Open Access
How to translate text using browser tools
1 September 2012 Predatory Mite, Amblyseius swirskii (Acari: Phytoseiidae), for Biological Control of Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae)
María Juan-Blasco, Jawwad A. Qureshi, Alberto Urbaneja, Philip A. Stansly
Author Affiliations +
Abstract

The Asian Citrus Psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is a serious pest of citrus in many citrus-producing regions. It vectors the bacterium ‘Candidatus Liberibacter asiaticus’ thought to be the causal agent of the devastating “Huanglongbing” (HLB) or citrus greening disease. Both pest and the disease are well established in Florida. Several insect predators, particularly lady beetles and the parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae), are known to cause significant mortality to ACP immatures. However, there are no reports on the effectiveness of predatory mites against ACP We evaluated the suitability of D. citri eggs and nymphs as prey for the predatory mite Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) in laboratory arenas, and its potential to reduce psyllid populations in the glasshouse on caged Murraya paniculata (L.) Jack plants. Mortality of D. citri eggs on M. paniculata shoots exposed to A. swirskii in plastic arenas was 4 times greater after 6 d compared to unexposed control plants. Mites were also observed sucking out body fluids of first instar nymphs. In the glasshouse, total number of D. citri adults collected over 8 wk from infested plants in ventilated cylinders with A. swirskii present averaged 80% less than the control without mites. These findings showed a significant negative impact of A. swirskii on D. citri under controlled conditions. Further research needs to focus on rates and frequency of release, impact of A. swirskii on D. citri populations in citrus and other hosts under field conditions, and interactions of A. swirskii and D. citri with native predatory mites.

The Asian Citrus Psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is an invasive pest of special concern, which has expanded its range throughout the citrus-producing regions of Asia and now the Americas. In the United States, the psyllid was first detected in Florida in Palm Beach, Broward and Martin Counties in June 1998 and quickly spread throughout the citrus-growing areas of the state (Halbert 1998; Halbert & Manjunath 2004; Michaud 2002; Tsai et al. 2002). It has also been identified in Texas, California, Arizona, and most of the south-eastern US (French et al. 2001, Qureshi & Stansly 2010). Host plants of D. citri are confined to Rutaceae, in particular the genus, Citrus and its relatives (Halbert & Manjunath 2004). The ornamental orange jasmine, Murraya paniculata (L.) Jack, a common hedge plant in south Florida, is considered a preferred host of ACP (Tsai et al. 2000). Direct injury to citrus by ACP results from phloem feeding on emerging foliage (flush), which causes permanent distortion or even abscission of new shoots with heavy infestation (Michaud 2004; Hall & Albrigo 2007). However, most economically important damage is caused by transmission of the bacterium ‘Candidatus Liberibacter asiaticus’, thought to be the causal agent of “huanglongbing” (HLB) or citrus greening disease (Halbert & Manjunath 2004). Symptoms indicating the presence of the bacterium are chlorosis resembling zinc deficiency, a more diagnostic blotchy or asymmetrical mottling of leaves, twig dieback with leaf and fruit drop, uneven coloring of fruits and reduction in fruit size and quality (Halbert & Manjunath 2004). Citrus greening disease was first detected in Florida in 2005 (Halbert 2005) and has spread throughout the state ( http://www.freshfromflorida.com/pi/chrp/ArcReader/mi2%20Sections%20in%20Florida%20Positive%20for%20HLB%2015%20Mile%20Buffer.pdf)

Integrated pest management (IPM) practices involving biological and chemical control strategies are being developed to suppress psyllid populations and to consequentially slow the spread of citrus greening (Qureshi & Stansly 2007, 2009, 2010). Native or exotic biological control agents of the psyllid include predators as diverse as ladybeetles (Coleoptera: Coccinellidae), lacewings (Neuroptera: Chrysopidae), spiders (Aranae), and hoverflies (Diptera: Syrphidae) that together can greatly reduce the reproductive potential of the ACP population by more than 90% (Michaud 2002, 2004; Pluke et al. 2005; Qureshi & Stansly 2008, 2009). Two exotic parasitoids of ACP, Diaphorencyrtis aligarhensis (Shafee, Alam and Agaral) (Hymenoptera: Encyrtidae) and Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) were introduced in Florida in 2000 against ACP (Hoy & Nguyen 2001). Tamarixia radiata is now widely distributed in the Florida citrus ecosystem at variable rates of parasitism (Qureshi et al. 2009) whereas D. aligarhenis has not established. Coccinellid predator species, Olla υ;-nigrum (Mulsant), Curinus coeruleus (Mulsant), Harmonia axyridis (Pallas), and Cycloneda sanguinea (L.) (Coleoptera: Coccinellidae), are thought to be the most important sources of biotic mortality on D. citri nymphs in Florida (Michaud 2002, 2004; Michaud & Olsen 2004; Qureshi & Stansly 2009). However, any single approach by itself is not going to provide enough reduction of the vector psyllid and citrus greening disease. Dormant season foliar sprays of broad spectrum insecticides in winter provide 5–27 fold reduction in ACP populations and opportunity for biological control in spring and summer (Qureshi and Stansly 2010). Nevertheless, the disease continues to advance, despite more frequent sprays of insecticides during growing season in many orchards.

This situation calls for a more proactive and augmentative approach to biological control, commencing with identification of other natural enemies of ACP. One avenue not yet investigated is biological control using predatory phytoseiid mites (Acari: Phytoseiidae) that could feed on the eggs and nymphs of D. citri. Phytoseiid mites are important agents of biological control on many pests in many crops. Depending on the species, their food may include mites, thrips and Hemiptera such as whiteflies and armored scales as well as pollen and honeydew (Dosse 1961; Putman 1962; McMurtry & Scriven 1964; Swirskii et al. 1967; Juan-Blasco et al. 2008). These findings have heightened interest in exploring additional possibilities for using mites to control different phytophagous organisms in many crops (Nomikou et al. 2001; Calvo et al. 2011). Thirty-eight species of phytoseiid mites have been reported in Florida citrus, although the biology of only a few has been studied (Abou-Setta & Childers 1987; Abou-Setta et al. 1997; Caceres & Childers 1991; Fouly et al. 1994; Yue et al. 1994). Much is yet to be learned about phytoseiids that colonize Florida citrus. We are aware of no published reports to date of any native or exotic phytoseiid attacking eggs or the first nymphal instar D. citri.

Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) has shown itself to be a very efficient biological control agent of thrips [Thrips tabaci Lindeman and Frankliniella occidentalis (Pergande)] (Thysanoptera: Thripidae), whiteflies [Trialeurodes vaporariorum Westwood and Bemisia tabaci (Gennadius)] (Hemiptera: Aleyrodidae) and phytophagous mites [Tetranychus urticae Koch (Acari: Tetranychidae) and Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae)] (Swirskii et al. 1967; Gerling et al. 2001; Nomikou et al. 2001; Calvo et al. 2011; Stansly & Castillo 2009, 2010). Eggs and crawlers (first instar nymphs) of D. citri are very similar in shape and size to those of B. tabaci. Eggs of D. citri are laid in the newly developing unfolded leaves where they and the first instar nymphs are protected from large predators, but easily accessible to predatory mites. For the same reason, and due to its commercial availability and effectiveness as biological control agent of whiteflies and other pests in greenhouse, open field vegetable and citrus production (Stansly & Castillo 2009, 2010; Calvo et al. 2011; Juan Blasco et al. 2008), A. swirskii was selected for a preliminary evaluation against D. citri.

Our objectives were to determine whether 1) A. swirskii mites use D. citri eggs and nymphs as prey and 2) the mites suppress D. citri populations on young isolated M. paniculata plants following controlled release in a glasshouse.

MATERIALS AND METHODS

Cultures and Source Material

Diaphorina citri used in the experiments was obtained from a colony housed at the Southwest Florida Research and Education Center (SWFREC) in Immokalee, Florida, USA since 2005. The colony was maintained on M. paniculata plants propagated from seed and grown in a greenhouse covered with “Antivirus” insect netting in 15 or 20 cm pots using a substrate consisting of processed pine bark, 60% + Canadian sphagnum peat and vermiculite. Plants were pruned 2 to 3 wk prior to use to induce emergence of new shoots before being moved to an air-conditioned glasshouse maintained at 27 ± 4 °C; 70 ± 10% RH. Six plants were placed in a wooden cage for oviposition twice a week (60 × 60 × 60 cm) with openings covered with fine polyester netting (40 × 10 mesh/ cm) containing 300 adult ACP. After 3 d, plants were shaken and remaining adults vacuumed off. Plants were then transferred into an empty cage and held until emergence of adult ACP to be used for experimentation or to replenish the colony. Used plants were pruned, sprayed with a 2% glycerin soap solution (Clearly Natural Essentials Honeysuckle, Pure and Natural Glycerine Soap) and recycled for later use. Amblyseius swirkii sustained on the dried fruit mite Carpoglyphus lactis (L.) (Acari: Carpoglyphidae), was provided by Koppert Biological Systems (SWIRSKI-MITE®; Howell, Michigan. USA). Experiments were conducted from Nov 2007 to Feb 2008.

Laboratory Experiment

Predation by A. swirkii on eggs and nymphal instars of D. citri was evaluated. Plants that had been pruned 8 d prior were placed in the oviposition cage with adult psyllids to infest new shoots as described above. A young shoot of M. paniculata infested with D. citri eggs was removed from a plant and placed inside an experimental arena consisting of a snap-cap polystyrene cylindrical vial (10 cm in length and 4 cm in diam). The bottom of the vial was removed and replaced by fine polyester organdy attached with hot glue. The polyethylene lid was perforated to receive a smaller plastic tube (length 1.7 cm, diam 0.7 cm) filled with water into which the stem of the shoot was inserted and sealed to the vial lid with plasticine to prevent escape of the mites. The vial was then inverted onto the cap to enclose the upper part of the shoot and placed in a metal grill over a plastic tray filled with water (Fig. 1).

Five A. swirskii adult females taken directly from SWIRSKI-MITE® bottles were placed in the experimental arena without alternative food. The experiment was set up the day SWIRSKI-MITE® bottles were received from manufacturer. Amblyseius swirskii females used in the experiment were neonate (maximum 2 days old) (Xu & Enkegaard 2010). There were 15 replicates of 3 treatments set out in a randomized complete block design: 1) shoots infested with D. citri eggs without A. swirskii, 2) A. swirskii adult mites with no D. citri or any other food source and 3) shoots infested with eggs of D. citri and A. swirskii adult mites. Vials were held in an air-conditioned rearing room maintained at 22 ± 2 °C, 63 ± 8% RH, 16:8 (L:D) photophase. Survival of A. swirskii adult females, the number of D. citri eggs and eventually D. citri nymphs were tallied under a stereoscopic microscope at intervals 0, 2, 4, and 6 d without replacement. Eggs and nymphs of D. citri were counted as dead when observed empty and desiccated.

Glasshouse experiment

The capacity of A. swirskii to suppress populations of D. citri on isolated plants was evaluated in an air-conditioned glasshouse maintained at 27 ± 4 °C; 70 ± 10% RH. Murraya paniculata plants, each in a 15 cm diam pot and with 4–6 young shoots were used for the experiment. Shoots were infested with D. citri eggs which were counted with the aid of a magnifying head set (2.75 X). Each plant was placed in a ventilated cylindrical cage made from a sealed sheet of clear plastic film covered on top with coarse mesh organdy (Qureshi et al. 2009, Fig. 2). Amblyseius swirskii adults were released on 4 plants at ratio of 1:2 (A. swirskii adults: D. citri eggs) inside of 30 mL plastic cups attached to the plant branch with wire. The correct number of A. swirskii was estimated by using a mean of 10 mites/gram of substrate obtained by counting mites in 10 randomly selected one-gram samples of substrate under a stereoscopic microscope. The control treatment consisted of plants infested with D. citri eggs but no mites. Emerging D. citri adults were aspirated off the plants and counted weekly for 8 wk. Leaves were inspected on the plant using the magnifying headset and phytoseiid eggs, larvae, nymphs and adults were recorded for 6 to 8 wk or until no more D. citri adults had been seen on the plants for 2 consecutive weeks. Larvae of the phytoseiids are easily distinguished from nymphs and adults by the presence of three pairs of legs. Nymphs and adults have four pairs of legs. Nymphs molt through the different nymphal stages (protonymph and deutonymph) to adult and leave the corresponding exuviae (Abad-Moyano et al. 2009). The counted exuviae were removed from plants.

Fig. 1.

Bioassay setup to test the effect of A. swirskii on D. citri eggs. A young shoot of M. paniculata infested with D. citri eggs was placed inside an experimental arena and exposed to mites or not. The experimental arena consisted of a snap cap polystyrene cylindrical vial (10 cm in length and 4 cm in diameter). The bottom of the vial was removed and replaced by fine polyester organdy and the lid was perforated to receive a smaller plastic tube (length 1.7 cm, diameter 0.7 cm) filled with water into which the stem of the shoot was inserted. The shoot was sealed to the vial lid with plasticine to prevent the escape of mites. The vial was then inverted onto the cap to cover the upper part of the shoot to prevent escape of the mites and the plastic tube attached to lid was placed in a plastic tray full of water.

f01_543.jpg

Data Analysis

A generalized linear mixed model (GLMM) (Breslow & Clayton 1993) was used to analyze treatment effects on D. citri eggs and nymphs and on survival of A. swirskii using PASW Statistics version 19.0.0 (IBM SPSS Inc., Chicago, Illinois, USA;  www.spss.com) for the laboratory experiment. Treatments (A. swirskii present or absent) were included as fixed effects, and shoots observed on d 2, 4 and 6 were included as a random effect. Selection of the best model was based on the Akaike Information Criterion (AIC). This revealed that the Poisson distribution with a logarithmic link was most appropriate to analyze for treatment effects.

The reduction of D. citri numbers attributable to A. swirskii predation on caged plants in the glasshouse was calculated using the HendersonTilton formula (Henderson & Tilton 1955). ANOVA was used to compare D. citri adult emergence between the A. swirskii and control treatments. Diaphorina citri adult emergence was square root transformed (sqrt (x)) to correct for heterogeneity of variance.

RESULTS

Laboratory Experiment

Adults of A. swirskii were observed preying upon eggs and first instar nymphs of D. citri on M. paniculata shoots. The predatory mites were observed sucking out the body fluids of the nymphs which then looked dried and empty. More dead D. citri eggs were observed in the presence of A. swirskii than in its absence (GLMM: F1,28 = 103.18, P < 0.001) (Fig. 3A).

The treatment effect on number of dead nymphs was not significant (GLMM:F 1,28 = 0.01, P = 0.935). Honeydew excretions from nymphs decreased over the 6-d observation period, indicating failure of the shoots to provide complete nutrition after the first few d which may have contributed to D. citri nymphal mortality. However, fewer live nymphs were observed on A. swirskii treated shoots than on untreated shoots (GLMM: F1,28 = 46.68, P < 0.001) (Fig. 3B). This suggests a negative effect on the development of nymphs from eggs in the presence of A. swirskii. Indeed, fewer D. citri nymphs (dead + live) were observed on shoots with A. swirskii adults compared with shoots without mites after 6 days (GLMM: F1,28 = 18.98, P < 0.001) (Fig. 3C). However, nymphal survival was low on both A. swirskii treated and control shoots. An average of 24 ± 9 (34%) live nymphs were observed in the control treatment at the end of the experiment out of the 79 ± 8 eggs at the beginning of the experiment compared with 6 ± 5 (14%) live nymphs observed in the A. swirskii treatment.

Survival of adult A. swirskii mites on shoots infested with D. citri eggs and nymphs was not different from shoots without D. citri eggs and nymphs up to 6 d (GLMM: F1,28 = 2.67, P = 0.114), which averaged 72 ± 8% on shoots infested with D. citri eggs and nymphs and 56 ± 13% on shoots without D. citri eggs and nymphs. Mite reproduction was limited over the 6 d period. One larva and 3 nymphs of A. swirskii were recorded in replicates with access to D. citri, and only 1 larva in replicates without D. citri.

Glasshouse Experiment

Initial numbers of D. citri eggs observed on A. swirskii treated and untreated plants averaged (± SE) 247 ± 37 and 240 ± 40 per plant, respectively. The total number of psyllid adults collected from plants with A. swirskii averaged 42 ± 11 which was 80% less than 204 ± 31 collected from control plants without A. swirskii (ANOVA: F1,7 = 28.79, P = 0.002) (Fig. 4). Most psyllid adults emerged during the second and third wk of observation. Most A. swirskii individuals (egg to adult) were observed 2 wk after release when a mean of 52 ± 15 per plant out of the initial 124 ± 21 per plant was found. The mean number of A. swirskii observed per plant had decreased the third week (24 ± 14), and then during wk 4 and 5 showed the minimum number of all life stages of A. swirskii observed, 5 ± 2 and 5 ± 3, respectively. Per plant numbers of all life stages of A. swirskii increased during wk 6, 7 and 8, averaging between 3 ± 0.5 – 5 ± 0.8, 9 ± 1.1 - 17 ± 1.8, 14 ± 1.5 - 33 ± 4.6, and 66 ± 5.7 - 86 ± 7.4 for eggs, larvae, nymphs and adults, respectively, during 3 wk period.

Fig. 2.

Potted Murraya paniculata plants isolated inside ventilated cylinders in the glasshouse experiment. The 30 ml plastic cups shown in the picture contained bran mixed with Amblyseius swirskii and the dried fruit mite, Carpoglyphus lactis (L.), as food.

f02_543.jpg

DISCUSSION

We observed that D. citri eggs on young shoots were preyed upon by A. swirskii mites under laboratory conditions and numbers of dead psyllid eggs were greater in the presence of the mites. To our knowledge this is the first time that a phytoseiid mite was recorded preying upon eggs of D. citri. Although, predation was also observed on first instar nymphs of D. citri (0–6 d in the laboratory experiment), there was no statistically significant difference in the number of dead nymphs between A. swirskii treated and control shoots, presumably due to low survivorship in untreated controls. Possibly, shoot quality declined over time and could not provide enough nutrition for nymphs as evidenced by reduced honeydew secretion and high control mortality. Removal of young shoots from plants may have inhibited photoassimilate transport from mature leaves to shoot apices where eggs were laid and newly hatched nymphs fed. In contrast, adult emergence was 85% from nymphs that developed on intact shoots of caged plants in the control treatment in glasshouse.

Fig. 3A.

Mean (± SE) number of Diaphorina citri dead eggs observed at 2, 4 and 6 days on infested shoots of Murraya paniculata that were exposed or not to 5 Amblyseius swirskii adult females. The days of evaluation are counted from the infestation of M. paniculata shoots during ≈ 48 h with fresh eggs of D. citri. The initial number of D. citri eggs on each shoot averaged 79 ± 8 on the first day of the trial.

f03a_543.jpg

Fig. 3B.

Mean (± SE) number of Diaphorina citri live nymphs observed at 2, 4 and 6 days on infested shoots of Murraya paniculata that were exposed or not to 5 Amblyseius swirskii adult females. The days of evaluation are counted from the infestation of M. paniculata shoots during ≈48 h with fresh eggs of D. citri. The initial number of D. citri eggs on each shoot averaged 79 ± 8 on the first day of the trial.

f03b_543.jpg

Fig. 3C.

Mean (± SE) number of Diaphorina citri total (dead + live) nymphs observed at 2, 4 and 6 days on infested shoots of Murraya paniculata that were exposed or not to 5 Amblyseius swirskii adult females. The days of evaluation are counted from the infestation of M. paniculata shoots during ≈ 48 h with fresh eggs of D. citri. The initial number of D. citri eggs on each shoot averaged 79 ± 8 on the first day of the trial.

f03c_543.jpg

Availability of alternative prey as well as nonprey food sources such as pollen and insect-produced honeydew are often important for predator establishment and persistence in the crop (González-Fernández et al. 2009; Nomikou et al. 2003, 2010). Non-prey food sources not only provide water and nutrients to complement a diet consisting of prey, but sometimes allow for predator reproduction. Nomikou et al. (2003) observed that cattail pollen supported survival, development and reproduction of the two phytoseiid species A. swirskii and Euseius scutalis Athias-Henriot. Similarly, honeydew from B. tabaci greatly increased survival of E. scutalis, and supported development to adulthood and a high rate of oviposition. In contrast, coccid-produced honeydew did not promote development or oviposition of E. scutalis or A. swirskii, indicating that honeydew from B. tabaci may be of higher quality than coccid-produced honeydew, at least for E. scutalis (Swirski et al. 1967). Survival of adult A. swirskii was high with or without pollen or honeydew from B. tabaci provided on cucumber leaves, but oviposition by adults and juvenile survival was very low on a diet of honeydew compared with pollen (Nomikou et al. 2003). However, others (Ragusa & Swirski 1977; Momen & El-Saway 1993) observed enhanced survival of A. swirskii on honeydew produced by B. tabaci. Therefore, psyllid honeydew could be used by predatory mites as an alternative food source while searching for prey in the field. Additionally, previous studies have demonstrated that other species of phytoseiid mites are able to feed on plant sap (Grafton-Cardwell & Ouyang 1996; McMurtry & Croft 1997). Further investigation is needed to determinate the suitability of psyllid honeydew for A. swirskii as well as the role that plant sap can play in their survival.

Fig. 4.

Mean (± SE) number of Diaphorina citri adults collected from Murraya paniculata plants infested with eggs of D. citri and placed under ventilated cylinder cages inside a glasshouse. Treatment plants received Amblyseius swirskii at a ratio 1:2 (A. swirskii adult: D. citri egg) compared with control plants with no mite release. Adults were collected weekly.

f04_543.jpg

Citrus pollen could also be a useful non-prey food source for A. swirskii. Villanueva & Childers (2004) found a positive relationship between the number of phytoseiids and pollen grains on grapefruit leaves during the period of citrus flowering at Lake Alfred, Florida. In addition to pollen and honeydew from psyllids, A. swirskii, a polyphagous predator, could also benefit from other potential preys that colonize citrus such as several species of mites and thrips. Mixed diets are sometimes better food than any single type of food (Messelink et al. 2008). Both A. swirskii and E. scutalis had higher oviposition rates on diets of spider mites and almond anthers than on either food alone (Swirski et al. 1967). Amblyseius swirskii demonstrated higher oviposition on a mixed diet of eriophyoid mites and castor bean pollen than on pollen alone (Ragusa & Swirski 1977).

The glasshouse experiment was conducted to test if prédation by A. swirskii upon D. citri observed on individual shoots could also be observed on isolated plants. Amblyseius swirski released at a 1:2 (A. swirskii adult: D. citri egg, 124:247) ratio reduced the D. citri population up to 85% compared with control plants. This result demonstrated the potential for psyllid control using A. swirskii. Nomikou et al. (2002) also showed suppression of B. tabaci on single plants of cucumber using A. swirskii. Stansly & Castillo (2009, 2010) observed significant suppression of broad mite Polyphagotarsonemus latus (Banks) in the field using A. swirskii on both pepper and eggplant. Also, eggplant receiving A. swirskii yielded significantly more fruit than untreated plants or even eggplants receiving sprays of the acaracide spiromesefen. In this study, the increase in number of immature A. swirskii 1 month after the initial release indicated that they were probably using psyllid immatures and honeydew to support reproduction along with the food mites present with the SWIRSKI-MITE® formulation.

In this study, the predator A. swirskii showed promise for biological control against D. citri show some promise, but further tests are necessary to determine its possible role in the management of D. citri. Amblyseius swirskii inoculations could be used to reduce psyllid populations on young plants in the nurseries and field and thus, be used as a preventive measure to reduce D. citri eggs (inoculum). Future research should be focused on appropriate host plants (e.g., varieties of citrus or citrus relatives), reproduction of A. swirskii on D. citri diet, its prey preference, rates and frequency of the releases, density dependent effects and impact on D. citri populations in the field. Other predators, particularly lady beetles and the parasitoid, T. radiata, are already well established in Florida citrus and known to cause significant mortality to psyllid populations in the citrus groves (Michaud 2004; Qureshi & Stansly 2009; Qureshi et al. 2009). If proved effective in the field, A. swirskii could be a useful addition to enhance natural mortality of D. citri through its impact on eggs and first instar nymphs which are protected in newly developing unopened leaves and difficult to reach by most predators. These early immature stages are not targeted by nymphal parasitoids which prefer later instars (Chu & Chien 1991). Finally, the predatory role of native mites on D. citri as well as their interactions with A. swirskii should also be evaluated.

REFERENCES CITED

1.

R. Abad-Moyano , T. Pina , F. Ferragut , and A. Urbaneja 2009. Comparative life history traits of three phytoseiid mites associated to Tetranychus urticae (Acari: Tetranychidae) colonies on clementine orchards in eastern Spain. Implications on biological control. Exp. Appl. Acarol. 47:121–132 Google Scholar

2.

M. M. Abou-Setta , and C. C. Childers 1987. Biology of Euseius mesembrinus (Acari: Phytoseiidae): life tables on ice plant pollen at different temperatures with notes on behavior and food range. Exp. Appl. Acarol. 3: 123–130. Google Scholar

3.

M. M. Abou-Setta , A. H. Fouly , and C. C. Childers 1997. Biology of Proprioseiopsis rotundus (Acari: Phytoseiidae) reared on Tetranychus urticae (Acari: Tetranychidae) or pollen. Florida Entomol. 80: 27– 33. Google Scholar

4.

N. E. Breslow , and D. G. Clayton 1993. Approximate inference in generalized linear mixed models. J. American Stat. Assoc. 88: 9–25. Google Scholar

5.

S. Caceres , and C. C. Childers 1991. Biology and life tables of Galendromus helveolus (Acari: Phytoseiidae) on Florida citrus. Environ. Entomol. 20: 224– 229. Google Scholar

6.

F. J. Calvo , K. Bolckmans , and J. E. Belda 2011. Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. Biocontrol 56: 185–192. Google Scholar

7.

Y. I. Chu , and C. C. Chien 1991. Utilization of natural enemies to control of psyllid vectors transmitting citrus greening, pp. 135–145 In K. Kiritani , J. Su H. and Y. I. Chu [eds.], Proc. Integrated control of plant virus diseases, 9–14 Apr 1990. Food and Fertilizer Technology Center for the Asian and Pacific Region, Taichung, Taiwan. Google Scholar

8.

G. Dosse 1961. Über die Bedeutung der Pollennahrung für Typhlodromus pyri Scheuten (= tiliae Oud.) (Acari, Phytoseiidae). Entomol. Exp. Appl. 4: 191– 195. Google Scholar

9.

A. H. Fouly , H. A. Denmark , and C. C. Childers 1994. Description of the immature and adult stages of Proprioseiopsis rotendus (Muma) and Properioseiopsis asetus (Chant) from Florida (Acari: Phytoseiidae). Intern. J. Acarol. 20(3): 199–207. Google Scholar

10.

J. V. French , C. J. Kahlke, and J. V. Da Graça 2001. First record of the Asian citrus psylla, Diaphorina citri Kuwayama (Homoptera: Psyllidae), in Texas. Subtrop. Plant Sci. 53: 14–15. Google Scholar

11.

D. Gerling , O. Alomar , and J. Arno 2001. Biological control of Bemisia tabaci using predators and parasitoids. Crop Prot. 20: 779–799. Google Scholar

12.

J. J. GonzáLez-FernáNdez , F. De La Peña , J. I. Hormaza , J. R. Boyero , J. M. Vela , E. Wong , M. M. Trigo , and M. Montserrat 2009. Alternative food improves the combined effect of an omnivore and a predator on biological pest control, a case study in avocado orchards. B. Entomol. Res. 99: 433–444. Google Scholar

13.

E. E. Grafton-Cardwell , and Y. Ouyang 1996. Influence of citrus leaf nutrition on survivorship, sex ratio, and reproduction of Euseius tularensis (Acari: Phytoseiidse). Environ. Entomol. 25: 1020–25. Google Scholar

14.

S. E. Halbert 1998. Entomology section. Tri-ology (May–June 1998) 37: 6–7. Google Scholar

15.

S. E. Halbert 2005. Pest Alert: Citrus greening/huanglongbing. Florida Dept. of Agr. and Customer Serv., Dept. of Plant Ind. Google Scholar

16.

S. E. Halbert , and K. L. Manjunath 2004. Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomol. 87: 330–353. Google Scholar

17.

D. G. Hall , and L. G. Albrigo 2007. Estimating the relative abundance of flush shoots in citrus, with implications on monitoring insects associated with flush. HortScience 42: 364–368. Google Scholar

18.

C. F. Henderson , and E. W. Tilton 1955. Tests with acaricides against the brown wheat mite, J. Econ. Entomol. 48: 157–161. Google Scholar

19.

M. A. Hoy , and R. Nguyen 2001. Classical biological control of Asian citrus psylla. Citrus Ind. 81: 48–50. Google Scholar

20.

M. Juan-Blasco , M. J. VerdÚ , and A. Urbaneja 2008. Depredación del piojo rojo de California, Aonidiella aurantii (Maskell), por frtoseidos depredadores. Bol. San. Veg. Plagas 34: 187–199. Google Scholar

21.

J. A. McMurtry , and G. T. Scriven 1964. Biology of the predaceous mite Typhlodromus rickeri (Acarina:Phytoseiidae). Ann. Entomol. Soc. Am. 57: 362–367. Google Scholar

22.

J. A. McMurtry , and B. A. Croft 1997. Life-styles of phytoseiid mites and their roles in biological control. Annu. Rev. Entomol. 42: 291–321. Google Scholar

23.

G. J. Messelink , R. Van Maanen , S. E. F. Van Steenpaal , and A. Janssen 2008. Biological control of thrips and whiteflies by a shared predator: two pests are better than one. Biol. Control 44: 372–379. Google Scholar

24.

J. P. Michaud 2002. Biological control of Asian citrus psyllid (Homoptera: Psyllidae) in Florida. A preliminary report. Entomol. News 113: 216–222. Google Scholar

25.

J. P. Michaud 2004. Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biol. Control 29: 260–269. Google Scholar

26.

J. P. Michaud , and L. E. Olsen 2004. Suitability of Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae) as prey for ladybeetles (Coleoptera: Coccinellidae). BioControl 49: 417–431. Google Scholar

27.

F. M. Momen , and S. A. El-Saway 1993. Biology and feeding behaviour of the predatory mite Amblyseius swirskii (Acari: Phytoseiidae). Acarologia 34: 199– 204. Google Scholar

28.

M. Nomikou , A. Janssen , R. Schraag , and M. W. Sabelis 2001. Phytoseiid predators as potential biological control agents for Bemisia tabaci. Exp. Appl. Acarol. 25: 271–291. Google Scholar

29.

M. Nomikou , A. Janssen , R. Schraag , and M. W. Sabelis 2002. Phytoseiid predators suppress populations of Bemisia tabaci on cucumber plants with alternative food. Exp. Appl. Acarol. 27: 57–68. Google Scholar

30.

M. Nomikou , A. Janssen , and M. W. Sabelis 2003. Phytoseiid predators of whiteflies feed and reproduce on non-prey food sources. Exp. Appl. Acarol. 31: 15–26. Google Scholar

31.

M. Nomikou , M. W. Sabelis , and A. Janssen 2010. Pollen subsidies promote whitefly control through the numerical response of predatory mites. Biocontrol 55: 253–260. Google Scholar

32.

R. W. H. Pluke , A. Escribano , J. P. Michaud , and P. A. Stansly 2005. Potential impact of lady beetles on Diaphorina citri (Homoptera: Psyllidae) in Puerto Rico. Florida Entomol. 88: 123–128. Google Scholar

33.

W. L. Putman 1962. Life history and behavior of the predaceous mite Typhlodromus caudiglans Schuster (Acarina: Phytoseiidae) in Ontario, with notes on the prey of related species. Canadian Entomol. 94: 163–177. Google Scholar

34.

J. A. Qureshi , and P. A. Stansly 2007. Integrated approaches for managing the Asian citrus psyllid Diaphorina citri (Homoptera: Psyllidae) in Florida. Proc. Florida State Hort. Soc. 120: 110–115. Google Scholar

35.

J. A. Qureshi , and P. A. Stansly 2008. Rate, placement, and timing of aldicarb applications to control Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae) in oranges. Pest Manag. Sci. 64: 1159– 1169. Google Scholar

36.

J. A. Qureshi , and P. A. Stansly 2009. Exclusion techniques reveal significant biotic mortality suffered by Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) populations in Florida citrus. Biol. Control 50: 129–136. Google Scholar

37.

J. A. Qureshi , and P. A. Stansly 2010. Dormant season foliar sprays of broad spectrum insecticides: An effective component of integrated management for Diaphorina citri (Hemiptera: Psyllidae) in citrus orchards. Crop Prot. 29: 860–866. Google Scholar

38.

J. A. Qureshi , M. E. Rogers , D. G. Hall , and P. A. Stansly 2009. Incidence of invasive Diaphorina citri (Hemiptera: Psyllidae) and its introduced parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in Florida citrus. J. Econ. Entomol. 102: 247–256. Google Scholar

39.

S. Ragusa , and E. Swirski 1977. Feeding habits, post embryonic and adult survival, mating, virility and fecundity of the predacious mite Amblyseius swirskii (Acarina: Phytoseiidae) on some coccids and mealybugs. Entomophaga 22: 383–392. Google Scholar

40.

P. A. Stansly , and J. A. Castillo 2009. Control of broad mite Polyphagotarsomeus latus and the whitefly Bemisia tabaci in open field pepper and eggplant with predaceous mites, pp. 145–152 In C. Castañe and D. Perdikis [eds.], Proc. Working Group Integrated control in protected crops, Mediterranean climate: IOBC WPRS Bull. Google Scholar

41.

P. A. Stansly , and J. A. Castillo 2010. Control of broadmites, spidermites, and whiteflies using predaceous mites in open-field pepper and eggplant. Florida State Hort. Soc. 122: 253–257. Google Scholar

42.

E. Swirski , S. Y. Amitai , and N. Dorzia 1967. Laboratory studies on the feeding, development and reproduction of the predaceous mites Amblyseius rubini Swirskii and Amitai and Amblyseius swirskii Athias (Acarina: Phytoseiidae) on various kinds of food substances. Israel J. Agric. Res. 17: 101–119. Google Scholar

43.

J. H. Tsai , J. J. Wang , and Y. H. Liu 2000. Sampling of Diaphorina citri (Homoptera: Psyllidae) on orange jasmine in southern Florida . Florida Entomol. 83: 447–459. Google Scholar

44.

J. H. Tsai , J. J. Wang , and Y. H. Liu 2002. Seasonal abundance of the Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae) in southern Florida. Florida Entomol. 85: 446–451. Google Scholar

45.

R. T. Villanueva , and C. C. Childers 2004. Phytoseiidae increase with pollen deposition on citrus leaves. Florida Entomol. 87: 609–611. Google Scholar

46.

B. Yue , C.C. Childers , and A. H. Fouly 1994. A comparison of selected plant pollens for rearing Euseius mesembrinus (Acari: Phytoseiidae). Intern. J. Acarol. 20: 103–108. Google Scholar

47.

X. Xu , and A. Enkegaard 2010. Prey preference of the predatory mite, Amblyseius swirskii between first instar western flower thrips Frankliniella occidentalis and nymphs of the twospotted spider mite Tetranychus urticae Journal of Insect Science, 10: 1–11 Google Scholar
María Juan-Blasco, Jawwad A. Qureshi, Alberto Urbaneja, and Philip A. Stansly "Predatory Mite, Amblyseius swirskii (Acari: Phytoseiidae), for Biological Control of Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae)," Florida Entomologist 95(3), 543-551, (1 September 2012). https://doi.org/10.1653/024.095.0302
Published: 1 September 2012
KEYWORDS
Citrus sinensis
Huanglongbing
Murraya paniculata
phytoseiid mites
predation
Back to Top