Review of control methods against the palm borers
Rhynchophorus ferrugineus (Olivier) (Coleoptera:
Curculionidae) and Paysandisia archon (Burmeister)
This review was written with support from the European Community’s Seventh Framework Programme under grant agreement No. FP7 KBBE 2011-5-289566 (PALM PROTECT): Eradication and containment strategies and tools for the implementation of EU legislation against the red palm weevil Rhynchophorus ferrugineus (Olivier) and Paysandisia archon (Burmeister).
AUTHORS
O. Dembilio1, N. Audsley2, Y. Cohen3, S. Colazza4, N. Isidoro5, F. Karamaouna6, D.
Kontodimas6, V. Navarro-Llopis7, E. Peri4, E. Quesada-Moraga8, P. Riolo5, D. Rochat9,
V. Soroker3 and JA Jacas1
1Universitat Jaume I; Unitat Associada d’Entomologia Agrícola UJI-IVIA; Campus del Riu Sec; E-12071-Castelló de la Plana (Spain)
2The Food and Environmental Research Agency; Sand Hutton; York; YO41 1LZ (United Kingdom)
3Agricultural Research Organization; The Volcani Centre; POB 6; Bet Dagan; 50250 (Israel)
4Università degli Studi di Palermo; Dipartimento DEMETRA; Palermo (Italy)
5Università Politecnica delle Marche; Dipartimento di Scienze Agrarie, Alimentari ed Ambientali, Facoltà di Agraria; via Brecce Bianche; 60131 Ancona (Italy)
6Benaki Phytopathological Institute; Laboratory of Agricultural Entomology; Department of Entomology and Agricultural Zoology; 8 St. Delta Str.; GR-145 61; Kifissia (Greece)
7Universidad Politécnica de Valencia; CEQA-IAM; Camino de Vera s/n; Edificio 6C-5ª; 46022- Valencia, Spain
8Universidad de Córdoba; Departamento de Ciencias y Recursos Agrícolas y Forestales; Edificio C4; Campus de Rabanales; 14071 Córdoba (Spain)
9Institut National de la Recherche Agronomique; UMR 1272; RD 10; 78026 Versailles (France)
Date of review: September 2012 1. INTRODUCTION
The red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera:
Curculionidae), and the moth Paysandisia archon (Burmeister) (Lepidoptera:
Castniidae) are currently considered as the most damaging invasive palm pests worldwide. Both spread extensively from their origin by trading of palm trees and offshoots from infested areas. The larvae of both R. ferrugineus and P. archon are the main damaging stage, boring into palm trees and feeding on the succulent plant material of stipes and/or leaves, remaining hidden through most of their life cycles. The first symptoms are often only visible long after infestation. At that stage damage is severe, generally resulting in the death of the palm (Ferry & Gomez, 2002; Faleiro,
2006; EPPO, 2008a; b; Faleiro et al., 2012).
1.1 The Red Palm Weevil, Rhynchophorus ferrugineus
Rhynchophorus ferrugineus is native to southern Asia and Melanesia, and is reported to attack more than 20 species of palms worldwide (Wattanapongsiri, 1966;
Sarto i Monteys & Aguilar, 2005; Faleiro, 2006; EPPO, 2008a; b; Dembilio et al., 2009;
Malumphy & Moran,2009; Dembilio & Jacas, 2010; Dembilio & Jacas, 2012), including date (Phoenix dactylifera L.), and coconut (Cocos nucifera L.) palms, as well as the
Mediterranean fan palm (Chamaerops humilis L.), the native Cretan date palm
(Phoenix theophrasti Greuter) [Kontodimas et al., 2006; Dembilio et al., 2011] and
Canary Islands date palm (Phoenix canariensis hort. ex. Chabaud) (Dembilio et al.,
2009). Currently, this pest has spread to many areas worldwide; its range now includes much of Asia, regions of Oceania, the Middle-East and North Africa, southern Europe, the Caribbean, and in October 2010, five specimens belonging to the genus
Rhynchophorus sp., were found in southern California (EPPO 2008; 2009; 2011). The high rate of spread of R. ferrugineus is most likely due to a combination of factors, including the lack of effective early detection methods. The transportation of infested date palm trees and offshoots from contaminated to uninfested areas has had a major impact.
In Europe, many preventative and curative procedures have been implemented with variable degrees of success to eradicate and contain R. ferrugineus (Buyukozturk et al., 2011; Dembilio & Jacas, 2011; Jacas et al., 2011; Nardi et al., 2011; Tapia et al.,
2011), but these have been hampered by environmental concerns related to the use of pesticides and legislation restricting their use such as EU Directives 91/414 and
2009/128/EC establishing a framework for Community action to achieve the sustainable use of pesticides. Many cities also tend to develop a ‘zero pesticides’ policy, which complicates the management of the palm weevil. This is compounded by the fact that most of the pest life cycle is endophytic, concealed deep within the palm stipe and leaf bases, thereby limiting effective delivery of pesticides, (Llácer et al.,
2010).
1.2 The Castniid Palm Borer, Paysandisia archon
The moth P. archon inhabits extensive open areas where wild palms grow in its native regions of South America. It was first reported in Europe in France and Spain in
2001, but is believed to have been introduced before 1995 on palm trees imported from
Argentina (Reid & Moran, 2009). It has since spread to other European countries
(France, Italy, Spain, Greece and Cyprus) with isolated reports in the UK, Bulgaria,
Denmark, Slovenia, Switzerland and Czech Republic, on palms imported from Spain and Italy (Vassarmidaki et al., 2006; Rochat et al., 2006b; EPPO 2008b; 2009; Longo et al., 2008; Buhl et al., 2009; Vassiliou et al., 2009; EPPO, 2010; CABI, 2012). This pest appears to have a large host range, including the native Mediterranean fan palm which is very susceptible to P. archon attack. Although P. archon has not been reported to be a significant pest in South America, with the exception of reports from
Buenos Aires (Sarto i Monteys & Aguilar, 2005), and rarely kills date or Canary palms, it has been the cause of serious damage and plant mortalities, mainly in ornamental palm nurseries, in France, Italy and Spain (Riolo et al., 2004; EPPO, 2008; Reid &
Moran, 2010; CABI, 2012). It may also increase the risk of R. ferrugineus spread by creating primary damage to palm trees, which will attract the weevil and facilitate oviposition (Dembilio et al., 2009). In the absence of suitable control methods, this insect presents a risk, particularly to nursery and amenity palms throughout the
Mediterranean region.
1.3 Current situation of palm borers in the Mediterranean Basin
The economic impact of R. ferrugineus and P. archon is completely different. R. ferrugineus is a pest of economic importance worldwide (Faleiro, 2006; EPPO, 2008a) mainly due to its impact on agricultural important crops including date, and coconut palms and ornamentally important palms such as P. canariensis. Once infested by R. ferrugineus, palms often collapse or die because of extensive damage to the meristematic tissue in the crown or to the vascular system of the palm stipe and/or offshoots. However, palms in the early stages of attack can recover if adequately managed. The amount of information available on control methods against R. ferrugineus has been increasing exponentially during recent years. These methods include physico-mechanical, biotechnological, biotechnical, chemical, and biological controls (Faleiro 2006; EPPO 2008a). Conversely, P. archon is not economically important in South America, hence there is little published information available about this pest and no specific control measures against it have been developed with the exception of a specific protective birdlime evaluated mostly in France (Bourquin, 1933;
Drescher & Dufay, 2002; Sarto i Monteys & Aguilar, 2005; EPPO, 2008b; Chapin &
André, 2010; Peltier et al., 2010; Pérez et al., 2010). The non-pest statuts of P. archon in its native habitat suggests the existence of effective natural mechanisms of regulation that remain unknown. Under European conditions, Sarto i Monteys & Aguilar
(2005) found three wild P. archon eggs with near-circular holes that could be bitten by oophagous parasitoids during emergence. Besides, the fact that P. archon needs to leave the palm stipe and fly during the adult stage, makes the early detection of this pest easier than that of R. ferrugineus.
Containment and eradication measures against R. ferrugineus have been implemented in several countries including the EU (OJEU, 2007; 2008; 2009; 2010).
Generally, official Plant Protection Agencies face difficulties in implementing compulsory measures against R. ferrugineus promptly because citizens, municipalities, nurseries, and other involved stakeholders frequently strongly oppose the cut and destroy of infested palm trees because of their economic (nurseries), touristic
(municipalities) and emotional value (citizens), and because of the high cost of this measure (Nardi et al., 2011).
Below we will discuss the pros and cons of the available control methods, mainly for
R. ferrugineus.
2. CONTROL METHODS AGAINST PALM BORERS
2.1. Plant quarantine treatments
As both R. ferrugineus and P. archon are invasive but well hidden within their host, quarantine is of high importance in controlling their spread. Both species are nowadays included in EPPO quarantine A2 list (EPPO, 2012) and although the establishment of a quarantine protocol within the EPPO region is not compulsory, it would be highly advisable. Nowadays, the EU requires complete physical protection for palms imported from infested areas during one year depending on the origin of this palms subsequent to their arrival into the EU. Only when these palms prove healthy during this confinement period, palms receive a plant passport and their movement within the EU is permitted (OJEU, 2007, 2008). However, the efficacy of this procedure remains unknown and would greatly increase if accompanied by an suitable quarantine treatment. The main procedures for eliminating arthropod pests from a commodity are classified broadly as chemical and physical treatments. Chemical treatments include fumigants, such as methyl bromide and phosphine that penetrate the commodity and are toxic to pests. Methyl bromide has been the most commonly used postharvest and quarantine treatment worldwide. However with the phasing out of ozone-depleting substances in accordance with the United Nations Montreal Protocol, it is currently forbidden as a postharvest treatment and its use is not permitted in the EU, even for quarantine purposes (OJEU, 1991). Phosphine will continue for the immediate future as an important and economically viable fumigant for widespread use against insect infestation (Bell, 2000; Donahaye, 2000). Good results obtained by Saleh et al. (1996),
Hussein (1998) and Messallam (2010) under field conditions and those reported by
Llácer & Jacas (2010) under containment suggest that low doses of aluminium phosphide can kill all stages of R. ferrugineus. Furthermore, the use of phosphine fumigation applied to infested canary palm crowns resulted in complete mortality of this pest (Llácer & Jacas, 2010). These results can be the basis for the development of a quarantine treatment against R. ferrugineus. However, further research is required to confirm that the dose obtained is not phytotoxic for palms and to explore the combination of this technique with other available physical methods (e.g. temperature).
If not damaging to palms, this treatment could be easily applied in sealed containers used to prepare and ship planting material and could significantly reduce the enormous phytosanitary risks that palm movement pose at this moment worldwide (Llácer &
Jacas, 2010).
2.2. Field sanitation and other agronomic practices
Field sanitation is one of the major components of the R. ferrugineus Integrated Pest
Management (IPM) programs for coconut palms in India (Abraham et al., 1989; Faleiro,
2006) and has also been used in relatively young date palm orchards in the Middle-
East, where infestation is most common to occur at the junction between offshoots and the mother stem within two meters of the ground (Azam & Razvi, 2001; Soroker et al.,
2012). This technique involves removing infested or dry off-shoots, removal of the infested palm tissues and pest specimens while filling the cavities with soil or pesticide- treated sawdust. The stipe is then wrapped with plastic sheets to prevent further attraction of weevils and new infestation of the wounded tree. If the damage is not too severe the palm usually recovers by filling the cavity with adventitious roots.
Sanitation has also been applied to P. canariensis, where infestation usually occurs in the crown. In this case, the technique is based on the process used for the traditional production of palm syrup in La Gomera Island (Canary Islands, Spain). This technique is adopted as last alternative in order to recover damaged palms. The objective is to clean up the entire infested canopy, by removal of nearly all the fronds, galleries and specimens, without damaging the meristematic tissues (Ferry & Gómez, 2008; Faleiro et al., 2012). Crown sanitation, is a complicated technique and requires high skills during its application. Once the palm is pruned, it is necessary to thoroughly wash the stipe. Afterwards, a spray treatment (chemical and/or biological) including a fungicide to prevent subsequent fungal infection should be applied. These treatments are repeated on a monthly basis. In some cases, the stipe of the palm is protected with a strong net with a fine mesh, not in contact with the apical zone, with the aim of reducing solar radiation and re-infestation. This method is extremely time-consuming and thus especially suited for old, high-value monumental specimens. Since infested material contains developing weevils, all the material removed from the palm should be shredded and, if possible, burned (see chapter on disposal, below). This field sanitation method has been applied to P. canariensis in urban areas of several European regions and a reduction in the numbers of infested palms has been reported in Italy (La Mantia et al., 2009; Nardi et al., 2011). In general, palm owners, both private citizens and public institutions, prefer to invest money in sanitation rather than in destruction.
However, treated palms present a high risk of asymmetric development and re- infestation has been reported to occur in more than 80 % of cases (La Mantia et al.,
2009). Moreover adverse climatic conditions (low temperatures during winter) increase mortality of treated plants (Nardi et al., 2011).
A microwave device has been designed to reduce R. ferrugineus populations (all developmental stages) directly inside the palm tree. Microwaves penetrate the wood mass and interact creating vibration and heating the water molecules that make up most organic materials, including those of internally feeding insects. Overheating and hyperthermia are used to destroy these living organisms. The range of temperatures applied in palms is presumed not to exceed 57° C. This treatment can be applied as a curative treatment. However, there are no reliable studies on the effects of these microwave treatments on palm physiology and survival. A study carried out by Massa et al. (2011) in artificially infested plants under greenhouse conditions showed that the irradiation of a palm with a 2.45 GHz magnetron produces a rapid increase of the temperature in the tissues that can reach up to 70°C in some parts of the palm tissues just 2 minutes after the radiation being switched on.
While other cultural techniques, such as irrigation or pruning, cannot be considered as control methods, their effect on R. ferrugineus and P. archon cannot be neglected and should be considered in any IPM program against these pests. Adult R. ferrugineus seem to use moist soil as temporary shelter and there are reports that flood irrigation increases infestation in date palm orchards (Aldryhim & Khalil, 2003; Aldryhim
& Al-Bukiri, 2003). The same can be true with sprinkle irrigation. Therefore, farmers are advised to prevent wetting the stipe next to the offshoots (Soroker et al., 2012).
Rhynchophorus ferrugineus is preferentially attracted by wound-emitted volatiles and oviposits in soft tissue, such as the cut ends of fronds and other wounds and cracks.
Therefore, removal of live green fronds, offshoots and other trimming practices should be followed by thorough treatment with an appropriate insecticide and preferably restricted to winter time (Dembilio & Jacas, 2011). For date palm trees, it is suggested to cover the wounds with pitch or with chemicals that efficiently seal and dry the wounded tissue (Soroker et al., 2012).
2.3. Chemical control
Many preventative and curative procedures have been designed with more or less success to limit and contain the spread of R. ferrugineus. Ideally an effective insecticide should have systemic properties to reach the pest hidden within the palm tissue, or contact activity to prevent establishment in a new host. However, in date producing areas pesticide residues in fruits is a critical issue. Both in commercial date orchards and public areas where ornamental palms are grown, concerns about the environmental pollution caused by these treatments exist (Faleiro, 2006; Dembilio et al.
2010a; Llácer et al., 2010). In addition, implementation of Directive 2009/128/EC on sustainable use of pesticides (OJEU, 2009) has restricted the available active substances authorized against both R. ferrugineus and P. archon in EU (Table 1).
Because of the concealed nature of the larvae, effective methods for the management of these pests have been difficult to develop and insecticides have to be applied frequently and over a long period of time for effective management of established populations, both of R. ferrugineus (Murphy & Briscoe, 1999) and P. archon (Nardi et al., 2009). Often, treatments were performed without sufficient information on the pesticide mobility and persistence within the palm tissue. Therefore, there is an urgent need for (1) new environmentally-safe insecticides, and (2) new delivery tools to make insecticides not only physiologically-selective but also ecologically-selective and user-friendly (Hernández-Marante et al., 2003; Dembilio et al., 2010a; Llácer et al., 2010).
Among the few active substances authorized in the EU against R. ferrugineus, neonicotinoids (e.g. imidacloprid) constitute one of the most effective insecticidal groups. Imidacloprid is a chloronicotinylnitroguanidine systemic insecticide that was first introduced into the USA in 1994. It is used as a crop and structural pest insecticide, a seed treatment and a flea-control treatment, and it works by disrupting the insect nervous system and is known from other insects to be effective by contact and ingestion (Elbert et al., 1990; Lagadic et al., 1993; Leicht, 1996). This product showed good efficacy against different stages of R. ferrugineus in both laboratory and glasshouse assays (El-Sebay, 2004; Kaakeh, 2006; Soroker et al., 2006; Llácer et al.,
2012). In a field assay, two soil injections of 2.4 g imidacloprid per year and palm successfully reduced mortality of 6-7 year-old P. canariensis palms to less than 27% compared to more than 84% for untreated control (Dembilio et al., 2010a). This product can be applied as a foliar spray, as drench, or by injection into the stem. However, the recent proof of negative impact on pollinators’ behaviour of imidacloprid and thiametoxam (Krupke et al., 2012) is questioning the use of neonicotinoids to control palm pests on a large scale. A mixture of abamectine and neem oil was tested in ornamental canary palms by drilling the palm stipe and injection at 1.5 atmospheres
(Polizzi et al 2009). In Egypt, El-Sebay (2004) used this method to test 15 insecticides against the weevil in date palm. The most effective active substances were chlorpyrifos, diazinon, phenthoate and methomyl. However, the effectiveness of these endotherapeutic treatments is still uncertain; these applications not always result in a strong mortality of R. ferrugineus larvae. Furthermore, most of these molecules are or will soon be banned in the EU (Lo Verde et al. 2008; Abbas, 2005).
Application through drip irrigation was successfully used in date palm plantations
(Soroker et al., 2005) and a palm nursery in Spain (Dembilio et al., 2010b).
Stem injection is another application method used against R. ferrugineus
(Hernández-Marante et al., 2003). Experiments carried out by El Sebay & Abbas
(2008) revealed that low pressure injection was effective and safer for palms than high pressure injection. However, there is a big debate about the pros and cons of the application of this technology to palms (Speranza, 2008). New assays aimed at disentangling how systemic products are translocated within palms and how palms heal wounded tissues could shed light on this alternative method for delivering chemicals to the target palm tissues.
Recent strategies, aimed at identifying compounds for the replacement of classical neurotoxic pesticides, have focused on exploiting naturally occurring toxins such as arthropod-derived hormones and venoms, and entomopathogenic fungi-derived insecticidal compounds (Quesada-Moraga et al., 2006; Ortiz-Urquiza et al. 2009; Ortiz-
Urquiza et al., 2010a;b; Mazet et al. 1994; Fitches et al., 2004; 2009; Quesada-Moraga
& Vey, 2004). These molecules are typically proteins or peptides showing specific antibiotic or insecticidal activities against invertebrates, and as such are ideal candidates for the development of new insecticides with improved target specificity, and therefore reduced environmental impact by comparison with conventional neurotoxic insecticides. In a complementary prospective direction, it would also be possible to target the weevil by disrupting its endosymbiotic bacteria, which contribute to their fitness and developmental success (Moran, 1998; Login et al., 2011; Faleiro et al., in press). Because this approach has not been evaluated against R. ferrugineus and P. archon, further research is needed.
2.4. Biological control
Biological pest control relies on use of natural enemies, either entomophagous arthropods (predators and parasitoids) or entomopathogenic microorganisms
(nematodes, bacteria, fungi and viruses). Few studies have been conducted on the natural entomophagous enemies of R. ferrugineus or other Rhynchophorus species
(Murphy & Briscoe 1999; Faleiro, 2006) and no data are currently available for P. archon. Conversely, entomopathogenic microorganisms, in particular mitosporic ascomycetes, have been reported to naturally regulate R. ferrugineus populations
(Dembilio et al., 2010b), and together with entomopathogenic nematodes (EPNs), have shown potential for R. ferrugineus control (Dembilio et al., 2010a; 2011). Moreover their effect is self-amplifying. In the case of EPNs, they can actively find and infect the target with its symbiotic pathogenic bacteria (Dolinski & Lacey, 2007; Lacey & Shapiro-Ilan,
2008). EPNs are safe for non-target vertebrates and for the environment, and production costs have been significantly reduced in recent times as they are mass produced in liquid media (Ehlers 2001, 2003). EPNs have been repeatedly tested against the red palm weevil (Abbas et al., 2001a; b; Elawad et al., 2007; Saleh & Alheji,
2003; Llácer et al., 2009; Dembilio et al., 2010a; Nardi et al., 2011). Although field experiments in date palms, conducted several years ago, produced inconsistent results
(Abbas et al., 2001a), recent laboratory, semi-field and field assays using Steinernema carpocapsae (Weiser) (Nematoda: Steinernematidae) with chitosan showed efficacies of around 80 % in P. canariensis (Llácer et al., 2009, Dembilio et al. 2010a) and P. theophrasti (Dembilio et al. 2011). Interestingly, the same species has proved effective against P. archon (Soto & Duart 2008, Nardi et al., 2009, Ricci et al., 2009). Trials in
France showed similar results but also pointed an important variability and the need for defining optimal application standards (Chapin & André, 2010; Pérez et al., 2010).
Because efficacies obtained by Dembilio et al. (2010) when combining treatments of imidacloprid and S. carpocapsae were not significantly different from those obtained with the same products when applied alone, the use of EPNs should be considered when developing guidelines for treatments against these species.
In addition to EPNs, entomopathogenic fungi (EPF) also fulfil all the criteria of a sound approach when looking for sustainable alternatives to chemical control. Unlike other insect pathogens, EPFs infect the host by contact, penetrating the insect cuticle.
The host can be infected both by direct treatment and by horizontal transmission from infected insects or cadavers to untreated insects or to subsequent developmental stages via the new generation of spores. Passive mechanical transmission of fungi within insect populations has been observed for various EPFs, e.g. Beauveria. bassiana, Metarhizium anisopliae and Isaria fumosorosea (Lacey et al., 1999;
Quesada-Moraga et al., 2004; 2008). These unique characters make EPFs especially important for the control of concealed insects. Some of these species have been isolated from field collected R. ferrugineus (El-Sufty et al., 2009; Sewify et al., 2009;
Tkaczuk et al 2009; Dembilio et al., 2010b) while different strains of M. anisopliae and
B. bassiana have been tested against R. ferrugineus (Gindin et al., 2006, El-Sufty et al., 2009; Sewify et al., 2009; Dembilio et al., 2010b). El-Sufty et al. (2009) obtained a mortality of 13–47 % in adult R. ferrugineus population in field assays using a strain of
B. bassiana isolated in the United Arab Emirates. Sewify et al. (2009) successfully reduced the incidence of R. ferrugineus under field conditions in Egypt using a native strain of B. bassiana isolated from a R. ferrugineus cadaver. In addition, a B. bassiana strain isolated from pupae of infested date palms in Spain proved to infect eggs, larvae and adults of R. ferrugineus (Dembilio et al., 2010b). Mortality was not the only indicator of treatment efficacy because adults of either sex inoculated with the fungus efficiently transmitted the disease to untreated adults of the opposite sex and significantly reduced fecundity (up to 63 %) and egg hatching (33 %) resulting in an overall 78 % progeny reduction. Semi-field preventive assays on potted 5-year old P. canariensis palms, with efficacies up to 86 %, confirmed the potential of this strain as a biological control agent against R. ferrugineus. Nonetheless, the few field assays reported up to now lack adequate experimental design, used low number of replicates, high natural infection rates, etc. (Güerri-Agulló et al., 2011). Therefore, it is urgent to perform sound open field experiments with B. bassiana strains to acutely explore their biocontrol potential.
The main difficulty in the implementation of the above mentioned approach is pest accessibility to these biocontrol agents. Being mostly hidden within the host tissue, a systemic distribution of the agent is highly desirable. It has been proved that fungal endophytes play an important role in protecting plants against herbivorous insects (Jallow et al., 2004; 2008) and plant pathogens (Ownley et al., 2008). Beauveria bassiana has been reported as an endophyte in a variety of plants from
Gymnospermae (Ganley & Newcombe, 2005), and Angiospermae (Bills &Polishook,
1991; Evans et al., 2003; Quesada-Moraga et al., 2006; Posada et al., 2007), including monocotiledoneous species such as maize (Bing & Lewis 1991; 1992a; b; Wagner &
Lewis, 2000) and Pinus monticola (Ganley & Newcombe 2005). In some cases these endophytic fungi have resulted in complete control of the target pest (Quesada-Moraga et al., 2006). However, the use of fungal strains of EPFs with endophytic behaviour is still a poorly explored tool for systemic protection of palms against R. ferrugineus and
P. archon.
The efficacy of the entomopathogenic bacterium Bacillus thuringiensis to control R. ferrugineus has been tested in laboratory conditions (Manachini et al., 2009). Although there were evidences indicating midgut damage and feeding inhibition among larvae that survived the treatments, results showed that the activity of B. thuringiensis against
R. ferrugineus immature stages was low.
Overall, to improve R. ferrugineus control by entomopathogenic microorganisms, a more deep investigation on the interaction between them and R. ferrugineus immune system is required. Studies, such as that of Manachini et al. (2011), who studied the response of R. ferrugineus larval hemocytes to infection by B. thuringiensis and
Saccharomyces cerevisiae could contribute to this final goal.
2.5. Control methods based on the use of semiochemicals.
Semiochemicals, which are often a key that guides insect behaviour, play a well- known role as specific and environment-compatible tools in pest management. First of all for monitoring the pest population allowing adjustment of management practices to the fluctuations in pest population and distribution patterns, but also directly for control.
In the latter case they can be used in various ways: either for mating disruption or combined with insecticide and/or traps. The commonly known methods are: mass trapping, attract-and-kill, attract-and-infest, and push-pull. The latter, combines both attractants such as pheromones and host attractants/repellents, which orientate the target insects away from the host towards the control, either biological or conventional, agents (Ridgway et al., 1991; Bjostad et al., 1993; El-Sayed et al., 2006; Oehschlager,
2006; 2009; Cook et al., 2007; Witzgall et al., 2010). Although these concepts are not new, positive results and worldwide application are not the rule to date. This is due to the complexity of developing strategies, which are economically profitable only in the mid or the long term, and basically depend on many biological and technical parameters pertaining to the target pests, semiochemicals, traps, and insecticide/biocontrol agents. Overall biological information indicates mass trapping suitability mainly for beetles and mating disruption and attract-and-kill for moths (El-
Sayed et al., 2006, Witzgall et al., 2010).
In R. ferrugineus (4S,5S)-4-methylnonan-5-ol and 4-methylnonan-5-one were described as aggregation pheromone (Hallet et al., 1993). Currently these compounds are used in monitoring and mass trapping traps combined with molasses, dates, or palm stems in order to improve their efficiency. Ethyl acetate as one of the kairomone components (El Sebay, 2003) has been used in order to improve the attraction like in other palm weevils such as R. palmarum (Jaffe et al., 1993). However, its efficiency as kairomone in R. ferrugineus is not clear because it has not increased trap captures in some trials in Spain (Alfaro et al., 2011). It is necessary to find new synthetic kairomones that improve R. ferrugineus attraction to increase the monitoring/control efficiency. A recent study carried out by Guarino et al. (2011) showed that palm esters such as ethyl acetate, ethyl propionate, ethyl butyrate, ethyl isobutyrate and ethyl lactate perform strong EAG activity on R. ferrugineus adults. The same study showed that the application of more than one of these compounds in the traps can enhance the number of adult catches, suggesting that the blend of esters mimics more strongly the palm odour than each of the individual esters alone (Guarino et al., 2011).
Mass trapping of adult R. ferrugineus with food-baited and later with pheromone/food-baited traps has been recommended as a component of the R. ferrugineus-IPM programme since 1975. Some successes with this approach, enforced by female biased captures, are reported in coconut and date palm plantations (India:
Faleiro et al., 2006 and Israel: Soroker et al., 2005, respectively). Moreover in Italy, mass trapping used within IPM strategies against R. ferrugineus in urban areas has showed positive results (Lo Bue et al., 2010; Nardi et al., 2011). In the city of Palermo, a two-year project (2009-2010) of R. ferrugineus mass trapping was carried out by distributing 500 traps baited with pheromone and kairomone in public and private gardens. In total, these traps caught about 140,000 R. ferrugineus adults.
Various trap densities for mass trapping have been suggested (El-Saeby, 2004;
Faleiro, 2006). While implementing traps is labour intensive and often sub-optimal as already stated, there is concern about endangering palms by inappropriate trap setting, excessive trap densities or setting traps too close to palms (Rochat 2006). Moreover, as in the case of monitoring, the density and the distribution of traps are largely pragmatic and density limited due to economic reasons rather than based on scientific data.
Improvement of traps is necessary to increase the efficiency of mass trapping or monitoring techniques. Traps of dark colour seem to be the most attractive to R ferrugineus (Hallett et al., 1999) and new designs were developed in 2010 (Alfaro et al.,
2011). Additional improvements are necessary to increase the ratio of weevils caught vs. weevils attracted, avoiding the infestation of healthy palms, adjacent to the traps, by long distance attracted weevils. In the case of P. archon, there is limited information published in relation to the use of semiochemicals for its management (Frérot & Ollivier, 2006; Sarto i Monteys et al.,
2012; Delle-vedove et al., 2012). Further research is therefore urgently needed to develop management approaches based on the use of these substances.
2.6. Disposal
Due to the ability of R. ferrugineus to develop in dead palms long after the palm is uprooted and their apical meristem is dead, the development and implementation of appropriate disposal protocols is critical. Any disposal protocol needs to meet the objectives of totally destroying the pest population in all its developmental stages within the palm, but also making the palm tissue unsuitable for further infestation. Existing disposal protocols, including recommendations about palm preparation, removal and transport to designated areas, actual ways of destruction and disposal at final site are often problematic and/or unrealistic. In principle, all the material removed from the infested palm and from healthy palms in infested areas, should be shredded and, if possible, burned. Palm stipes maintain their humidity and tissue freshness for months and are not easily burned. Fumigation is effective, but its residual activity is unknown.
Shredding the palm requires heavy complex machinery which is usually expensive and unavailable. Furthermore, inadequate transportation of infested material to designated areas for shredding may contribute to the spreading of the pest.
3. CONCLUSIONS
Successful control and containment of the invasive palm borers R. ferrugineus and
P. archon is a complicated operation, especially if environmental issues need to be considered. Substantial effort conducted over the years worldwide, suggests several control avenues, but large gaps of knowledge still exist before effective and environmentally acceptable control measures can be implemented. The fact that most of the pests' life cycle passes concealed within the palm tree limits effective delivery of pesticides, while the lack of effective early detection methods, further complicates the situation. Under these circumstances, preventive integrated management currently appears to be the best approach.
AUTHOR CONTRIBUTIONS. JA Jacas and O. Dembilio organized the document and wrote the manuscript. S. Colazza, F. Karamaouna and D. Rochat provided the information about authorized products in Italy, Greece and France, respectively. V.
Navarro-Llopis and D. Rochat contributed to the section dealing with semiochemicals, as E. Quesada-Moraga did with that dealing with entomopathogens. In addition to these authors, N. Audsley, Y. Cohen, N. Isidoro, D. Kontodimas, E. Peri, P. Riolo and
V. Soroker critically commented the manuscript and actively contributed to its final form.
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Table 1. Active substances, doses, and application techniques authorized against Rhynchophorus ferrugineus and Paysandisia archon in the EU (September 2012).
Active substance Country Dose of Application technique/s Additional information commercial specialties Abamectin 1.8 EC (W/V) 1Spain 20-80 ml per palm Stem injection. One single application or two (half dose) Authorized in public at 15-45 day interval. Application by authorized gardens companies only. 2Greece 20-80 ml per palm Crown or Stipe injection. Two applications at 15-45 day Against R.ferrugineus only; interval. Application by authorized companies only. Authorized under expert Additionally: crown or Stipe injection are authorized surveillance; restricted authorization 3Italy 25 ml per palm Stipe injection Authorized in public gardens, nurseries and open field Cifluthrin 2.4 % + 3Italy 120 ml hl-1 Foliar spray Authorized in public Imidacloprid 7.1 % EC gardens, nurseries and open field
Chlorpyrifos 48 % EC 1Spain 150 -200 g hl-1 Foliar spray (W/V) Chlorpyrifos metil 22,1% 3Italy 500 ml hl-1 Foliar spray Authorized in public EC gardens, nurseries and open field
Clothianidin 50% WG 2Greece 15 -20 g hl-1 Foliar spray; Applications at 15-20 days interval. (W/W) 10 g ml1 per palm Stipe injection. Applications at 15-20 days interval. Authorized under expert 30 g 50ml1 of Authorized use for palms in nurseries. Spray of the surveillance; restricted water per 50 m2 ground area under the foliar. Applications at 15-20 days authorization interval. Diflubenzuron 150 g l-1 SC 4France 66 ml hl-1 Spray located on top 50 cm of stipe and bases of Against P. archon only rachis. Authorized in public gardens and nurseries Imidacloprid 20 % OD 1Spain 50-75 ml hl-1 Foliar spray. Stipe injection authorized in (W/V) 8-10 l ha-1 Drench application allowed in nurseries only. Maximum public gardens of two applications 30-40 days apart per year. Stipe injection every 45-55 days from March to 4-10 ml per palm November. Injection 1.5-2.0 m below the crown by authorized companies only. Imidacloprid 20 % SL 1Spain 50-75 ml hl-1 Foliar spray. Authorized in public (W/V) 8-10 l ha-1 Drench application allowed in nurseries. Maximum of gardens two applications 30-40 days apart. 4-10 ml per palm Stipe injection every 45-55 days from March to November. Injection 1.5-2.0 m below the crown by authorized companies only. 2Greece 50-75 ml hl-1 Foliar spray. Also authorized for preventive use in Against R. ferrugineus only; nurseries (maximum of two applications). authorized under expert surveillance; restricted 8-10 l ha-1 Drench application for palms of low height. Maximum of authorization two applications at 30-40 days interval. 4-10 ml per palm Crown or Stipe injection. Maximum of two applications at 45-55 days interval. Additionally: foliar spray, drench application and crown or stipe injection are authorized Spray authorized for treatment of palm parts for disposal. Imidacloprid 20 % SC 4-7France 35 ml hl-1 Foliar spray and drench application; 2 to 8 applications Against Rhynchophorus between March and November separated by 3 to 4 ferrugineus only weeks in combination with application of entomopathogenic nematodes
Soil irrigation for palm in containers in nurseries only 0.25 l hl-1 twice a year at 6-month interval. 2 ml * 4 holes per Stipe injection 4 times a year as in Spain, in selected Authorized in public palm per injection experimental areas by authorized companies only. gardens and nurseries (under conditions) Lambda cyhalothrin 4France 15 ml hl-1 Foliar spray 100 g l-1 CS Authorized for treatment of aerial parts of ornamental trees and shrubs against miscellaneous and xylophagous pests Phosmet 50 % WP (W/V) 1Spain 150-250 g hl-1 Foliar spray Spinosad 120 g l-1 EC 4France 0,3 l hl -1 Spray located on top 50 cm of stipe and bases of Against Paysandisia archon rachis; 2 applications with a maximum of 3 per year. only; authorized in public gardens and nurseries Thiametoxam 25% WP 1Spain 40 g hl-1 Foliar spray Authorized in public (W/W) 400 g ha-1 Maximum of two applications 7-14 days apart gardens 400 h ha-1 Drench application. Maximum dose per application 5-20 g per palm Stipe injection 2Greece 40 g hl-1 Foliar spray. Maximum of two applications at 7-14 days Against R.ferrugineus only; (Max 400 g ha-1 interval. Also authorized for preventive use in nurseries authorized under expert per application) (maximum of two applications). surveillance; restricted Drench application at palms of low height. Maximum authorization. 5-20 g 20-200 ml1 one application. per palm Crown or Stipe injection. Minimum dose for low palms– maximum dose for high palms. Maximum of two applications at 7-14 days interval. Additionaly: Foliar spray, drench application and crown or stipe injection are authorized. Spray authorized for treatment of palm parts for disposal. Sources: 1MAGRAMA (2012). Registro de Productos Fitosanitarios. http://www.magrama.gob.es/es/agricultura/temas/medios-de-produccion/productos- fitosanitarios/registro/menu.asp (July 2012) 2MARDF (2012). Data base of Authorized Plant Protection Products (September 2012) 3Assessorato Regionale delle Risorse Agricole e Alimentari. http://www.regione.sicilia.it/agricolturaeforeste/assessorato/ServizioFitosanitarioRegionale.htm (March 2012) 4MAAPRAT (2012). Le catalogue des produits phytopharmaceutiques et de leurs usages, des matières fertilisantes et des supports de culture homologués en France. http://e-phy.agriculture.gouv.fr/. (September 2012) 5MAAPRAT (2009). Arrêté du 5 juin 2009 relatif à l’utilisation de traitements dans le cadre de la lutte contre Rhynchophorus ferrugineus (Olivier), Rhagoletis completa (Cresson), Paysandisia archon et les larves d’Hoplochelus marginalis et d’Alissonotum piceum. 6MAAPRAT (2010). Arrêté du 21 juillet 2010 relatif à la lutte contre Rhynchophorus ferrugineus (Olivier). 7MAAPRAT (2012).Note de service DGAL/SDQPV/N2012-8071 pour la mise en œuvre du dispositif expérimental concernant l’injection dans le cadre de la lutte obligatoire contre le charançon rouge du palmier.