Functional response of two soil-dwelling predatory
mites, Macrocheles mammifer (Berlese) (Acari:
Macrochelidae), and Stratiolaelaps scimitus (Womersley)
(Acari: Laelapidae), on thrips Megalurothrips usitatus
(Bagnall) (Thysanoptera: Thripidae)

Jiawei Zhu, Xiangxin Cui, Jian Yang, Xingming Lin, Yi Yan, Ducheng Cai, Jinhua Li

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Jiawei Zhu, Xiangxin Cui, Jian Yang, Xingming Lin, Yi Yan, et al.. Functional response of two soil-dwelling predatory mites, Macrocheles mammifer (Berlese) (Acari: Macrochelidae), and Stratiolaelaps scimitus (Womersley) (Acari: Laelapidae), on thrips Megalurothrips usitatus (Bagnall) (Thysanoptera: Thripidae). Acarologia, 2023, 63 (4), pp.1039-1047. 10.24349/gbg7-7c27. hal-04228002

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# Functional response of two soil-dwelling predatory mites, *Macrocheles mammifer* (Berlese) (Acari: Macrochelidae), and *Stratiolaelaps scimitus* (Womersley) (Acari: Laelapidae), on thrips *Megalurothrips usitatus* (Bagnall) (Thysanoptera: Thripidae)

Jiawei Zhu IDª, Xiangxin Cui IDª, Jian Yang IDª, Xingming Lin IDª, Yi Yan IDᵇ, Ducheng Cai IDª, Jinhua Li IDª

## Original research

### ABSTRACT

*Megalurothrips usitatus* (Bagnall) (Thysanoptera: Thripidae), commonly known as the Asian bean thrips, is a destructive pest of leguminous crops, causing significant damage and economic losses. In the present study, the functional responses and predation rates of two predatory mites *Macrocheles mammifer* Berlese (Macrochelidae) and *Stratiolaelaps scimitus* (Womersley) (Laelapidae) on *M. usitatus* pupae were evaluated. The former was discovered in a cowpea *Vigna unguiculata* (Linn.) Walp. field of southern China, while the latter is commonly used as a biological control agent for soil-dwelling pests. Both *M. mammifer* and *S. scimitus* females consumed more *M. usitatus* than protonymphs, and the predation rate of the adult stage of *M. mammifer* was found to be significantly higher than that of *S. scimitus*. Likewise, logistic regression analysis revealed that both predators exhibited a type II functional response. Females of *M. mammifer* and *S. scimitus* displayed a higher attack rate and shorter handling time (T_h) compared to conspecific protonymphs when preying on pupae of *M. usitatus*. Female *M. mammifer* recorded the highest attack rate (a) of 4.028, closely followed by female *S. scimitus* at 3.994. The protonymph of *M. mammifer* had an attack rate of 2.651, while the protonymph of *S. scimitus* displayed the lowest rate of 1.402. Female *M. mammifer* exhibited the shortest handling time (0.089), indicating superior prey-handling ability. Overall, the predatory mites *M. mammifer* and *S. scimitus* demonstrated considerable promise for managing *M. usitatus*, with *M. mammifer* displaying higher efficacy than *S. scimitus*.

**Keywords** biological control; attack rate; handling time; Asian bean thrips; predation rate

### 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)

Received 14 March 2023
Accepted 09 August 2023
Published 03 October 2023

Corresponding author
Jinhua Li ID: lijinhua0801@126.com

Academic editor
Palevsky, Eric

https://doi.org/10.24349/gbg7-7c27

ISSN 0044-586X (print)
ISSN 2107-7207 (electronic)

<figure><img src="image_7.png" /></figure>

Zhu J. et al.

Licensed under
Creative Commons CC-BY 4.0

<footnote>ªKey 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.</footnote>

<footnote>ᵇDepartment of Entomology, College of Plant Protection, Shandong Agricultural University, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, Taian, China.</footnote>
(Thysanoptera: Thripidae) is the primary pest that affects leguminous crops in China, partic-
ularly 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 (20°05'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 (18°41'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,

<figure><img src="image_8.png" /><figcaption>**Figure 1** The experimental arena consisted of cells made of three transparent acrylic slides. 1: a dovetail clip; 2: a small compartment; 3: a small cotton ball; 4: an upper board; 5: a hollow middle board; 6: a black paper piece; 7: a lower board.</figcaption></figure>
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<sub>e</sub>/N<sub>0</sub>) in relation to the initial thrips pupae density (N<sub>0</sub>) (Juliano 2001; Timms *et al.* 2008).

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

where N<sub>e</sub>, N<sub>0</sub>, 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<sub>h</sub>) and attack rate (a). The Type II functional response equation is N<sub>e</sub>=N<sub>0</sub>{1-exp[a(T<sub>h</sub>N<sub>e</sub>-T)]}, Where N<sub>e</sub> 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; N<sub>0</sub> is the initial density of the thrips, and a and T<sub>h</sub> 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).
<figure><img src="image_9.png" /><figcaption>**Figure 2** The consumption of *Megalurothrips usitatus* by the females (A) and protonymphs (B) of *Macrocheles mammifer* and *Stratiolaelaps scimitus* at different thrips densities after 24 h. The asterisk in the figure indicates a significant difference in the feeding amount between *S. scimitus* and *M. mammifer* under different densities (one-way ANOVA, LSD, p<0.05).</figcaption></figure>

## 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<sub>h</sub>) 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<sub>h</sub>) 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).

<table><caption>**Table 1** Estimates of coefficients in a polynomial logistic regression of the proportion of thrips consumed by adult females and protonymphs of *Macrocheles mammifer* and *Stratiolaelaps scimitus*.</caption><thead><tr><th>Predator and stage</th><th>Type</th><th>Parameters</th><th>Estimate</th><th>SE</th><th>Z</th><th>P > |Z|</th></tr></thead><tbody><tr><td><i>Macrocheles mammifer</i> Adult female</td><td>II</td><td>Linear (b)</td><td>-0.1211</td><td>0.0104</td><td>-11.575</td><td>&lt; 0.0001</td></tr><tr><td><i>Macrocheles mammifer</i> protonymph</td><td>II</td><td>Linear (b)</td><td>-0.1871</td><td>0.0287</td><td>-6.4994</td><td>&lt; 0.0001</td></tr><tr><td><i>Stratiolaelaps scimitus</i> Adult female</td><td>II</td><td>Linear (b)</td><td>-0.1189</td><td>0.01</td><td>-11.889</td><td>&lt; 0.0001</td></tr><tr><td><i>Stratiolaelaps scimitus</i> protonymph</td><td>II</td><td>Linear (b)</td><td>-0.1312</td><td>0.028</td><td>-4.6736</td><td>&lt; 0.0001</td></tr></tbody></table>
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<sub>h</sub>) estimated for adult females of *M. mammifer* was 11.23 (T/T<sub>h</sub>), 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

<table><caption>**Table 2** Attack rate and handling time (days) (means ± SE) for protonymphs and adult females of *Macrocheles mammifer* and *Stratiolaelaps scimitus* when feeding on the pupae of *Megalurothrips usitatus*.</caption><thead><tr><th>Predator and stage</th><th></th><th>Instant attack rate (a)<br>(Asymptotic 95% CI)</th><th>Handling time (T<sub>h</sub>)<br>(Asymptotic 95% CI)</th><th>Maximum attack rate<br>(T/T<sub>h</sub>)</th><th>P > F</th></tr></thead><tbody><tr><td rowspan="2">Macrocheles mammifer</td><td>Adult female</td><td>4.028±0.556(3.179-5.224)</td><td>0.089±0.005(0.082-0.096)</td><td>11.23</td><td>&lt;.0001</td></tr><tr><td>protonymph</td><td>2.651±0.745(1.773-4.469)</td><td>0.243±0.026(0.210-0.277)</td><td>4.12</td><td>&lt;.0001</td></tr><tr><td rowspan="2">Stratiolaelaps scimitus</td><td>Adult female</td><td>3.994±0.646(3.004-5.716)</td><td>0.121±0.007(0.112-0.129)</td><td>8.26</td><td>&lt;.0001</td></tr><tr><td>protonymph</td><td>1.402±0.391(0.990-2.208)</td><td>0.225±0.038(0.179-0.278)</td><td>4.44</td><td>&lt;.0001</td></tr></tbody></table>
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 handling 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 environ-
ments. 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).

ORCID

Jiawei Zhu https://orcid.org/0009-0005-9412-3507

Xiangxin Cui https://orcid.org/0009-0001-4771-2406

Jian Yang https://orcid.org/0009-0007-6521-8149

Xingming Lin https://orcid.org/0009-0000-2771-0502

Yi Yan https://orcid.org/0000-0002-4041-3366

Ducheng Cai https://orcid.org/0009-0002-8853-1449

Jinhua Li https://orcid.org/0000-0002-9127-7763

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