A simple method of rearing insect natural enemies of spider mites

Biological Control 80 (2015) 70–76

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A simple method of rearing insect natural enemies of spider mites Takeshi Shimoda ⇑, Youichi Kobori 1, Kaori Yara 2, Norihide Hinomoto NARO, Agricultural Research Center, Tsukuba, Ibaraki 305-8666, Japan

Rearing method

Rearing efficiency 120

Honey for F. acarisuga adults

100 b 80 a

60 40

a

20 0 Komatsuna (n = 6)

i n f o

Article history: Received 30 April 2014 Accepted 24 September 2014 Available online 7 October 2014 Keywords: Rearing method Scolothrips takahashii Feltiella acarisuga Stethorus spp. Oligota spp. Spider mite

Lima bean (n = 6)

120

Potted Komatsuna plants with spider mites

250

**

60 30 0 Komatsuna (n = 6)

Kidney bean (n = 6)

b

200 150 a

100 50 0

Lima bean (n = 6)

Feltiella acarisuga

90

Scolothrips takahashii Moist vermiculite for Oligota pupae

Komatsuna (n = 6)

a r t i c l e

Predator death by hooked trichomes

Feltiella acarisuga No. of predator larvae entrapped

Plankton net

No. of predator larvae entrapped

predator groups of pest spider mites.  Rearing these insect predators is difficult due to the lack of suitable host plants.  Prey spider mites can be efficiently maintained on komatsuna plants (Brassica rapa).  The insect predators can be efficiently reared on prey-infested komatsuna plants.

No. of predator adults / container

 We have four important insect

g r a p h i c a l a b s t r a c t

No. of predator adults / container

h i g h l i g h t s

120

Kidney bean (n = 5)

Stethorus spp.

*

90 60 30 0 Komatsuna (n = 5)

Lima bean (n = 4)

a b s t r a c t Establishing effective methods of rearing natural enemies can facilitate basic and applied studies on their use in biological pest control. Insect predators of four genera (Oligota, Stethorus, Scolothrips and Feltiella) and predatory mites are important natural enemies of pest spider mites in agricultural crops. However, fewer laboratory studies have focused on insect predators due to the difficulty of their rearing. To establish a simple rearing method, we compared the rearing efficiency of four insect predator groups (Oligota spp., Stethorus spp., Scolothrips takahashii and Feltiella acarisuga) on potted komatsuna plants (Brassica rapa) infested with the two-spotted spider mite Tetranychus urticae, a new plant-prey combination for predator rearing in large containers, with that on potted bean plants infested with T. urticae. Significantly more Feltiella acarisuga and Stethorus spp. adults were obtained when offered T. urticae-infested komatsuna plants than infested lima bean or kidney bean plants (Feltiella: 70, 9 and 0 adults, respectively; Stethorus: 72, 3 and 0 adults, respectively). More adults of S. takahashii and Oligota spp. were obtained on T. urticae-infested komatsuna than on infested lima bean (Scolothrips: 181 and 27 adults, respectively; Oligota: 152 and 16 adults, respectively). Many individuals of all four predator groups such as larvae of F. acarisuga and Stethorus spp. were entrapped by the hooked trichomes on lima and kidney bean leaves, whereas no entrapped predators were observed on the komatsuna plants. These results show potted komatsuna plants infested with T. urticae to be suitable for efficient rearing of all four predator groups. Ó 2014 Elsevier Inc. All rights reserved.

1. Introduction

⇑ Corresponding author. Fax: +81 29 838 8846. E-mail address: [email protected] (T. Shimoda). Present address: Tropical Agriculture Research Front (TARF), Japan International Research Center for Agricultural Sciences (JIRCAS), Ishigaki, Okinawa 907-0002, Japan. 2 Present address: NARO, Institute of Vegetable and Tea Science, Shimada, Shizuoka 428-8501, Japan. 1

http://dx.doi.org/10.1016/j.biocontrol.2014.09.015 1049-9644/Ó 2014 Elsevier Inc. All rights reserved.

Establishing effective methods of rearing natural enemies is a prerequisite for facilitating basic and applied studies on their use in biological pest control (Van Lenteren and Woets, 1988). For example, large numbers of predators or parasitoids must be provided to evaluate their susceptibility to various pesticides in the laboratory; for this purpose, information on (mass-) rearing

T. Shimoda et al. / Biological Control 80 (2015) 70–76

methods of some beneficial insects and mites has been reported (Sterk et al., 1999). We need more information about efficient rearing methods for other natural enemies to clarify their pesticide susceptibility, biological characteristics and ecological interactions with pest arthropods. Spider mites are an important pest of crops, fruit and ornamental plants (Helle and Sabelis, 1985a; Huffaker et al., 1970). Chemical control of spider mites is challenging, so their natural enemies, which can be roughly classed into predatory mites and insect predators, have received attention in past decades (Helle and Sabelis, 1985b; McMurtry and Croft, 1997). Predatory mites can depress spider mite populations to low densities (Amano, 2001; Chazeau, 1985), while voracious insect predators may prevent outbreaks of spider mites (Gagné, 1995; Kishimoto and Adachi, 2008; Takahashi et al., 2001). Because of the ease of rearing predatory mites, their biological characteristics have been studied extensively (Dicke and Baldwin, 2010; Ellner et al., 2001; Kappers et al., 2005; McMurtry and Croft, 1997; Sabelis and Van De Baan, 1983), and some of them are commercially available for biological pest control (Escudero and Ferragut, 2005; Fournier et al., 1985; Van Lenteren et al., 1997). In contrast, fewer laboratory studies have focused on insect predators, due to the difficulty of rearing them (but see e.g., Gotoh et al., 2004; Kishimoto and Adachi, 2008; Shimoda, 2004). Four genera of insect predators are important natural enemies of spider mites: Oligota (Coleoptera: Staphylinidae), Stethorus (Coleoptera: Coccinellidae), Scolothrips (Thysanoptera, Thripidae), and Feltiella (Diptera: Cecidomyiidae) (Abe et al., 2011; Biddinger et al., 2009; Shimoda and Takabayashi, 2001; Takahashi et al., 2001). Low densities of these insect predators can be reared on detached bean leaves placed on moist cotton wool, called ‘‘leaf discs,’’ infested with the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) in small containers (Gotoh et al., 2004; Kishimoto and Adachi, 2008). However, this rearing system tends to be arduous and inefficient, because prey-infested leaf discs must be supplied frequently (often every few days) for voracious predators (Chazeau, 1985; Gotoh et al., 2004); and the hooked trichomes on bean leaves may affect predator survival (Riddick and Wu, 2011; Sengonca and Gerlach, 1984). The aim of this paper was to establish a simple and improved method for rearing high densities of insect predators of the four genera on whole plants cultivated in a pot, hereafter called ‘‘potted plants’’, that support abundant prey. We have focused on a brassica vegetable, komatsuna (Brassica rapa L., var. perviridis), as a candidate for the host plant, since: (1) it can be easily cultivated in the laboratory or greenhouse; (2) many individuals of T. urticae can be maintained on potted komatsuna plants for several weeks; and (3) it has no hooked trichomes to interfere with insect predators. In this study, we compared the efficiency of rearing the chief natural enemies of the four insect groups in Japan [Oligota spp., Stethorus spp., Scolothrips takahashii Priesner and Feltiella acarisuga (Vallot)] on T. urticae-infested komatsuna plants in large containers with the same process on infested lima bean and kidney bean plants. We show that potted komatsuna plants infested with T. urticae are suitable for efficient rearing of all four predator groups.

2. Materials and methods 2.1. Plants and insects Three lima bean plants (Phaseolus lunatus L., cv. Sieva) or five kidney bean plants (Phaseolus vulgaris L., cv. Nagauzuramame) were cultivated in a plastic pot (diameter: 9 cm, depth: 7 cm) in a climate-controlled room (23 ± 1 °C, 60 ± 10% RH and 16 L: 8 D).

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Three komatsuna plants (B. rapa L., var. perviridis, cv. Rakuten) were cultivated in a plastic pot in a greenhouse (23 ± 3 °C and 16 L: 8 D). T. urticae was reared on potted kidney bean plants in a climate-controlled room (23 ± 1 °C, 60 ± 10% RH and 16 L: 8 D). Several pieces of T. urticae-infested kidney bean leaves were placed on potted lima bean (2–3 weeks after germination), kidney bean (2–3 weeks after germination) or komatsuna plants (4–5 weeks after germination) for 1 day; each potted plant had approximately 4000 mites at all stages (ca. 400 were adult females) and was used for the rearing experiments. Oligota spp. [O. kashmirica benefica Naomi and O. yasumatsui Kistner; which may be involved in the genus Holobus (Hoy, 2011; Löbl and Smetana, 2004)], Stethorus spp. [Stethorus japonicus H. Kamiya and Stethorus pusillus (Herbst)], S. takahashii, and F. acarisuga were collected from kudzu vine plants (Pueraria lobata [Wild] Ohwi) infested with the red spider mite T. pueraricola Ehara & Gotoh in Tsukuba, Ibaraki Prefecture, Japan, in 2009, 2010 and 2011 (Fig. 1). S. takahashii adult females, discriminated morphologically from males, were used in the rearing experiments. Adults of Oligota spp. and Stethorus spp. were individually introduced into a plastic container (diameter: 9 cm, height: 4.5 cm), containing a T. pueraricola-infested kudzu vine leaf disc, for 24 h in a laboratory (25 ± 1 °C, 30 ± 10% RH and 16 L: 8 D); female predators laying eggs were selected for the experiments. Because of the difficulty in discriminating the sexes in F. acarisuga, both adult females and males emerging from the pupae on kudzu vine leaves in a netted plastic cage (25  33  30 cm) were used. Because the taxonomy of the genus Feltiella is ambiguous (Abe et al., 2011; Ganaha-Kikumura et al., 2012), identification of F. acarisuga was confirmed by sending the specimens to Dr. Junichiro Abe at NARO, Western Region Agricultural Research Center, Fukuyama, Hiroshima, Japan. 2.2. Rearing experiments Three Stethorus spp. females were introduced, using a fine paintbrush, onto potted komatsuna, lima bean or kidney bean plants infested with T. urticae in a columnar acrylic container (diameter: 30 cm, height: 40 cm: Fig. 2) in a climate-controlled room (25 ± 1 °C, 30 ± 10% RH and 16 L: 8 D). To supply additional prey, a new pot of each plant species carrying the mites was placed in the container every 5–10 days (Fig 2, Fig. S1). Thirty days after predator introduction, the numbers of adult and other stages (egg, larva and pupa) in the container were counted under a binocular microscope (Leica MZ16; Leica, Tokyo, Japan). Six replicates were made for each plant species. Five adult females of S. takahashii were introduced into a container in which a potted komatsuna or lima bean plant, infested with T. urticae, had been placed. The numbers of adult and other stages (larva and pupa) were investigated 30 days later. Other conditions and procedures were the same as those for Stethorus species. Six replicates were made for each plant species. Thirty adults (including females and males) of F. acarisuga in the netted cage were collected using a glass tube (diameter: 1 cm, length: 7.5 cm) and then transferred into a container with a pot of komatsuna, lima bean or kidney bean plants infested with T. urticae. Small amounts of honey were applied to the wall of the container: F. acarisuga adults feed on sugary foods and do not attack spider mites (see Figs. 1d, 2). A new pot of each plant species with the mites was supplied every 5–7 days. Two weeks later, the number of adult stages was investigated. The other conditions and procedures were the same as those for Stethorus species. Six replicates were made of each plant species. Fully-developed Oligota spp. larvae on prey-infested leaves will die within a few days if they cannot burrow into moist soil to pupate (Shimoda, 2004). Thus, four female predators were introduced onto a pot of prey-infested komatsuna or lima bean plants

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(a)

(b)

(c)

(d)

Honey as adult food

Fig. 1. Insect predators of spider mites used in the rearing experiments. (a) Oligota spp. (O. kashmirica benefica and O. yasumatsui), (b) Stethorus spp. (S. japonicus and S. pusillus, (c) Scolothrips takahashii and (d) Feltiella acarisuga. Adult F. acarisuga eats sugary foods and does not attack spider mites, whereas its larva eats spider mites. The other insect species attack spider mites in both the adult and larval stages. For more details, see the text.

1 cm

Plankton net (20 X 15 cm, mesh size: 30 µm)

Connection to isolate mites and predators

Honey for F. acarisuga adults

Moist vermiculite for Oligota pupae

Potted Komatsuna plants with spider mites 10 cm

Fig. 2. Columnar container used for the rearing experiments. The upper and lower parts of the container fit together to prevent the escape of prey and predators, while the upper part can be opened to add new potted plants with Tetranychus urticae and collect predators. Small amounts of honey are applied to the walls of the container for the F. acarisuga adults. Moist vermiculite is prepared for the pupation site of Oligota spp. For more details, see the text.

placed on moist vermiculite (Fukushima Vermi KK, Japan) in a container (Fig. 2). A new pot of each plant species with the mites was supplied every 5–10 days. The number of adult stages was counted 40 days after predator introduction. Other conditions and procedures were the same as those for the Stethorus species. Four replicates were made for each plant species.

2.3. Statistical analysis The number of insect predators on each host plant species was subjected to the Kruskal–Wallis test followed by the Mann– Whitney U-test weighted by the Bonferroni correction (P < 0.05/ a = 0.016, a = 3: the number for all combinations of the three plant

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species). Statistical analyses were performed using JMP (ver. 10.0.2, SAS Institute Inc., Cary, NC, USA) (Sokal and Rohlf, 1995).

3. Results There was a significant difference between the three plant species in the number of adult F. acarisuga two weeks after predator introduction (Kruskal–Wallis test: H = 13.168, df = 2, P < 0.01); approximately 70 adults were obtained per container when offered T. urticae-infested komatsuna plants, whereas approx. 9 and 0 adults, respectively, were obtained on infested lima bean and kidney bean plants (Fig. 3a). Similar results were obtained for adults of Stethorus spp. when offered the three plant species (Kruskal–Wallis test: H = 13.132, df = 2, P < 0.01): there were 72 adults on T. urticaeinfested komatsuna plants 30 days after predator introduction, whereas 3 and 0 adults were observed, respectively, on infested lima bean and kidney bean plants (Fig. 3b). A significant difference was also found in the numbers of all stages (eggs, larvae and pupae, adults) between the three plant species (n = 4 each, median, lower and upper quartiles; komatsuna: 226, 170.5 and 366.3; lima bean: 6.5, 3 and 16.8; kidney bean: 0, 0 and 9.8 individuals, respectively) (Kruskal–Wallis test: H = 8.495, df = 2, P < 0.05, Fig. S2).

(b) 120

Feltiella acarisuga

No. of predator adults / container

100 b

80 a

60 40

a

20

No. of predator adults / container

(a) 120

As for S. takahashii, 181 adults were observed on T. urticaeinfested komatsuna plants 30 days after predator introduction, whereas 27 adults were observed on infested lima bean plants (U-test: Z = –2.486, df = 1, P < 0.05, Fig. 4a). A significant difference was also seen in the numbers of all stages except eggs (adults, nymphs and pupae) between the two plant species (n = 6 each, median, lower and upper quartiles; komatsuna: 472, 364.8 and 607.8; lima bean: 30, 0 and 153 individuals, respectively; U-test: Z = –2.807, df = 1, P < 0.01). Approximately 152 adults of Oligota spp. were observed on T. urticae-infested komatsuna plants 40 days after predator introduction, whereas 16 adults were observed on infested lima bean plants (U-test: Z = –2.165, df = 1, P < 0.05, Fig. 4b). The lima bean and kidney bean plants were sometimes defoliated due to infestation damage by spider mites, and mold sometimes covered the walls of the container as well as the decayed leaves, which resulted in a decrease in both predators and spider mites (Fig. 5a and b). We did not, however, observe any such leaf abscission in infested komatsuna plants (Fig 2). Many immatures and adults of all four predator groups were entrapped by the hooked trichomes on lima and kidney bean leaves (Fig. 5c and d); in some cases, however, we could not count the numbers of entrapped predators, due to the mold covered the

Stethorus spp.

b

100 80 60 40

a

a

Lima bean (n = 6)

Kidney bean (n = 6)

20 0

0 Komatsuna (n = 6)

Lima bean (n = 6)

Komatsuna (n = 6)

Kidney bean (n = 6)

Fig. 3. The numbers of (a) Feltiella acarisuga adults 14 days after introduction of predators (30 adults) and (b) Stethorus spp. adults 30 days after the introduction of 3 adult females to the three plant species. Dots indicate observations; tops and bottoms of boxes indicate lower and upper quartiles, horizons indicate medians, and the vertical lines indicate the ranges of the largest and smallest observations. Figures followed by different letters are significantly different (U-test with Bonferroni correction, df = 1, P < 0.016).

250

b

Scolothrips takahashii

200

150 a 100

50

(b) No. of predator adults / container

No. of predator adults / container

(a)

200

b

Oligota spp.

150

100

a

50

0

0 Komatsuna (n = 6)

Lima bean (n = 6)

Komatsuna (n = 4)

Lima bean (n = 4)

Fig. 4. The numbers of (a) Scolothrips takahashii adults 30 days after introduction of the predators (5 adult females) and (b) Oligota spp. adults 40 days after introduction (4 adult females) in the two plant species. Dots indicate observations, tops and bottoms of boxes indicate lower and upper quartiles, horizons indicate medians, and the vertical lines indicate the ranges of the largest and smallest observations. Figures followed by different letters are significantly different (U-test, df = 1, P < 0.05).

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(a)

(b)

(c)

(d)

Fig. 5. Factors of the increased mortality of insect predator species in bean plants; (a) defoliation of kidney bean plants by spider mite damage, (b) fouling of a container by decayed kidney bean leaves (c) entrapment of Feltiella acarisuga larva on bean leaves, and (d) entrapment of Scolothrips takahashii female on bean leaves.

120

(b)

Feltiella acarisuga

** 90

60

30

No. of predator larvae entrapped

No. of predator larvae entrapped

(a)

120

Stethorus spp.

*

Komatsuna (n = 5)

Lima bean (n = 4)

90

60

30

0

0 Komatsuna (n = 6)

Kidney bean (n = 5)

Fig. 6. Numbers of dead larvae of (a) Feltiella acarisuga and (b) Stethorus spp. entrapped on each plant. Dots indicate observations; tops and bottoms of boxes indicate lower and upper quartiles; horizons indicate medians; and the vertical lines indicate the ranges of the largest and smallest observations (U-test, df = 1, ⁄⁄: P < 0.01, ⁄: P < 0.05).

defoliated bean leaves. For example, many dead entrapped larvae of F. acarisuga were observed on kidney bean leaves, whereas none were observed on komatsuna plants (U-test: Z = 2.887, df = 1, P < 0.01, Fig. 6a). This was also the case for larvae of Stethorus spp. on lima bean leaves and on komatsuna plants (U-test: Z = 2.549, df = 1, P < 0.05, Fig. 6b). Entrapment of Oligota spp. (89 larvae, n = 1) and S. takahashii (25.5 adults, n = 2) was also observed on lima bean leaves, whereas no entrapped predators (Oligota: n = 4, Scolthrips: n = 6) were observed on the komatsuna plants.

4. Discussion The results show that potted komatsuna plants infested with T. urticae are suitable for rearing Oligota spp. (= Holobus spp., Löbl and Smetana, 2004), Stethorus spp., S. takahashii and F. acarisuga, the

chief insect natural enemies of spider mites in Japan. Significantly more adults of each predator species were obtained in T. urticaeinfested komatsuna plants than those obtained in infested lima bean and/or kidney bean plants. This can be partly explained by predator entrapment by hooked trichomes on bean leaves. Trapped predators were chiefly observed on the undersides of bean leaves (Fig. 5c and d), whereas no predators were trapped on komatsuna plants, due to the absence of hooked trichomes (Fig. 6). The influence of the hooked trichomes on bean leaves has also been reported with other insect predators of spider mites, such as Scolothrips longicornis Priesner (Sengonca and Gerlach, 1984), Stethorus punctum punctum (LeConte) (Biddinger et al., 2009), and Stethorus punctillum Weise (Riddick and Wu, 2011). Another explanation for the fewer predators in bean plants may be the influence of leaf abscission in response to mite-infestation damage (Fig. 5a). Insect predators suffered from a prey shortage when leaf abscission

T. Shimoda et al. / Biological Control 80 (2015) 70–76

occurred, and after leaf abscission, decayed leaves fouled the environment in the rearing container (Fig. 5b). Presumably, leaf abscission of bean plants indirectly influences the survival, oviposition and development of the insect predators, whereas this was not the case with komatsuna plants. Our simple rearing method appears to be an improvement on previous practices in terms of both ease and rearing efficiency. Traditional methods are generally complicated and rely on the frequent supply of mite-infested leaf discs (Gotoh et al., 2004; Kishimoto and Adachi, 2008; Perumalsamy et al., 2009). Nevertheless, insect predators sometimes overexploit prey and then die of starvation, cannibalism or for other reasons (Shimoda, 2004). In contrast, our method requires the simple process of providing potted plants with abundant prey every 5–10 days. We can maintain, for example, 200 or more adults of Oligota or Stethorus spp. on potted komatsuna plants with T. urticae in a large container (Figs. 2, S2), whereas only 20 or fewer adults of these insects can be maintained on a T. urticae-infested lima bean leaf disc in a small container (Shimoda et al., unpublished). To our knowledge, this is the first report to show that insect predators of four genera (Oligota, Stethorus, Scolothrips, and Feltiella) can be efficiently reared in the same way. Thus, our rearing method may be applicable to other insect natural enemies of spider mites. S. punctillum, for example, is an important and commercially available predator of Tetranychus mites in greenhouses and orchards (Biddinger et al., 2009; Raworth, 2001; Rott and Ponsonby, 2000). Commercial mass-rearing methods of S. punctillum were developed in the late 1990s (Raworth, 2001). However, maintaining the beetles and their prey at high densities may be problematic for most researchers. S. punctillum larvae often die on lima bean leaves infested with T. urticae, due to the hooked trichomes (Riddick and Wu, 2011). Potted komatsuna plants with T. urticae are thus likely to excel T. urticae-infested lima bean plants for rearing S. punctillum. As for Oligota species, Oligota pygmaea (Solier) can ben reared on tea leaf discs infested the red spider mite Oligonychus coffeae (Nietner) (Perumalsamy et al., 2009). However, the frequent collection of (prey-infested) leaves from deciduous tea trees, as well as from other deciduous plant species, may be difficult in autumn and winter (Kishimoto and Adachi, 2008; Mori et al., 2005). In contrast, potted komatsuna plants can be cultivated in the laboratory or greenhouse at all seasons. Although we showed the usefulness of T. urticae-infested komatsuna for supporting the four insect predator groups, three questions remain to be clarified. First, it is still unclear why T. urticae can be so easily maintained on komatsuna plants. In spite of there being more than 900 potential host plant species for T. urticae (Navajas, 1998), komatsuna has not been reported as a favorable host. Second, further studies should aim to explore other plants that might be applicable to our rearing system. For example, T. urticae can be maintained on potted vegetables (e.g., cabbage, Chinese cabbage, radish, lettuce and spinach) in the laboratory (Shimoda, unpublished), although T. urticae is only a minor nuisance in these vegetables. Third, there is a need to evaluate the potential for use of other prey species, since T. urticae is a potential pest. For example, F. acarisuga can be maintained on corn plants infested with the Banks Grass Mite Oligonychus pratensis (Banks) (Acari: Tetranychidae) (Xiao et al., 2011). Finding other suitable prey that is not known as a serious pest, and its host plant, may contribute not only to future laboratory studies of insect predators, but also to their release as biological control agents of spider mites. Acknowledgments We thank Dr. Junichiro Abe for his identification of F. acarisuga. We also thank Ms. Yumiko Togashi, Kimiko Kanbe and Yoshiko Ishimura for rearing the spider mites and growing the plants. This

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