Persian Gulf Crop Protection Available online on: www.cropprotection.ir ISSN: 2251-9343 (online) Volume 3 Issue 1, March 2014 Pages 92-118

Area-wide Integrated Management of Red Palm Weevil, Rhynchophorus ferrugineus (Olivier 1790) (Coleoptera: Curculionidae) in Date Palm Plantations: A Review

H.A.F. El-Shafie 1*

1- Date Palm Research Center of Excellence, King Faisal University, P. O. Box 400 Al-Ahsa- 31982, Saudi Arabia (*Corresponding author e-mail: [email protected]).

Abstract : The red palm weevil (RPW), Rhynchophorus ferrugineus is an internal tissue borer that inflicts serious damage to date palm and other palm trees. It causes a particular economic threat to date palm growers in the Middle East and North African countries. The cryptic nature of the weevil protects it from harsh external environmental conditions and makes its early detection and control extremely difficult. This article reviews the progress that has been made in area-wide management of RPW during the last decade. Emphasis was given to management tactics such as mass trapping using aggregation pheromone, early detection, and biological control.

Key Words: Date palm, red palm weevil, mass trapping, area-wide management, ferrugineol, action threshold

Persian Gulf Crop Protection, 3(1): 92-118 92

Introduction appeared to be a major pest of date palm in The date palm, Phoenix dactylifera L. the Middle East during the mid-1980s (family Arecaceae, syn. Palmaceae) is a (Abraham et al., 1998). Intensive date diploid, perennial, dioecious, and palm farming practices, the morphology of monocotyledonous plant adapted to arid date palm tree and the microclimatic environments (Chao and Krueger, 2007). conditions prevailing in the date palm Beyond the arid climates, date palm can plantation in the Middle East provided also be grown in many other countries for suitable breeding sites for RPW (Faleiro, food or as an ornamental plant including 2006). The RPW is now managed through the continents of Americas, southern RPW-IPM program using an array of Europe, Asia, Africa, and Australia. The management tactics (Abraham et al., majority of date palm-growing areas are 1998). This article reviews the progress located in developing or underdeveloped thathas been made in area-wide countries where date fruit is considered the management of RPW during the last primary food and cash crop (Sanderson, decade with emphasis on management 2001). The earliest evidence of date palm tactics including mass trapping, early cultivation goes back to 4000 BCE in Ur, detection and biological control. The future lower Mesopotamia (now Iraq), while in prospect of AW-RPW-IPM, in the light of the Nile Valley, date palm cultivation goes advances in biological sciences, is back to 3000 BCE (Erskine et al., 2011). discussed. The area under date palm cultivation Biology and bionomics of RPW: The host almost doubled from 1990 to 2007 (0.63 to range of RPW covers primary three palm 1.23 million hectares). The total world families, viz., Arecaceae, Agavaceae, and productionof dates was 7.51million metric Poaceae. In the Arecaceae, 30 plant species tons (MMT) in 2011, which represented were reported to be hosts for the weevil. analmost 120% increase as compared to Only one host plant species each was the 1990 production of 3.43 MMT reported from the two other families: meaning that world date cultivation and Agave Americana L. (Agavaceae) and production have shown positive growth Saccharum officinarum L. (Poaceae). (FAO, 2012). Diseases and pests are the Thus, RPW is regarded as a pest with high main biotic constraints that hamper date specificity to the family Arecaceae palm cultivation and production, but the (Murphy and Briscoe, 1999; Faleiro, 2006; nature and severity of the problems vary Blumberg, 2008; Dembilio and Jacas, with cultivar, location, weather, and 2012). The adult is reddish brown cultural practices (Carpenter and Elmer, cylindrical weevil with a long curved and 1978; Zaid et al., 2002).In recent time, the pointed snout or rostrum. The male can be red palm weevil (RPW) Rhynchophorus distinguished from the female by the ferrugineus (Olivier 1790) (Coleoptera: presence of a turf of reddish brown hairs Curculionidae) poses a serious threat to along the dorsal aspect of the snout commercial date groves, ornamental (Blumberg, 2008).Adult weevils have dark landscape plantings and native stands of spots on the upper side of the thorax. The palm trees worldwide (Rugman-Jones et head and rostrum comprise about one third al., 2013). It causes a particular economic of total body length. In male, a patch of threat for date palm growers in the Middle short brownish hairs covers the dorsal East and North African countries (Al- apical half of the rostrum. Instead, the Ayedh and Rasool, 2010). The center of female rostrum is bare, more slender, origin of RPW is thought to be Southeast curved and little longer than in male. Adult Asia and Melanesia where it is a key pest females are significantly bigger than males of coconut Cocos nucifera(Nirula, 1956; (Dembilio and Jacas, 2011). Adult red Wattanapongsiri, 1966). The weevil only palm weevils display a high degree of

Persian Gulf Crop Protection, 3(1): 92-118 93

color polymorphism that has challenged elongate, oval cylindrical cocoons made taxonomists and other researchers for over out of fibrous strands. Pre-pupal and pupal two centuries (Rugman-Jones et al., 2013). stages take 3 and 12-20 days respectively Normally the newly emerged adults remain (Faleiro, 2006) and the total life cycle of in the pupal cocoons for few days before the pest may vary from 45 days to 139 they mate and take off to new host. The days (Esteban-Duran et al., 1998, Murphy female starts oviposition 1 to 7 days after and Briscoe, 1999). (Dembilio and Jacas, mating and continues for 25 to 63 days 2011) reported that larger larval instars laying about 276 eggs (Leo Justin et al., feed in the palm core and smaller ones in 2008). The female digs out small holes by the periphery of canary palms. They also its rostrum on tender tissues of young reported that the thermal constant for eggs palms up to 7 years old and lays eggs in to hatch was 40.4 DD (degree days) under the leaf axils. Wounds and cuts in palms laboratory conditions and for complete serve as oviposition sites for females. larval development in Canary palm was Injuries made by rhinoceros beetles or by 666.5 DD and another 282.5 DD to reach diseases predispose palm to infestation by adulthood. They concluded that the weevil the red palm weevil. No elaborate may complete two generations per year courtship behavior was observed in this under the prevailing environmental weevil and mating take place at any time conditions in Spain, and in cooler place, of the day and the weevil becomes active the weevil may complete only one during twilight (Nirula, 1956). The female generation. They observed that a minimum mates several times (polygamous) during of two generation are necessary to kill a its life cycle and the sperms of latest Canary palm. This has an important matings are used for fertilizing the eggs. implication for the management of the Interspecific mating is possible in the pest. (Rahalkar et al., 1972) reported the absence of elaborate mating behavior and occurrence of 3 to 4 generations per year in differences in genetalia (Ramachandran, India in sugarcane. Depending on the 1998). RPW is a holometabolous lower temperature threshold (LTT) and with four distinct stages viz., egg, larva, thermal constant, the number of pupa and adult. The egg is creamy white in generations can be determined. However, color, elongate oval in shape and measures most of the work done so far was on 2.62 mm in length and 1.12 mm in width. artificial diet, palm logs which is far away It hatches in 2-3 days into legless from what is actually running inside a (apodous) larva or grub which bore into the living palm. Penetration sites are usually interior of the palm and feeds on the covered with offshoots and fibers as the succulent tissues. The larva moves through larvae feed they produce frass (chewed up peristaltic muscular contraction of the plant fibers) which combine with plant sap bodyand undergoes several instars before and this fills the tunnels made by the larvae the pupal stage. The full-grown larva or (Blumberg, 2008). (Dembilio and Jacas grub is stout, fleshy, apodous and with a 2011) estimated the mean immature conical body bulged in the middle and mortality to be 66.7% when they tapering towards the ends (Leo Justin, introduced a total of 2304 neonate larvae in 2008). It measures about 50mm in length 144 Canary palms and after dissecting the and 20mm in width on an average and palms they recovered a total of 555 larvae, fully-grown instar can weigh about 7.2 g 135 pupae, and 87 adults. They observed (Elshafie et al., 2013). The larval period the maximum mortality rate (100%) in lasts for 25-105 days (Wattapogansri, December and January and maximum 1966; Avand Faghih, 1996; Abraham et survival rate during April through al., 2002) while pupal development may September. High peaks of weevil activity, take 11- 45 days and the grub pupate in during April-May followed by another

Persian Gulf Crop Protection, 3(1): 92-118 94

peak in October-November, was reported mobility of the weevil has resulted in its from Kingdom of Saudi Arabia widespread within the palm groves (Vidyasager et al., 2000), Egypt (El-Sebay, (Wattanapongsiri, 1966). The relatively 2003), Israel (Soroker et al., 2005) and long life of the larvae or grubs which are Spain (Llacer et al., 2009). (Faleiro et al., the destructive stage, they can live 25-105 2002) evaluated population dispersion days and undergo several larval instars parameters and different dispersion indices before pupation. The longer the larval for weevil capture with pheromone traps in stage, the greater is the damage caused by coconut plantation of Goa in India. His them. The adult weevil can move more data revealed that RPW population than 900 m in a single flight, and as much followed an aggregated or contagious as 7 km in 3-4 days (Abbas et al., 2006). spatial distribution pattern and owing to The RPW spread from its origins to new this aggregation pattern, infestations by areas has been rapid during the past two RPW were reported to occur in clusters in decades. The weevil invaded 50% of date date plantation of Saudi Arabia. This palm and 15% of coconut palm growing spatio-temporal distribution of RPW has an countries respectively (Faleiro, 2006). important implication regarding the During the period form 1985-2010, RPW management of the pest. has been reported in 50 countries Invasive potential and global worldwide, distributed in 5 continents as distribution of RPW: The invasive follows: Oceania (4), Asia (28), Europe potential of RPW is due to combinations of (10), Africa (5) and America (3) (Fiaboe et factors including ability of the weevil to al., 2012). The spread of RPW seems to be complete several generations in a year, on the rise unless very strict quarantine even in the same tree (Rajamanickam et measures are taken regarding the global al., 1995, Avand Faghih, 1996). Adults and movement of live planting materials. larvae have demonstrated antimicrobial Invasive species are an issue of great resistance that may allow this species to concern globally in light of the ever- live in habitat full of microorganism such increasing scale of human movement and as the interior of infested date palm tissue trade globalization (Hulme, 2009). (Mazza et al., 2011). The cryptic nature of Predicating locations suitable for its the weevil protects it from harsh external establishment may enable decision-makers environmental conditions and enables it to and agricultural and environmental live and breed in a wide range of climate protection officers to initiate preventive (Murphy and Briscoe, 1999), and also measures or rapid responses in timely facilitate the spread through transportation manner (Fiaboe et al., 2012). Given the of palms and offshoots (Faleiro, 2006). economic impact and continuing spread of The cryptic life of the pest makes its RPW, there is a considerable need to be control difficult, and eradication of the pest able to anticipate new areas of the pest's has not been achieved in any of the invasion (Fiaboe et al., 2012). The authors invaded areas (Fiaboe et al., 2012). used ecological niche modeling to predict Penetration sites of RPW on date palms are the spread of RPW. The areas where the always covered with offshoots and fibers pest has not been yet reported were found making it difficult to detect infestation at to be suitable for invasion in sub-saharan early stages.The high fecundity of the Africa, Southern, Central, and northern weevil is an important factor in its success America, Asia, Europe and Oceania. (Ju of rapid colonization of new ecological and Ajlan, 2011) used a phenology model niches. A single female can lay 58-760 approach for China to predict the spread of eggs in its lifetime which can extend for 4 RPW. months (Abraham et al., 2002; Faleiro, Nature of damage, economic significance 2006; Prabhu and Patil, 2009).The high and action threshold: Developing larvae

Persian Gulf Crop Protection, 3(1): 92-118 95

of RPW dig deep into the palm trunk to respond to odors released by infested feeding on the soft plant tissues, palms (Mukhtar et al., 2011), but these are compromising its structural integrity and not amenable to rapid processing. The disrupting nutrient transport to the upper RPW spatio-temporal distribution should part of the tree, which lead ultimately to be an important factor in decision making death of the tree, if not properly managed for RPW (Faleiro, 2006). The value of the (Murphy and Briscoe, 1999). The feeding damage caused by RPW is not quantified activity of the grubs results in the and it's not clear whether the control costs destruction of the apical meristem and balance the prevented damage. The impact eventually the death of the tree (Dembilio on individual farmer may be devastating, & Jacas, 2011). Usually palms in the initial however the main importance of RPW stage of attack by RPW respond to remain to be political. The general insecticide treatment and can be saved symptoms of RPW damaged palm are the while palms in the advanced stage of presence of tunnels on the trunk and base infestation, exhibiting extensive tissue of frond petiole, oozing out of sticky thick damage have to be eradicated (Al-Shawaf brown exudates from the tunnels, et al., 2012; Faleiro, 2006, Abraham et al., scattering of chewed plant tissues (frass) 1998). Infestation may adversely affect the with typical fermented odour in and around potential yield, lower the plant growth rate the tunnels, fall empty pupal cases and and eventually causes its collapse and dead adults weevil around heavily infested death (Blumberg, 2008).The efficacy of palm, collapse of the trunk or toppling of any management program is highly crown in case of severe infestation, drying dependent on accurate and time efficient of infested offshoots, and gnawing sound pest sampling. The recommended action due to feeding by the grubs (Abraham et threshold for executing R. ferrugineus al., 1966; Faleiro, 2006). The infested date treatments (mass pheromone trapping and palm may exhibit one or more of the above pesticide applications) is when 1% of date mentioned symptoms depending on the palms are infested (Faleiro et al., 2010). stage of infestation and the degree of Sequential sampling plans based on the tolerance of palm. Green leaves may easily number of infested palms detected per unit come off when pulled as the basal portion area sampled have been developed to guide of such leaves have been eaten by up by decisions pertaining to the initiation of the larvae (Ramachandran, 1998). The total control programs based on a 1% action number of leaves on an infested palm threshold (Faleiro et al., 2010). This decreases due to the early drying of the decision-making approach based on tree bottom whorls and delayed emergence of inspections is considered more accurate fresh ones. Because RPW is not a direct than relying on pheromone trap capture pest on date fruits, few data are found in rates which may either under or the literature describing such damage, and overestimate pest and subsequent the impact of the pest infestation on the infestation severity in the field (Faleiro et final yield. However, in infested al., 2010). However, weevil infestations in plantations, yield has been estimated to plantations are highly aggregated and the have dropped from 10 tons to 0.7 tons per major shortcoming with tree inspections hectare (Gush, 1997). Adult R. ferrugineus for R. ferrugineus management is being female weevils usually prefer to infest able to quickly and accurately identify young palms, and hence, as intensive new palms in the very early stages of infestation date palm plantation monocultures are when curative treatments are most likely to established in the Gulf and Mediterranean be successful. Several detection methods regions, there is the opportunity for R. have been investigated including acoustic ferrugineus to attack them. Recent reports sensors (Mankin, 2011), and dogs trained suggest that the annual loss in Saudi

Persian Gulf Crop Protection, 3(1): 92-118 96

Arabia alone due to eradication of severely Stadelbacher, 1983; Kogan, 1998). The infested palms by R. ferrugineus has been concept of AWPM is some form or another estimated to range from US $1.74 to 8.69 has been practiced since the late 1800s million at 1–5% infestation, respectively (Faust, 2008). (Knipling and Stadelbacher (El-Sabea et al., 2009). The high value of 1983) advanced the idea of area-wide the date palm and the lethal nature of RPW management of pest populations in control imply immediate action against the pest, of early season generations before they which may be initiated either when one build up. The concept of AW pest control, infested palm is observed for developed by USDA under the direction of smallholdings or if 1% infestation has been E. F. Knipling, has been closely identified recorded in large plantations (Faleiro, with the program to eradicate the new 2006). world screwworm, Cochliomyia The concept of area-wide pest hominivorax (Coquerel), which started in management (AWPM): Through its Florida in 1957 and reached Panama in history, the IPM concept preached 2001 (Klassen and Curtis, 2005). During utilization of numerous approaches and this period many academic institutions technologies that would help attaining a developed and promoted IPM paradigm. sustainable solution to pest problems For several decades, IPM and AW pest (Byers and Castle, 2005). Thus, while control were seen as competing paradigms being a practical field, IPM relies heavily with different objectives and approaches on scientific and conceptual advances in (Perkins, 1982) and each competing the biological sciences whether in the against the other with its own core ecology, molecular biology or modeling organizational base i.e. state universities approaches (Gerling and Legg, 2005). (IPM) versus federal research and Making ecologically and economically regulatory agencies (AW) or suppression sound pest management decisions within versus eradication or correctly elimination. an IPM framework often is a complex Over time, the schools have gradually process that involves weighing effects of converged and the differences between many kinds of uncontrolled variables on them have turned out to be less critical possible outcomes (Prokopy and Roitberg, than originally perceived (Kogan, 1998, 2005). Relevant variables include Faust, 2001; Yu and Leung, 2006). AW- biological characteristics of targeted pests, IPM is very broad and flexible concept and level at which pest can be tolerated, degree is increasingly accepted for those situations of protection afforded by candidate of mobile pests when management at a management tactics, cost of management larger scale is advantageous to maximize tactics, current and prospective future AW, not necessarily local, efficiency of biotic and abiotic states of the management tactics (Cronin et al., 1999). environments within which pest The synchronous AW application of management tactics are applied, and an control measures is generally more array of social, cultural, legal and political efficient to preclude pest population elements that may override other variables refugia (Byers and Castle, 2005). (Gerling and Legg, 2005).Insect The term areawide pest management populations can be monitored during the (AWPM) is increasingly used in research season in each field so that when the reports and usually means a cooperative population exceeds a predetermined management program applied to a regional density or damage level, termed the area by using several complementary treatment threshold, action threshold or methodologies of IPM (Kogan, 1995; economic threshold, then insecticides Calkins, 1998; Brewster et al., 1999; Elliot treatments are applied as needed (Byers et al., 2008). From the definition AWPM is and Castle, 2005; Knipling and characterized by a defined large

Persian Gulf Crop Protection, 3(1): 92-118 97

geographical area, management is commitment to an organized effort and its organized by organization rather than by funding requirements, but relies on individual producer, reduction or remedial interventions triggered when pest maintaining of pest population below at an populations reach a certain threshold. acceptable low density. The advantage of Field- by- field pest control is therefore, AWPM is that it can offer a long-term largely a reactive approach to protect solution to agricultural pest problem as human, , crops and forests, rather opposed to quick-fix solution on individual than a preventive pest population on small acreage (Faust, 2008). management approach (Pedgley, 1993). As Implementation of AWPM will require a result of the complexity of many agro- overall participation and compliance of ecosystems, as well as the site-specific growers in the area under the strategy for nature of majority of pest problems, optimum success, as well as frequent predetermined thresholds often become evaluation to measure effectiveness and to operationally intractable and in some pest assure that goals are being met (Faust, situations, the threshold is zero tolerance 2008). Models and expert system, (Ehler and Bottrell, 2000). Operational including prediction types and decision AW-IPM programs are complex, long-term support system for pest-plant/ and proceed from basic research, through environmental integration. Understanding method development, feasibility studies, and exploitation of information on commercialization and regulation to field movement and dispersal of pest and pilot studies, which could eventually beneficial species, timing of population culminate into an operational program suppression measures or technologies to (Faust, 2001). Social, political and coincide with low pest population economic factors must come together with densities. The economics of the strategy science before an AW-IPM program can are vitally important to adoption (Faust, be developed and implemented. Successful 2008). (Knipling 1960, 1972) used simple field operation requires close collaboration population models to show that small between researchers, extension specialists, fractions of an insect pest population left community leaders, agriculture, natural uncontrolled can rapidly nullify the resources and public health communities. benefits of strongly suppressing the main (Byers and Castle, 2005)developed a population in a large area. From this, simulation model where insect populations Knipling deduced the basic principle of varied in exponential growth in fields and total population control "uniform dispersed to adjacent field each day of the suppressive pressure applied against the season. Their first model monitored total population of the pest over a period of population of individual field in a grid of generations will achieve greater fields and treated any field with insecticide suppression than a higher level of control if it exceeded the treatment threshold on most, but not all, of the population each (asynchronous model) as done in generation". Insect pests mobility in traditional IPM. The second model treated addition to beingtransported passively with the entire grid of fields with insecticides wind, animal hosts, and infested when the average population of all fields commodities traded locally or exceeded the threshold (synchronous internationally, severely compromise the model). They found that the synchronous effectiveness of uncoordinated farm-by- model at all growth and dispersal rates farm, orchard-by-orchard, or herd-by-herd tested had average field populations during control efforts and results in the frequent a season that were significantly lower and need for curative or therapeutic back-up required fewer treatments than the measures (Lewis et al., 1997). Field by asynchronous model. The simulation also field control does not demand long-term indicated that cooperation among growers

Persian Gulf Crop Protection, 3(1): 92-118 98

in areawide monitoring of fields to obtain is important to save infested palm, because an average population estimate for use in at this stage, the apical meristem (the palm treatment thresholds would result in heart) is not damaged and the trunk is still significantly less insect damage and fewer stable and hence the tree can be saved. insecticidal treatments. The synchronous Monitoring of RPW is essential model is more efficient because population particularly at ports of entry and at new refugia are precluded from which dispersal sites of infestation (Soroker et al., 2013). could reintroduce (Boivin et al., Early symptoms of infestation by RPW are 1991). (Kogan, 1995), Chandler and Faust very much dependent on the site of (1998) listed the following criteria for infestation, physiological age and status of successful implementation of AWPM: attacked palm as well as palm species and 1) The program should be defined by some cultivars. RPW infest the lower part of the geographic entity that encompasses farms stem in date palm, while crown infestation as well as all non-farm components of the is common in canary palm and the inner landscape crown fronds in coconut palms. Visual 2) The target pest should be amenable to inspection needs a well-trained person or control using the areawide concept over an expert to detect early symptoms. The large geographical area that may extend process is also laborious for experts, time across country consuming, costly and yet inaccurate. To 3) Understanding of pest biology, ecology, overcome the problem of visual inspection, genetic, behavior, physiology, interactions several approaches have been tried using with other organisms chemicals (odors), acoustic (sounds), and An areawide program should be thermal imaging techniques. It was found coordinated by group of key participants as that RPW larval sounds typically are opposed to by just individual producers or produced as bursts (trains of 7-200 other end-users, the program should individual, 3-30 ms impulses spaced < involve federal (as needed), state and local 0.25s apart) interspersed by longer, quite extension, commodity and private growers intervals (Mankin et al., 2008). Based on groups, communities, agribusiness and distinct sounds reported from pest infested other stakeholders in a true partnership palms, acoustic detection of RPW larvae (Faust, 2008). was proposed. It has been used for Suppression technologiescurrently used detection of presence or absence of the in AW-RPW-IPM : The main larvae in suspected coconut palm trees components of current AW-RPW-IPM (Siriwardena et al., 2010; Hetzroni et al., strategy include mass trapping of adult 2004; Soroker et al., 2004). In late weevil using food baited pheromone traps, infestation, when a large number of older regular inspection of palms to detect larvae are inside the palm trunk, larval infestations, periodic preventive and need- sounds can be even detected with the based curative insecticidal treatments and naked trained ear, however, by that time it eradication of severely infested palms may be too late to save the palm. It is (Abraham et al., 1998). In addition, difficult to hear the sounds of small larvae biological and biorational control tactics at an early stage of infestation and also are also used in the management of RPW difficult to distinguish sounds of larvae (Murphy and Briscoe 1999;Faleiro, 2006; form the background. (Pinhas et al., 2008) Llacer et al., 2009). evaluated human labeling of audio clips Surveillance and early detection: To and found that the human detection is manage RPW successfully, one needs to unreliable. (Mankin et al., 2011) used accurate monitor the population, forecast digital laser vibrometer (PDV-100, its dispersal and evaluate the success of Polytec, Waldbronn, Germany) to record control programs. Early detection of RPW sound from infested palms. He reported

Persian Gulf Crop Protection, 3(1): 92-118 99

that the device exhibited a good signal-to- network is already established in noise ratio, comparable or superior to other surveillance of fruit flies (Liu et al., 2009). acoustic methods tested in previous Acoustic detection of RPW was suggested studies. Surveillance of RPW can be done based on distinct sounds produced inside by either individual tree inspection or by the palm by larval activities such as trapping adult weevils using baited feeding or moving (Hetzroni et al. 2004; pheromone traps. The main drawback of Soroker et al., 2004). Acoustic sensors tree inspection is that it can detect with special probes are inserted in the palm infestation only after the weevil has been tree trunk in order to record sounds for a long time enough for the symptom of produced by the insect especially in the infested tree to be visible. Detection of early larval stages of its life, where the RPW infestation at an early stage of attack feeding and other activities of the insect is the utmost and crucial step towards are at their maximum. The acoustic sensors implementation of a successful RPW-IPM had drawbacks as having low capability of program (Faleiro, 2006). Food-baited distinguishing sounds produced by larvae pheromone traps (FBPTs) are commonly from background noise when insects were used to detect the red palm weevil, hidden in stiff, fibrous structures (Mankin however, this traditional method is labor- et al., 2008). Electronic gas sensors have intensive, expensive to implement, been used to detect volatile emitted by particularly over large areas, and unreliable plants infested by insects. Unfortunately, for early detection (Al-Saqer, 2012). these sensors are also highly sensitive to FBPTs require a very high level of the presence of other different compounds servicing, as bait and water need to be such as alcohols, ketones, fatty acids and replaced regularly (El-Shafie, 2011). esters (Magan, 2001). This would FBPTs trap only 20% the weevil negatively interfere with the performance population that is found outside date palm of gas sensors. Therefore, these approaches trees and this is not an indication of early suffered from limitations that hamper their detection, since the captured weevil could success in detecting RPW at its early have come from a population existing for a growth stages. Despite the intensive effort long period over so many generations. Due in development of the RPW detection to the concealed nature of the pest and its techniques, technologies including presence inside the infested tree, visual tree chemical, acoustical, and thermal methods inspection by specialist can only detect the are yet falling back from being practical or weevil after certain symptoms become feasible. Detection is only dependent on visible and by that time it will be too late visual inspection in most of the infested to save the infested tree. Future efforts in areas. Chemical detection is based on the early detection research could focus on the assumption that RPW infested palms use of field-deployable automated produce or emit volatile organic electronic sensors that rapidly identify compounds (VOCs), directly from the unique volatiles chemical signatures weevils, weevils frass, thick brown liquid specific to RPW infested palms (Hoddle et composed of chewed plant tissue with al., 2013). In this respect, (Al-saqer, 2012) fermenting odor oozing out from the developed a reliable identification system wounds of infested tree, and herbivore- to identify RPW. The neural networks induced cues. However, none of specific were developed by using between three to cues emitted by RPW infested palm have nine image descriptors as input and a large yet been identified (Soroker et al., 2013). database of insects' images was used for (Nakash et al., 2000) confirmed the ability training. The system is capable of 100% of sniffer dog of the breed Golden recognition of RPW and 93% recognition Retrievers to successfully detect the oozing of other insects. The use of wireless sensor secretion collected from RPW infested date

Persian Gulf Crop Protection, 3(1): 92-118 100

palm. Chemical detection can be improved while filtering out the environmental noise; and taken further towards automatic target and an output device that allows the user to detection on large scale by applying determine whether the palm is infested. olfactory sensors (electronic nose or Detection of visible symptoms, which tongue). Automatic olfactory detection is normally appear in the tree only after implemented in industry for quality severe infestations, is considered too late to control, environmental monitoring, health prevent the spread of the infestation or to and security (Sindhuja et al., 2012). rescue the tree. (Bokhari and Abuzuhairah, 1992) indicated Mass trapping: Ferrugineol (4-methyl-5- the possibility of detection of physiological nonanol), anaggregations pheromone changes in the infested palms. Several produced and released by male weevils observations reported temperature attract other male and female weevils to a elevations at the trunks of infested palms palm was first identified and synthesized in as detected by infrared cameras. Pest early 1990s (Hallett et al., 1993). This feeding within the palm trunk causes pheromone (attractant) is commercially intensive fermentation of plant tissues available and has been used for detection, which increases the total temperature monitoring population changes and mass inside the crown/trunk above ambient level trapping of RPW. Mass trapping using (30º C and above 45º C) (Abe et al., 2010; odor-baited traps is one of the older Suma and Longo, 2009). The tunneling approaches to direct control of insect for insects destroy the vascular system of palm population suppression and eradication and create local conditions of water stress. (Steiner, 1952). One of the major This "crop water status" could be sensed advantages of pheromone-baited traps is through inspection of the thermal portion that they release pheromone continuously, of the spectrum of reflected irradiation whereas female insects do so only during (Ehrler, 1973). Recently, (Cohen et al., restricted periods as synchronized by 2012) has shown that aerial thermal images circadian rhythms (El-Sayed and Trimble, are promising tool to map water status of 2002 b). Appropriate trap density and date palm trees on a commercial scale. placement are also vitally important for They developed a semi-automated effective mass trapping and success has procedure based on the watershed been achieved only where the ratio of traps segmentation analysis which allows (in female equivalents) to wild females is detection of all palm trees in the thermal sufficiently high. Trap density that have images with no false alarms and the achieved successful mass trapping of low extraction of canopy temperature of density pests generally fall in the range of individual palm trees. Likewise, detection 10-40 traps per hectare. However, high of canopy temperature based on aerial densities have sometimes been required thermal images using semi-automated (Sternlicht et al., 1990). Trapping of RPW procedures can be used to map potential dated back to the beginning of the nineteen infestation in palm trees in homogenous century when (Henry ,1917) suggested that plantation on a wide area scale (Soroker et fermenting kitul palm Caryota urens al., 2013). Recent advances using software (Arecaceae) wood might be effective in to select frequencies specific to red palm trapping adult weevil. weevil have shown promising results in the Mass trapping is a widely used laboratory (Pinhas et al., 2008) and field semiochemicals-based pest management (Siriwardena et al., 2010). The acoustic approach. (El- Sayed et al., 2006) device consists of a sensor to acquire the identified key factors that can contribute to sound signals from an infested palm; a success of failure of mass trapping. They signal processing unit to capture and stated that competitiveness of synthetic amplify the sound acquired by the sensor lures with wild females is a crucial factor

Persian Gulf Crop Protection, 3(1): 92-118 101

in the success of mass trapping and it is conceived in semiochemicals-based pest essential to optimize both blend and dose. management, the numbers of studies Isolation and low population density of the dealing with mass trapping are declining target pest are other factors for success of (El-Sayed, 2006). The conventional food mass trapping. Understanding biology of baited pheromone traps (FBPTs) have to the target pest can be very important, be periodically serviced (change food bait because mass trapping is likely to be more and insecticide solution) which is labor efficient against univoltine, monophagous intensive. Therefore, a bait-free method to and monogamous species compared with ‘attract and kill’ RPW adults, has recently multivoltine, polyphagous, and been developed for weevil control in date polygamous species. The most important palm (ElShafie et al., 2011).Bait-free factors affecting the efficiency of mass attract and kill technologies uses an inert trapping are the need for low population synthetic matrix from which ferrugineol density of the target pest, followed by trap (15%), the aggregation pheromone is design and related issues such as released, and within which a contact pheromone blend dosage or release rate, insecticide (5%) is contained. In field and trap density (Nakasujiand Fujita, trials, bait-free attract and kill technology 1980). (Fisher et al., 1985) introduced the has been shown to be as effective as concept of a critical minimum pheromone traditional pheromone bucket traps for release rate required for eradication of a attracting R. ferrugineus. Importantly, the given species, below which only inert matrix containing aggregation population reduction but not eradication pheromone and insecticide can be applied could be achieved and above which mating directly to the trunks of palms > 20 yr or disruption might occur. Mass trapping and non-host trees at heights where they pose lure &kill use similar approaches, and no risk to domestic animals and people. mass trapping can be considered as subset Weevils are attracted the matrix because of of the concept of lure and kill (Al-Sayed et the pheromone and are killed when they al., 2006). The method of killing differs in come in contact with the insecticide each approach and this result in an impregnated matrix. Bait-free attract and operational differences, Lure & kill, it is kill strategies may significantly reduce also called attract and kill that use gel costs and could allow per ha deployment droplet or dollops require the insect to rates much greater than what is feasible approach and contact a point source with baited bucket pheromone traps for R. (Brockerhoff and Suckling, 1999), whereas ferrugineus management (El-Shafie et al., traps with a larger killing surface do not 2011). usually need to elicit the same extent of Eradication of severely infested palms: close-range behavior (El-Sayed et al., (Abraham et al., 2000) reported that for 2006). Mating disruption on the other any successful AW-RPW-IPM program, hand, relies on the principle of preventing eradication of severely infested palms pheromone communication between sexes should be less than 20%. The process of by saturating the area with a high removal of an infested palm where in concentration of pheromone (Gaston et al., plantation or landscape, is very expensive 1967). The most common method of operation and should be done carefully to measuring control efficiency of mass avoid dissemination of the pest, since it trapping is to monitor trap catches to can harbor many of adult weevils. In Al- determine whether they decline overtime, Ahsa where over 12000 ha (~ 3 million thereby providing an indirect measure of palms) are under AW-RPW-IPM operated insect removal(Faccioli et al., 1993; by the directorate of agriculture (Al- Mottus et al., 1996). Although mass Shawaf et al., 2012), the removal of trapping was the first approach to be infested trees is assigned to a contractor

Persian Gulf Crop Protection, 3(1): 92-118 102

whose responsibility is to collect infested of drip irrigation instead of flooding, palms after being marked (with red and reduce irrigation rate at time of RPW peak white tape) by the inspector teams. Infested abundance (March-April), concentrate palms are then pulverized in an isolated inspection to detect infestation in locations place with baited-pheromone traps set with high humidity and set traps at location around to trap any weevil that escapes. The with high moisture content. Females (over biomass of pulverized palm tissues is 80%) are sexually mature and ready to recycled and used in production of oviposit (Faleiro, 2006; Lo Bue et al., compost and as alternative plant growth 2010). These observation coupled with medium instead of peat moss. In the past preferential trapping of females over males farmers used to burn the infested palms, a (Faleiro et al., 2000) will reduce the weevil practice which was inefficient. Severely population. However, if weevil populations infested palms that have to be eradicated in garden and public parks are not properly often harbor adult weevils; therefore managed, they will represent hot spots contribute to within grove infestation. which will constitute a source for the Burning of severely infested palms is not weevil to invade managed areas. It is worth recommended as destruction mean because to mention that in area wide pest palms do not burn easily and complete management, landscape plantations are destruction of RPW could not be also considered for management. While guaranteed in this case. cutting the leaves, care should be taken to Other agro-technical measures: avoid wounds and injuries to palm which Availability of suitable breeding sites is an serve as oviposition sites for females, such important limiting factor of RPW wound should be treated with proper population (Kalshoven, 1981). These sites insecticides and covered with mud or will be far numerous in a managed cement. The leaves may be cut leaving a plantation than natural habitat (Murphy petiole length of 20 cm away from the base and Briscoe, 1999). This can explain that of the leaves to prevent the larvae from within southern India, a country that falls entry through the cut ends. It is to be within part of the weevil native range it is ensured that even if the cut petiole considered a rare and local pest (Nirula, attracted the weevils for oviposition, the 1956). The presence of natural enemies in emerged grubs would not reach the main south east Asia are likely to be a limiting stem, as the petioles will dry up and fall factor in checking distribution and within a one month period (Leo Justin et incidence of red palm weevil (Murphy and al., 2008). Management of R. ferrugineus Briscoe, 1999). Over 99% of the reported may be enhanced from research addressing natural enemies of RPW so far are from the effects of irrigation methods, spacing South East Asia, mainly India, Indonesia designs that reduce humidity levels and and Singapore which represent the center increases sun penetration between palms in of origin of this pest. The apparent general plantations, and mixed cultivar plantings absence of natural enemies in date on pest infestation rates, and perhaps, the plantations in the countries of the Middle development of transgenic dates that East would explain why red palm weevil express insecticidal genes lethal to red has had a particularly devastating impact in palm weevil larvae and adults (Hoddle et this region (Murphy and Briscoe 1999). al., 2013). The role of irrigation method on the Host plant resistance: Tolerance, infestation level by RPW was studied by antibiosis and antixenosis are the several authors who concluded that flood conceptually recognized three modes of irrigation increases infestation in date palm plant resistance to (Horber, (Aldryhim and Khalil, 2003; Aldryhim and 1982; Smith, 2005). Tolerance is a plant's Al-Bukiri, 2003; Sallam, et al., 2012). Use ability to withstand or recover from

Persian Gulf Crop Protection, 3(1): 92-118 103

damage. Antibiosis adversely which was statistically similar to the affects arthropod development, cultivars Reziz, Sheshi and Hatmi. The reproduction, or survival, and antixenosis cultivars Khasab, Shahal and Gaar (non-preference) prevent arthropod exhibited high degree of non-preference colonization of a host plant. A plant may (antixenosis). exhibit two or more modes of resistance Chemical control: Chemical control and in some cases it may be difficult to against RPW is mainly based on repeated differentiate between antixenosis and application of large quantities of synthetic antibiosis as they may both affect insecticides, which are applied in a range arthropod populations (Smith, 2005). of preventive and curative procedures Ideally, antibiosis and antixenosis may be designed to limit and contain the spread of mutually reinforcing modalities of infestation. Because of the cryptic nature resistance i.e. antixenosis may deter of the boring stages of the pest, chemical antibiosis-resistance-breaking biotypes insecticides have to be applied frequently from colonizing a plant, and antibiosis may and over a long period of time for effective reduce the fitness of those individuals that management of established populations colonized (Hesler and Dashiell, 2011). (Murphy and Briscoe, 1999; Ferry and Resistance of some date palm cultivars is Gomez, 2002). However, there are deep not yet exploited as an IPM component in concerns about environmental pollution the management of red palm weevil. caused by these treatments, especially in Washingtonia filifera and Chamaerops public areas where palms are grown as humilis showed antibiotic and antixenotic ornamental (Faleiro, 2006). The main mechanisms respectively against RPW, purposes of IRM are: rational use of while Phoenix canariensis was highly pesticides, reducing the number of preferred (Dembilio et al., 2009). The treatments, combating resistance to coconut cultivar chowghat Dwarf Green is available and effective insecticides, most preferred for egg laying by the RPW prolonging the life span of new while malyan dwarf was least preferred insecticides by optimizing their use, and (Faleiro and Rangnekar, 2001). Calcium preserving natural enemies (Horowitz et inhibited RPW growth while, date palm al., 1995). The injection of systemic varieties with high sugar levels enhanced insecticides directly into affected trunks oviposition and growth while reducing and drenching of the crown of infested mortality of RPW (Farazmand, 2002). The trees with insecticides (Kurian and longest male lifespan was recorded on Mathen, 1971; Abuzuhairah et al., 1996; El cultivar Khalas followed by Sillaj, Sukary Ezaby, 1997) which, in the sandy soil and Khasab. Though more cocoons were conditions of the Gulf, must be performed harvested from Khalas, frequency of adult carefully to prevent pollution of water emergence was better on Sukary (Al- courses in areas with palm weevil Ayedh, 2008; Al-Ayedh and Rasool, infestation. High reliance on a limited 2010). (Faleiro and Elshafie 2013) number of insecticide classes in AW- assessed the degree of preference by RPW RPW-IPM may make the development of in seven major date palm cultivars of Al- pesticide resistance highly likely, which Ahsa viz. Khalas, Sheshi, Reziz, Khasab, could jeopardize the efficacy and future Hatmi, Shahal and Gaar by determining the use of attract and kill baits (Hoddle et al., attraction of RPW to fresh palm volatiles 2013). Total population management is emitted from date palm frond tissue also required to reduce the probability of through four-arm choice olfactometer the development of insecticide resistance, assays. Their results revealed that the or the emergence of strains of a pest weevil was most attracted to the palm capable of overcoming host resistance. tissue volatiles of the cultivar Khalas Area wide management strategies, guided

Persian Gulf Crop Protection, 3(1): 92-118 104

by the effective use of geographic backpack sprayer to the trunk and base of information systems (GIS) technology, can the frond on each palm until run-off. be applied to achieve effective resistance Efficacies were about 80 percent for management (Carriĕre et al., 2001; Sexson curative treatment and up to 98 percent for and Wyman, 2005).However, there is a the preventive treatment. Because this potential danger in AW population formulation of S. carpocapsae survived in suppression, since continuous and the palm for a minimum of 2 weeks, thorough suppression applied on an Aw applications could be repeated every 2 to 3 basis will select genes in the pest's gene weeks during critical periods for pool that enable the pest to overcome the continuous control of RPW (Llácer et al., survival threatening control agent. 2009). (Dembilio et al., 2009) also found Repeated AW application of an insecticide that S. carpocapsae to be highly effective will select for resistance to that insecticide against red palm weevil in the field. The and likewise repeated use of bait or efficacy of S. carpocapsae/Chitosan WG continuous planting of the same resistant (SteomerBiorend R®) was equivalent to crop will select genes for avoidance that of the systemic insecticide behavior and overcoming the crop's host imidacloprid and they were compatible. resistance (Hendrichs et al., 2007). The idea of the sterile insect technique Pesticide resistance in arthropod pests, (SIT) may well have been triggered in part insects and mites, is a seriously increasing by the observation of monogamy in female phenomenon in crop protection. Based on screwworms. However, (Bushland, 1960) the Arthropod Pesticide Resistance asserted that, in instances in which Database (APRD), more than 550 species irradiation induces dominant lethal of arthropods have developed resistance to mutations in sperm which can still pesticides (Whalon et al. 2008). Pesticide penetrate eggs, female monogamy is not a resistance causes the disuse of effective requirement of the SIT and this was pesticides and diminishes the pesticide accepted by (Knipling, 1979). The sterile diversity that is one of the basic principles insect technique (SIT) is an approach of in pest resistance management. pest control that uses area-wide release of Bio-pesticides and biologically based sterile insects to reduce fertility of a field (bio-rational) control: Agents such as population of the same species (Hendrichs viruses, bacteria, fungi and and Robinson, 2009; Lance and Mclnnis, entomopathogenic nematodes (EPN) can 2005). The technique has been tested all be mass-produced, formulated and against red palm weevil and various applied to target pests in a similar manner methods of sterilizing males were adopted. and with the same equipment that is used Chemosterilization (Rahalkar et al., 1975), for chemical pesticides, hence the gamma irradiation (Ramachandran, 1991), collective term bio-pesticides (Murphy and and X-ray radiation (Rahalkar et al., 1973) Briscoe, 1999). Even when effective under proved successful in the laboratory to laboratory conditions, many biological reduce egg hatching when sterilized males control agents do not provide adequate were allowed to mate with untreated control of red palm weevil in the field females. Field studies were also carried out (Abbas et al., 2001; Salama et al., 2004; with promising results (Ranavara et al., Faleiro, 2006; Gindin et al., 2006, Murphy 1975; Rahalkar et al., 1977). In recent and Briscoe, 1999). The nematode years, gamma-irradiation of RPW males Steinernema carpocapsae, in the has been used in different studies on the commercial formulation Biorend R® basic biology of the pest (Gothi et al., provided excellent control of all stages of 2007; Al-Ayedh & Rasool, 2009; Prabhu et RPW in Spain (Llácer et al., 2009). The al., 2010). These studies proved that product was applied with a manual gamma-irradiation of male weevils induces

Persian Gulf Crop Protection, 3(1): 92-118 105

permanent sterility without drastic effect and desiccation (Mrácek, 2003). In on mating behavior such as mate addition to EPNs, entomopathogenic fungi recognition time, mating duration and (EPFs) can also provide an excellent mating frequency, one of the requirements alternative to chemical control. EPFs infect for successful application of the technique the host by direct contact and by horizontal (Lance and Mclnnis, 2005). Llácer et al., transmission from infected insects or (2013) concluded that irradiation of one cadavers to health insects (Quesada- day old males with gamma irradiation (15 Moranga et al., 2004). The unique and 25 Gy) did not affect male sexual characteristics of both EPNs and EPFs are competitiveness but sperm quality. They especially important for the biological suggested the use of gamma-irradiated control of concealed pests such as RPW. males to spread a pathogenic strain of the (El-Sufly et al., 2009) successfully reduced entomopathogenic fungus Beauveria the incidence of RPW under field bassiana (Ascomycota: Clavicipitaceae) as conditions in Egypt using an indigenous a new method to improve the biological isolate of Beauveria bassiana. The same control of R. ferrugineus. The use of results were reported in Spain under semi- entomopathogenic nematodes (EPNs) field conditions with efficacies of about could offer an alternative to chemical 85%. Fungus-challenged males were able control of RPW (Abbas et al., 2001; to transmit the disease to healthy females Elawad et al., 2007; Saleh and Alheji, in the laboratory and the infection resulted 2003). EPNs are safe for non-target in a subsequent reduction in fecundity and vertebrates and to the environment and can egg hatching (Dembilio et al., 2010b). be mass produced in liquid media with low Validating AW-RPW-IPM program: cost of production (Ehlers, 2003). These Validation of the benefits of control nematodes (Steinernematids) are soil- programs in practices is difficult because inhabiting EPNs, and have free living, of the biological complexity (Menke and parasitic and saprophytic stages (Mracek, Greene, 1976; Welch et al., 1981; Boivin 2003). The infective third juvenile stages et al., 1991). The advantages of area-wide (dauer Juvenils, DJ) survive outside the program are difficult to establish with insect and can either actively search for scientific rigor because treatment and host (cruisers) or wait for host to pass by control areas are confounded by (ambushers). DJs enter the insect host differences in temporal and spatial through any opening (mouth, anus, dimensions. For example, differences in spiracle) and grow into the parasitic stage. time or space as well as the large scale The death of the insect due to nematode required make it difficult to compare a parasitism is caused by Gram-negative method using traditional IPM thresholds bacteria which are carried within the gut of and treatments of individual field in a the DJs (Frost and Clarke, 2002). The mosaic to a method using the same species of EPNs Steinernema carpocapsae threshold applied simultaneously over the (Weiser) (Nematoda: Steinernematidae, entire mosaic of fields (Byers and Castle, which is mutuallistically, associated with 2005). Area-wide management programs the bacterium Xenorhabdus nematophila are whole ecosystem experiments which (Enterobacteraceae) is the most studies, are subjected to experimental perturbation available and versatile of all EPNs. This (i.e. the management program), they are species is atypical ambusher and effective often not replicable (because of cost, against highly mobile surface-adapted public policy, or the uniqueness of the insects (Gaugler, 2007). It is adaptable to system under study) and they lack controls cryptic habitat which enhances its (Carpenter et al., 1995). Ideally, systems infectivity due to minimization of are monitored for sufficiently long enough nematode death from ultraviolet radiation prior to the perturbation and pre and post-

Persian Gulf Crop Protection, 3(1): 92-118 106

perturbation data are compared to assess an area of 4000 ha (1.08 million palms) the effect of treatment (Carpenter et al., which constitutes about 35% of the total 1995). Program evaluation is needed to area of the oasis for six months (April- assess the effectiveness and to ensure September). The criteria of their evaluation suppression goals are being met (Faust, were mean monthly value for weevil 2008). Assessment metrics include capture in FBPTs, infestation levels, and measurement of pest densities before and eradication of severely infested palms. after program initiation (Lloyd et al., 2010; Their results indicated that infestation in Mau et al., 2007; Vargas et al., 2008) and the operational areas were found to be reduction in crop losses and pesticide well below 1% action threshold in the East application frequencies within treated of the oasis, nearing 1% in the center while zones (Knight, 2008; Vargas et al., 2008). being well above 1% threshold in the It is important to measure the efficiency of north. Accordingly, adjustment of the IPM mass trapping and interpret the evidence of strategy is need in the center and major changes in population data (El-Sayed et improvement is required in the north to al., 2006). Mark-release-recapture of males bring infestation level below the 1% (Reddy and Urs, 1996) can be used to threshold. (Hoddle et al., 2013) collected measure the effectiveness of trapping. data spanning a six yr period (2007 to Modeling has provided insight into 2012) from Al Ghowaybah, a 1,104 ha date understanding the critical issues affecting producing region in the Al- Ahsa efficiency of mass trapping which can be Directorate in Saudi Arabia, and analyzed compared with the practical experience of it to assess the impact enhanced field practitioners (El-Sayed et al., management efforts that commenced in 2006).Modeling indicates that the Oct. 2009 had against this pest. Mean efficiency of mass trapping increases as weekly trap captures ofR. ferrugineus and target population density decreases (i.e., the percentage of traps capturing weevils, inverse density dependence) (Knipling, as measured by “weevil” and “trap” days 1972; Li, 1991). Simulation of mass declined significantly from 2009 to 2012 trapping in confined areas indicates that by 65% and 90%, respectively, indicating the time required to catch all the insects in that trapping and dispersal pressure was an area increases logarithmically with reduced. Additionally, over the same time increases in initial target density (Byers, period, insecticide application and palm 1993b). (Al-Shawaf et al., 2012) validated eradication rates dropped by 91% and area wide management of RPW in date 89%, respectively. The total number of R. plantation of Al-Ahsa, Saudi Arabia. ferrugineus captured in 2012 declined by Case studies: RPW-IPM program in Al- 86% when compared to total captures for Ahsa oasis, kingdom of Saudi Arabia cover 2010. It is concluded that the enhanced over 12000ha with three million palms management program against R. (Al-Shawaf et al., 2012). The program is ferrugineus in Al Ghowaybah had a operated by the Directorate of Agriculture significant and rapid impact against this of the Ministry of Agriculture. The IPM pest. In 1999 Israel detected a single RPW package of the program includes mass infested date palm in the Jordan valley. For trapping of adult weevils using 8000 food- two years following detection, spraying baited pheromone traps (FBPTs), regular and soil application of insecticides as well inspection of palms to detect infestations, as trapping of adult weevils using FBPTs periodic preventive and need-based were operated in 450ha date plantations. curative insecticidal treatments, as well as Traps were used at a density of 10 traps/ha eradication of severely infested palms in order to monitor the weevil infestation (Abraham et al., 1998). (Al-Shawaf et al., and to reduce population by mass trapping. 2012) evaluated the operational program in In 2002 a significant decrease in

Persian Gulf Crop Protection, 3(1): 92-118 107

population was observed which was Considering the large areas under continued in 2003. The sex ratio of trapped cultivation with date palm which is a crop weevils was skewed towards females and with high economic value and the threat the Israeli authorities suggested that mass caused by RPW to this crop, the future trapping of adult RPW weevil and the fact prospect for the management of RPW on that more females were trapped had a large scale is good. The potential exist of significant role in the suppression of the an effective package of control tactics that weevil. During the period 1999-2002 are applicable on an area-wide basis numbers of infested palms were 60 of including pheromone-based mass-trapping which only 4 were severely infested and and selective biorational insecticides. needed to be eradicated. No infestations Geographic information system (GIS) have been detected in palms after 2002 based techniques can be used to check the although regular inspections continue and efficiency of pheromone traps in area of weevils continue to be captured (Soroker et high and low RPW activity. In this respect, al., 2005). a statistical model has been proposed based Challenges and future prospects of AW- on weevil capture information and support RPW-IPM: Challenges expected to face use of GIS in weevil management the implementation of AW-IPM strategies (Massoud et al., 2011). Pest operational program in general can be population can be controlled by push and either technical or managerial. The pull or stimulo-deterrent diversionary technical include defining the geographic strategy which keep them away from area, obtaining the extensive biological and plants by a combination of repellents that ecological baseline data needed to push them away and attractive pheromone- understand the pest population dynamics, based traps which pull them in (Cook et ecological relationship and distribution in al., 2007; Hassanali et al., 2008). Nontoxic space and time, determining gene flow solutions based on manipulation of insect between reproducing pest individuals in behavior by semiochemicals as chemical the target population and neighboring cues often play a key role in insect population and developing and integrating orientation to a host (Witzgall et al., 2010). appropriate and compatible control tactics Some research is going on to find (Thomas, 1999). In this respect, inhibitory semiochemicals or repellents for (Blumberg, 2008) and (Soroker, 2004) RPW population in date palm plantations emphasized that the cryptic nature of RPW as well as landscape and urban has made it difficult to understand its environment and combination of repellent biology and ecology. Managerial and attractant semiochemistry may be used challenges include obtaining the in push-pull tactics to manage red palm commitment of all private and public weevil (Guarino et al., 2013).The stakeholders to support and participate in application of biotechnology for crop the program, carrying out of appropriate protection commenced on a large scale in feasibility studies, developing professional 1996, and had increased 67-fold by 2007, business plan for the program, establishing making it the fastest adopted crop an effective and dedicated organization technology in recent history (James, 2008). with full time staff to coordinate and The more recent types of biotechnology implement the program, implementing a applied to crop protection include the use training program and establishing a system of transgenic insects with conditional lethal of program evaluation (Lindquist, 2001). genes for area-wide insect suppression The main challenge remain to be addressed (Alphey, 2007), symbiotic control of crop in AW-RPW-IPM is to develop an diseases and pests (Miller, 2004)and effective, non-destructive devices for early conversion of symbionts into population detection of RPW on large scale. suppression agents (Zabalou et al.,

Persian Gulf Crop Protection, 3(1): 92-118 108

2004).A high level international The concealed nature of RPW infestation conference on research and management has made it difficult to manage the pest strategies for red palm weevil was held on effectivelyin date plantation. Due to this 16-18 march 2013 in King Abdullah fact, early detection of the weevil University of Science and Technology infestation is the key element in the (KAUST), Thuwal, Saudi Arabia. In this management process. In spite of the great conference, novel approaches to manage efforts that have been exerted so far to RPW were discussed. These include the make a breakthrough in this area, still bacterium, Wolbachia pipientis practical effective methods of detection of (‘Wolbachia’) which is widespread and RPW on large scale are not available. For abundant secondary cytoplasmic- the moment, AW-RPW-IPM is largely symbionts of arthropods and nematodes. dependent on food baited pheromone traps Wolbachia spp. are involved largely in with a varying field density ranging from manipulation of their host’s reproductive 1trap/ha up to 10traps/ha depending on the properties including the induction of infestation levels and logistics available. parthenogenesis, feminization, male killing and cytoplasmic incompatibility (CI) References (Stouthamer et al., 1999). Another 1] Abe F, Ohkusu M, Kubo T, Kawamoto approach is the Release of insect with S, Sone K & Hata K. 2010. Isolation of dominant lethal (RIDL). This is a potential yeasts from palm tissues damaged by the pest suppression approach that involves red palm weevil and their possible effect modification of insects by engineering on the weevil overwintering. Mycoscience, 51: 215-223. conditional lethal genes. RIDL males are 2] Abbas, M. S. T.; Saleh, M. M. E.; and released to mate with wild female pest Akil, A. M. 2001. Laboratory and field insects; their progeny inherit the RIDL evaluation of the pathogenicity of gene and do not survive to adulthood. This entomopathogenic nematodes to the red method is intended to replace irradiation as palm weevil Rhynchophorus ferrugineus it is currently used for SIT (sterile insect (Olivier) (Coleoptera: Curculionidae). technique). The lethal gene accumulates in Journal of Pest Science, 74: 167-168. a population and, over several generations, 3] Abbas, M.S.T., Hanounik, S.B., causes a decrease in population size Shahdad, A.S. & Al- Bagham, S.A. (Alphey, 2007). Intensive research is being (2006) Aggregation pheromone traps, a carried out worldwide on recent RPW major component of IPM strategy for the red palm weevil, Rhynchophorus control strategies, which rely on the gene ferrugineus in date palms (Coleoptera: regulatory and enhancing defense Curculionidae). Journal of Pest Science mechanisms in plants through gene 79, 69–73. silencing and/or RNA interference (RNAi). 4] Al-Shawaf, A. M. A., Al-Abdan, S., Al- (Wang et al., 2013) published the sequence Abbad, A. H., Abdallah, A. B. & of the first large-scale full-length Faleiro, J. R. (2012). Validating Area- complementary DNA (cDNA) from the wide management of Rhynchophorus RPW to open an avenue for the future ferrugineus (Coleoptera: Curculionidae) genome annotation. This high-tech in Date Plantations of Al-Hassa, Saudi research particularly on genomic or large- Arabia. Indian Journal of Plant scale transcriptomic data of the RPW are protection, 40 (4): 255-259. 5] Abraham V. A., Mahmood Al-Shuaibi, of paramount importance to find novel Faleiro J. R., Abozuhairah R. A. and management strategies for this notorious Vidyasagar P. S. P. V. (1998) An pest. integrated approach for the management of red palm weevil Rhynchophorus Conclusion ferrugineus Oliv.—A key pest of date palm in the Middle East. Sultan Qaboos

Persian Gulf Crop Protection, 3(1): 92-118 109

University Journal for Scientific (Agricultural and marine Sciences) 8, Research, Agricultural Science 3, 77–83. 87-90. 6] Abraham V. A., Faleiro J. R., Nair C. P. 14] Avand Faghih A. (1996). The biology of R. and Nair S. S. (2002). Present red palm weevil, Rhynchophorus management technologies for red palm ferrugineus Oliv. (Coleoptera: weevil Rhynchophorus ferrugineus Curculionidae) in Saravan region (Sistan Olivier (Coleoptera: Curculionidae) in and Balouchistan Province, Iran). palms and future thrusts. Pest Applied Entomology and Management in Horticultural Phytopathology 63, 16–18. Ecosystems 8, 69–82. 15] Al-Saqer, S. M. 2012. A reliable 7] Abraham, V. A., Mathen, K. and Kurian, identification system for red palm C. (1966). Aids to detect red palm weevil. American Journal of applied weevil infestation in coconut palm. science 9 (8): 1150-1157. Coconut Bulletin 20, 148-152. 16] Alphey L. S. 2007. Engineering insects 8] Abozuhairah RA, Vidyasagar PSPV & for the sterile insect technique. In: Abraham VA. (1996). Integrated Vreysen MJB, Robinson AS, Hendrichs management of red palm weevil, J (Eds.) Area-Wide Control of Insect Rhynchophorus ferrugineus F., in date Pests. Springer-Verlag, Berlin, pp. 51– palm plantations of the Kingdom of 60. Saudi Arabia. 20th International 17] Byers, J. A. and Castle, S. J. 2005. Congress of Entomology, Florence, Areawide Models Comparing Italy, August 1996, Paper 17-033. Synchronous Versus Asynchronous 9] Al-Ayedh, H.Y. & Rasool, K.G. (2010). Treatments for Control of Dispersing Determination of the optimum Insect Pests. J. Econ. Entomol. 98(6): sterilizing radiation dose for control of 1763-1773. the red date palm weevil Rhynchophorus 18] Byers, J. A. 1993b. Simulation and ferrugineus Oliv. (Coleoptera: equation models of insect population Curculionidae). Crop Protection 29, control by pheromone-baited traps. J. 1377–1380. Chem.Ecol. 19: 1939-1956. 10] Al-Ayedh HY & Rasool KG. (2009) Sex 19] Brewster, C. C., J. C. Allen, and D. D. ratio and the role of mild relative Kopp. 1999. IPM from space: using humidity in mating behaviour of red satellite imagery to construct regional date palm weevil Rhynchophorus crop maps for studying crop-insect ferrugineus Oliv. (Coleoptera: interaction. Am. Entomol. 45: 105-117. Curculionidae) gamma-irradiated adults. 20] Bottrell, D. G. 1979. Integrated pest Journal of Applied Entomology 134, management. Council on 157-162. EnvironmentalQuality,US Government 11] Al-Ayedh, H. 2008. Evaluation of date Printing Office, Washington, DC., USA. palm cultivars for rearing the red palm 21] Bushland, R. C. 1960. Male sterilization weevil, Rhynchophorus ferrugineus for the control of insect, pp. 1-25. In: (Coleoptera: Curculionidae). Florida Metcalf, R. L. (ed.), Advances in pest Entomol. 91(3): 353-358. control research, volume III. 12] Aldryhim, Y. and Al-Bukiri, S. 2003. Interscience Publishers, New York, NY, Effect of irrigation on within-groove USA. distribution of red palm weevil, 22] Blumberg, D. (2008). Review: Date Rhynchophorus ferrugineus. Sultan Palm Arthropod Pests and Their Qaboos University Journal for Scientific Management in Israel. Phytoparasitica Research (Agricultural and marine 36(5): 411-448. Sciences) 8, 47-49. 23] Bokhari U. G., Abuzuhairah R. A., 1992 13] Aldryhim, Y and Khalid, A. 2003. - Diagnostic tests for red palm weevil. Effect of humidity and soil type on Rhynchophorus ferrugineus infested survival and behavior of red palm date palm trees. Arab Journal of weevil, Rhynchophorus ferrugineus Scientific research 10, 93-104. (Oliv.) adults. Sultan Qaboos University 24] Boivin, G. A., B.J.P. R. Le, and J. A. Journal for Scientific Research Adams. 1991. Spatial dispersion and

Persian Gulf Crop Protection, 3(1): 92-118 110

sequential sampling plan for the formulation against the red palm weevil, tarnished plant bug (Hemiptera: Rhynchophorus ferrugineus (Olivier) Miridae) on celery. J. Econ. Entomol. (Coleoptera: Curculionidae) in Phoenix ,canariensis. Pest Management Science 164ذ158 :84 25] Brockerhoff, E. G., and D. M. Suckling. 66(4): 365-370. 1999. Development of an attracticide 35] Dembilio, ó, Quesada-Moraga, E.; against light brown apple Santiago-Àlvarez, C. and Jacas, J. A. (: Tortricidae). J. Econ. (2010b). Potential of an indigenous Entomol. 92: 853-859. strain of the entomopathogenic fungus, 26] Carpenter, J.B. and H.S. Elmer. 1978. Beauveria bassiana as biological control Pests and diseases of the date palm. agent against the red palm weevil, United States Department of Rhynchophorus ferrugineus. Journal of Agriculture, Agriculture Handbook no. Invertebrate Pathology, 104, 214-221. 527. United States Department of 36] Dembilio Ó & Jacas JA. (2011) Basic Agriculture, Washington DC. bio-ecological parameters of the 27] Carriere, Y., Dennehy, T. J., Pedersen, invasive Red Palm Weevil, B., Haller, S., Ellers-Kirk, C., Antilla, Rhynchophorus ferrugineus (Coleoptera: L., Liu, Y., Willot, E., and Tabashnik, B. Curculionidae), in Phoenix canariensis 2001. Large-scale management of insect under Mediterranean climate. Bulletin of resistance to transgenic cotton in Entomological Research 101, 153-163. Arizona: can transgenic insecticidal 37] Dembilio Ó, Quesada-Moraga E, crops be sustained? Journal of Economic Santiago-Álvarez C & Jacas JA. Entomology 94: 315-325. (2010b). Biocontrol potential of an 28] Cohen Y., Alchanatis V., Prigojin A., indigenous strain of the Levi A., Soroker V., Cohen Y., 2012 - entomopathogenic fungus Beauveria Use of aerial thermal imaging to bassiana (Ascomycota; Hypocreales) estimate water status of palm trees. against the red palm weevil, Precision Agriculture 13, 123-140. Rhynchophorus ferrugineus (Coleoptera: 29] Calkins, C. O. 1998. Review of the Curculionidae). Journal of Invertebrate codling moth areawide suppression Pathology 104, 214–221. program in the western United States. J. 38] Dembilio Ó, Llácer E, Martínez de Agric. Entomol. 15: 327-333. Altube M.M & Jacas JA. (2010a). Field 30] Chandler, L.D. and Faust, R.M. (1998) efficacy of imidacloprid and Overview of areawide management. Steinernema carpocapsae in a chitosan Journal of Agricultural Entomology 15, formulation against the red palm weevil 319-325. Rhynchophorus ferrugineus (Coleoptera: 31] Chao, C.T., & Krueger, R.R., 2007. The Curculionidae) in Phoenix canariensis. Date palm (Phoenix dactylifera L.): Pest Management Science 66, 365-370. Overview of biology, uses, and 39] Dembilio, ó and Jacas, J. A. 2012. Bio- cultivation. HortScience 42(5): 1077- ecology and integrated management of 1082. the red palm weevil, Rhynchophorus 32] Cronin, J. T., P. Turchin, J. L. Hayes, ferrugineus (Coleoptera: Curculionidae) and C. A. Steiner. 1999. Area-wide in the region of Valencia (Spain). efficacy of a localized forest pest Hellenic Plant Protection Journal 5: 1- management practice. Environmental 12. Entomology 28: 496-504. 40] Elawad SA, Mousa SA, Shahdad AS, 33] Cook, S. M., Khan, Z. N., & Pickett, J. Alawaash SA & Alamiri AMA. (2007) A. (2007). The use of push and pull Efficacy of entomopathogenic strategies in integrated pest nematodes against red palm weevil in management. Annual Review of UAE. Acta Horticulturae 736, 415-420. Entomology, 52, 375-400. 41] El-Ezaby F. (1997). A biological in vitro 34] Dembilio, O.; Llácer, E.; Martinez de study on the red Indian date palm Altube, M. M. and Jacas, J. A. 2009. weevil. Arab Journal of Plant Protection Field efficacy of imidacloprid and 15, 84–87. Steinernema carpocapsae in a chitosan

Persian Gulf Crop Protection, 3(1): 92-118 111

42] Ehler, L. E., and D. G. Bottrell. 2000. 50] El-Sayed, A. M., Suckling, D. M., The delicate balance: environment, Wearing, C. H. and Byers, J. A. (2006). economics, development. The illusion of Potential of mass trapping for long-term integrated pest management. Issues in pest management and eradication of Science and Technology, Spring 2000: invasive species. J. Econ. Entomol. 1-6. 99(5): 1550-1564. 43] Esteban-Duran, J. E., Yela, J.L., Crespo, 51] El-Sufty, R., Al-Awash, S.A., Al- F. B. and Alvarez, A. J. 1998. Biology Bgham, S., Shahdad, A.S. & Al-Bathra, of red palm weevil, Rhynchophorus A.H. (2009). Pathogenicity of the ferrugineus (Olivier) Coleoptera: fungus Beauveria bassiana (Bals.) Vuill Curculionidae: Rhynchophorinae, in the to the Red Palm Weevil, Rhynchophorus laboratory and field, life cycle, ferrugineus (Oliv.) (Col.: Curculionidae) biological characteristics in its zone of under Laboratory and Field Conditions. introduction in Spain, biological method Egyptian Journal of Biological Pest of detection and possible control. Control 19, 81–85. BoletinSanidad Vegetal Plagas 24: 737- 52] Erskine W, Moustafa AT, Osman AE, 748. Lashine Z, Nejatian A, Badawi T, Ragy 44] El-Sabea, A.M.R., Faleiro, J.R., Abo-El- SM. 2011. Date palm in the GCC Saad, M.M. 2009. The threat of red palm countries of the Arabia Peninsula. weevil Rhynchophorus ferrugineus to Available at plantations of the gulf region in the http://www.icarda.org/aprp/datepalm/int Middle East: an economic perspective. roduction/intro-body.htm (accessed Outlooks of Pest Manag. 20, 131-134. November 23, 2013). 45] El-Sayed, A. M., and R. M. Trimble. 53] Faleiro, J. R. and Rangnekar, P. A. 2002b. Pheromone content of (2001). Ovipositional preference of red azinphosmethyl-susceptible and palm weevil, Rhynchophorus azinphosmethyl resistant oblique banded ferrugineus Oliv. to coconut cultivars. leafrollers (Lepidoptera: Tortricidae) as Indian coconut Journals 32, 22-23. a function of time of day and female 54] Faleiro, J. R. 2006. Insight into the age. Can. Entomol. 134: 331-341. management of red palm weevil 46] El-Sebay Y. (2003) Ecological studies Rhynchophorus ferrugineus (Olivier) on the red palm weevils Rhynchophorus based on experiences on coconut in ferrugineus Oliv. (Coleoptera: India and date palm in Saudi Arabia. In Curculionidae) in Egypt. Egyptian Proceedings of the first international Journal of Agricultural Research 81, workshop on red palm weevil, 28-29, 523–529. November 2005, IVIA, Valencia, Spain. 47] Ehrler W. L., 1973 - Cotton leaf 55] Faleiro, J. R., El-Shafie, H. A. F. 2013. temperatures as related to soil water Preference of Rhynchophorus depletion andmeteorological factors. ferrugineus to date palm cultivars: Agronomy Journal, 65, 404–409. Olfactometer assays. ESA 61st Annual 48] El-Shafie, H.A.F., Faleiro, J.R., Al- Meeting, Presentation 1892, Nov. 10-13, Abbad, A.H., Stoltman, L., Mafra-Neto, 2013, Austin, Texas, USA. A. 2011. Bait-free attract and kill 56] Faleiro, J. R., Abraham, V. A., Boudi, technology (HookTMRPW) to suppress N., Al Shuaibi, M.A., Premkumar, T. red palm weevil, Rhynchophorus (2000). Field evaluation of different ferrugineus (Coleoptera: Curculionidae) types of red palm weevil Rhynchophorus in date palm. Fla. Entomol. 94, 774-778. ferrugineus pheromone lures, Indian 49] El Shafie, H. A. F.; Faleiro, J. R.; Abo- Journal Entomology 62: 427- 433. El-Saad, M. M. and Aleid, S. M. 2013. 57] Faleiro J. R., Ashok Kumar J. and A meridic diet for laboratory rearing of Rangnekar P. A. (2002). Spatial red palm weevil, Rhynchophorus distribution of red palm weevil ferrugineus (Coleoptera: Curculionidae). Rhynchophorus ferrugineus Oliv. Scientific Research and Essays, 8(39): (Coleoptera: Curculionidae) in coconut 1924-1932. plantations. Crop Protection 21, 171– 176.

Persian Gulf Crop Protection, 3(1): 92-118 112

58] Faleiro, J.R., Ben Abdullah, A., Kumar, 67] Ferry M & Gómez S. (2002). The red J.A., Shagagh, A., Al Abdan, S. 2010. palm weevil in the Mediterranean area. Sequential sampling plan for area-wide Palms 46,172-178. management of Rhynchophorus 68] Fisher, M. E., P. van den Driessche, and ferrugineus (Olivier) in date palm H. J. Barclay. 1985. A density plantations of Saudi Arabia. Int. J. Trop. dependent model of pheromone Ins. Sci. 30, 145-153. trapping. Theor. Popul. Biol. 27: 91-104. 59] Farazmand, H. (2002). Investigation on 69] Gaston, L. K., Shorey, H. H., and C. A. the reasons of food preference of red Saario. 1967. Insect population control palm weevil, Rhynchophorus by the use of sex pheromones to inhibit ferrugineus Oliv. Applied Entomology orientation between the sexes. Nature and phytopathology 70, 11-12. (Lond.) 213: 1115. 60] Fiaboe, K.K.M., Peterson, A.T., Kairo, 70] Gerling, D. & Legg, J. P. 2005. M.T.K., Roda, A.L. 2012. Predicting the Implications of biological sciences for potential worldwide distribution of the pest management. African Crop Science red palm weevil Rhynchophorus Conference Proceedings, Vol. 7, pp. ferrugineus (Olivier) (Coleoptera: 509-514. Curculionidae) using ecological niche 71] Gaugler, R. (2007). Nematodes modeling. Fla. Entomol. 95, 559-673. (Rhabditida: Steinernematidae & 61] Faleiro, J.R., Ben Abdullah, A., Kumar, Heterorhabditidae). Available on line at: J.A., Shagagh, A., Al Abdan, S. 2010. www.nysaes.cornell.edu/ent/biocontrol/ Sequential sampling plan for area-wide pathogens/nematodes.html(accessed. management of Rhynchophorus Cited 25_Jul_2013. ferrugineus (Olivier) in date palm 72] Gindin, G. S. Levski; Glazer, I. and plantations of Saudi Arabia. Int. J. Trop. Soroker, V. 2006. Evaluation of the Ins. Sci. 30, 145-153. entomopathogenic fungi, Metarhizium 62] Faleiro, J.R. 2006. A review of the anisopliae and Beauveria bassiana issues and management of the red palm against the red palm weevil, weevil Rhynchophorus ferrugineus Rhynchophorus ferrugineus. (Coleoptera: Rhynchophoridae) in Phytoparasitica, 34: 370-379. coconut and date palm during the last 73] Gush, H. 1997. Date with disaster. The one hundred years. Int. J. Trop. Insect Gulf Today, September 29, p. 16. Sci. 26, 135-150. 74] Guarino, S., Peri, E. and Lo Bue, P. 63] Faccioli, G., Pasqualini, E., and Baronio, (2013). Assessment of synthetic P. 1993. Optimal trap density in Cossus chemicals for disruption of cossus (Lepidoptera: Cossidae) mass Rhynchophorus ferrugineus response to trapping. J. Econ. Entomol. 86: 850-853. attractant-baited traps in an urban 64] FAO [Food and Agriculture environment. Phytoparasitica 41: 79-88. Organization]. 2012. Crop production 75] Hallett, R. H., Gries, G., Borden, J. H., and trade data. Available at Czyzewska, E., Oehlschlager, A. C., http://faostat.fao.org/site/291/default.asp Pierce Jr., H. D., Angerilli, N. P. D., x (accessed November 23, 2013). Anrauf, A. 1993. Aggregation 65] Faust, R. M. 2008. General introduction pheromones of two Asian palm weevils, to areawide pest management. In: Koul, Rhynchophorus ferrugineus and O., Cuperus, G., Elliot, N. (Eds.), Rhynchophorus vulneratus Areawide pest management: Theory and Naturwissenschaften, 80, 328-331. Implementation, CABI, Oxfordshire, 76] Hassanali, A., Herren, H., Khan, Z. R., U.K., pp. 1-14. Pickett, J. A. & Woodcock, C. M. 66] Faust, R. 2001. Forum on invasive (2008). Integrated pest management: the species and area-wide pest management: push-pull approach for controlling insect what we have learned, pp. 2. In pest and weeds of cereals, and its Agricultural Research,November 2001. potential for other agricultural systems USDA, Washington, DC., USA. including animal husbandry. Philosophical Transaction of the Royal Society B, 363, 611-621.

Persian Gulf Crop Protection, 3(1): 92-118 113

77] Hendrichs, J.; Kenmore, P., Robinson, 87] Ju, R-T. & Ajlan, A. 2011. A. S. and Vreysen, M. J. B. 2007. Area- Establishment and potential risks of a wide integrated pest management (AW- new invasive pest, red palm weevil IPM): Principles, Practice and Prospects. Rhynchophorus ferrugineus in China. In: Vreysen, M. J. B., Robinson, A. S. Arab Journal of Plant protection 29(1): and Hendrichs, J. (eds.). Area-wide 122-130. Control of Insect Pests, pp.3-33, IAEA. 88] Kalshoven, L.G.E. (1981). Pests of 78] Hoddle M.S., Al-Abbad A.H., El-Shafie crops in Indonesia. P.T. Ichtiar Baru- H.A.F., Faleiro J.R., Sallam A.A., Vanhoeve, Jakarta. Indonesia, pp. 720. Hoddle C.D. (2013). Assessing the 89] Klassen, W., and C. F. Curtis. 2005. impact of areawide pheromone trapping, History of the sterile insect technique, pesticide applications, and eradication of pp. 3-36. In Dyck, V. A., J. Hendrichs, infested date palms for Rhynchophorus and A. S. Robinson (eds.), sterile insect ferrugineus (Coleoptera: Curculionidae) technique. Principles and practice in management in Al Ghowaybah, Saudi area-wide integrated pest management. Arabia. Crop Protection 53: 152–160. Springer, Dordrecht, the Netherlands. 79] Hetzroni A., Mizrach A., Nakache Y., 90] Knipling, E. F. 1960. Use of insects for Soroker V., 2004 - Developing spectral their own destruction. Journal of model tomonitor activity of red palm Economic Entomology 55: 782-786. weevil. Alon Hanotea, 58, 466-469. 91] Knipling, E. F. 1972. Entomology and 80] Hesler, L. S. & Dashiell, K. E. 2011. the management of man’s environment. Antixenosis to Soybean Aphid in Journal of the Australian Entomological Soybean Lines. The open Entomology Society 11: 153-167. Journal, 5, 39-44. 92] Knipling, E. F. 1979. The basic 81] Henry G. M. (1917). The coconut red principles of insect population weevil, Rhynchophorus ferrugineus. suppression and management. Tropical Agriculture 48, 218–219. Agriculture Handbook Number 512. 82] Horber, E. 1982. Types and 93] SEA, USDA,Washington, DC., USA. classification of resistance. In: Maxwell 94] Knipling, E. F. 1979. The basic FG Jennings PR, Eds. Plant resist to principles of insect population insects. New York: John Wiley 1982; suppression and management. 15-21. Agriculture Handbook Number 512. 83] Hendrichs, J., Robinson, A., 2009. USDA, Washington, DC, USA. Sterile insect technique. In: Resh, V.H., 95] Knipling, E. F., and E. A. Stadelbacher. Carde, R.T. (Eds.), Encyclopedia of 1983. The rationale for area-wide Insects, second ed. Academic Press, management of Heliothis (Lepidoptera: Elsevier Science Publisher, New York, Noctuidae) populations. Bull. Entomol. pp. 953e957. Soc. Am. 29: 29-37. 84] Horowitz AR., Forer G, Ishaaya I. 96] Kogan, M. (1995) Areawide (1995). Insecticide resistance management of major pests: is the management as a part of an IPM strategy concept applicable to the Bemisia in Israeli cotton fields. In: Constable complex? In: Gerling, D. and Mayer, GA, Forrester NW (Eds.) Challenging R.T (eds.) Bemisia: , Biology, the Future: Proc. World Cot Res Conf. Damage, Control and Management 1. CSIRO, Melbourne, pp. 537–544. 1995. Intercept, Andover, UK, pp. 643- 85] Hulme, P, E. (2009). Trade, transport 657. and trouble: managing invasive species 97] Kurian C. and Mathen K. (1971) Red pathways in an era of globalization. J. palm weevil-Hidden enemy of coconut Appl. Ecol. 46: 10-18. palm. Indian Farming 21, 29–31. 86] James C (2008). Global Status of 98] Lance, D.R. & McInnis, D.O. (2005) Commercialized Biotech/GM Crops: Biological Basis of the Sterile Insect 2007. ISAAA Briefs No. 37 Technique. pp. 69–94 in Dyck, V.A., International Service for the Acquisition Hendrichs, J. & Robinson, A.S. (Eds) of Agri-biotech Applications, Ithaca, Sterile Insect Technique: Principles and NY. Practice in Area-Wide Integrated Pest

Persian Gulf Crop Protection, 3(1): 92-118 114

Management. Dordrech, the Arabia. Journal of plant protection Netherlands, Springer. research, 51, 281-286. 99] Liu, Y. J., Zhang, M., Richards, B., 106] Mankin, R.W. 2011. Recent Pham and P. Roe. 2009. Towards development in the use of acoustic continuous surveillance of fruit flies sensors and signal processing tools to using sensor networks and machine target early infestations of red palm vision. Proceedings of the fifth weevil in agricultural environments. Fla. International Conference on wireless Entomol. 94, 761-765). communications networking and Mobile 107] Mankin R.W., Hagstrum D. W., Smith Computing, Sept.24-26, Beijing, and pp: M. T., Roda A. L., Kairo M. T. K., 2011 4705-4709. - Perspectiveand Promise: a Century of 100] Lindquist, D. A. (2001). The advantages Insect Acoustic Detection and of area-wide insect control, pp. 55-61. In Monitoring. AmericanEntomologist, 57, Proceedings: Sterile insect technique as 30-44. an environmentally friendly and 108] Mankin R. W., Mizrach A., Hetzroni A., effective insect control system. Seminar Soroker V., 2008 - Temporal and organized by the Regiao Autonoma de spectral features of sounds of wood- Madeira Governo Regional and the boring beetle larvae: identifiable European Uniion, 12-13 November patterns of activity enable improved 1999, Funchal, Madeira, Portugal. discrimination from background noise. Madeira Regional Direction of The Florida Entomologist, 91, 241-248. Agriculture, Madeira, Portugal. 109] Mazza, G., Arizza, V., Baracchi, D., 101] Llácer, E.; Martinez de Altube, M. M. Barzanti, GP. Benvenuti, C., Francardi, and Jacas, J. A. 2009. Evaluation of the V., Frandi, A., Gherardi, F., Longo, S., efficacy of Steinernema carpocapsae in a Manachini, B., Perito, B., Rumine, P., chitosan formulation against the red Schillaci, D., Turillazzi, S., and Cervo, palm weevil, Rhynchophorus R. 2011. Antimicrobial activity of the ferrugineus in Phoenix canariensis. red palm weevil, Rhynchophorus BioControl, 54: 559-565. ferrugineus. Bulletin of Insectology 64 102] Leo Justin, C. G., Leelamathi, M., (1): 33-41. Thangaselvabai, T. & Nirmal Johnson, 110] Mrácek, Z. (2003). Use of S. B. (2008). Bioecology and entomopathogenic nematode EPANs in management of the red palm weevil, Biological Control. In: Upadhyay RK Rhynchophorus ferrugineus Oliv. (ed). Advances in Microbial Control of (Coleoptera: Curculionidae) on coconut- Insect Pests. Plenum Pub Corp. New A review. Agric. Rev., 29(2): 117-124. York, USA. 103] Llácer, E., Santiago-Àlvarez, C. and 111] Menke, W. W., and G. L. Greene. 1976. Jacas, J. A. 2013. Could sterile males be Experimental validation of a pest used to vector a microbiological control management model. Fla. Entomol. agent? The case of Rhynchophorus 59:135-142. ferrugineus and Beauveria bassiana. 112] Mukhtar, M., Rasool, K.G., Parrella, Bulletin of Entomol. Res., 103, 241-250. M.P., Sheikh, Q.I., Pain, A., Lopez- 104] Murphy, S. T. and Briscoe, B.R. 1999. Llorca, L.V., Aldryhim, Y.N., Mankin, The red palm weevil as an alien R.W., Aldawood, A.S. 2011. New invasive: Biology and the prospects for initiatives for management of red palm biological control as a component of weevil threats to historical Arabian data IPM. Bio- control News Inform. 20: palms. Fla. Entomol. 94, 733-736. 35N-45N. 113] Mottus, E., Liblikas, I., Williams, I. H., 105] Massoud, A. M. Faleiro, J.R., Abo El- Kuuaik, S., Laanmaa, M., Nilson, A. and Saad, M.M., Sultan, E. (2011). Nomm, V. 1996. Performance of Cydia Geographic information system for pomonella, conjugella, assessing the activity of red palm weevil Plutella xylostella, and Archips podana Rhynchophorus ferrugineus (Olivier) in attractant dispensers in Estonia. Proc. the date palm oasis of Al-Hassa, Saudi Estonian Acad. Sci. Biol. 45: 155-170.

Persian Gulf Crop Protection, 3(1): 92-118 115

114] Miller TA (2004). Rachel Carson and ferrugineus Oliv. On sugarcane. Indian the adaptation of biotechnology to crop Journal Entomology 34, 213-215. protection. Am. Entomol.50: 194–198. 125] Rajmanickam K., Kennedy J. S. and 115] Nakash J., Osam Y. and Kehat M. Christopher A. (1995). Certain (2000) A suggestion to use dogs for components of integrated management detecting red palm weevil for red palm weevil, Rhynchophorus (Rhynchophorus ferrugineus) infestation ferrugineus, (Curculionidae: Coleoptera) in date palm in Israel. Phytoparasitica on coconut. Mededelingen Faculteit 28, 153–154. Landbouwkundige en Toegepaste 116] Nirula, K. K. (1956). Investigations on Biologische 60, 803–805. the pests of coconut palm. Part 126] Rahalkar, G.W., Harwalkar, M.R. & IV.Rhynchophorus ferrugineus. Indian Rananavare, H.D. (1975). Laboratory Coconut Journal 9, 229-247. studies on sterilization of male 117] Perkins, J. 1982. Insects, experts, and Rhynchophorusferrugineus. pp. 261–267 the insecticide crisis: the quest for new in Sterility Principle for Insect pest management strategies. Plenum Control1974. International Atomic Press, New York, USA. Energy Agency (Ed.), Vienna,Austria. 118] Pedgley, D. E. 1993. Managing 127] Rahalkar, G.W., Harwalkar, M.R., migratory insect pests- a review. Rananvare, H.D., Kurgan, C.,Abrham, International Journal of Pest V.A. & Koya, K.M.A. (1977) Management 39: 3-12. Preliminary field studies on the control 119] Pinhas J., Soroker V., Hetzroni A., of the red palm weevil, Rhynchophorus Mizrach A., Teicher M., Goldberger J. ferrugineus using radio sterilized males. 2008 - AutomaticAcoustic Detection of Journal of Nuclear Agriculture and the Red Palm Weevil. Computers and Biology 6, 65–68. Electronics in Agriculture 63 ,131-139. 128] Ranavara, H.D., Harwalkar, M.R. & 120] Prabhu, S.T. & Patil, R.S. (2009) Rahalkar, G.W. (1975). Studies on the Studies on the biological aspects of red feasibility of using sterile females along palm weevil Rhynchophorus ferrugineus with sterile males in the control of red (Oliv.). Karnataka Journal of palm weevil, Rhynchophorus Agricultural Sciences 22, 732–733. ferrugineus Oliv. (Coleoptera: 121] Prabhu, S.T., Dongre, T.K. & Patil, R.S. Curculionidae). pp. 861–868 in Use of (2010) Effect of irradiation on the Radiations and Radioisotopes in Studies biological activities of red palm weevil, of Plant Productivity: Proceedings of a Rhynchophorus ferrugineus Olivier. Symposium held at G.B. Pant University Karnataka Journal of Agricultural of Agriculture and Technology, Sciences 23, 186–188. Pantnagar, India, 12–14 April 1974, 122] Quesada-Moraga, E., Santos-Quiros, R., Department of Atomic Energy, Bombay, Valverde-Garcia, P. &Rahalkar, G.W., India. Harwalkar, M.R., Rananavare, H.D., 129] Ramachandram, C.P. (1991) Effect of Shantaram, K. & Ayengar, A.R.G. gamma radiation on various stages of (1973) Laboratory studies on radiation red date palm weevil, Rhynchophorus sterilization of Rhynchophorus ferrugineus Oliv. Journal of Nuclear ferrugineus males. Journal of Plantation Agriculture and Biology 3, 218–221. Crops 1, 141–145. 130] Reddy, G.V.P., and K.C.D. Urs. 1996. 123] Ramachandran, C. P. (1998). Biotypic Studies on the sex pheromone of the variability among four populations of diamondback moth, Plutella xylostella red palm weevil, Rhynchophorus (Lepidoptera: Yponomeutidae) in India. ferrugineus Oliv. From different parts of Bull. Entomol. Res. 86: 585-590. India. Coconut Research and 131] Rugman-Jones, P. F.; Hoddle, C. D.; Development (CORD) 14, 26–41. Hoddle, M. S.; Stouthamer, R. 2013. 124] Rahalkar GW, Harwalkar MR & The lesser of two weevils: Molecular Rananavare, HO. (1972) Development genetics of pest palm weevil populations of red palm weevil, Rhynchophorus confirm Rhynchophorus vulneratus (Panzer 1798) as a valid species distinct

Persian Gulf Crop Protection, 3(1): 92-118 116

from Rhynchophorus ferrugineus of males. Entomol. Exp. Appl. 55: 59- (Olivier 1790), and reveal the global 68. extent of both. PLos one 8(10): e78379. 141] Stern, V. M., R. F. Smith, R. Van den Doi: 10.1371/journal.pone.0078379. Bosch, and K. S.Hagen. 1959. The 132] Sanderson G. 2001. Natural history of integrated control concept. Hilgardia 29: the date palm – Phoenix dactylifera. 131-154. Available at 142] Steiner, L. F. 1952. Methyl eugenol as http://enhg.4t.com/articles/date.htm an attractant for oriental fruit fly. J. (accessed March 23, 2013). Econ. Entomol. 45: 241-248. 133] Saleh, M.M.E. & Alheji, M. (2003) 143] Sindhuja S., Lav R. K, Suranjan P., 2012 Biological control of red palm weevil - Biology and applications of olfactory with entomopathogenic nematodes in sensingsystem: A review. Sensors and the eastern province of Saudi Arabia. Actuators B: Chemical, 171–172, 1–17. Egyptian Journal of Biological Pest 144] Siriwardena K. A. P., Fernando L. C. P., Control 13, 55–59. Nanayakkara N., Perera K. F. G., 134] Santiago-Álvarez, C. (2004) Virulence, Kumara A,Nanayakkara T., 2010 - horizontal transmission, and sublethal Portable acoustic device for detection of reproductive effects of Metarhizium coconut palms infestedby anisopliae (anamorphic fungi) on the Rhynchophorus ferrugineus (Coleoptera: German cockroach (Blattodea: Curculionidae). Crop Protection 29, 25- Blattellidae). Journal of Invertebrate 29. Pathology 87, 51–58. 145] Soroker, V.; Suma, P.; La Pergola, A.; 135] Sallam, A. A., Elshafie, H. A. F. & Al- Cohen, Y.; Alchanatis, V; Golomb, O; Abdan, S. (2012). Influence of farming Goldshtein, E.; Hetzroni, A.; Galazan, practices on infestation by red palm L.; kontodimas, D; Pontikakos, C; weevil Rhynchophorus ferrugineus Zorovic, M.; Brandstetter, M. 2013. (Olivier) in date palm: a case study. Early detection and monitoring of red International Research Journal of palm weevil: Approaches and Agricultural science and soil science challenges. AFPP- Palm pest 2(8): 370-376. Mediterranean Conference, Nice-16-18 136] Salama H. S., Foda M. S., El-Bendary January, 2013, France. M. A. and Abdel- Razek A. (2004) 146] Soroker, V.; nakacha, Y.; Landau, U.; Infection of red palm weevil Mizrach, A.; Hetzroni, A. and Gerling, Rhynchophorus ferrugineus, by spore- D. 2004. Utilization of sounding forming bacilli indigenous to its natural methodology to detect infestation by habitat in Egypt. Journal ofPest Science Rhynchophorus ferrugineus on palm 77, 27–31. offshoots. Phytoparasitica, 32: 6-8. 137] Sexson, D. L., and J.A.Wyman. 2005. 147] Soroker, V.; Blumberg, D.; Haberman, Effect of crop rotation distance on A.; Hamburger-Rishard, M.;Rench, S.; populations of Colorado potato beetle Talebaev, S.; Anshelevich, L. and (Coleoptera: Chrysomelidae): Harari, A. R. 2005. Current status of red development of area-wide Colorado palm weevil in date palm plantations in potato beetle pest management Israel. Phytoparasitica, 33: 97-106. strategies. Journal of Economic 148] Sexson, D. L., and Wyman, J. A. 2005. Entomology 98: 716-724. Effect of crop rotation distance on 138] Smith, C. M. 2005. Plant resistance to population of Clorado potato beetle arthropods. Dordrechdt. The (Coleoptera: Chrysomelidae): Netherlands; Springer 2005. development of area-wide Clorado 139] Steiner, L. F. 1952. Methyl eugenol as potato beetle pest management an attractant for oriental fruit fly. J. strategies. Journal of Economic Econ. Entomol. 45: 241-248. Entomology 98: 716-724. 140] Sternlicht, M., I. Barzakay, and M. 149] Stouthamer R, Breeuwer JAJ, Hurst Tamim. 1990. Management of Prays GDD (1999). Wolbachia pipientis: citri in lemon orchards by mass trapping microbial manipulator of arthropod

Persian Gulf Crop Protection, 3(1): 92-118 117

reproduction. A Rev Microbiol 53: 71– 155] Wang L., Zhang X.-W., Pan L.-L., Liu 102. W.-F., Wang D.-P., Zhang G.-Y., Yin 150] Suma P., Longo S., 2009 - Applicazioni Y.-X., Yin A., Jia S.-G., Yu X.-G., Sun di termografia, endoscopia ed analisi G.-Y., Hu S.-N., Al-Mssallem I.S., Yu J. indiretta per la diagnosi precoce degli (2013). A large-scale gene discovery for attacchi di punteruolo rosso. In: Regione the red palm weevil Rhynchophorus Siciliana - Assessorato Agricoltura e ferrugineus (Coleoptera: Curculionidae). Foreste. La ricerca scientifica sul Insect Science. doi: 10.1111/j.1744- Punteruolo rosso e gli altri fitofagi delle 7917.2012.01561.x palme in Sicilia. Vol. 1, pp 103-106. 156] Wattanapongsiri A. (1966). A revision SBN Pal0217180. of the genera Rhynchophorus and 151] Thomas, M. B. (1999). Ecological Dynamis (Coleoptera: Curculionidae). approaches and the development of Department of Agriculture Science "truly integrated" pest management. Bulletin 1, 328 pp. Bangkok, Thailand. Proceedings national academy of Sciences 96: 5944-5941. 157] Welch, S. M., B. A. Croft, and M. F. 152] Thomas DD, Donnelly CA, Wood RJ, Michels. 1981. Validation of pest Alphey LS (2000). Insect population management models. Environ. Entomol. control using a dominant, repressible, 10: 425-432. lethal genetic system. Science 287: 158] Witzgall, P., Kirsch, P., & Cork, A. 2474–2476. (2010). Sex pheromones and their 153] Vidyasagar PSPV, Mohammed H, impact on pest management. Journal of Abozuhairah RA, Al-Mohanna OE & Chemical Ecology, 36, 80-100. Al-Saihati AA. (2000). Impact of mass 159] Yu, R. & Leung, P. 2006. Optimal pest pheromone trapping on red palm weevil: management: A reproductive pollutant adult population and infestation level in perspective. International Journal of Pest date palm gardens of Saudi Arabia. management 52: 155-166. Planter 76, 347-355. 160] Zabalou S, Riegler M, 154] Whalon ME, Mota-Sanchez D, Theodorakopoulou M, Stauffer C, Hollingworth RM (2008). The Savakis C, Bourtzis K (2004). Arthropod Pesticide Resistance Wolbachia induced cytoplasmic Database. Michigan State University. incompatibility as a means for insect http://www.pesticideresistance.org pest population control. Proc Natl Acad Sci USA 101: 15042–15045.

Persian Gulf Crop Protection, 3(1): 92-118 118