Zhu, Jiawei ¹ ; Cui, Xiangxin ² ; Yang, Jian ³ ; Lin, Xingming ⁴ ; Yan, Yi ⁵ ; Cai, Ducheng ⁶ and Li, Jinhua ⁷

¹Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.
²Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.
³Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.
⁴Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.
⁵Department of Entomology, College of Plant Protection, Shandong Agricultural University, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, Taian, China.
⁶Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.
⁷✉ Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou, China.

2023 - Volume: 63 Issue: 4 pages: 1039-1047

Original research

Keywords

Abstract

Introduction

Fabaceae is one of the most important crop groups in many Asian countries, such as China, Iran and India (Dialoke 2013; Sherasia et al. 2018). Megalurothrips usitatus (Bagnall) (Thysanoptera: Thripidae) is the primary pest that affects leguminous crops in China, particularly cowpea Vigna unguiculata (Linn.) Walp. and snap beans Phaseolus vulgaris (Linn.) (Mirab-Balou et al. 2011). The life cycle of this thrips consists of egg, two active feeding larval instars, two non-feeding instars (pre-pupae and pupae), and adult stages (Reitz et al. 2011). Megalurothrips usitatus can cause significant damage to its host plant through oviposition and feeding. Both adults and juvenile larvae directly feed on young tissues, flowers and fruits of cowpea, which often results in the deformation, crinkling or wilting of leaves and flower buds, and seriously affects the formation of fruit pods (Chen 1980; Shipp 2000; Tang 2015). Adult female thrips insert their eggs into cowpea tissue using a sharp ovipositor, causing spots on developing fruits that continue to expand as the cowpea matures, potentially impacting fruit marketability (Xu 1987; Wang et al. 1989). The non-feeding stages of thrips play a crucial role in their overall occurrence because they mark the transition from the final larval instar to the adult stage. The quantity of pupae can have an impact on the emergence of adults, which, in turn, can influence the peak population densities and cause subsequent damage to crops. Furthermore, pupae of M. usitatus tend to pupate in the soil layer adjacent to plants (Chang 1989), which renders chemical treatment ineffective since they typically target above ground stages (Lewis 1973; Loomans & Lenteren 1995). Additionally, M. usitatus has a short generation time and has developed resistance to many insecticides, making it difficult to control (Fu et al. 2014, 2022; Tang et al. 2016; Yuan et al. 2022; Gao et al. 2023). Therefore, there is an urgent need for alternative and effective methods to control M. usitatus, especially during the pupal stage.

Biological control is a promising measure for thrips control (Shipp et al. 1991; Premachandra et al. 2003; Berndt et al. 2004; Murunde et al. 2019), and a range of natural enemies have been reported to be effective against thrips larvae, pupae, and adults. For example, Yao et al. (2014) conducted a study on the predation potential of three predatory mites in a climatic chamber, and found that Neoseiulus cucumeris (Oudemans) (Phytoseiidae), N. barkeri (Hughes), and Euseius nicholsi (Ehara et Lee) (Phytoseiidae) can reduce populations of first-instar larvae of Thrips flavidulus (Bagnall) (Thysanoptera: Thripidae), and the predation rate increased with the increasing number of thrips provided. Saito and Brownbridge (2022), combined laboratory assays and greenhouse experiments, assessed the efficacy of the generalist predatory mite Anystis baccarum (Linn.) (Anystidae) against western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), and they found that A. baccarum could be an important biocontrol agent for western flower thrips. Furthermore, some edaphic species were reported as suitable biological control agents for F. occidentalis pupae in the soil-dwelled stage (Rueda-Ramírez et al. 2021). In comparison to F. occidentalis, there have been limited natural enemies reported for M. usitatus. Chang et al. (1990) found a parasitoid Ceranisus menes (Walker) (Hymenoptera: Eulophidae) of M. usitatus larvae in Taiwan, and subsequently other natural enemies including two predatory bugs (Geocoris ochropterus (Fieber) (Hemiptera: Geocoridae) and Geocoris xishaensis (Zhou, Cai & Gao) (Hemiptera: Geocoridae)), Chrysopa pallens (Rambur) (Neuroptera: Chrysopidae) and a ladybeetle Menochilus sexmaculata (Fabricius) (Coleoptera: Coccinellidae) were reported (Tang et al. 2017; Li et al. 2021; Li et al. 2022). As of now, no effective predatory mites that can adequately control M. usitatus have been found.

Species of the Macrocheles genus, one of the most abundant and diverse group of macrochelid mites living in animal dung or the nests or decomposing animals, have been reported as important biological agents for controlling soil-dwelling pests (Wallace and Holm 1983; Behan-Pelletier 2003; Perotti and Braig 2009; Emberson, 2010). Macrocheles robustulus (Berlese) has been used for controlling F. occidentalis that dwell in soil, exhibiting significantly better predatory efficiency than that of Hypoaspis aculeifer (Canestrini) (Laelapidae) (70% vs. 50 reduction) (Messelink and van Holsten-Sai 2008). In southern China, we discovered a population of predatory mites belonging to the genus Macrocheles, specifically Macrocheles mammifer (Berlese), in the soil of cowpeas (unpublished data). Another predatory mite, Stratiolaelaps scimitus (Womersley) (Acari: Laelapidae), previously classified in the genus Hypoaspis or mistakenly identified as Stratiolaelaps miles, has been widely recognized as an effective predator for thrips in the soil-dwelling stages and is commercially produced and marketed as a predatory mite (Saito and Brownbridge 2016). In this study, we evaluated the functional response of M. mammifer and S. scimitus to the pupae of M. usitatus, with the aim of exploring the potential of both predators for thrips management.

Material and methods

Stock cultures of predators and prey

For stock culture initiation M. mammifer were collected from cowpea soil in October 2021 at the Agricultural Science Base of Hainan University (20º05′N,110°32′E) Haikou, China and reared in 0.4-liter glass jars (d=6 cm, h=8 cm), covered with gauze to prevent the mites from escaping. Soil organisms such as saprophytic nematodes, organisms on rotten plant tissue and pupae of certain insects were provided to M. mammifer as prey. All rearing units were maintained at 26 °C± 1 °C, 60% ± 5% RH and a 16:8 h (L:D) photoperiod. The predatory mites S. scimitus were purchased from Fuzhou Yuyi Natural Enemy Biotechnology Corporation in Fuzhou, China.

The thrips M. usitatus were initially collected from cowpea flowers in January 2019 in Lingshui City, located in Hainan province, China (18º41′N,109°88′E). They were subsequently reared with cowpea in 0.4-liter glass jars (d=6 cm, h=8 cm), covered with gauze. The jars were kept in a climate chamber at 26±1 °C, relative humidity of 60±5%, and a photoperiod of 16:8 h (L:D).

Experimental arenas

The experimental arena consisted of cells (35 x 35 mm) made of three transparent acrylic slides securely clamped together with metal clips to form an enclosed cell. The top and bottom slides were 2 mm thick and a piece of black paper (35 x 35 mm) was inserted between the middle and bottom slides. The middle slide 5-mm thick had a 10-mm diameter hole in the center and a piece of wet cotton (4 mm diameter) (Fig. 1).

Functional response

The predation experiment was carried out in experimental arenas, and the predatory mites M. mammifer and S. scimitus were starved for 24 h before experiments. Pupae of thrips were offered as prey for both M. mammifer (protonymphs and female adults) and S. scimitus (protonymphs and female adults). After introducing thrips pupae into the experimental cells, starved predatory mites (both protonymphs and female adults) were randomly selected and individually transferred into the cells using a fine camel-hair brush. M. mammifer and S. scimitus protonymph cells were randomly assigned one of six densities of thrips (2, 4, 6, 8, 10 and 12 pupae), while M. mammifer and S. scimitus female adult cells were randomly assigned one of six densities of thrips (3, 5, 10, 15, 20 and 25 pupae). After 24 h, the number of thrips that were consumed was recorded. Each density treatment was replicated 15 times.

Statistical analysis

To discriminate between type II and type III functional responses of the predatory mites M. mammifer and S. scimitus against M. usitatus pupae, a polynomial logistic regression was performed using R4.2.2 (Pritchard et al. 2017) to calculate the proportion of thrips pupae consumed (N_e/N₀) in relation to the initial thrips pupae density (N₀) (Juliano 2001; Timms et al. 2008).

\[\frac{N_e}{N_0} = a + bN_0 + cN_0^2 + dN_0^3 + e\]

where N_e, N₀, a, b, c, and d were number of thrips consumed, the initial number of prey thrips, the intercept, linear, quadratic and cubic coefficient, respectively. A Type II functional response was indicated if b < 0, suggesting that the proportion of thrips pupae consumed declines monotonically with the initial number of thrips. On the other hand, a Type III functional response was indicated if b > 0 and c < 0.

Since prey depletion allowed during the experimental period, the random predator equation (Rogers 1972) for Type II functional response was used to estimate the handling time (T_h) and attack rate (a). The Type II functional response equation is N_e=N₀\{1−exp[a(T_hN_e−T)]\}, Where N_e is the number of successful attacks per M. mammifer or S. scimitus during a specific time period (T), which in this case is 1 d; N₀ is the initial density of the thrips, and a and T_h are the rate of successful attack and the time required to handle the thrips pupae (handling time), respectively. The handling time and attack rate were estimated using maximum likelihood estimation in R 4.2.2 (Pritchard et al. 2017). The consumed amounts of predators at different densities were analyzed with ANOVA (Tukey's test) in SPSS 28.0. The difference in consumption between M. mammifer and S. scimitus at the same density of thrips pupae was analyzed using LSD test in SPSS 28.0.

Results

Predation of Macrocheles mammifer and Stratiolaelaps scimitus

The predation of M. mammifer and S. scimitus significantly increased with increasing density of thrips pupae (M. mammifer female: P < 0.0001; M. mammifer protonymph: P < 0.0001; S. scimitus female: P < 0.0001; S. scimitus protonymph: P < 0.0001), and the females of both M. mammifer and S. scimitus consumed more thrips than counterpart protonymphs. The predation of M. mammifer adult and S. scimitus adult showed no significant difference at low densities (density of 3 and 5, the corresponding P values are 0.862 and 0.297, respectively). However, the predation rate of M. mammifer adult was significantly higher than that of S. scimitus adult at densities greater than 10 (P < 0.0001). The actual maximum number of thrips killed by one S. scimitus female and protonymph was 7.13 and 3.33, respectively, and the actual maximum number of thrips consumed by one M. mammifer female and protonymph was 9.46 and 3.53, respectively (Fig 2).

Functional response of Macrocheles mammifer and Stratiolaelaps scimitus to Megalurothrips usitatus

With the polynomial logistic regression, the functional responses of two predatory mites M. mammifer and S. scimitus to M. usitatus were analyzed. The results showed that both protonymphs (b < 0) and adult females (b < 0) of M. mammifer, as well as S. scimitus, exhibited a type II functional response to thrips (Table 1). These findings indicate that the rate of predation by M. mammifer and S. scimitus on M. usitatus pupae increases rapidly with an increase in thrips density, followed by a decrease until it reaches a plateau.

The findings suggest that M. mammifer had a higher attack rate (a) in protonymphs towards M. usitatus pupae, which was 1.89-fold higher than that of S. scimitus protonymphs. And for adult females, M. mammifer exhibited a slightly higher attack rate value at 4.028, compared to S. scimitus with a rate of 3.944 (Table 2). The theory maximum attack rate (T/T_h) was estimated to be 11.23 for adult females of M. mammifer, which was 1.32-fold higher than that of S. scimitus. Amongst the protonymphs, S. scimitus (4.44) demonstrated slightly higher maximum attack rate in comparison to M. mammifer (4.12) (Table 2). The handing time (T_h) of M. mammifer (0.089 for females and 0.243 for protonymphs) was shorter than that of S. scimitus (0.121 for females and 0.225 for protonymphs) (Table 2).

Discussion

Predatory mites are important predators used for the control of many agricultural pests including thrips (Gerson 2003). In the present study, the functional responses of the soil-dwelled predatory mites, M. mammifer and S. scimitus, to thrips M. usitatus pupae were determined. The results revealed that both mites were effective predators of M. usitatus pupae. Specifically, adult females of M. mammifer consumed more prey than S. scimitus, indicating a higher predation capacity. Additionally, the predation rate was found to be greater in adult female mites as compared to protonymphs, attributable to their larger body size and increased energy requirements for maturation and reproduction. The maximum attack rate (T/T_h) estimated for adult females of M. mammifer was 11.23 (T/T_h), which outperforms that of N. barker on M. usitatus (2.36) (Huang 2022). The results indicate that M. mammifer and S. scimitus may be promising biocontrol agents that can be integrated into the management strategy of M. usitatus.

Previous studies have suggested that S. scimitus is highly effective in predating against thrips (Rahman et al. 2011; Saito 2016). Berndt et al. (2004) found that with the introduction of S. scimitus, a maximum mortality rate of 75.7% was achieved in F. occidentalis populations. Jung et al. (2019) conducted a greenhouse study and discovered that S. scimitus suppressed chrysanthemum thrips population by 74.9%. Park et al. (2021) showed that S. scimitus actively preyed on three thrips species, F. occidentalis, Frankliniella intonsa (Trybom) (Thysanoptera: Thripidae), and Thrips palmi (Karny) (Thysanoptera: Thripidae). The present study demonstrated that S. scimitus has substantial potential for controlling M. usitatus, with a maximum predation rate of 7.13 per day when females preyed on M. usitatus pupae. This rate is higher than that observed when preying on F. occidentalis (Wu et al. 2014; Park et al. 2021). In addition, our laboratory research showed that M. mammifer, a predatory mite discovered in cowpea soil, exhibited even greater efficiency in preying on M. usitatus pupae compared to S. scimitus. Other Macrocheles species, such as M. muscaedomesticae, have been reported as active predators of soil-dwelling stage pests, including Tyrophagus putrescentiae (Schrank) (Sarcoptiformes: Acaridae), Musca domestica (L.) (Diptera: Muscidae), and two Drosophila species (Drosophila melanogaster Meigen (Diptera: Drosophilidae) and Drosophila suzukii (Matsumura) (Diptera: Drosophilidae)) (Qin 2018). Additionally, one study found that Macrocheles. glaber (Mesostigmata: Macrochelidae) consumed up to 3.74 individuals of Cobolidia fuscipes (Meigen) (Mesostigmata: Cobolidae) per day (Wen 2015), while M. robustulus also showed great suppression on F. occidentalis (Messelink et al. 2008). In the present study, the species M. mammifer showed great potential for controlling the Asian long bean thrips M. usitatus.

The type II functional response is the most common predation response observed in predatory mites. In a study conducted by Yao et al. (2014), the predation of three predatory mites, N. cucumeris, N. barkeri, and E. nicholsi, was investigated, and it was found that all three species exhibited a type II functional response when preying on T. flavidulus. Phytoseiid species, Amblyseius andersoni (Chant) and Neoseiulus neoreticuloides (Liang & Hu), also exhibited a type II functional response to Aceria pallida Keifer (Eriophyidae) adults (Fu 2021). Similarly, Amblyseius cucumeris (Oudemans) (Phytoseiidae) was found to display a type II response when preying on F. occidentalis (Shipp and Whitfield 1991). In this study, both M. mammifer and S. scimitus displayed a type II response while preying on thrips M. usitatus. However, it should be noted that in certain predator-prey interactions involving predatory mites, a type III response may also be observed. The functional response may vary due to a variety of factors, such as the sex and developmental stages of both predator and prey, the searching arena and the abiotic environment (Hassell 1978; Lima et al. 2012; Teodoro et al. 2020).

The attack rate and handling time determine the magnitude of the functional response (Pervez and Omkar 2005). Handling time refers to the amount of time it takes for a predator to identify, attack and consume its prey after an encounter, and it varies in proportional to the amount of prey consumed. The lowest handing time in the present study was observed in M. mammifer females, demonstrating the superior handling ability of M. mammifer when preying on M. usitatus. Additionally, female individuals in both M. mammifer and S. scimitus predators exhibited superior handling abilities with shorter handling times compared to protonymphs. Handling time is affected by several factors including the species of predators, predator age and the density of predator/prey (Thoeming and Poehling 2006; Dalir et al. 2021). The larger size and greater mobility of adult female may be associated with their higher predation ability.

However, simplistic experiments cannot fully simulate the complexity of natural environments. In our study, the potential existence of alternative prey in the field was ignored, which may lead to an overestimate of the predation ability to some extent. Therefore, further field research is necessary to determine the predator efficiency under actual conditions. Whatever, the results achieved in the present study provide a reference for utilizing the local predatory mite M. mammifer and S. scimitus as biological control agents against M. usitatus in southern China.

Acknowledgements

We thank Yi Tanci from the College of Agriculture Guizhou University for his efforts on the predatory mite identification. This work was financially supported by Hainan Provincial Natural Science Foundation of China (323MS018), the Startup Foundation for Introduced Talents of Hainan University (KYQD-ZR-1962) and Hainan academician Innovation Platform research project (YSPTZX202021).

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