Journal of Biological Control, 28(1): 1–16, 2014 Review Article The most common predators of Bemisia tabaci (Genn.): Biology, predation, preferences, releases, alternative food resources, combined use, current efforts and future perspectives FIRAS A. AL-ZYOUD Dept. of Plant Protection and IPM, Faculty of Agriculture, Mu’tah University, Karak, 61710 Jordan Corresponding author email: [email protected] ABSTRACT: The cotton whitefly, Bemisia tabaci (Genn.) (Hom.:Aleyrodidae) is a serious pest of greenhouses, horticulture and field crops, and ornamentals worldwide. B. tabaci has been spreading into new territories and causing extensive damage for almost a century and continues to be a severe pest worldwide. However, resistance to insecticides has rendered chemical control ineffective for the management of B. tabaci. Thus, biological control serves as an alternative and has great potential for use against B. tabaci. Biological control of B. tabaci has been used since more than 40 years, and many attempts have ended with complete success. Biological control of B. tabaci by predators represents a key strategy whose potential has gone largely unrealized in many cropping systems. While a great deal of information is available concerning parasitoids of B. tabaci, much less is known about potential of predators as bio-agents. Concomitantly, this paper reviews predators’ biology, predation, preferences and releases. In addition, combined use of predators and parasitoids, intraguild predation, alternative food resources and omnivory of predators were discussed. In addition, the paper presents the efforts in biological control of B. tabaci using selected predators, and highlights research gaps and directions deserving further development to create a better understanding of these predators on different crops to control B. tabaci. In spite of hundreds of predators attacking B. tabaci, this review is restricted to the most common predators namely; beetles (Serangium parcesetosum, Delphastus catalinae and Nephaspis oculatus), bugs (Orius laevigatus, Macrolophus caliginosus and Nesidiocoris tenuis), lacewings (Chrysoperla carnea and C. pallens), and mites (Amblyseius swirskii and Euseius ovalis). In conclusion, based on information presented herein it appears that predators might be best suited for inclusion in multiple species biological control program for B. tabaci. It is hoped that this paper will help in better understanding of types of future studies necessary for implementing successful biological control programs. KEY WORDS: Bemisia tabaci, whiteflies, predators, biological control, predation, preferences, alternative food resources, combined use (Article chronicle: Received: 08-03-2014 Revised: 20-03-2014 Accepted: 22-03-2014) BACKGROUND The binomial B. tabaci is here used in the broadest sense to include all members of the species complex. Bemisia tabaci The cotton whitefly causes damage to plants in The cotton whitefly, Bemisia tabaci (Genn.) (Homop- three ways; firstly by sucking the plant sap, thus weak- tera: Aleyrodidae) is a highly polyphagous pest of more than ening plant growth shown by leaf chlorosis, reduction 600 plant species in tropics and subtropics (Oliveira et al., in plant vigor, and general plant stunting (Bedford et al., 2001), and temperate regions of the world (Greenberg et al., 1994). Physiological disorders caused by direct nymphal 2000). Bemisia tabaci ranks among the most serious pests at- feeding include irregular ripening and incompletely de- tacking greenhouse crops (Gerling et al., 2001), horticultur- velopment of external color. Secondly, B. tabaci secretes al crops (Ko et al., 2002), field crops and ornamental plants large amount of honeydew which enhances the growth of worldwide (Al-Zyoud and Sengonca, 2004a; Goolsby et al., sooty moulds causing negative effect on plant photosyn- 2005). Bemisia tabaci likely came from India, and it is now- thesis (Abboud and Ahmad, 2006), and this results in less adays considered a noxious species in much of the World. growth, lower yield and poor plant quality (Brown et al., B. tabaci was firstly classified as a pest in Greece around 1995), finally lessening the plant market value or yields 1889 and in the USA in 1897 (Brown et al., 1995). becoming unmarketable (Giustina et al., 1999). Thirdly, Bemisia tabaci outbreaks in cotton firstly occurred in late B. tabaci is considered the most common vector of plant 1920s in India, and then in the Sudan and Iran in the 1950s viruses worldwide. More than 150 plant viruses are known (Horowitz, 1986). In greenhouses, Bemisia tabaci was re- to be transmitted by B. tabaci and the number continues corded to cause serious damage to vegetables in 1974 in to grow up (Jones, 2003). Being a vector of hundreds of Turkey and to poinsettia in 1986 in the USA (Ohto, 1990). plant viruses, a small population of B. tabaci is sufficient 1 AL-ZYOUD to cause considerable damage to plants. These viral plant suppression (Khan and Wan, 2008a, b). Natural enemies diseases have resulted in devastating crop reduction rang- are operating continuously on all life stages of the white- ing from 20% to 100% throughout plant growing regions fly, and keepB. tabaci populations under control (Goolsby in the world with losses estimated at billions of dollars et al., 2005). Although biological control alone has not (Giustina et al., 1999). completely been able to solve B. tabaci problem in crops, The pest has a high reproductive potential and can reach natural enemies still play an important role in IPM pro- up to 400 eggs/female. Eggs are laid on the under part of grams of agricultural crop (Naranjo and Ellsworth, 2009). the leaves in groups. After the egg stage, B. tabaci hatchling Nevertheless, interest in biological control continues to in- develops through four nymphal instars until it reaches adult- crease worldwide (Castane, 2002) due to the development hood (Brown et al., 1995). The insect has 11-15 generations/ of pesticide resistance (Elbert and Nauen, 2000; Kranthi year, and the development occurs between 10°C and 32°C, et al., 2001) and successful use of natural enemies against but 27°C appears to be the optimum (Giustina et al., 1999). B. tabaci (Stansly et al., 2005). Nowadays, research efforts are focusing on controlling B. tabaci through Biological control mechanisms that do not cause side effects to human and its environment (Al-Zyoud, 2012). Public concern for The cotton whitefly has been spreading into new ter- health risks associated with pesticides is evidenced by the ritories, causing severe damage for almost a century and increasing market for organic produce, valued in the USA continues to be a serious pest of vegetables and field crops at $10 billion and in the EU at $13 billion (Dimitri and in much of the World (Gerling et al., 2001). Farmers de- Oberholtzer, 2005). pend heavily on the use of insecticides for B. tabaci con- trol (Manzano et al., 2003; Naveed et al., 2011). However, Importance of predators B. tabaci population quickly reappears after insecticide applications because immatures are distributed on the un- Biological control of B. tabaci through the release of derside of plant leaves (Al-Zyoud and Sengonca, 2004a), natural enemies (parasitoids, predators and pathogens) has and are not in contact with insecticides applied through fo- been used since more than 40 years, and many attempts liar application. In addition, B. tabaci has been declared a have ended with complete success. One biological control difficult pest to control by insecticides because of its high mechanism of controlling B. tabaci is the use of fungal mobility, high reproductive rate, and quick life cycle (Drost pathogens. Some species of fungi have been developed as et al., 1998; Gerling and Steinberg, 2003). High doses bio-agents against B. tabaci (Meekes et al., 1996; Chen and and frequent pesticide application have adversely affected Feng, 1999; James and Jaronski, 2000). But, fungi are slow B. tabaci natural enemies (Lacey et al., 1993) and human acting compared to insecticides, exhibit poor adulticidal ac- life by increasing pollution as well as disturbed the whole tivity, incompatible with many commonly used fungicides, ecosystems (Ashraf et al., 2010). Furthermore, reliance relatively expensive, have limited shelf life, and dependent on chemical applications for managing B. tabaci leads to on favorable environmental conditions (Faria and Wraight, development of resistance by the pest to many common- 2001). In addition, development of fungi as bio-agents of ly used conventional insecticides (Elbert and Nauen, 2000; B. tabaci is still at a fairly early stage, and some strains of Kranthi et al., 2001). The resistance of B. tabaci to insecti- whitefly have developed resistance to their fungal patho- cides has rendered chemical control ineffective (Prabhaker gens, i.e. Verticillium lecanii (Hoddle, 1999). et al., 1985). Thus, concerns about human health and envi- Other natural enemies of B. tabaci are parasitoids, ronment mandate the development of alternatives to chem- which kill their host once their development has been com- ical control of B. tabaci. pleted. Extensive listed fauna of parasitoids were used to There is a growing body of interest in finding control control B. tabaci (DeBarro et al., 2000). The best studied methods for B. tabaci other than insecticides, particularly and used of these parasitoids are various Eretmocerus spe- in regions which are unable to sustain heavy pesticide us- cies (i.e. Er. mundus Mercet) (Stansly et al., 2005; Urbaneja age (Gerling et al., 2001). During the past decades more et al., 2007), and many species of the genera Encarsia (i.e. efforts have been made towards the development of safe En. formosa Gahan) (DeBarro et al., 2000; Hu et al., 2003). alternatives for B. tabaci management. Thus, biological Nevertheless, in spite of B. tabaci being a host of many control has great potential for use against B. tabaci based parasitoids, it seems that control of this pest by parasitoids on the abundance of potential bio-agents (Heinz et al., is not achieved due to the extensive host range and mobility 1999). Biological control is an ecological approach that of the pest (Gerling and Steinberg, 2003).