Predatory insect species, and patterns of abundance of two common thrips species (Thysanoptera) and their predators on common crops

Description of sampling sites

In 2019-2020, a study was conducted to investigate thrips and predatory insect species diversity, their seasonal densities, and distributions in location Balcalı, Adana Province, Türkiye. The study focused on three distinct ecological areas where various plant species were cultivated for both production and research purposes. Specifically, in the Research and Application Area of the Department of Plant Protection, University of Çukurova, field crops such as cotton, soybean, sesame, and peanuts were sampled. In the Research and Application Area of the Department of Field Crops, the study concentrated on citrus and temperate climate fruits, including apples, nectarines, and loquats. These efforts were complemented by detections of thrips species in fruit trees in the Research and Application Area of the Horticultural Department. The research application sites are located 500–1000 m apart at different distances from one another.

Experimental procedures and insect samplings

For winter vegetable plants, plots were created in four territorial units using a randomised block trial design. The plants included spinach (Spinacia oleracea ), lettuce (Lactuca sativa ), cauliflower (Brassica oleracea var. botrytis ), red cabbage (Brassica oleracea var. appitate f. rubra ), cabbage (Brassica oleracea ), rocket (Eruca vesicaria ), peppergrass (Lepidium sativum ), radishes (Raphanus sativus ) and broad beans (Vicia faba ). Each plot consisted of four rows, with fifteen plants in each row. A free space of 1.5 m was left between plots, and there were 5 m between the blocks. A similar trial model was created for the following summer vegetable plant species: cucumber (Cucumis sativus ), squash (Cucurbita moschata ), beans (Phaseolus vulgaris ), peppers (Capsicum annuum ), tomatoes (Solanum lycopersicum ), potatoes (Solanum tuberosum ) and eggplants (Solanum melongena ). In order to examine the prevalence of thrips and predatory insects in specific field crops, four replicates of a randomised block design were used to create plots of cotton (Gossypium hirsutum ), sesame (Sesamum indicum ) and soybean (Glycine max ). The plot size for each plant species was designed as 96 m² with a row length of 10 m, consisting of ten rows, with a distance of 0.80 m between rows. A free space of 2 m was left between the plots and 5 m between the blocks. Nectarines (Pyrus persicae ) and pomegranates (Punica granatum ) were planted with 3 × 5 spacing, apples (Malus domestica ) with 1 × 4 spacing, pears (Pyrus communis ) with 4 × 6 spacing, plums (Prunus persica ), lemons (Citrus lemon ) and almonds (Prunus dulcis ) with 5 × 5 spacing and loquats (Eriobotrya japonica ) with 7 × 7 spacing. Ten rows of each fruit tree species were planted, with 20 trees in each row. There was a 20-m gap between the large plots representing each fruit species, and they were lined up next to each other. Each tree species planted was nearly 15 years old. In the samplings, 20 plants from annual herbaceous crops (vegetable species and field crops) and 20 plants from perennial woody crops (fruit trees) were randomly selected. In general, the plants with flowers were taken into consideration in the samplings, which started with the beginning of the flowering period of the different plant groups. This choice was taken because Orius and thrips, their main prey, are primarily located on flowers. When there is no prey, these predatory species feed on the nectars and pollens in the flowers (Riudavets & Castane, 1994RiudavetsJ, CastenaC, 1994. Abundance and hosts plant preferences for oviposition of Orius spp. (Heteroptera: Anthocoridae) along the Mediterranean coast of Spain. IOBC/WPRS Bull17(5): 230-236.; Hansen et al., 2003HansenEA, FunderburkJE, ReitzSR, EgerJ, RamachandranS, McAuslaneHJ, 2003. Within plant distribution of Frankliniella thrips and Orius insidiosus on field pepper. Environ Entomol2: 1035-1044. 10.1603/0046-225X-32.5.1035; Kasina et al., 2009KasinaM, NderituJ, NyamasyoG, WaturuC, OlubayoF, ObudhoE, YoberD, 2009. Within-plant distribution and seasonal population dynamics of flower thrips (Thysanoptera: Thripidae) infesting French beans (Phaseolus vulgaris L.). Span J Agric Res7(3): 652-659. 10.5424/sjar/2009073-450; Funderburk et al., 2000FunderburkJE, StaviskyJ, OlsonS, 2000. Predation of Frankliniella occidentalis (Thysanoptera: Thripidae) in field peppers by Orius insidiosus (Hemiptera: Anthocoridae). Environ Entomol29: 376-382. 10.1093/ee/29.2.376; 2018FunderburkJ, ReitzS, StanslyP, FreemanJ, MillerC, McavoyG, et al., 2018. Managing thrips in pepper and eggplant. IFAS Extension, University of Florida, pp: 1-10. https://edis.ifas.ufl.edu/publication/IN40.); 20–30 cm flowering or fruiting shoots oriented in four directions on the trees were chosen at random for sampling. In herbaceous plants, the upper halves of the plants were considered in the sample. In the surveyed areas, shoots or plants were shaken for 5–10 seconds into a white container measuring 34 × 23 × 7 cm, and the Orius species and herbivorous insects that fell into the container were lifted out by a suction tube and/or fine brush and placed in Eppendorf tubes containing 70% ethanol. Insect samples collected from each plant species on each sampling date were placed in a tube. The information about the samplings of insects in various plant groups is summarised in Table 1. Sampling was carried out in three different ecological areas on the same day between 08:00 and 12:00. Insect samples (Orius and herbivorous pest insects) were brought to the laboratory and placed in petri dishes to be counted under a stereo binocular microscope, to classify them as thrips, aphids or leafhoppers without making any distinction between species. While making the diagnosis, nymphs of Orius and larvae of thrips were sampled from the most common broad bean plants but were not evaluated because they were found only in very small numbers. Orius adults were separated according to morphological characteristics, after which they were identified.

Thrips and predatory insects’ identifications

Microscopic preparations were done for the identifications of the collected Thysanoptera species. The samples, which were kept in tubes containing ethanol (60%), were taken to the AGA solution including ethanol, glacial acetic acid, and glycerin (9:1:1), for 2 days in order to soften the body tissues and partially empty the body contents (Zur Strassen, 2003Zur StrassenR, 2003. Die Terebranten Thysanopteren Europas und des Mittel Gebietes. Die Tierwelt Deutschlauds, Beggründet 1925 von Friedrich Dahl, 74. Teil. Goecke & Evers, Keltern, Deutschland, 277 pp.). For interim preparations, light samples were incubated at 60 ^oC for approximately 30 minutes in 10% sodium hydroxide (NaOH) medium, while dark samples were incubated at 60 ^oC for approximately one hour, or until a little color shift occurred. The body contents of the samples were completely discharged by rubbing their bodies from the ventral or dorsal side in 96% ethanol. Individuals were placed in Hoyer medium and microscopic slides were made. A key identification guide according to Zur Strassen (2003Zur StrassenR, 2003. Die Terebranten Thysanopteren Europas und des Mittel Gebietes. Die Tierwelt Deutschlauds, Beggründet 1925 von Friedrich Dahl, 74. Teil. Goecke & Evers, Keltern, Deutschland, 277 pp.) was used to assist in the identification of the thrips specimens. Under a stereo-binocular microscope with 45 magnifications, the morphological traits of Orius species and other hemipteran predators were inspected. Their identifications were made using the key identifications published by Péricart (1972PéricartJ, 1972. Hémiptères: Anthocoridae, Cimicidae et Microphysidae de l'Ouest Paleartique. Masson, Paris, 402 pp.), Önder (1982ÖnderF, 1982. Taxonomic and faunistic studies on the Anthocoridae (Heteroptera) fauna of Turkey. Ege University Faculty of Agriculture Publications, No: 459, 159 pp. (in Turkish with English abstract).), and Çakır & Önder (1990ÇakırS, ÖnderF, 1990. Türkiye Geocorinae (Het.:Lygaeidae) altfamilyası üzerinde sistematik ve faunistik araştırmalar. Türk Entomol Derg14(1): 37-52. (in Turkish with English abstract).). The key identification provided by Uygun (1981UygunN, 1981. Türkiye Cocinellidae (Coleoptera) faunası üzerinde taksonomik araştırmalar. Çukurova Üniversitesi Ziraat Fakültesi yayınları, No: 157, 110 pp. Dilek Matbaası, Adana.) was used to help identify the Coccinellidae species.

Statistical analysis

Some of the identified hemipteran predators and coleopteran predators were not assessed because they were only occasionally collected in small numbers from herbaceous plants and fruit trees. The abundance patterns of thrips and predatory insects (Orius spp.) were determined in plant species where the insect species commonly occurred, representing various plant groups, including winter and summer vegetables, fruit trees, and field crops. To compare the seasonal average population densities of both thrips and predatory insects in different plant species, we applied a homogeneity test by Shapiro-Wilk test, confirming their normal distribution. We used analysis of variance (ANOVA) on the means, and when significance was found, we conducted post-hoc analyses using the Tukey test (p<0.05). In different plant groups, we assessed plant, insect and plant × insect interactions through a two-way analysis of variance. Additionally, we evaluated the relationships between thrips and Orius population patterns using Pearson correlation analysis at the p<0.05 significance level. For this analysis, we considered 15 average values for winter vegetables, 20 for fruit trees, 23 for summer vegetables, and 15 for field crops. The data were analyzed by statistical package program SPSS^© version 25 (IBM Corp., 2017).

Predatory insect species identified on plants

Predatory insect species were collected in 28 plant species from 11 plant families, along with thrips (Table 2). A total of 11 predatory insect species were identified, including 3 Coccinellidae, 2 Lygaeidae, 2 Miridae, and 4 Anthocoridae (Table 3). Predatory insects were not detected in winter vegetable species, except for cauliflower. From the predatory insects, only those found on summer cabbage were recorded, with a total of 270 individuals.

The highest number of predatory insect species was found in plant species belonging to the Fabaceae with a total of 161 insects (Table 2). More individuals were collected from broad beans and beans in this family. In sesame plants, which are field crops, 5 predator species were identified, with a total of 23 individuals. Also, a total of 23 individuals were collected in potato which is grown as a rotation crop and harvested at the end of May in the Cukurova region. O. laevigatus (19 individuals) was mostly found on potato flowers. In fruit trees, generally 2-3 species were identified, and the number of individuals was quite low, with the highest number being 8 individuals of O. laevigatus in apple flowers.

Population densities and dynamics of two thrips species and predatory Orius spp. in plant species

Table 4 shows that in winter vegetables, the interaction between insect species and plant species was found to be significant, while insect species alone appeared as an important factor in fruit trees. For summer vegetables, plant species, insect species, and the interaction between them were identified as crucial factors influencing population densities. In the case of field crops, only insect species was recognized as a significant factor affecting population densities.

Winter vegetables

The population changes of two common harmful thrips species and Orius species in three winter vegetable species were recorded (Fig. 1). Very few thrips individuals were recorded in pea flowers. Mostly, adult Orius individuals were collected from pea flowers. The density of adult Orius individuals appears to be higher when the number of flowers is high (January-February) (Fig. 1a). On cauliflower plants, mainly T. tabaci adult individuals were recorded. The highest number of individuals in this plant was on November 6 (12.75±1.10 individuals/plant) and November 20 (10±1.08 individuals/plant) (Fig. 1b). On cauliflower, no F. occidentalis individuals were found. Orius spp. individuals were recorded only on January 29 (2.00±0.40 individuals/plant) (Fig. 1b). Cabbage plants only had T. tabaci individuals (Fig. 1b), and cabbage plants had its higher population densities in October-November than other sampling period. Thrips individuals were not observed in winter and early spring (March). The highest population density of T. tabaci was found on November 20, with 14.25±0.47 individuals/plant. Among the winter vegetables, only in pea plants, a statistically significant relationship was found between Orius and thrips (r (15) = 0.57, p = 0.024).

Figure 1 Mean numbers of two pest thrips species and Orius spp. on broad beans (a), cauliflower (b) and red cabbage (c) in Adana Province, Türkiye, during 2019-2020 

Overall, the seasonal mean population densities of F. occidentalis were similar in pea, cauliflower, and cabbage plants, while T. tabaci was significantly found on cauliflower (F_2,177= 8.974, p<0.0001; Table 5). Orius individuals were collected in significant numbers from pea flowers (F_2,177= 42.444, p<0.0001; Table 5).

Fruit trees

In fruit trees, the most common species was T. tabaci and it was recorded with the period of high flowering (Fig. 2a). During this period, Orius individuals were also recorded alongside thrips. Orius population showed a significant positive relationship with the thrips population (r (15) = 0.99, p<0.0001). In loquat trees, during the period of high flower density in the region, mostly T. tabaci individuals were found, and during this period (Fig. 2b), Orius individuals were also recorded alongside thrips (Fig. 2b). A high and significant positive relationship was found between Orius and thrips individuals (r (15) = 0.88, p<0.0001). During the fruiting period, thrips and Orius individuals were not found. Thrips individuals on nectarine were recorded at the beginning of flowering (Fig. 2c). Thrips tabaci showed a peak in the average number of individuals on April 1 (2.75± individuals/shoot) (Fig. 2c).

Figure 2 Mean numbers of two pest thrips species and Orius spp. on apple (a), loquat (b) and nectarine (c) in Adana Province, Türkiye, during 2019-2020. 

The mean numbers of F. occidentalis and T. tabaci individuals in apple, loquat, and nectarine trees were similar (p>0.05; Table 5). Seasonal mean numbers of Orius spp. adult individuals in apple and loquat flowers were statistically significant compared to nectarine (F₂,₂₃₇ = 4.473, p = 0.024; Fig. 2b).

Summer vegetables

In bean plants, both F. occidentalis and Orius individuals were collected during planting and November, even though there was low flower density (Fig. 3). In the following spring plantings, during the dates of intense flowering (April 29 to July 3), both thrips species and predatory individuals were observed to have high densities (Fig. 3a). On bean flowers during these dates, F. occidentalis had an individual count of 2 or more, and the density of T. tabaci reached its peak on June 3, recording 13.5±0.64 individuals. During these dates, Orius spp. had an average individual count ranging from 0.5 to 1.5 individuals/plant. However, in beans, population change was only observed in relation to Orius individuals and F. occidentalis individuals (r (15) = 0.57, p = 0.05). In pepper plants, the population densities of thrips species and Orius individuals remained below 1 individual on a random sampling date (Fig. 3b). No relationship was found between thrips and Orius individuals (p>0.05). In potatoes, mainly T. tabaci individuals were caught. During the mid-April to late May period when flowering was intense, the average number of T. tabaci individuals was just over 10 individuals/plant. When the thrips population decreased in early June, adult Orius individuals were observed for a short time. No relationship was observed between Orius individuals and the populations of the two thrips species (p>0.05).

Figure 3 Mean numbers of two pest thrips species and Orius spp. on bean (a), pepper (b) and potato (c) in Adana Province, Türkiye, during 2019-2020 

Frankliniella occidentalis was collected more from bean plants (F_2,261 = 5.807, p = 0.003) than those found in other plant species, while T. tabaci was significantly recorded in potato flowers (F_2,261= 7.024, p = 0.001; Table 5). Numbers Orius spp. were similar in vegetable species (p>0.05; Table 5).

Field crops

In the autumn month of 2019 (October), very few thrips and Orius individuals were collected from cotton, soybean, and sesame plants, and T. tabaci individuals were not found (Fig. 4a,b,c). In 2019, as flowering began in the plants, F. occidentalis was recorded in relatively higher numbers. On August 19, the numbers of thrips or Orius spp. in cotton (thrips: 2.50±0.64 individuals/plant, Orius spp. 2.00±0.40 individuals/plant), soybean (thrips: 4.25±0.62 individuals/plant), and sesame plants (thrips: 2.50±0.64 individuals/plant, Orius spp.: 1.00±0.40 individual/plant) were higher compared to those numbers found on other sampling dates. Positive correlations were found between Orius and F. occidentalis individuals in cotton (r (15) = 0.86, p<0.0001) and in sesame (r (15) = 0.61, p = 0.040) plants.

Figure 4 Mean numbers of two pest thrips species and Orius spp. on cotton (a), sesame (b) and soybean (c) in Adana Province, Türkiye, during 2019-2020. 

The seasonal mean densities of F. occidentalis and T. tabaci were similar in cotton, sesame, and soybean flowers, while Orius individuals were captured in significant numbers in cotton and sesame plants, but in soybean plants, they were significantly fewer (F_2,177 = 6.616, p = 0.020; Table 5).

Seasonal distribution of two thrips species and predatory Orius spp. on various plant species (%)

On broad beans among winter vegetables, it was observed that predatory Orius was the main predatory insect during the sampling period (Table 6). Thrips individuals were observed on cauliflower between October and January, and the main harmful thrips species was T. tabaci.

Thrips individuals and Orius spp. were recorded on apple trees in April and May, with the harmful T. tabaci being the most common species on the flowers, followed by predators at percentages of 26% and 38%, respectively (Table 6). In loquat flowers, predators were most commonly found in February (60%), while in March and April, T. tabaci was quite common (60% and 100%, respectively). Thrips tabaci was the predominant species in nectarine flowers only in April (77%).

On beans, F. occidentalis was more common in October to December, while T. tabaci became the main thrips species in April to June (Table 6). Orius spp. was only commonly found in November (60%). In pepper flowers, F. occidentalis was generally common in October to December, but in November, Orius individuals were mostly found (83%) (Table 6). Thrips tabaci was found in the highest percentage (58%) in May. In potato flowers, T. tabaci individuals were primarily recorded. In June, when Orius individuals were common (92%), thrips individuals were detected in small numbers.

Throughout the samples, F. occidentalis individuals were recorded at high rates in cotton flowers. In sesame, Orius individuals were mostly found in the autumn months, while F. occidentalis became the main thrips species in the summer months. In soybean flowers, only F. occidentalis was recorded (Table 6).