Spider mites (Acari: Tetranychidae) are important pests in apple (Rosaceae) orchards in Japan, and they cause damage to leaves each year. The two-spotted spider mite, Tetranychus urticae Koch, is the dominant spider mite species in many apple orchards in Japan. Tetranychus urticae is difficult to control in apple orchards because it develops resistance to acaricides easily (Funayama Reference Funayama2018). Biological control of T. urticae by conserving native phytoseiid (Mesostigmata) mites in Japanese apple orchards therefore has been the subject of keen research interest in recent years (Funayama Reference Funayama2018). Three dominant native phytoseiid mite species, Neoseiulus womersleyi Schicha (Acari: Phytoseiidae), Typhlodromus vulgaris Ehara (Acari: Phytoseiidae), and Amblyseius tsugawai Ehara (Acari: Phytoseiidae), have been observed in apple orchards in northern Japan (Funayama et al. Reference Funayama, Komatus, Sonoda, Takahashi and Hara2015). Phytoseiid mites are classified into four types (I–IV), based on food habits, biological traits, and morphological traits (McMurtry and Croft Reference McMurtry and Croft1997; McMurtry et al. Reference McMurtry, Morraes and Sourassou2013). Typhlodromus vulgaris and A. tsugawai are Type III, which are generalist predators that feed on various food resources, including tetranychids, eriophyids, and pollen. In contrast, N. womersleyi is Type II, a specialist predator of tetranychid mites (McMurtry and Croft Reference McMurtry and Croft1997). These three native phytoseiid mite species differ in their habitats in apple orchards: most T. vulgaris live on apple leaves, whereas most A. tsugawai inhabit the undergrowth (Funayama et al. Reference Funayama, Komatus, Sonoda, Takahashi and Hara2015). Neoseiulus womersleyi occurs not only on apple leaves but also in the undergrowth, where T. urticae also occurs (Funayama et al. Reference Funayama, Komatus, Sonoda, Takahashi and Hara2015).
In an earlier study (Funayama Reference Funayama2016), I described how each of the three phytoseiid mite species contributes to T. urticae control in apple orchards in northern Japan. First, when T. urticae females that have diapaused under rough bark on trees or in ground litter move to the undergrowth in the spring to reproduce (Gotoh Reference Gotoh1997), A. tsugawai predation suppresses increases in T. urticae numbers in the undergrowth, thereby helping to reduce the numbers of T. urticae that later climb into the trees’ canopies. Second, T. vulgaris on the apple leaves protect the canopy from T. urticae after the latter leaves the undergrowth. Finally, N. womersleyi in the undergrowth rapidly climb the trees to prey upon the increasing T. urticae populations on the apple leaves. In this way, the functions of each of the three native phytoseiid mite species can combine to control T. urticae in Japanese apple orchards.
In 2022, however, I found many Amblyseius andersoni (Chant) (Acari: Phytoseiidae) in an apple orchard (39.23° N, 140.56° E) at the Akita Fruit Tree Experiment Station, in Yokote, Akita Prefecture, northern Japan. The specimens were identified from their external and internal morphology by Dr. Hidenari Kishimoto of the National Agriculture and Food Research Organisation’s Institute for Plant Protection. In the orchard, A. andersoni had not been observed until at least 2018 – before then, only the three above-mentioned native phytoseiid mite species had been observed. Amblyseius andersoni was found for the first time in Japan in 2014, in apple and apricot orchards in Nagano Prefecture in central Japan (Toyoshima et al. Reference Toyoshima, Kishimoto, Kaneko and Amano2016).
Amblyseius andersoni is the dominant phytoseiid species in European apple orchards (Tixier et al. Reference Tixier, Lopes, Blanc, Dedieu and Kreiter2014) and is classified as a Type III generalist predator (Koveos and Broufas Reference Koveos and Broufas2000; McMurtry et al. Reference McMurtry, Morraes and Sourassou2013). It is an important predator of tetranychid mites in European vineyards (Lorenzon et al. Reference Lorenzon, Pozzebon and Duso2012) and is commercially available. There is concern about the potential for interaction and food competition between A. andersoni and native phytoseiid species – especially the generalists – in Japanese apple orchards. In the present study, I compared the seasonal occurrences of N. womersleyi, T. vulgaris, A. andersoni, and T. urticae on leaves in the apple orchard (2000 m2) at the Akita Fruit Tree Experimental Station in 2018 and 2022.
In the orchard, “Fuji” apple trees (older than 20 years; approximately 4 m high) are grown at a spacing of 4 × 3 m. As described in Funayama et al.(Reference Funayama, Komatus, Sonoda, Takahashi and Hara2015), the orchard is managed by spraying with insect growth regulator, the narrow spectrum insecticides, and fungicides; no acaricides are applied. In 2018 and 2022, 20 leaves were sampled from each of six apple trees at 7-day intervals from June to September (340 leaves per tree). A brushing machine (DKI-7200, Daiki Co. Inc., Tokyo, Japan) was used to collect material from both surfaces of the leaves into glass Petri dishes (120 mm diameter). Tetranychus urticae adults, nymphs, and larvae were counted under a binocular microscope. Phytoseiid mites were mounted in Hoyer’s medium, after which a binocular microscope was used to count only the adult females, which were identified to species level from their external and internal shapes, per Toyoshima et al.(Reference Toyoshima, Kishimoto and Amano2013). This investigation was not performed in 2019–2021.
I plotted the seasonal occurrences of the three phytoseiid mites and T. urticae on apple leaves in the apple orchard in 2018 and 2022 (Fig. 1). The relationship between the seasonal occurrences of T. urticae and N. womersleyi was similar in both years: the number of T. urticae increased rapidly and peaked in mid-August in 2018 and in late July in 2022. The population then rapidly decreased, and the species was seldom observed in September in both years.
Figure 1. Seasonal occurrences of the three phytoseiid mites (Neoseiulus womersleyi, Typhlodromus vulgaris, Amblyseius andersoni) and Tetranychus urticae on apple leaves in a Japanese apple orchard in A) 2018 and B) 2022. The orchard was managed by selective chemical spraying in both years. Leaves were collected from six trees in each year. Numbers for each tree are means ± standard error (vertical line) on 20 leaves.
Neoseiulus womersleyi occurred and rapidly increased in numbers in mid-August in 2018 and late July to early August in 2022 – slightly after the population increase of T. urticae – and rapidly decreased thereafter. The mean numbers of N. womersleyi and of T. urticae per tree did not differ significantly between the two years (N. womersleyi, P = 0.090 and T. urticae, P = 0.469 by Mann–Whitney U-test; JMP 8, SAS Institute, Cary, North Carolina, United States of America; Table 1). Generally, the density of specialist phytoseiid mites in orchards, including N. womersleyi, increases continuously during the summer in a time-lagged response to increases in the density of T. urticae (e.g., Kishimoto Reference Kishimoto2002). Therefore, the seasonal occurrences of N. womersleyi and T. urticae in the two years (Fig. 1) appeared to follow the normal pattern, suggesting that the occurrence of A. andersoni would have little impact on the predatory activity of N. womersleyi against T. urticae.
Table 1. Numbers of mites of each species collected on leaves in apple orchards in 2018 and 2022
Note: Significance: **P < 0.01 (Mann–Whitney U-test).
* Twenty leaves were collected from each tree every week from June to September (340 leaves per tree).
† Total number of adults, nymphs, and larvae.
‡ Number of adult females.
However, in 2022, as occurred with N. womersleyi, the increase in the numbers of A. andersoni was synchronised with the increase in the population of T. urticae (Fig. 1). Moreover, the mean maximum density of T. urticae in 2022 (mean ± standard error 66.7 ± 12.8 per tree) was significantly lower than it was in 2018 (mean ± standard error 164.2 ± 24.9 per tree; P = 0.008 by Mann–Whitney U-test). Although A. andersoni is a generalist predator, this finding suggests that the nonnative phytoseiid was actively targeting T. urticae as prey. Fu et al. (Reference Fu, Liu, Liu and Meng2021) reported that A. andersoni shows a Type II response to Aceria pallida Keifer (Acari: Eriophyoidae), an important pest of goji berry, Lycium baebarum (Solanaceae). Amblyseius andersoni therefore might come to supplant N. womersleyi in helping to suppress increases in the T. urticae population. If this is the case, a detailed investigation will be required to determine whether A. andersoni influences the availability of food for N. womersleyi.
In 2018, T. vulgaris occurred from mid-June and increased rapidly in numbers after late August, when the T. urticae population decreased. Many T. vulgaris individuals were observed in September (Fig. 1). It is possible that the main food resource of T. vulgaris is pollen grains that are derived from various plants and that stick to the apple leaves (Funayama Reference Funayama2016); therefore, T. vulgaris populations can remain steady even if spider mites are not present (Funayama et al. Reference Funayama, Komatus, Sonoda, Takahashi and Hara2015). Moreover, T. vulgaris has commonly been observed on apple trees, and this mite’s numbers have been observed to increase after T. urticae numbers decrease due to predation by N. womersleyi (Funayama et al. Reference Funayama, Komatus, Sonoda, Takahashi and Hara2015), a pattern also noted in 2018 in the present study. This pattern is likely caused by the fact that generalist phytoseiid mites, including T. vulgaris, are severely impeded by the complex webs of T. urticae (Shimoda et al. Reference Shimoda, Kishimoto, Takabayashi, Amano and Dicke2009). In addition, T. urticae is not a suitable food source for T. vulgaris (Toyoshima Reference Toyoshima2003). However, I found in the present study that the number of T. vulgaris per tree was significantly lower in 2022 than in 2018 (P = 0.002 by Mann–Whitney U-test; Table 1). In 2022, only a few T. vulgaris individuals were observed in early August and early September, whereas many A. andersoni were present at that time (Fig. 1). These data suggest that, in the four years between 2018 and 2022, A. andersoni had displaced T. vulgaris.
Displacement of phytoseiid mite species has occurred previously in Japanese fruit-tree orchards. Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) was found for the first time in Tokyo in 1964, and in commercial orchards in the Kanto region, the dominant native species, N. womersleyi, was replaced by N. californicus in the 1990s (Kishimoto Reference Kishimoto2002; Gotoh et al. Reference Gotoh, Hanawa, Shimazaki, Yokoyama, Fu, Sugawara and Yano2014). The possibility that A. andersoni distribution could expand widely in Japanese apple orchards, as had occurred with N. californicus, is a matter of concern.
Among potential factors that may have allowed the displacement of T. vulgaris by A. andersoni, weather conditions between 2018 and 2022 likely were not significant: according to weather data collected by the Japan Meteorological Agency (JMA) automated meteorological data acquisition system (AMeDAS) for Yokote city (39° 30′ N, 140° 55′ E; 6.6 km from the orchard), daily annual mean temperatures barely fluctuated during that time, ranging from 11.6 to 12.2 °C, and daily annual mean cumulative precipitation ranged from 52.5 to 85.0 mm. Orchard management practices, including agrochemical spraying and mowing, were also consistent through these years. Laboratory tests indicate that the two factors behind the 1990s displacement of N. womersleyi by N. californicus in the Kanto region were (1) different degrees of pesticide susceptibility (Ullah et al. Reference Ullah, Hanawa and Gotoh2016) and (2) asymmetrical intraguild predation (Gotoh et al. Reference Gotoh, Hanawa, Shimazaki, Yokoyama, Fu, Sugawara and Yano2014). In contrast, it is unlikely that different degrees of pesticide susceptibility are behind the displacement of T. vulgaris by A. andersoni: in both years, the study orchard was managed by the same spraying regime, which involved narrow-spectrum insecticides and fungicides. Moreover, the susceptibility of T. vulgaris to broad-spectrum chemicals, including pyrethroids and organophosphates, has decreased considerably in commercial apple orchards (Ogasawara et al. Reference Ogasawara, Hirayama, Togawa and Ishiguri2022). It was also not clear in the present study whether T. vulgaris displacement by A. andersoni is occurring through asymmetrical intraguild predation. Detailed investigations are needed to determine the cause of this phenomenon and to assess whether the occurrence of A. Andersoni in Japanese apple orchards will change the control of pest T. urticae by the three native phytoseiid mite species, including A. tsugawai (Funayama Reference Funayama2016).
