Amblyseius swirskii - Wiley Online Library

Entomological Research 47 (2017) 263–269

RES EAR CH P APE R

Performance of the predator Amblyseius swirskii (Acari: Phytoseiidae) on greenhouse eggplants in the absence and presence of pine Pinus brutia (Pinales:Pinaceae) pollen Halil KUTUK Abant Izzet Baysal University, Faculty of Agriculture and Natural Science, Bolu, Turkey

Correspondence Halil Kutuk, Abant Izzet Baysal University, Faculty of Agriculture and Natural Science, Department of Plant Protection, Bolu, Turkey. Email: [email protected] Received 12 May 2016; accepted 17 January 2017. doi: 10.1111/1748-5967.12222

Abstract In Turkey, the western thrips Frankliniella occidentalis (Pergande) is a key pest affecting eggplants grown in greenhouses for which an appropriate control strategy is under investigation. It was observed in a previous study that the release of the beneficial predatory mite Amblyseius swirskii (Athias-Henriot) alone did not result in an effective control of thrips on eggplants. Since pollen is known to improve control efficiency of predators, this study was undertaken to investigate if provision of pollen to eggplants can greatly improve the efficiency of A. swirskii in controlling thrips. The experiments were carried out in both greenhouse and low tunnel. The provision of pollen led to a significant increase in the predator population density on the eggplants but did not result in an effective control of the thrips populations. In this paper, various factors are discussed that could have affected the efficiency of the predatory mite in controlling F. occidentalis on eggplants. Key words: Amblyseius swirskii, eggplant, Frankliniella occidentalis, pine pollen.

Introduction An important characteristic of a biological control agent is its ability to use alternative food sources, which promote its persistence in the field when prey is absent or scarce, and facilitate mass rearing of the agent for augmentative biological control purposes (Ramakers 1990; Van Rijn & Sabelis 1990; Nomikou et al. 2001). Phytoseid mites are important biological control agents of different kinds of pests on various greenhouse crops worldwide (Gerson & Weintraub 2012). Much attention has been given to the preventive releases of generalist phytoseiid species as a control strategy to suppress pest organisms on crops (Weintraub et al. 2009; Nomikou et al. 2010). The feeding habits of phytoseiid species can range from specialists (only feeding on spider mites) to generalists (feeding on various types of foods including pollen, nectar, insects and plant exudates) (McMurtry & Croft 1997). The Western thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), is one of the most significant insect pests found on the Mediterranean coast of Turkey (Tunc &

© 2017 The Entomological Society of Korea and John Wiley & Sons Australia, Ltd

Gocmen 1994; Keçeci et al. 2007). It causes serious damage to eggplants in commercial greenhouses in Turkey. To control this pest, some commercial companies have suggested the use of Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) as it has been successful in the control of pests on pepper and cucumber in greenhouses. A. swirskii is considered a beneficial predatory mite in the Mediterranean region. It is associated with plant species of more than 35 families, but most commonly found in citrus plantations (Swirski & Amitai 1997; Zannou & Hanna 2011). In a previous study by Kutuk et al. (2016), A. swirskii was found to fail in the control of F. occidentalis on eggplants grown in a greenhouse. This predator is a well-known pollenophagous species, and its failure to control F. occidentalis could be in part attributed to the lack of alternative food sources, such as pollen, on these plants. Eggplants not only produce little pollen in winter but also the pollen produced by these plants is generally of very low quality (Abak & Güler 1994). The availability of pollen as alternative food, the presence of oviposition sites and shelter are factors that play an important role in the establishment and efficiency of biological control agents

H. Kutuk

(Kreiter et al. 2002; Nomikou et al. 2010; Romero & Benson 2005; Walter 1996; Wackers 2005). The results from related studies by Kutuk and Yigit (2011) and Kumar et al. (2015) indicated that early establishment of A. swirskii can be ensured on pepper plants if, in the absence of prey, that pollen is provided as an alternative food source. Therefore, we hypothesized that the provision of pollen to eggplants would be a viable strategy to improve the effectiveness of A. swirskii in controlling F. occidentalis on greenhouse eggplants. Thus, the objective of this study was to investigate the effect of provision of pollen on population dynamics of A. swirskii and on F. occidentalis population on greenhouse eggplants.

Materials and Methods Cultures The predatory mite A. swirskii was obtained from Koppert Turkey Co. Ltd. Sti. Antalya, Turkey, six months prior to undertaking this study. A colony of A. swirskii was maintained on Carpoglyphus lactis (Acari: Acaridae) in a climate room (25°C, 60 % RH, 14 h light: 10 h dark LD 14: 10) at the Biological Control Research Station in Adana, Turkey. The mites were reared in plastic arenas (8 × 15 cm) placed over a wet sponge in a plastic tray containing water (Overmeer 1985). Strips of wet tissue were placed over the plastic arena along its periphery to allow the predators access to water. Carpoglyphus lactis was reared on dried apricots, and apricots infested with all stages of C. lactis were supplied as food sources to A. swirskii.

Pollen source Plants of the families Betulaceae and Pinaceae are considered the most important pollen providers for generalist Typhlodromus species in spring (Addison et al. 2000). The pollen used in this study was collected from pine (Pinus brutia) trees in 2010 at the base of Taurus Mountains then dried in an oven for 3 days at 37°C and kept in a refrigerator at 10°C.

Plastic greenhouse experiment The eggplants cultivar “Faselis” was planted in a 120-m2 plastic greenhouse two weeks prior to the commencement of the experiments. The greenhouse was divided into three plots separated by polyethylene film, each consisting of five subplots of three rows (0.8 m apart), each row containing 10 plants spaced 0.4 m apart. The cultivation practices were the same as those recommended for commercial production in the area.

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The experiment was set up in a completely randomized design with three treatments each replicated five times: (A) 50 A. swirskii m2 + pollen sprayed at 5 kg/ha; (B) 50 A. swirskii m2 alone; and (C) 0 A. swirskii m2 and all the plants were sprayed only with water. The active stages of A. swirskii were directly released onto plants. Three releases were performed during the whole experimental period; first on 22 October 2010 (when the plants started flowering), and second and third on 17 March 2011 and 7 May 2011, respectively. For the plots treated with “treatment A”, the plants were first sprayed with pine pollen before releasing the predatory mite. The pollen was suspended in water and sprayed on the plants with hand equipment using a coarse nozzle. The pollen spray was repeated three times on the same dates (22 October, 17 March, and 7 May). Commencing three weeks after the first release of A. swirskii, sampling was conducted once every 10 days to monitor the population dynamics of F. occidentalis and the predatory mite. A total of 28 samples were obtained from 11 November 2010 to 8 June 2011. Samples from 10 leaves and five flowers were randomly collected from each plot, wrapped in a paper towel to prevent moisture buildup, placed in plastic ice bags and brought to the laboratory. The numbers of F. occidentalis (nymphs and adults) and A. swirskii (all stages) on each leaf or flower were recorded under a binocular microscope at 30 times magnification. Temperature and relative humidity were monitored during the experiment with HOBO (Onset Computer, Bourne, MA, USA) data loggers. The mean 10 days interval temperature during the experiment ranged from 23.3°C on 22 October 2010 to 24.8°C on 8 June 2011, whereas the maximum and minimum values during this period were 24.8°C and 12.1°C, respectively. During the mean 10 days interval, relative humidity fluctuated from 30.3 % to 83.6 %, with the minimum value during this period being 30.3 %.

Low polythene tunnel experiment This experiment was conducted in a commercial eggplant field in Tarsus County in Icel province on the East Mediterranean coast of Turkey. The eggplants cultivar “Cukurova topagi” were planted on 20 February 2011 and covered with low polythene tunnels. The tunnels were removed in early May. The colonization and control efficiency of A. swirskii were evaluated in three treatments in a randomized block design, replicated four times: (A) 50 A. swirskii m2 + pollen sprayed at 5 kg/ha; (B) 50 A. swirskii m2 alone; (C) 0 A. swirskii m2 and all plants being sprayed with only water. The experimental layout consisted of four plots of 100 eggplants; each plot was subdivided into three sub-plots, and the treatment allocation within each sub-plot was randomized.

Entomological Research 47 (2017) 263–269 © 2017 The Entomological Society of Korea and John Wiley & Sons Australia, Ltd

Performance of Amblyseius swirskii

During the whole experimental period, three releases were performed; on 22 March 2011 (when the plants started flowering), 27 April 2011 and 26 May 2011. For plots treated with “treatment A”, plants were sprayed with pine pollen before releasing the predatory mite. The pollen spray was repeated three times on the same dates (22 March, 27 April, and 26 May). The mean weekly temperature during the experiment ranged from 21.8°C on 30 March 2011 to 26.7°C on 15 June 2011 and the minimum value during this period was 16.5°C. The mean weekly relative humidity fluctuated from 82.1 % to 75.1 %, with a minimum value during this period of 67.8 %. Three weeks after the first release of A. swirskii, weekly sampling was undertaken to monitor the population dynamics of F. occidentalis and the predatory mite. A total of 12 samples were conducted from 30 March 2011 to 15 June 2011. Samples of 13 leaves and six flowers were randomly collected from each plot, wrapped in a paper towel to prevent moisture buildup, placed into plastic ice bags and brought to the laboratory. The numbers of F. occidentalis (nymphs and adults) and A. swirskii (all stages) on each leaf or flower were recorded under a binocular microscope at 30 times magnification. The fields used for both experiments were treated with compatible insecticides: chlorantraniliprole (Altacor) and pymetrozine (Plenum) against Spodoptera littoralis and Aphis spp. Neither of these insecticides negatively affect A. swirskii (Kutuk & Karacaoglu 2012).

Data analysis The numbers of thrips and predators were compared between treatments for both experiments using a repeated measure ANOVA, with the sample date as the repeated measure. For the presence of pollen, a repeated measure ANOVA with the time and presence or absence of pollen as the factors was performed on average numbers of thrips (leaves + flowers) and the average numbers of the predatory mite (leaves + flowers) as dependent variables.

Results and Discussion Plastic greenhouse experiment Throughout the experiment, the thrips densities were similar during the three treatments (Fig. 1; F (2, 12) = 0.15, P = 0.985). The density of F. occidentalis remained very low in all the treatments throughout autumn and winter. However, the thrips populations gradually increased after mid-April reaching a peak on 18 May of 24.5 thrips per flower in the control plot (treatment C), 26.4 thrips per flower in one of


the release plots (treatment B) and 25.32 thrips per flower in the remaining release plots (treatment A). A significantly higher number of predators was recorded on plants that received pollen (treatment A) than on the plants that received no pollen (treatment B) (Fig. 2; F (1, 8) = 386.8, P = 0.000), although similar density of thrips were recorded on plants with pollen (treatment A) and plants without pollen (treatment B), (F (1, 8) = 0.004, P = 0.949). The average numbers of predators were 1.5 and 0.78 per leaf/flower for plants with pollen and plants without pollen, respectively.

Low polythene tunnel experiment Thrip densities were not significantly different among the three treatments (Fig. 3; F (2, 9) = 0.689, P = 0.527). The highest density was found on 26 May with about 13 thrips / flower in the control treatment and 14.6 thrips/ flower in the other two treatments (treatment A and B). However, plants treated with pollen had significantly more predators (Fig. 4; F (1, 6) = 16.06, P = 0.007) than those that had not received pollen. Contrary to our expectation, the provision of pollen to the eggplants did not result in improved control of the thrips F. occidentalis by the predatory mite A. swirskii although a significant increase was observed in the number of predators. This result corroborates previous observations by Kutuk and Yigit (2011) and Kumar et al. (2015) suggesting that, in contrast with our findings, pollen is not the main factor of the lack of performance of A swirskii in the control of thrips on eggplants grown in greenhouses. The inability of A. swirskii to effectively control thrips on the greenhouse eggplants may result from various other factors. First, solanaceous species including eggplant are particularly rich in trichomes (Tissier 2012). These trichomes have been shown to inhibit the movement of a variety of predators and parasitoids, and glandular trichomes can even be toxic to their natural enemies (Bottrell & Barbosa 1998; Cortesero et al. 2000). Thus, plant morphology that is beneficial to one natural enemy may be harmful to another (Seelmann et al. 2007; Speight et al. 2009). Recent literature has established that many phytoseiids exhibit preferences for pubescent leaves and that the presence of trichomes increases the abundance of phytoseiids (Schmidt 2014). However, a study by Seelmann et al. (2007) indicated that there are examples of phytoseiid species that are better adapted to the environment of glabrous leaves. Amblyseius andersoni (Chant) is found in higher densities in glabrous varieties of grapes in the field (Camporese & Duso 1996). Neoseiulus californicus (McGregor) exhibits a lower functional response on the tomato plant, which contains numerous glandular trichomes, than on other plants (Cedola et al. 2001). Krips et al. (1999) found that Gerbera jamesonii Bolus ex Hook. f.

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Figure 1 The influences of presence or absence of pine pollen and Amblyseius swirskii releases on Frankliniella occidentalis population dynamics in plastic greenhouse experiment. ↓ Arrows indicate the dates of the release of A. swirskii and pine pollen spraying.

Figure 2 Effects of the presence of pollen on the numbers of the predatory mite, Amblyseius swirskii in the plastic greenhouse experiment. ↓ Arrows indicate the dates of the release of A. swirskii and pine pollen spraying.

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Figure 3 The influences of presence or absence of pine pollen and Amblyseius swirskii releases on Frankliniella occidentalis population dynamics in low polythene tunnel experiment. ↓ Arrows indicate the dates of the release of A. swirskii and pine pollen spraying.

varieties with higher trichome densities decrease the predation rate of Phytoseiulus persimilis Athias-Henriot. The results of a study by Buitenhuis et al. (2014) showed that trichome density could explain some of the variability in efficacy of A. swirskii on different crops. However, further studies are needed to comparatively evaluate the controlling efficiency of this predatory mite on different eggplant varieties with varying trichome densities. Second, although enhanced thrips control was observed after pine pollen was provided to populations of the predatory


mite A. swirskii on pepper plants (Kutuk & Yigit 2011), the type of crop in which alternative or supplemental food is applied can also affect the results through the indirect effects of plant metabolites on the predation and oviposition rates of predatory mites (Koller et al. 2007). In the present study, no enhanced predation of thrips was found as a result of presence of pollen (Figs 1,3), as was found earlier on pepper. Crop differences may partly explain why A. swirskii was not effective in the current study. Leman and Messelink (2015) suggested that the application of extra food to a crop must

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Figure 4 Effects of the presence of pollen on the numbers of the predatory mite, Amblyseius swirskii in the low polythene tunnel experiment. ↓ Arrows indicate the dates of the release of A. swirskii and pine pollen spraying.

be undertaken with caution because the results may strongly depend on the initial predator–prey ratio, the nutritional quality of the alternative food source, the species of predatory mites, the distribution of the food in the crop and the type of crop. Further investigation may also be needed to determine the nutritional quality of pine pollen for A. swirskii and also the initial density ratios of A. swirskii and thrips in presence of pine pollen.

Acknowledgments We are grateful to the Ministry of Food, Agriculture and Livestock of Turkey for funding the project supporting this research.

References Abak K, Güler HY (1994) Pollen fertility and the vegetative growth of various eggplant genotypes under low temperature greenhouses conditions. Acta Horticulturae 366: 85–91. Addison JA, Hardman JMJ, Walde SJ (2000) Pollen availability for predaceous mites on apple: spatial and temporal heterogeneity. Experimental and Applied Acarology 24: 1–18. Bottrell DG, Barbosa P (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annual Review of Entomology 43: 347–367. Buitenhuis R, Shipp L, Scott-Dupree C, Brommit A, Lee W (2014) Host plant effects on the behavior and performance of Amblyseius swirskii (Acari: Phytoseiidae). Experimental and Applied Acarology 62: 171–180.

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Camporese P, Duso C (1996) 1996Different colonization patterns of phytophagous and predatory mites (Acari: Tetranychidae, Phytoseiidae) on three grape varieties: a case study. Experimental and Applied Acarology 20: 1–22. Cedola CV, Sanchez NE, Liljesthrom GG (2001) Effect of tomato leaf hairiness on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae). Experimental and Applied Acarology 25: 819–831. Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding and manipulating plant attributes to enhance biological control. Biological Control 17: 35–49. Gerson U, Weintraub PG (2012) Mites (Acari) as a factor in greenhouse management. Annual Review of Entomology 57: 229–247. Keçeci M, Ceylan S, Kahveci L, Ülker Y, Toprakci N (2007) Studies on greenhouse pests and their population fluctuation on greenhouse peppers in Antalya province of Turkey. In: Proceedings of the 2nd National Plant Protection Congress, 27–29 August; Isparta, Turkey. Abstract B 38. Koller M, Knapp M, Schausberger P (2007) Direct and indirect adverse effects of tomato on the predatory mite Neoseiulus californicus feeding on the spider mite Tetranychus evansi. Entomologia Experimentalis et Applicata 125: 297–305. Kreiter S, Tixier M-S, Croft BA, Auger P, Barret D (2002) Plants and leaf characteristics influencing the predaceous mite Kampimodromus aberrans (Acari: Phytoseiidae) in habitats surrounding vineyards. Environmental Entomology 31: 648–660. Krips OE, Kleijn PW, Willems PEL, Gols GJZ, Dicke M (1999) Leaf hairs influence searching efficiency and predation rate of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). Experimental and Applied Acarology 23: 119–131. Kumar V, Xiao Y, McKenzie CL, Osborne LS (2015) Early establishment of the phytoseiid mite Amblyseius swirskii (Acari:



Phytoseiidae) on pepper seedlings in a Predator-in-First approach. Experimental and Applied Acarology 65: 465–481. Kutuk H, Karacaoglu M (2012) Testing for non-target effects of some fungicides and insecticides on western flower thrips and their predator Amblyseius swirskii, under plastic tunnel conditions. Bulletin IOBC-WPRS 80: 199–203. Kutuk H, Yigit A (2011) Pre-establishment of Amblyseius swirskii (Athias-Henriot) (Acari:Phytoseiidae) using Pinus brutia (Ten.) (Pinales: Pinaceae) pollen for thrips (Thysanoptera: Thripidae) control in greenhouse peppers. International Journal of Acarology 37: 95–101. Kutuk H, Karacaoglu M, Tufekli M, Villanueva RT (2016) Failure of biological control of Frankliniella occidentalis on protected eggplants using Amblyseius swirskii in the Mediterranean region of Turkey. Turkish Journal of Agriculture and Forestry 40: 13–17. Leman A, Messelink GJ (2015) Supplemental food that supports both predator and pest: A risk for biological control? Experimental and Applied Acarology 65: 511–524. Nomikou M, Janssen A, Schraag R, Sabelis MW (2001) Phytoseiid predators as potential biological control agents for Bemisia tabaci. Experimental and Applied Acarology 25: 271–291. Nomikou M, Sabelis MW, Janssen A (2010) Pollen subsidies promote whitefly control through numerical response of predatory mites. BioControl 55: 253–260. Overmeer WPJ (1985) Rearing and handling. In: Helle W, Sabelis MW (eds) Spider mites, their biology, natural enemies and control, pp 161–170. Elsevier, Amsterdam. Romero GQ, Benson WW (2005) Biotic interactions of mites, plants and leaf domatia. Current Opinion in Plant Biology 8: 436–440. Schmidt RA (2014) Leaf structures affect predatory mites (Acari: Phytoseiidae) and biological control: a review. Experimental and Applied Acarology 62: 1–17.


Seelmann L, Auer A, Hoffmann D, Schausberger P (2007) Leaf pubescence mediates intraguild predation between predatory mites. Oikos 116: 807–817. Speight MR, Hunter MD, Watt AD (2009) Insect pest management. In: Speight MR, Hunter MD, Watt AD (eds) Ecology of insects, pp 429–513. Wiley- Blackwell, Oxford, UK. Swirski E, Amitai S (1997) Annotated list of phytoseiid mites (Mesostigmata: Phytoseiidae) in Israel. Israel Journal of Entomology 31: 21–46. Tissier A (2012) Glandular trichomes: what comes after expressed sequence tags? Plant Journal 70: 51–68. Tunc I, Gocmen H (1994) New greenhouse pests, Polyphagotarsonemus latus and Frankliniella occidentalis in Turkey. FAO Plant Protection Bulletin 42: 218–220. van Rijn PCJ, Sabelis MW (1990) Pollen availability and its effect on the maintenance of populations of Amblyseius cucumeris, a predator of thrips. Bulletin IOBC/WPRS 13: 179–184. Wackers FL (2005) Suitability of (extra-) floral nectar, pollen and honeydew as insect food sources. In: Wackers FL, van Rijn PCJ, Bruijn J (eds) Plant-provided food for carnivorous insects: a protective mutualism and its applications, pp 17–74. Cambridge University Press, Cambridge, UK. Weintraub PG, Kleitman S, Mori R, Gan-Mor S, Gannot L, Palevsky E (2009) Novel application of pollen to augment the predator Amblyseius swirskii on greenhouse sweet pepper. Bulletin IOBC/WPRS 50: 119–124. Zannou ID, Hanna R (2011) Clarifying the identity of Amblyseius swirskii and Amblyseius rykei (Acari: Phytoseiidae): are they two distinct species or two populations of one species? Experimental and Applied Acarology 53: 339–347.

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