols developed from light loam, underlaid by medium loam, which is suitable for wheat production [22]. In each year of the study, the soybean was grown under the same habitat conditions, next to the site of the previous year’s cultivation. A slight change in the site of the research plantation was made in accordance with the principles of crop rotation. The forecrop was always winter wheat of the Ostroga variety (Danko, Kościan, Poland). Wheat was always harvested with a combine harvester in the first ten days of August, and the crop residues were left in the field. Autumn tillage treatments included pre-winter ploughing and treatments with a tillage unit (spring cultivator + spring roller). In spring, the field was fertilized with the following doses (kg ha−1) 60 P2O5, 120 K2O and 30 N. In addition, a starting dose (28–30 kg/ha N) was applied prior to the symbiosis of plants with Bradyrhizobium japonicum. In each study year, soybean seeds were sown with a plot seeder in the third decade of April. The sowing depth was 3–4 cm. Before the emergence of soybean, herbicide treatments were applied to reduce the occurrence of dicotyledonous weeds (Afalon 450 SC with linuron as active ingredient, Agan Chemical Manufactures Ltd., Ashdod, Israel) at a dose of 1.5 dm3 ha−1. In the second decade of May, after emergence, a treatment was applied against dicotyledonous and some monocotyledonous weeds (Corum 502.4 SL, bentazon and imazamox as the active ingredients, BASF SE, Ludwigshafen, Germany) at a dose of 1.25 dm3 ha−1, combined with an adjuvant containing methyl oleate and fatty alcohol (Dash HC, BASF SE, Ludwigshafen, Germany) at a dose of 0.6 dm3 ha−1. No insecticide or fungicide treatments were applied in the field trial. Soybean was harvested in the middle of September each year when the pods were fully ripe.
In Location 2, soybean was grown under the same habitat conditions in each year of the study (2016–2018), next to the field location of the previous year. A slight change in field site was necessary due to crop rotation principles. In each year, soybean was grown in soil belonging to the brown soil type and its soil suitability complex was defined as very good rye. In each year, the forecrop was winter wheat of the Dakotana variety (KWS Lochow, Poland). In spring, pre-sowing fertilization was applied in the following doses: P2O5—20 (kg ha−1), K2O—40 (kg ha−1), MgO—31 (kg ha−1), S—26 (kg ha−1) and N—28 (kg ha−1). In addition, a starting dose (28–30 kg/ha N) was applied prior to the symbiosis of plants with Bradyrhizobium japonicum. The differential fertilization of soybean at both experimental locations depended on the content of macronutrients in the soil. Soybean was sown in the third decade of April. The sowing depth was 4 cm. Pre-emergence herbicide treatments were applied throughout the plantation to reduce dicotyledonous weeds (Sencor Liquid 600 SC (metribuzin as the active ingredient, Bayer SAS, Lyon, France) + Command 480 EC (clomazone, FMC Chemical, Brussels, Belgium) at doses of 0.6 and 0.2 dm3 ha−1 respectively). The post-emergence treatment against dicotyledonous and some monocotyledonous weeds (Corum 502.4 SL, bentazon and imazamox) was applied at a dose of 1.25 dm3 ha−1 together with an adjuvant containing methyl oleate and fatty alcohol (Dash HC) at a dose of 0.6 dm3 ha−1 and Select Super 120 EC (cletodymium, Arysta LifeSciences S.A.S., Nogueres, France) at a dose of 0.8 dm3 ha−1). Different weed infestations at both locations resulted in the use of slightly different control strategies. No insecticide or fungicide treatments were applied in the field trial. The seeds were harvested when the soybean plants were fully mature, in the middle of September.

2.2. Experiment Layout

The experimental factors in Location 1 were different row spacings (15 cm and 30 cm) and the number of soybean seeds sown per square meter (50 and 90) (Table 1). The experiment was designed as a complete randomized block design with four replications. A total of 16 plots were used for the entomological study. Each experimental plot was 10 m long and 3 m (30 m2) wide.
At the second site (Location 2), the field experiment was conducted in a randomized block design with three replications. The experimental factors were row spacing and soybean varieties. The research was carried out in the following variants: row spacing of 12 cm and 45 cm and soybean varieties: Abelina (Saatbau Linz, Austria, variety 1) and Lissabon (Saatbau Linz, Austria, variety 2) (resulting in 12 research plots in total) (Table 1). Each plot was 5 m long and 4 m wide (20 m2).

2.3. Insect Sampling

Arthropod collection on soybean plants was carried out at two locations using the same methodology. The collection was carried out using an entomological net with a diameter of 40 cm and a telescopic handle of 80 cm. The mesh size was 0.1 mm. The collection was carried out in three phenological stages of the soybean, i.e., before flowering (BBCH 12–49 stage), during flowering (BBCH 51–60) and after flowering (BBCH 61–71). The collection was carried out by moving along the longer side of the plot, in its central part. Twenty movements with the entomological net were made in each plot. Arthropods caught were immediately killed by poisoning with ethyl acetate. The entomological material was taken to the laboratory of the Department of Plant Protection and preserved in a 75% ethanol solution. All collected thrips were counted and identified to species. The following keys were used to identify species on the basis of morphological characteristics: ‘Thysanoptera. Handbooks for the Identification of British Insects’ [23], ‘Pictorial key to the economically important species of Thysanoptera in Central Europe’ [24], ‘Thysanoptera: an identification guide’ [25], and ‘Die terebranten Thysanopteren Europas und des Mittelmeer-Gebietes’ [26].

2.4. Data Analysis

The data (total number of thrips and the numbers of the most abundant species) from Location 1 and Location 2 were analyzed separately. The analysis was performed using a fitted Generalized Linear Model (GLM) with a negative binomial distribution in Python. The response variable was the thrips count, while the predictor variables were year, phenological stage, row spacing, number of seeds (only for Location 1), and soybean variety (only for Location 2). The Log-Likelihood and Pseudo R-squared provided information on the goodness of fit of the model. Meaning the variance exceeds the mean. Thrips count data typically exhibit overdispersion, making the negative binomial distribution a more appropriate choice than the Poisson distribution. Post-hoc comparisons between specific treatments were conducted using Tukey’s test to identify significant differences following the analysis.
The thrips species communities in each location and sampling year were correlated with sampling date, row spacing, sampling density (Location 1) and variety (Location 2) using redundancy analysis. The contribution of the explanatory variables to the explained variance was determined using factorial analysis. The analyses were carried out in Canoco 5. The species community in Location 1 and Location 2 was compared using PERMANOVA analysis. In addition, rarefaction curves were constructed for the species community in both localities. The analyses were carried out using PAST software 4.03.

3. Results

The thrips communities were relatively abundant, with mean counts ranging from 20 to 60 individuals per plot in Location 1 and from 5 to 20 individuals per plot in Location 2 on different sampling dates (Figure 1 and Figure 2). In the soybean crop, a total of 20 thrips species were identified at two different locations, with 19 species observed at each location. The predominant species at both locations was Thrips tabaci (D = 42.54% in Location 1 and 35.17% in Location 2), followed by Aeolothrips intermedius (D = 15.95% in Location 1 and 11.04% in Location 2) and T. fuscipennis (D = 11.75% in Location 1 and 6.94% in Location 2) (Table 2). Apart from these three species, the composition of dominant species within the communities varied between the two locations. Statistical analysis using PERMANOVA revealed significant dissimilarities in the thrips species communities between Location 1 and Location 2 (p = 0.0001) (Table 3).
The effects of the row spacing, soybean variety (Location 2), seed density (Location 1), as well as the effects of the year and phenological stage (both localities) were tested for the thrips community (Thrips all) and the three most abundant species (T. tabaci, A. intermedius, T. fuscipennis). In both locations, data analysis indicated no significant effects of row spacing and seed density (Location 1) or row spacing and variety (Location 2) on thrips abundance (Table 4 and Table 5). However, both the year and the phenological stage of the soybean influenced the occurrence of thrips. Specifically, in Location 1, the phenological stage influenced the occurrences of the thrips community and the three studied species: thrips community (z = −3.591, p < 0.001), T. tabaci (z = −5.488, p < 0.001), A. intermedius (z = −5.311, p < 0.001), and T. fuscipennis (z = −6.254, p < 0.001) (Table 4, Supplementary Table S1). The peak of abundance was observed during flowering compared to the stage before flowering, and the lowest abundances were found after flowering (Figure 1).
In Location 2, the abundances of the thrips community (z = 6.489, p < 0.001), T. tabaci (z = 6.498, p < 0.001), and A. intermedius (z = 5.242, p < 0.001) increased during the season, with the highest abundances observed after flowering, while T. fuscipennis (z = 4.285, p < 0.001) increased during flowering and remained stable through the stage after flowering (Figure 2, Table 5, Supplementary Table S2).
Most of the identified species exhibit phytophagous behavior and have a wide range of host plants that are not exclusively associated with soybean cultivation but are able to survive and reproduce in soybean plantations (Table 6). The species associated with soybean include mainly T. tabaci and T. fuscipennis. The prevalence of polyphagous species suggests a lack of specialized thrips species closely associated with soybean cultivation at both locations. Oligophagous species such as Neohydatothrips gracilicornis and Odontothrips loti were present in smaller numbers, but were trapped throughout the growing season, indicating potential feeding on soybean beyond their primary trophic spectrum (Table 6).
The predatory Aeolothrips intermedius was prominently represented, along with the less abundant A. fasciatus. Both of these species primarily prey on other thrips species, including adults and larvae; however, feeding on other small arthropods is also possible. After flowering, a number of species associated with monocotyledonous plants appeared, including Limothrips cerealium, Haplothrips aculeatus, H. leucanthemi and Chirothrips manicatus. Interestingly, infestations of these species coincided with the harvest period of cereals, suggesting that thrips migrate to soybean fields due to a lack of preferred food plants.

4. Discussion

The spatial structure of the canopy is determined by the spacing of plant rows; the distance between plants in a row significantly alters the microclimate that influences the habitat conditions of a specific crop. The arrangement of plants and their density per unit area can affect the number of herbivores that inhabit the crop and, consequently, their harmfulness [40]. In the case of soybean, there has been no comprehensive study of the influence of canopy plant density, seeding density or row spacing on the occurrence of pests, including thrips. Only preliminary studies on herbivores and beneficial carabid beetles have been published [41]. Meanwhile, Santos et al. [42] mentioned that thrips are an emerging problem that leads to soybean yield losses of up to 15%. In the experiment, neither the arrangement nor the variety had a significant effect on the abundance of thrips. Consequently, altering the sowing density, the spacing of the rows or the variety of the plants will not reduce the pressure of the thrips. The resource concentration hypothesis predicts that the density of insect herbivores per plant will increase as the density of host plants increases [43]. However, this is not in line with our studies. Pobereżny et al. [44] captured more Oulema beetles and larvae collected with an entomological net in spring wheat grown at a seed density of 600 seeds/m2 (the highest number of seeds used in the experiment described). In addition, dense plant assemblages provide a more stable habitat for herbivores and increase reproductive potential [45]. Research by Krobb et al. [46] suggests that cotton plant density has a significant effect on the appearance of thrips and the extent of damage within plantations. More specifically, the results indicated that the thrips injury ratings were higher as the plant density decreased. Underwood and Halpern [47] showed that increasing plant density, as well as plant size and canopy architecture, had non-linear effects on herbivore damage, influencing both the extent and impact of its presence on plant performance. Nowatzki et al. [48] studied how row spacing affects corn rootworm damage in maize. They found that decreasing the spacing from 76 cm to 38 cm did not lead to more root damage from Diabrotica virgifera larvae in the following year. However, there were more adult corn rootworms in the current year with narrower row spacing. The study indicated that while the number of adult corn rootworms increased with narrower rows in the planting year, there was no increased in larval damage the following year, regardless of row spacing.
Thysanoptera, an important group of phytophagous insects, are known to feed on various crops, including plants from the Fabaceae family [49]. However, in Poland, there has been no assessment of their occurrence specifically on soybean plantations, nor has there been a comprehensive identification of Thysanoptera species in this context. Research has shown that the species composition and abundance of thrips change with the development of the host plant. Most of the thrips species captured at the study sites exhibit polyphagous behavior, with T. tabaci and T. fuscipennis being the most abundant, neither of which is specifically associated with soybean cultivation. In particular, K. robustus, a species typically associated with legumes, was absent from all surveyed locations. This prevalence of generalist thrips species suggests that they are adaptable feeders rather than specialized for soybean. Thrips species with consistent populations throughout the growing season include T. tabaci, T. fuscipennis, and the predatory Aeolothrips intermedius. These species appear early in the plantation and persist until the end of the season, benefiting from a diverse diet that enables their successful colonization of soybean crops. The most notable population dynamics of these species occur during the flowering period, which coincides with the increased availability of high-protein food sources such as soybean flower pollen. This period promotes significant population growth due to the abundant food resources available. During flower feeding, thrips can cause anthers to rupture, resulting in pollen loss, a common symptom that reduces flower pollination and ultimately reduces the yield [50,51]. In addition, thrips’ damage to flowers and fruit buds often results in deformation, inhibition of fruit growth or even complete fruit mortality [51]. Similar trends regarding the occurrence of T. tabaci, T. fuscipennis, and A. intermedius were observed in different cultures of Fabaceae in Poland. The less abundant species F. intonsa occurred in our study before and during the flowering period, similar to studies conducted in Poland [49] and Hungary [52]. Larvae of this species feed on pollen grains from leguminous plants [49].
The second group of thrips, including T. flavus, T. major, Frankliniella intonsa, and Haplothrips aculeatus, is less abundant but is present from early in the season and continues to feed on soybean until the end of the growing period. These generalist species have a broad host range and no specific habitat preferences [53]. In contrast, the specialist species Odontothrips loti, which is exclusively associated with legume crops, was found in low numbers. O. loti is closely related to legumes and can only complete its life cycle by supplementing itself with pollen from plants of this genus [54,55]. In Romania, O. loti, together with the related species O. confuses and O. phaleratus, has been identified as a significant pest of lucerne, alfalfa and white clover used for green fodder, causing substantial yield losses [55]. Another species, N. gracilicornis, known to be associated with legumes, especially Vicia species such as V. cracca [34,35], was present in small numbers at both locations.
Taking into account the expected expansion of soybean production in Poland and Europe, it is likely that the pressure from thrips will increase. So far, the number of thrips on soybean, especially species related to Fabaceae, is not large, and most of them are not known to cause crop damage. However, their presence on plants can be misleading for farmers [20]. They are known for their mass flights and random landings on plants, especially during the harvest season of various crops, including cereals. Population size and economic damage inflicted by thrips species are thus essentially unpredictable in terms of time, space, and crop [56]. The emergence of more specialized pests specific to soybean is also a possibility. Despite the fact that various plant arrangements and densities do not show a significant impact on thrips abundance, understanding their feeding patterns and seasonal dynamics is crucial for developing innovative pest management strategies. Special attention should be paid to periods of peak abundance, especially during flowering, when thrips can cause significant damage.

5. Conclusions

The study provides valuable insights into the occurrence of thrips associated with soybean crops, emphasizing the role of phenological stages in their occurrence and potential harmfulness. The abundance and species composition of the thrips were revealed in different varieties of soybean grown with various plant arrangements at different phenological stages. Neither the arrangement nor the variety had a significant effect on the abundance of thrips. The significant factor that influenced the Thysanoptera assemblages was the phenological stage of soybean. The number of thrips increased significantly during the flowering period and shortly after flowering, making them a notable threat to plants at this time. Among the 20 identified species of thrips, most exhibit polyphagous behavior, with Thrips tabaci and T. fuscipennis being the most abundant. Among the dominant species in all experimental variants, the predatory Aeolothrips intermedius was also abundant, especially during the soybean flowering period, which coincides with the increased availability of other thrips as prey, as well as flower pollen being a high-protein supplemental food source. Less abundant generalist species such as T. flavus, T. major, Frankliniella intonsa, and Haplothrips aculeatus were present from the beginning of the season and continued to feed on soybean until the end of the growing period. Odontothrips loti, which is exclusively associated with legume crops, was found in small numbers. It can be concluded that during soybean flowering, thrips can cause some damage, such as rupturing anthers, which results in pollen loss. This is a common symptom that reduces flower pollination and ultimately decreases yield. However, the harmfulness of thrips in soybean should be subject to further observations, especially since the expansion of soybean production is expected in Poland and Europe.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture14091501/s1, Table S1. The statistical details of the Generalized Linear Model (GLM) with a negative binomial distribution conducted for the data from Location 1; Table S2. The statistical details of the Generalized Linear Model (GLM) with a negative binomial distribution conducted for the data from Location 2; Figure S1. Pictures of selected thrips species (by coauthor Marcin Cierpisz).

Author Contributions

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

Funding

This research was partially financed from the multi-annual programme 2016–2020 by the Ministry of Agriculture and Rural Development titled “Increasing the use of domestic fodder protein for the production of high-quality animal products in the conditions of sustainable development”, Resolution No. 222/2015 of the Council of Ministers of 15 December 2015 (Poland).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data are contained within the article.

Acknowledgments

The cooperation and support of Hanna Kucharczyk (Department of Zoology, Maria Curie-Sklodowska University in Lublin) in identification of thrips are greatly appreciated.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 14 01501 g001
Figure 1. The total abundance of thrips in three phenological stages in Location 1. 1, 2, 3—Phenological stages: 1—before flowering (BBCH 12–49), 2—during flowering. (BBCH 51–60) 3—after flowering (BBCH 61–71). a, b, c—different lowercase letters on the graphs indicate significant differences according to the post hoc Tukey test.
Figure 1. The total abundance of thrips in three phenological stages in Location 1. 1, 2, 3—Phenological stages: 1—before flowering (BBCH 12–49), 2—during flowering. (BBCH 51–60) 3—after flowering (BBCH 61–71). a, b, c—different lowercase letters on the graphs indicate significant differences according to the post hoc Tukey test.
Agriculture 14 01501 g001
Agriculture 14 01501 g002
Figure 2. The total abundance of thrips in two years of the study in Location 2. 1, 2, 3—Phenological stages: 1—before flowering (BBCH 12–49), 2—during flowering. (BBCH 51–60); 3—after flowering (BBCH 61–71). a, b, c—different lowercase letters on the graphs indicate significant differences according to post hoc Tukey test.
Figure 2. The total abundance of thrips in two years of the study in Location 2. 1, 2, 3—Phenological stages: 1—before flowering (BBCH 12–49), 2—during flowering. (BBCH 51–60); 3—after flowering (BBCH 61–71). a, b, c—different lowercase letters on the graphs indicate significant differences according to post hoc Tukey test.
Agriculture 14 01501 g002
Table 1. Experiment treatments at soybean fields in two research locations.
Table 1. Experiment treatments at soybean fields in two research locations.
Wrocław-Pawłowice (Location 1)
Row SpacingNumber of Seeds Sown per 1 m2
1550
1590
3050
3090
Łosiów (Location 2)
Row Spacing (cm)Soybean Variety
12Abelina (variety 1)
12Lissabon (variety 2)
45Abelina (variety 1)
45Lissabon (variety 2)
Table 2. The dominance structure of the thrips species found in both locations.
Table 2. The dominance structure of the thrips species found in both locations.
Dominance D (%)
SpeciesLocation 1Location 2
Thrips tabaci42.5435.17
Aelothrips intermedius15.9511.04
Thrips fuscipennis11.876.94
Limothrips denticornis1.502.52
Limothrips cerealium4.825.99
Thrips flavus0.821.42
Chirothrips manicatus1.222.52
Thrips nigropilosus4.873.94
Anapothrips obscurus1.051.74
Thrips physapus2.524.42
Thrips major0.650.79
Thrips atratus2.024.73
Odontothrips loti2.354.10
Neohydatothrips gracilicornis0.300.16
Haplothrips aculeatus0.670.00
Limothrips spp.3.205.21
Aeolothrips fasciatus0.070.16
Frankliniella intonsa0.370.63
Haplothrips spp.3.176.47
Chirothrips spp.0.002.05
Table 3. The results of the PERMANOVA analysis comparing the thrips species communities in Locations 1 and 2.
Table 3. The results of the PERMANOVA analysis comparing the thrips species communities in Locations 1 and 2.
Permutation NTotal Sum of SquaresWithin-Group Sum of SquaresFp
99993.63.11932.870.0001
Table 4. The results of the Generalized Linear Model (GLM) with a negative binomial distribution for the species found in Location 1.
Table 4. The results of the Generalized Linear Model (GLM) with a negative binomial distribution for the species found in Location 1.
CoefStand Errzp > |z|[0.0250.975]
Thrips All
Intercept4.98820.49510.0680.0004.0175.959
Phenological stage−0.37270.104−3.5910.000−0.576−0.169
Year−0.18590.104−1.7920.073−0.3890.017
Row spacing−0.00340.011−0.3000.764−0.0260.019
Seed density−0.00480.004−1.1410.254−0.0130.003
Thrips tabaci
Intercept4.91250.5139.5680.0003.9065.919
Phenological stage−0.59240.108−5.4880.000−0.804−0.381
Year−0.42720.108−3.9640.000−0.638−0.216
Row spacing−0.00150.012−0.1320.895−0.0240.021
Seed density−0.00710.004−1.6090.108−0.0160.002
Aeolothrips intermedius
Intercept3.78130.5506.8700.0002.7034.860
Phenological stage−0.62030.117−5.3110.000−0.849−0.391
Year−0.38100.116−3.2820.001−0.609−0.153
Row spacing−0.00410.013−0.3230.747−0.0290.021
seed density−0.00470.005−1.0050.315−0.0140.005
Thrips fuscipennis
Intercept3.12050.5695.4830.0002.0054.236
Phenological stage−0.76540.122−6.2540.000−1.005−0.526
Year−0.17480.120−1.4550.146−0.4100.061
Row_spacing0.00400.0130.3060.760−0.0220.030
Seed_density−0.00400.005−0.8100.418−0.0140.006
Table 5. The results of the Generalized Linear Model (GLM) with a negative binomial distribution for the species found in Location 2.
Table 5. The results of the Generalized Linear Model (GLM) with a negative binomial distribution for the species found in Location 2.
CoefStand Errzp > |z|[0.0250.975]
Thrips All
Intercept:1.38490.6022.3010.021−2.564−0.205
Phenological stage1.04030.1606.4890.0000.7261.355
Year0.82230.2583.1850.0010.3161.328
Row spacing0.00140.0080.1830.854−0.0140.017
Variety−0.08910.258−0.3460.729−0.5940.416
Thrips tabaci
Intercept:1.21350.4381.5660.0002.0075.923
Phenological stage−0.38420.1506.4980.000−1.007−0.341
Year−0.24530.1502.3470.000−0.3120.009
Row spacing−0.01320.0110.0230.5611−0.0270.064
Variety−0.00240.024−0.0240.4388−0.0170.032
Aeolothrips intermedius
Intercept:3.78130.5501.4820.0002.7234.865
Phenological stage−0.62030.1175.2420.000−0.888−0.541
Year−0.38100.1162.2450.000−0.672−0.131
Row spacing−0.00410.013−0.0440.5611−0.0290.021
Variety−0.00470.005−1.0540.4388−0.0140.005
Thrips fuscipennis
Intercept:3.12050.5691.2430.0003.9084.241
Phenological stage−0.76540.1224.2850.000−0.624−0.126
Year−0.17480.120−0.0540.000−0.638−0.381
Row spacing0.00400.013−0.0560.5611−0.0310.021
Variety−0.00400.005−1.0050.4388−0.0230.019
Table 6. Ecological characteristics of the thrips species identified in soybean at two locations.
Table 6. Ecological characteristics of the thrips species identified in soybean at two locations.
SpeciesAbbreviationTrophic GroupFood SpecializationMain Host Plants
(If Applicable)		References
Aeolothrips fasciatus
(Linnaeus, 1758)		AelFascpredatorymainly adult and larvae of thrips, supplements the diet with plant pollen [27,28]
Aeolothrips intermedius * (Bagnall, 1934)AeolIntrpredatorymainly adult and larvae of thrips and mites, supplements the diet with plant pollen [21,29,30,31]
Chirothrips manicatus (Haliday, 1836)ChirMancherbivoreoligophagousmonocotyledonous [15,29]
Haplothrips aculeatus (Fabricius, 1803)HaplAculherbivoreoligophagousmonocotyledonous[28,29]
Haplothrips leucanthemi (Schrank, 1781)HaplLeucherbivoreoligophagousmonocotyledonous[29]
Limothrips cerealium (Haliday, 1836)LimtCereherbivoreoligophagousmonocotyledonous [28,29]
Limothrips denticornis (Haliday, 1836)LimtDentherbivoreoligophagousmonocotyledonous [28]
Odontothrips loti (Haliday, 1852)OdonLotiherbivoreoligophagousFabaceae[29,32,33]
Neohydatothrips gracilicornis (Williams, 1916)NGraclherbivoreoligophagousFabaceae, often on Vicia spp.[34,35]
Thrips atratus (Haliday, 1836)ThripAtrherbivorepolyphagousfeeds on flowers on a wide range of host plants, often on Asteraceae and Fabaceae [30,34]
Frankliniella intonsa (Trybom, 1895)FranIntherbivorepolyphagousfeeds on flowers and leaves on a wide range of host plants often on Fabaceae[32,36,37]
Haplothrips niger (Osborn, 1883)HaplNigrherbivorepolyphagousfeeds on flowers on a wide range of host plants, often on Fabaceae[38]
Thrips flavus
(Schrank, 1776)		ThripFlavherbivorepolyphagousfeeds on flowers on a wide range of host plants, often on Fabaceae[30,32]
Thrips fuscipennis (Hailday, 1836)ThripFuscherbivorepolyphagousfeeds on flowers and leaves on a wide range of host plants, often on Rosaceae and Fabaceae[30,32]
Thrips major
(Uzel, 1895)		ThripMajrherbivorepolyphagousfeeds on flowers and leaves on a wide range of host plants, often on Rosaceae and Fabaceae[30,32]
Thrips nigropilosus Uzel, 1985ThripNigrherbivorepolyphagousfeeds on flowers on a wide range of host plants including Fabaceae[33,39]
Thrips tabaci (Lindemann, 1889)ThripTabcherbivorepolyphagousfeeds on flowers on a wide range of host plants including Fabaceae[30]
* The pictures of the selected species are included in Figure S1.
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Twardowski, J.; Gruss, I.; Cierpisz, M.; Twardowska, K.; Magiera-Dulewicz, J.; Kozak, M. Diversity of Thrips Species Associated with Soybean Grown in Different Plant Arrangements at Various Phenological Stages. Agriculture 2024, 14, 1501. https://doi.org/10.3390/agriculture14091501

AMA Style

Twardowski J, Gruss I, Cierpisz M, Twardowska K, Magiera-Dulewicz J, Kozak M. Diversity of Thrips Species Associated with Soybean Grown in Different Plant Arrangements at Various Phenological Stages. Agriculture. 2024; 14(9):1501. https://doi.org/10.3390/agriculture14091501

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Twardowski, Jacek, Iwona Gruss, Marcin Cierpisz, Kamila Twardowska, Joanna Magiera-Dulewicz, and Marcin Kozak. 2024. "Diversity of Thrips Species Associated with Soybean Grown in Different Plant Arrangements at Various Phenological Stages" Agriculture 14, no. 9: 1501. https://doi.org/10.3390/agriculture14091501

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