Cord 2006, 22 (1)
Cocoa pod borer threatening the sustainable coconut-cocoa cropping system in Papua New Guinea
S. P. Singh¹ and P. Rethinam¹
Abstract
Cocoa pod borer Conopomorpha cramerella Snellen is an important pest of cocoa. Its recent invasion of cocoa in Papua New Guinea is threatening the sustainable coconut-cocoa cropping system. C. cramerella occurs only in South-East Asia and the western Pacific. It has been the single most important limiting factor to cocoa production in Indonesia, Malaysia and the Philippines. C. cramerella attacks cocoa, Theobroma cacao; rambutan, Nephelium lappaceum; cola, Cola acuminate; pulasan, Nephelium mutabile; kasai, Albizia retusa, nam-nam,Cynometra cauliflora; litchi (Litchi chinensis); longan (Dimocarpus longan) and taun, Pometia pinnata. The possible mode of its spread is through seed pods/fruits carried from previously infested regions. However, there is possibility of local adaptations of rambutan-feeders or nam-nam-feeders to cocoa.
Females lay their eggs (50-100) on the surface of the unripe pods (more than five cm in length), which hatch in about 3-7 days and the emerging larvae tunnel their way to the center of the pod where they feed for about 14-18 days before chewing their way out of the pod to pupate. The pupal stage lasts 6- 8 days. The larval feeding results in pods that may ripen prematurely, with small, flat beans, often stuck together in a mass of dried mucilage. The beans from seriously infested pods are completely unusable and in heavy infestation over half the potential crop can be lost.
Over four dozen species of natural enemies (parasitoids, predators, and entomopathogens) attack eggs, larvae, pupae and adults of C. cramerella. Egg parasitoids Trichogrammatoidea bactrae fumata and T. cojuangcoi, egg-larval parasitoid Chelonus chailini, predatory ants particularly Iridomyrmex spp., Dolichoderus thoracicus and Anoplolepis spp. are commonly recorded.
The most effective control methods are frequent harvesting, destruction of ripe pods and husks to prevent pupation in the field and selective spraying of resting sites with deltamethrin or cypermethrin or carbaryl. Pheromone mixtures have potential for use in traps as a quarantine surveillance technique and for control. Encouragement of predatory ants and parasitoids, and use of egg parasitoid T. bactrae fumata are potential biological control techniques. Pod sleeving with bags have been able to control cocoa pod borer in smallholders garden but not in larger plantations. Some of the clones have shown resistance against the cocoa pod borer.
Success achieved in the project-Sustainable Cocoa Extension Services for Smallholders (SUCCESS) implemented in Indonesia in conjunction with the American Cocoa Research Institute and BCCCA, a British counterpart, ACDI/VOCA could be emulated for C. cramerella management, which included training of farmers to adopt frequent harvesting, pruning, sanitation and fertilization.
Key words: Coconut, cocoa, cocoa pod borer, Conopomorpha cramerella, rampasan & harvesting, natural enemies, biological control, pheromone trapping, management.
1 Asian Pacific Coconut Community, Jakarta, Indonesia
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Introduction Cocoa pod borer (CPB)Conopomorpha (=Acrocercops = Gracillaria = Zarathra) Coconut palm known as ‘Tree of Life' cramerella Snellen (Lepidoptera: and cocoa tree belonging to the genus Gracillariidae) is known by several other Theobroma, meaning 'food of the Gods' in common names such as cocoa pod borer, Greek are essentially crops of small farmers. cocoa moth, rambutan borer, nam-nam In Papua New Guinea (PNG) coconut-cocoa borer, javanese cocoa moth, polilla javanesa is a popular cropping system, cocoa grown del cacao (Spanish), teigne javanaise du as companion crop in coconut under the cacaoyer (French) Motte, Javanische Kakao shade. Copra and cocoa are major export (Germany), and hama penggerek buah kakao commodities. Recently Dr. S. P. Singh (Bahasa- Indonesia) (CABI,2002). Project Coordinator IPM, Asian Pacific Coconut Community visited Cocoa and C. oceania, C. sinensis and C. litchiella Coconut Institute, Tavelo and National are three congeneric species found in South- Agricultural Research Institute (NARI), East Asia which are very similar to C. Keravat, Papua New Guinea (PNG). He met cramerella. They can be differentiated from Dr. John Moxon, Team Leader, NARI and C. cramerella by wing pattern and male and visited fields around these two Institutes. Dr. female genitalia (Bradley, 1986). Moxon informed about the severe incidence of cocoa pod borer in some of the blocks Strains belonging to NARI. The incidence varies from one to hundred per cent in different C. cramerella was collected from cocoa blocks. The pest was detected for the first and rambutans in the field at four sites in time in March 2006. The staff of NARI is Malaysia in 1984 and analysed by making vigorous efforts to eradicate the polyacrylamide gel electrophoresis. pest. It may be mentioned here that in PNG Hexokinase was polymorphic at one site and and several other countries combination of fluorescent esterase at all four sites. Two coconuts with cocoa is common farming zones of malate dehydrogenase (MDH) were system. But this system is now threatened by observed: c-MDH was monomorphic in all the advent of cocoa pod borer four populations while MDH-1 was (Conopomorpha cramerella Snellen) in polymorphic in three populations (Tan et al., PNG. The work conducted on C. cramerella 1988). Peptidase 2 was polymorphic in the was reviewed earlier (Lim et al., 1987a,b; Sabah sample while alpha-GPDH [glycerol- Ooi et al., 1987). This article provides some 3-phosphate dehydrogenase] was basic information on C. cremerella coupled polymorphic in the other sample. This with its management options. Bibliography differentiation may reflect geographical is also provided. variation of the same species (Saahlan et al.,
1985). Although 30 enzymes and general Taxonomy and nomenclature proteins were successfully demonstrated on zymograms, none could be used as The earliest damage caused by cocoa diagnostic markers to separate the two pod bore was noted by Jansen (1860), which biotypes (Muhamad et al., 1989). was first taxonomically described at the beginning of the 20th century as Host plants Acrocercops cramerella (Snellen, 1904). Subsequently the generic placement of this Indigenous sapindaceous and species has been revised to Conopomorpha leguminous species (rambutan, pulasan, cramerella (Bradley, 1985), which is now kasai and nam-nam) appears to be the widely accepted. original hosts of C. cramerella as they are indigenous to the region to which the moth
77 Cord 2006, 22 (1) is restricted, whereas cocoa is a recently cocoa expansion in the late 1980's and early introduced species(CABI, 2002) and the pest 1990's.Approximately 20% of all cocoa in appears to have shifted to this perennial Indonesia could be infected by C. host. Rambutan and nam-nam produce fruits cramerella. In May 1998 Landell-Mills with pulp similar to cocoa (Wood, 1980). estimated the reduction in cocoa production However, they tend to be more seasonal than potential by cocoa pod borer in Southeast cocoa and so may not provide the right Asia at 40,000 tonnes. The estimated losses conditions for permanent establishment. in dollars due to cocoa pod borer This could limit populations in local areas approached $20m in 1998. The cocoa pod (CABI, 2002). borer has been the single most important limiting factor in cocoa production in C. cramerella infests cocoa, Theobroma Indonesia. Cocoa pod borer infestation has cacao; rambutan, Nephelium lappaceum; severely affected the quantity and quality of cola, Cola acuminate; pulasan, Nephelium cocoa production and farmer income. The mutabile; kasai, Albizia retusa, nam- cocoa pod borer is prevalent in all producing nam,Cynometra cauliflora; litchi (Litchi areas, and is causing an income loss of chinensis); longan (Dimocarpus longan) and approximately 40% to individual farmers, or taun, Pometia pinnata. over $400 per hectare per year. With limited control, production losses in infested areas are significant (between 20% - 50%) for Damage smallholders (with average farm size of 1.5
ha) who rely on the year-round cash income The larvae of C. cramerella bore into provided by cocoa. For Sulawesi alone, the soft tissues in the pod wall, which estimated losses caused by cocoa pod borer provide the nutrients for the development of are approximately US$150 million per year, the beans. Once inside it is safe from almost all to smallholder cocoa farmers. In insecticides for most parts of its life. The light infestations the loss may be slight, but attacked pods ripen prematurely, and control efforts may be needed to prevent produce small, flat beans. In heavy higher infestation from developing. infestations, the beans are often stuck together by mucus and in this condition; they have no market value. In heavy Pest status and damage identification infestation over half the potential crop can be lost. C. cramerella has become the most important insect pest of cocoa in many parts When <60% of harvested cocoa pods of its distribution.Quarantine and showed internal attack, yield loss was <5%, surveillance for C. cramerella remains a but with 90% of pods attacked yield loss problem in areas of South-East Asia in was about 40%. In Sabah, Malaysia, annual which the pod borer does not presently yield losses ranged from 22 to 54%. Losses affect cocoa (Thailand and Sri Lanka). for the whole estate were estimated from Rambutan or nam-nam borers are already estate records, and for the same years ranged known from Thailand, Sri Lanka and New from 42 to 49% (Day, 1989).The number of Britain (Papua New Guinea). C. cramerella hardened beans and the number of beans in has also been found from unspecified hosts, the pod were the most vital contributing in Western Samoa and the Northern parameters accounting for more than 80% of Territory of Australia early in the 20th the variation about the mean in the observed century (Mumford, 1986). Live borers can bean loss (Davis, 1989b). travel long distances within rambutan fruit: healthy C. cramerella pupae were found on Numerous outbreaks of C. cramerella Thai rambutans in a supermarket at Riyadh, have occurred in Indonesia following the Saudi Arabia in 1986 (CABI, 2002).
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approximately 300,000 cocoa farmers, so Inspection methods are usually based on also in Bali and Papua. assessing pods for larval damage. Exit holes or larval debris on the pods are a clear It is possible that a cocoa form of C. indication of the presence of the pest. Within cramerella was introduced into Sabah, East a crop, uneven or premature ripening of Malaysia during the post-1977 'cocoa boom', pods, recognised by a yellowing of the with pods brought from Indonesia or the surface, is also a good indication of internal Philippines. A similar introduction from a feeding activity by the larvae. previously infested area may have occurred in Malacca and Negeri Sembilan in West Once pods are opened, characteristic Malaysia prior to the discovery of C. tunnels caused by larvae and their presence cramerella in those states in 1986. However, within such tracts is confirmatory evidence in both cases it is also possible that there of the pest's presence. Extensive feeding were local adaptations of rambutan-feeders within the pod commonly leads to individual or nam-nam-feeders to cocoa (CABI, 2002). beans sticking together, which often means that bean extraction from the pod is difficult. The infestation in Sabah spread rapidly Pupae can be found on the pods or on leaf from Tawau (south-east Sabah) across the litter and this is often a primary source of entire state during a 3-year period (Tay, pest infestation. 1987), and it soon spread to Sarawak. C. cramerella was found infesting cocoa pods for the first time in two plantations in Distribution Sarawak, Malaysia, in 1983-84 (Kueh et al.,
1985).The initial infestations discovered in C. cramerella occurs only in South-East West Malaysia were contained for several Asia and the western Pacific, and its origin years, thanks to vigorous quarantine efforts within this area has been the subject of based on experience from east Malaysia speculation since the turn of the century (Chin, 1987; Ling et al., 1987). (Mumford, 1986). Cocoa is not the original Unfortunately scattered outbreaks began to host, since it has been introduced into the appear in other parts of West Malaysia region to which the moth is restricted. during the first half of 1988 and it was not
possible to extend this vigorous containment C.cramerella is a major pest of cocoa in and eradication effort to a wider area (CABI, Indonesia (Wardojo, 1980a).After the 2002). appearance of cocoa pod borer at Manado in the 1840's the cocoa industry in North The spread of C. cramerella northwards Sulawesi declined rapidly (Toxopeus and in Peninsular Malaysia is described, Gieserger, 1983). The industry began to following the arrival of the pest in major move elsewhere, to the Philippines and to cocoa growing areas of Kuala Selangor and Java. Long distance movement of the cocoa Hilir Perak. The pest is now widespread in pod borer must almost certainly have taken cocoa-growing areas with the exception of place through the movement of infested those in Terengganu and Kelatan. The mode pods, as there is no indication that moths can of dispersal of the pest is considered as man- fly long distances. In about 1880 cocoa was assisted dispersal, it is suggested that a small introduced into Central Java on a plantation number of migrating adults move to a new scale to replace coffee (van Hall, 19i9). area and reproduce, forming an 'epicentre'.
Their offspring are spread by air currents to I n 1992, cocoa pod borer reemerged in the surrounding region. In a survey in an Sulawesi in Toli Toli (Central Sulawesi). 'epicentre' area, on average of 90% cocoa Currently it has a spread all over Sulawesi, pods were infested (Zam and Azhar, 1992). present on almost 100% of the farms of
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In Asia it is distributed in Brunei through or tunnels along the surface of the Darussalam, China, Taiwan (China), sclerotic layer for up to several centimeters Indonesia (Bali, Papua, Java, Kalimantan, before penetrating the husk. Once inside the Maluku, Sulawesi and Sumatra), India, pod, tunnelling becomes less directional, the Malaysia (Peninsular Malaysia, Sabah and inner surface of husks, pulp of beans and Sarawak), Philippines, Saudi Arabia, Sri placentae being randomly tunnelled into and Lanka and Thailand. Its earlier records from fed upon. In younger pods, early-instar Oceania, Australian Northern Territory, larvae could penetrate the testa of Papua New Guinea and Samoa from other developing beans, and in some cases hosts never mentioned it as a serious pest of cotyledons could be attacked. Such feeding cocoa (CIE, 1984; CABI, 2002). causes scarification and subsequent sticking of the beans. Damage to the funicles of pods Biography often results in beans being malformed and under-sized, significantly reducing quality The small brown adult moth with bright and thus the value of the processed beans. yellow patches at the tips of the forewings is Feeding in pods also causes them to yellow about 7 mm in length with a wingspan of or ripen unevenly and prematurely, about 12 mm. The moths have very long confusing ripeness standards for harvesting antennae which are swept backwards in their (CABI, 2002). natural resting position (CABI, 2002). The entire larval stage takes 14-18 days The moths are most active at night. A to complete, with 4-6 instars. Late-instar female can normally produce 50-100 eggs in larvae are about 10 mm long and creamy her lifetime. During the day, adult moths coloured while still inside the pod, but normally rest underneath horizontally greenish after they emerge from the pod. inclined branches of the cocoa tree, and their The larvae tunnel out through the pod wall cryptic coloration blending with the resting to pupate, leaving an easily identifiable exit place makes them very difficult to spot. hole (CABI, 2002). Adult longevity is 1-30 days, but adults generally live for about a week (CABI, Pupae lie beneath a light-brown 2002). waterproof silken membrane tightly drawn over a depression on a pod surface or leaf. The female may lay eggs anywhere on Once outside the pod, larvae crawl or lower the surface of host-plant pods more than 5 themselves by a silk thread to a suitable site cm in length although there appears to be for pupation. The pupation site could be in a some preference for primary or secondary furrow of the pod, or green dried leaves and furrows of pods. Eggs are yellow-orange, other debris. Once at this site the larvae spin flattened and just visible to the naked eye oval-shaped cocoons and enter a short (0.5 x 0.2 mm). Rectangular indentations prepupal stage before forming obtect pupae. cover the surface of the egg. On hatching, The pupal stage normally takes 6-8 days to eggs become translucent, the shell being complete. It is also at this stage that the pest whitish but darkened by faeces within is most likely to be transported by man to (CABI, 2002). other cocoa-growing areas through movement of pods/fruits, leaves and other First-instar larvae are translucent white objects to which pupae are attached. in colour and about 1 mm long. On hatching, Unnoticed transport of rumbutan with pupae the first-instar larva tunnels through the is the example of record of this pest in Saudi floor of the egg shell and bores Arabia. In total, the entire life cycle takes perpendicular to the pod surface until it one month to complete. reaches the sclerotic layer of the husk. At this point the larva either tunnels directly
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The adult moth is small, well attached to leaves or ground litter, including camouflaged and difficult to locate in the discarded wrappings. The mean duration of farm, thus making them difficult to control the egg, larval and pupal stages were 3.3, 8.8 with chemical or bio control agents. and 7 days, respectively. The longevity of the adult was approximately 6-8 days. The In the laboratory in Sabah, Malaysia, difference in the abdominal tip or labial palp the egg, larval and pupal periods averaged of adults was used to distinguish the two 3.28, 17.64 and 6.68 days, respectively, and sexes. The sex ratio of male and female was there were estimated to be 4 larval instars. 1:1(Hwang and Hsieh, 1989). The life-span of adults averaged 4.5 days in the laboratory, but under field conditions it Semisynthetic diet averaged 3.21 days for males and 5.14 days for females. The sex ratio (males to females) A semisynthetic diet for C. cramerella was 1:1.2 in the laboratory and 2:1 in the was developed in order to test the toxicity of field. The preoviposition period averaged experimental compounds to larvae (Furtek et 2.96 and the oviposition period 2.72 days, al., 2001) as well as to multiply host specific and the number of eggs laid averaged 61.00. parasitoids. The mean hatch was 69.64% in the Sampling technique laboratory and 95.12% under field conditions. The eggs were laid singly, A sampling scheme called the stratified mainly in the furrows of the middle and top systematic technique was developed which of the cacao pod, and up to 35 eggs were stratifies a cocoa field into 6 strata and found on a pod (Lim et al., 1982). systematically samples the centre of 6 trees
of each stratum. This approach gave more The eggs showed logarithmic representative results than random sampling distributions with mean densities ranging (Davis, 1989a). from 0.75 to 3.338 eggs per pod. Iwao's
Mean Crowding Index and Taylor's Power Field Monitoring/Economic Threshold Law indicated consistent positive Levels relationships between mean and variance of number of eggs per pod and their parameters In preliminary studies aimed at finding were used to develop a sequential sampling an economic threshold of infestation, below scheme which should be useful for cocoa 50% infestation gave less than 5% yield loss growers (Azhar and Long, 1991). and no detectable reduction in bean size.
Losses increased rapidly when infestation C. cramerella is an important pest of exceeded 60%, and at 80-90% infestation litchi (Litchi chinensis) and longan yield losses could exceed 30% and bean size (Dimocarpus longan) trees in Taiwan could be reduced by 10% (Day, 1983a,b; (Hwang and Hsieh, 1989).C. cramerella was 1989). active in litchi and longan orchards during the fruit developing season (April to Damage function for C. cramerella September) (Hwang and Hsieh, relating the loss of yield to percentage 1989).Studies on the biology of C. infestation in harvested pods was studied cramerella collected from this ecosystem (Day,1985). The function indicated almost revealed that the mean number of eggs no loss with infestations up to approximately deposited by females was 114.1 and the rate 60%, and rapidly increasing losses with of egg hatchability was 97%. Shortly after higher infestations (over half the crop lost in hatching, larvae bore into the fruit to feed on very heavy infestations). While this is a the seed or fruit pulp, which caused the fruit reasonably practical way of estimating to drop. When fully grown, larvae left the damage, the relationship is inevitably feeding site to pupate in a flat cocoon
81 Cord 2006, 22 (1) inaccurate at higher infestation levels. Low effort into even better routine harvesting and infestations (20-40%) consist of a small maintenance may obviate the need for the proportion of pods each with only one larva census (CABI, 2002). inside, whereas high infestations (80-100%) could have many pods with 2, 3 or up to 30 An important problem with census larvae inside. Percentage infestation does systems is, understanding the significance of not give a good measure of the actual the results from individual census rounds. C. number of larvae in the pods at high cramerella losses result from a combination percentages, while it does at low of numbers of larvae and numbers of pods at percentages. However, for setting priorities an attractive, susceptible stage of maturity for control action this is probably adequate: (the last 6-8 weeks before ripeness, as a infestations high enough to be in the general rule). The infestation in a cohort of inaccurate area would certainly need control mature pods reflects C. cramerella attack anyway, while at lower infestations when over one and half to two generations of there is more doubt about the immediate moths, it is not a point sample. Furthermore, need for control, the function appears to be a 50% infestation one month after the peak reasonably accurate (CABI, 2002). will surely rise over the next 2 months, causing higher proportional damage but on a An absolute measure of C. cramerella falling crop, while a 50% infestation 6 damage can only be obtained by comparing weeks before a peak will almost certainly the yields over an entire cropping period, fall, as pod numbers are likely to increase looking at the overall tonnage produced and faster than C. cramerella populations in especially at the dry bean kg/harvested pod normal crop cycles. Therefore, the ratio, which shows the proportion of interpretation of any single census figure discarded pods and beans across the (percentage infestation) depends on a cropping period. It is important to look at prediction of the numbers of pods reaching the whole cropping period because losses for maturity over the following 3 months. This the season are made up of a mix of high means that in addition to the fairly simple proportional losses on the low crop and task of monitoring percentage infestations, lower proportional losses in the high crop the pod-age structure should also be (CABI, 2002). monitored, which is not as easy (CABI, 2002). Many estates have tried to develop C. cramerella census systems to estimate losses Pheromone traps provide another and to plan control programmes. The most possible form of monitoring, but they only common form has been to establish a grid of provide a relative measure of populations, as marked sample trees or rows in each block the range of attraction is unknown and which are monitored regularly for variable. The problem of two races of C. infestation (clean, infested and very highly cramerella greatly reduces the value of infested pods are recorded). Control, usually pheromone traps for estimating numbers of pod or branch spraying, would then be moths, as it is not clear whether both types applied to blocks either over a preset are equally attracted, nor whether other threshold or up to a predetermined number races remain undetected. Pheromone traps of blocks in priority set by the census results may, however, be useful for quarantine (for instance, the worst 20%). Estates with detection in uninfested areas (CABI, 2002). census systems almost always obtained better control than those without, but an Natural enemies and biological control estate manager who can organise a good census plan is also likely to be harvesting In Sabah, Malaysia, two pupal more frequently and spraying well- parasitoids, one egg parasitoid and 22 maintained trees. Putting some of the census
82 Cord 2006, 22 (1) species of predators are reported (Lim et al., actually due to the small 'sugar' ants, 1982). Iridomyrmex spp., which are much more difficult to augment or manipulate (Day, Over 20 parasitoids have been listed 1985). Ant predation was almost constant at from Malaysia, the Philippines and Sri around 40% of pupae each month Lanka (Ooi et al., 1987).The egg parasitoids throughout a 4-year period (Day, 1985). included Trichogrammatoidea bactrae Predation levels were independent of fumata and T. cojuangcoi; larval and pupal C. cramerella pupal density, as would be parasitoids recorded included Apanteles sp., expected from generalist predators. Bracon sp., Ceraphron aguinaldoi, Chelonus chailini, Chrysonotomyia, In Malaysia, Dolichoderus thoracicus in Elasmus sp., Goryphus fasciatipennis, G. managed and dense canopies of cocoa trees javanicus, G. mesoxanthus, Nesolynx was present in 6.0 and 6.4%, respectively, thymus, Ooencyrtus ooii, Paraphylax sp., D. thoracicus was observed to be associated Paraphylax fasciatipennis, Pediobius soror, with Cataenococcus hispidus and Ebhul Phanerotoma sp., Photoptera erythronota varium, and it is suggested that the numbers and Tetrastichus sp. The pathogens recorded of the formicid may be dependent on the included - Beauveria bassiana, numbers of these Hemiptera present (Azhar, Paecilomyces fumosoroseus and 1992). Paecilomyces lilacinus. Entomophilic nematode Steinernema sp. has also been Cocoa is commonly grown under partial recorded. shade provided by coconut palms and others. Coconut palms clearly favour the Ooencyrtus ooii sp. nov., an encyrtid black cocoa ant. Where the ant is well prepupal parasitoid of C. cramerella, is established, active trails can be seen running described from Malaysia, may be of some between the cocoa trees and the crowns of importance in the natural control of this pest coconut palms, even those more than 18 m of cocoa in Malaysia (Noyes, 1991). tall. More importantly, the coconut palm is an excellent source of shelter for the ant. Two species of parasitoids, The coconut palm has huge leaves or fronds, Phanerotoma sp. and Apanteles sp., were and each leaf consists of many leaflets. identified from pupae of C. cramerella. Two Aggregations of D.thoracicus can be found other parasitoids Tetrastichus sp. and under some of these leaflets. When a leaf Elasmus sp. were reared from C. cramerella becomes old and drops from the palm, the larvae (Hwang and Hsieh, 1989). drying leaflets form long tubes; D.thoracicus loves to nest in these tubes. Natural parasitism is detected at Strong colonies of D.thoracicus can be significant levels only at the peak-crop found nesting in the cocoa leaf litter if the period when C. cramerella numbers are layer is thick. highest. The knowledge that D. thoracicus likes The most studied natural enemies are to nest in the coconut leaflet tubes and cocoa predatory ant Dolichoderus thoracicus and leaf litter, has been used to construct egg parasitoidTrichogrammatoidea bactrae artificial nests for manipulating the ant. fumata (refer Bibliography). Artificial nests are made either by stuffing cocoa leaf litter into polythene bags or by Natural mortality from predation in the tying coconut leaflets into bundles. Placed in field appears to be greatest from general an area where D. thoracicus activity is high, predators of pupae; in particular the artificial nests are quickly colonized. A Iridomyrmex spp. Normal predation levels colonization rate of more than 90% within a are in the range 40-60%. Most predation was month is normal. The colonized artificial
83 Cord 2006, 22 (1) nests can then be collected and introduced possible that natural enemies were partially into the area desired. Uncolonized artificial responsible for keeping the populations at nests are also used to aid ant establishment low levels. and to supplement natural nesting sites when Searches for parasites were extended by they are lacking. IIBC's Malaysian research station to Indonesia, the Philippines, Sri Lanka and Many queens are present in a nest Papua New Guinea, and two wasp species (polygyny). In some species of ants a colony (Ceraphron and Ooencyrtus) were consists of several nests, one of which introduced in the field in small numbers to contains the queen; in others, a single queen Sabah, while a third species (Nesolynx) is present in a nest. Since the queen is the failed to establish in field cages. None of only individual in a colony which is capable these has established successfully; general of reproduction, when harvesting nests, the predation was cited as a possible explanation polygynous habit makes it very unlikely that for the failure of these introductions (CABI, a nest would be without at least a queen. The 2002). black cocoa ant readily colonizes suitable nesting sites. The use of the egg parasitoid, Trichogrammatoidea bactrae fumata, for the In Malaysia it was determined that the control of the cocoa pod borer (Bong et al., cost of establishing and maintaining the 1999) in Malaysia since 1983 showed that it black cocoa ant for 30 months over an area is an effective bioagent for the management of 7 ha was US$ 22 per ha per year. The cost of C. cramerella. Large-scale mass of insecticidal control of the cocoa pod borer production of Trichogrammatoidea species alone is estimated to be US$ 192 per ha per in Malaysia (Lim,1991; Lim and Chong, year. Looking at monetary cost (and 1987; Awang et al.,1999a,2003b) and the disregarding the social and environmental Philippines (Nagaraja et al., 1985b) by both costs of using insecticides), pest control Agriculture Departments and private employing the black cocoa ant therefore has industry have had much greater success and a clear advantage over insecticidal control. have given approximately 50% reduction in losses, but at costs much higher than Low levels of natural pupal parasitism spraying insecticides. The use of egg were found in Sabah, Malaysia, but little parasites has been practised on many estates progress was made in finding alternative (CABI, 2002). hosts for the parasitoids. No practical control effort was made using indigenous Control by egg parasitoids had pupal parasitoids, as there was no indication originally been dismissed because of the of significant parasitism. However, due to small size and dispersed distribution of C. the presence of natural predators and cramerella eggs. However, considerable parasitoidss of C. cramerella, and due to effort by Lim and his colleagues concern for the natural control of other demonstrated the presence of a parasitic cocoa pests such as stem and branch borers wasp (Trichogrammatoidea sp.) in Sabah and bagworms, selective spraying was (Lim and Chong, 1987). An intensive recommended so that natural enemies (and programme of rearing these wasps on an pollinators) were not disrupted. alternative host (Corcyra cephalonica) in laboratories and commercial breeding Exploration was also undertaken to find rooms, and releasing them into the field, exotic natural enemies to import into Sabah, gave surprisingly good levels of control, but centring at first on Peninsular Malaysia. A at prohibitive costs for about 12 500 or relatively low level of C. cramerella was 25000 wasps/ha/day (CABI, 2002). known to exist on rambutan and other non- Research continues by the Malaysian Cocoa cocoa hosts in West Malaysia, and it was Board (MCB) assisted by the American
84 Cord 2006, 22 (1) cocoa Research Institute (ACRI) to develop However, the greatest benefit from rearing and release methods that will be frequent, complete harvesting is likely to be economically competitive with current gained if it is done during the low-crop control systems. period through the first half of the rising crop. Complete, frequent, regular harvesting The pathogenicity of Beauveria (CFRH) is to some extent an extension of bassiana is indicated in the high rate of the principle of rampasan, but aimed at recovery (75%-100%) of the larval emergence rather than oviposition. entomopathogen from the dead larvae, While CFRH does not completely break the pupae and moths sampled from the treated life cycle, it should help to keep the C. pods but not from the live larvae or pupae or cramerella population low (as occurs at the moths sampled from pods not exposed to B. low-crop period), and thorough early bassiana (Bong et al., 1999). harvesting helps to keep the C. cramerella population relatively low during the time when the rising peak crop is most Management susceptible to oviposition (about 2 months
after the low-crop point)(CABI, 2002). Harvesting (Rampasan)
In C. cramerella-infested areas in the In the early days rampasan was southern Philippines, some cocoa has been considered to be the only feasible control planted at very high densities in hedges with method (Roepke,1912d,1913b). Removing access for small tractors between pairs of all pods longer than 6-7 cm from a field for rows. Trees have been kept to a low height 6 weeks would break the life cycle of C. so that all harvesting can be done within cramerella, as female moths will not usually easy reach. Mechanization allows frequent, lay eggs on younger pods. But without regular harvesting, and the hedge-like heavy pruning, complete elimination of a structure of the crop (1 m squares within the population of C. cramerella through double rows, and 2-3 m between rows for rampasan is extremely unlikely (Mumford, mini-tractor access) allows very complete 1986; Mumford and Ho, 1988; Wood et al., harvesting. Under this sytem, infestations of 1992). C. cramerella were at insignificant levels
during the late 1980s, without any other The great majority of C. cramerella form of control being applied) (CABI, larvae emerge from cocoa pods after they 2002). become ripe, and that if pods are picked at the earliest stage of ripeness then almost More synchronous cropping, whether 90% of larvae will still be inside the pods achieved by plant-growth regulators or (Mumford, 1986; Mumford and Ho, 1988). selection of more seasonal cropping If pods are broken quickly and the husks cultivars or clones, creates problems with destroyed, larval mortality will be very high more seasonally varied labour demands. and a good degree of control may be achieved. Effectiveness in large trial areas In Malaysia, economic control is over a period of several seasons was achieved if 50% or fewer pods are infested, confirmed (Wood et al., 1992). Thorough and this was easily achieved by CFRH. A harvesting is required at intervals of 14 days late commercial-scale trial confirmed that it or less in order to be sure to collect pods could reduce infestation, whilst spraying before they mature and before larvae emerge with deltamethrin made little difference in the field. Unsatisfactory results may arise (Wood et al., 1992). from incomplete harvesting.
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Good management of the cocoa area Recent innovations, particularly at BAL and complete frequent regular harvesting is Estates in Sabah, in clonal tissue culture and having good results in containing the pest. grafting clonal tissue on to mature stems, may allow partial host-plant resistance to Mechanical control (Sleeving) play a much greater part in C. cramerella control in the future (CABI, 2002). The idea of sleeving pods with bags of plastic or other materials to prevent egg Based on the husk thickness ratio, laying originated in Indonesia. Thin plastic hardness and thickness of the sclerotic layer, bags with open bottoms for ventilation, average damage severity index and the placed on very young pods (less than 7 cm number of eggs per pod, a resistance index long) and left throughout the pod maturation to C. cramerella was calculated for each of period, can result in virtually complete 53 cocoa clones in studies in Sabah, protection from C. cramerella. In Malaysia, Malaysia.The resistance index for the bagging pods (with plastic bags (14 X 10 resistant category ranged from 4.2 for inches) open at both ends) was more LAFI7 to 19.4 for NGK28; 20.2 for 1466 to effective than removing all pods at the end 30.0 for NGK16 in the moderately resistant of the season or physical collection of pupae category; and 32.4 for NGK13 to 45.6 for (Vanialingam et al., 1982).Though costly, ICS39 in the susceptible category (Azhar et the enclosure of developing pods in paper or al., 1995). polythene bags that are open at the bottom has proved effective in the Philippines Genetic engineering (Wood, 1980). Biodegradable plastic sleeves could be used. Sleeving is unlikely to be a Out of twelve Cry proteins from feasible option for cocoa growers, other than Bacillus thuringiensis tested in bioassays on those with young trees, inexpensive family cacao plantations in Indonesia for activity labour, or those in a desperate position to against the larvae of cocoa pod borer, five ensure a partial crop) (CABI, 2002). toxins that were more active than others and three Cryl proteins with relatively little Host-plant resistance homology were all found to be toxic, opening perspectives for controlling cocoa Early Dutch interest in host-plant pod borer by expression of Cry proteins in resistance focused on the surface of the pod. transgenic plants. Eggs were generally found in the furrows on the pod surface, smoother pods being less There is however concern about the attractive than deeply ridged cultivars, safety of GM plants.The immense gulf though this appears not to have been tested between the industry perception of GM crop or developed. Subsequently no obvious safety and the environmental groups’ differences were found in egg laying on perception of their hazards stays on. It is different cultivars (Day, 1985), but crucial to distinguish between interest-based considerable differences in larval mortality and value-based motivations. Where were found inside pods of different motivation is value-based, as for cultivars. Greater mortality occurred in pods environmental pressure groups that have an with either thicker or harder stony endocarp almost religious commitment to their cause, layers in the pod wall. Larval survival was then it cannot be swayed by facts and as much as 10 times greater in soft/thin- rational argument. This issue has to be walled cultivars. Hardness of the sclerotic addressed. layer was the important factor (Azhar and Lim, 1987). Chemical control
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Agrocide (26% benzene hexachloride) the sprayed area were 12.1-33.7 percentage at 0.2% was best at reducing adult points lower than in the control area, giving populations and subsequent pod damage. an estimated net benefit of up to RM978/ha Decis (deltamethrin) 2.5% and Lannate in one season, assuming a cocoa price of (methomyl) were effective as ovicides. In RM4000/tonne. Losses in the sprayed area heavily infested areas Agrocide and Decis, still ranged from 7.0 to 43.1% and did not used alternately at weekly intervals, reduced decline over successive seasons. There was C. cramerella incidence by about 80% after some evidence for immigration into the two months but pod borer infestation sprayed area, but it is suggested that rapid increased significantly three months after recovery of populations following spraying the last application (Vanialingam et al., is also due to the high potential rate of 1982). increase of the insect in susceptible cocoa varieties. In susceptible cocoa varieties In Malaysia, application of Nurelle D control is always likely to be difficult, but in 505 EC, a formulation of chlorpyrifos at 500 less susceptible varieties, and with well and cypermethrin at 50 g a.i./litre, was maintained trees, chemical control by effective at 0.36 lit/ha, 6 spray applications selective application to adult resting sites significantly reducing the mean number of could be a practical component of integrated eggs and percentage pod infestation on control (Day et al., 1995). cocoa, and controlling populations for up to about 8 weeks after the last application Cocoa in South-East Asia could not (Azhar and Sabudin, 1987). survive continuous blanket sprays of broad- spectrum insecticides, because of destructive Monitoring of populations with outbreaks of secondary pests freed from pheromone traps, and a preliminary study of their normal control by natural predators and painting cocoa pods with chemical- parasitoids (Conway, 1973; Toxopeus and incorporated formulations, were also Giesberger, 1983). The long-term practical undertaken (Leong, 1987). use of insecticides for control of C. cramerella requires that the chemical is Lambda-cyhalothrin (Karate) was tested applied selectively, either to undersides of for the control of C. cramerella on cocoa in the lower branches where natural enemies Malaysia. Fortnightly spray applications at are less common, or at times when natural 14-25 ppm significantly reduced damage. enemies are less abundant. Application of 5 rounds at 2.5-3.0 g a.i./ha per round protected the subsequent crop and Adult C. cramerella rests during day reduced pod infestation to <20% and crop time on the undersides of lower branches in losses to <5%. Pod infestation levels cocoa, and this provides an ideal site for differed between pods on the trunk and selective spraying as it is relatively dry, branches of tall unpruned bushes. This dark, inert and accessible. Relatively small difference was reduced following height amounts of contact insecticide, either reduction and canopy pruning and pyrethroid or carbamate, applied to these insecticide application (Ngim et al., 1992). resting sites during the low-crop period, kept The daytime resting sites of all C. C. cramerella populations below economic cramerella were found on the undersides of damage levels during subsequent peak branches 45° or less from horizontal, and 1.5 populations (Day, 1985; Mumford and Ho, cm or more in diameter; 90% were found in 1988). As with cultural controls, heavy the lower half of trees. 25 ppm deltamethrin pruning and height maintenance ensure that was applied with knapsack sprayers to these all the lower branches are accessible. Branch sites. Five applications were made at 10-day spraying was advocated only in the low-crop intervals, each crop season (6 months), over period because this was believed to give the a 2-year period. Mean estimated losses in greatest returns, as it protected the
87 Cord 2006, 22 (1) susceptible peak crop developing in the were trapped using synthetic pheromones several months immediately following (traps baited with a polyethylene vial spraying. Protection afforded by the sprays impregnated with 1.2 mg of a mixture of only applies to the relatively low crop (4E,6Z,10Z)- and (4E,6E,10Z)- isomers of maturing in the 3 months after the peak. 4,6,10-hexadecatrienyl acetate and the corresponding alcohols, and of hexadecyl A farmer practising insecticidal control alcohol in 40:60:4:6:10 ratio) than could be of the borer is likely to spray a synthetic caught in traps baited with virgin female C. pyrethroid every other week throughout the cramerella moths (Beevor et al., 1986a,b; year. This practice increases cost of 1993); these traps could be used for both production substantially besides being a monitoring and control. Control is achieved threat to the ecosystem. Furthermore, if a large proportion of male moths are development of insecticidal resistance is a trapped before they can mate, thus reducing worry. the overall mating success of female C. cramerella moths and lowering fecundity. During the 1950's numerous trials were conducted in Indonesia on insecticide A large-scale (200-ha) trial was control, using cover sprays of broad- conducted over 4 years at BAL Estates in spectrum organochlorine insecticides. Initial Sabah during the mid 1980s, to test the results appeared to be promising for a effect of pheromone trapping as a control control, but on at least one estate in Java method (Beevor et al., 1993). Trials and over 1000ha's of cocoa had to be destroyed commercial-scale control using traps were in the late 1950's (after five years of general also undertaken on several other estates in insecticide application) due to outbreaks of Sabah. Trap densities of four and eight per stem and branch bores, which were no ha were used to give economic control. longer adequately controlled by their natural Results of these trials indicated that losses enemies. were reduced by about one-third in trapped areas compared with untreated areas. A Aerial spraying was tried in Sabah, major problem with pheromone-trapping without good results. The pesticide is mainly trials was in finding adequate untreated deposited on the shade trees where C. control areas. The pheromones were shown cramerella moths may spend some time to catch moths as far as 800 metres from between 21.00 and 06.00 h, based on the infested cocoa, and so the size of both relatively high catches of moths in treated and untreated areas needed to be pheromone traps placed above the cocoa very large to give good comparisons. canopy.Aerial spraying during the C. Neighbouring areas were also subject to cramerella quarantine-eradication effort in pruning, harvesting and spraying actions West Malaysia greatly reduced mosquito which may have distorted results. It is infestations in the estates. The best return concluded that control of C. cramerella by from pod spraying is likely to come from pheromone-baited mass trapping may reduce applications during the early stage of a pod damage and may prove to be cost rising crop, soon after the low-crop period. effective (Beevor et al., 1993). Spraying alone was not effective (Wood et al., 1992). In 1987 a race of C. cramerella was found in West Malaysia that did not respond Pheromone trapping to the pheromone used in Sabah. Analysis showed that the mixture of pheromone Female C. cramerella moths attract molecules in the new race was very different males by releasing a pheromone (Day, 1985; from the original formula, and the new Beevor et al., 1986a,b), which was identified mixture was shown to catch C. cramerella and synthesized. Many more male moths moths in West Malaysia. The new mixture
88 Cord 2006, 22 (1) also caught large numbers of C. cramerella Malaysia but they may not have good moths in Sabah, casting doubt on the future agronomic traits, thus requiring further cross of mass trapping and raising questions about breeding with the agronomically good the origins and interactions of the two races. clones. There was an immediate problem of keeping the two mixtures separated; when used The most effective control methods are together in the same trap no moths of either frequent harvesting, destruction of ripe pods type would be caught. More importantly, and husks to prevent pupation in the field however, there was a fear that further races and selective spraying of resting sites with could develop or appear which would deltamethrin, cypermethrin or lindane. require frequent changes of pheromone Pheromone mixtures have potential for use components, adding to costs and limiting in traps as a quarantine surveillance efficacy. As a result, pheromones are not technique and for control. Parasitoids, used to control C. cramerella at present, particularly T. bactrae fumata, also have although occasional commercial interest is potential as biological control agents shown in developing new pheromone (Mumford and Ho, 1988). mixtures (CABI, 2002). Success achieved in the project- Integrated Pest Management Sustainable Cocoa Extension Services for Smallholders (SUCCESS) Harvesting (Rampasan) and chemical implemented in Indonesia in conjunction control are generally adopted. The most with the American Cocoa Research immediate reductions in C. cramerella are likely to come about through better managed Institute and BCCCA, a British harvesting and spraying. Both of these rely counterpart, ACDI/VOCA could be on well-pruned trees (pruning every 3 emulated. Through SUCCESS a large- months to keep canopy light and open and scale training programme was organized remove chupon growth monthly) kept to a on integrated pest management and height low enough to collect and/or spray all pesticide-free control of the cocoa pod pods. borer. The programme included frequent harvesting, pruning, sanitation and Longer term control may be improved fertilization. Crop losses to the cocoa by grafting or replanting with hard-walled pod borer dropped from nearly 40 clones. Further releases of exotic natural percent to 15 percent, which amounted enemies may provide additional partial control, if suitable parasitoids can be found. to an increase of 12,800 tons per year worth $13.5 million. SUCCESS has In Malaysia, cocoa black ant demonstrated the potential to produce (Dolichoderus thoracicus) and egg good quality cocoa with yields at least parasitoid,(Trichogrammatoidea bactera double the local averages. The project fumata) have been found to be potential bio- provided positive effects for farmers, control agents in limiting cocoa pod borer communities and the environment. infestation. Integration of weekly harvesting SUCCESS is also encouraging the use of and spraying of Beauveria bassiana every other environmentally friendly two weeks was the most effective method to interventions for the management of control cocoa pod borer infestation in cocoa pod borer such as pheromones, Indonesia .Pod sleeving with plastic bags have been able to control cocoa pod borer in biological control, pest resistant cocoa smallholders garden but not in larger varieties and side-grafting to revitalize plantations. Some of the clones have shown unproductive cocoa trees. resistance against the cocoa pod borer in
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Note Anonymous, 1991. Cocoa pod borer management. The Planter, Kuala If any body has suggestions for the Lumpur 67: 299-300. effective management of cocoa pod borer, Awang, A. 1995. Potential use of black please forward your suggestions to Dr. cocoa ant and pheromone for the John Moxon, Research Programme management of cocoa pod borer. Paper Leader, Wet Lowland Islands presented at Workshop on Recent Programme, National Agricultural Advances in the Management of Cocoa Research Institute (NARI), Keravat, P.O. Pod Borer (with special reference to Box 204, Kopoko 613, East New Britain Tbf), Marco Polo Hotel, Tawau, Sabah. Province, Papua New Guinea Tel: (675) 29 June 1995. 983 9145/983 9200, Fax: (675) 475 1034 Email: [email protected] and Dr. Vele Awang, A. 1997. Potential use of Ila‘va, CEO, Cocoa & Coconut Institute, Trichogrammatoidea bactrae fumata Tavilo Research Station – ENBP, P.O. Nagaraja for the management of cocoa Box 1846, Rabaul, ENBP, Papua New pod borer, 12 pp. Paper presented at Guinea, Tel.: +675 983-9115, Fax: +675 ASEAN Cocoa Club Workshop on 983-9116, Email: [email protected]; Cocoa Primary Production Technology ccriento @datec.net.pg. and Quality Management, Marco Polo Hotel, Tawau, Sabah, Malaysia, 2-4 October 1997. Bibliography Awang, A. 1998. Management of cocoa Abdullah, R. B., Azhar, I. and Hassan, S. T. pests in Malaysia. Paper presented at S. 2001. Role of cocoa black ant International Cocoa Pests and Disease. (CBA), Dolichoderus thoracicus, in the Cote d’Ivorie, 19-21 January 1996. dispersal of cocoa mealybug, Awang, A. 2002a. Kawalan agen biologi Cataenococcus hispidus. Paper serangga perosak koko. Kertas kerja Presented at the FRIM ENTOMA dibentangkan di Persidangan ke 2 Seminar on Insect Diversity, 2-3 Kakitangan Kumpulan Sokongan II di October 2000, FRIM, Kuala Lumpur. Pusat Latihan BSN, Bangi, Selangor on Alba, M. C., Salvador, A. C., Galbizo, T. C. 7-10 Aug 2002. and Easaw, P. T. 1985. Additional Awang, A. 2002b. Teknologi Pengurusan information on the biology of Serangga Perosak Koko. Kertas kerja Acrocercops cramerella Snellen dibentangkan di Kursus Teknologi (Lepidoptera: Gracillariidae) in the Koko, Pusat Penyelidikan dan Philippines. Philippine Entomol. 6: 243- Pengeluaran Koko, Hilir Perak. 2-6 253. September 2002. Anonymous, 1980. Editorial, An industry in Awang, A. 2002c. Teknologi Pengurusan peril. The Planter 56: 359-361. Serangga Perosak Koko. Kertas kerja Anonymous, 1987a. Editorial, The decline dibentangkan di Kursus Teknologi and (hopefully) fall of the cocoa pod Koko, Pusat Penyelidikan dan borer in Peninsular Malaysia. The Pengurusan Kualiti Koko, Tawau, Planter 63: 484-486. Sabah. 19-24 September 2002. Anonymous, 1987b. Introduction to the Awang, A. and Lee, M. T. 1998. Research cocoa pod borer, pp. 1-6. In: on mass rearing and field release of egg Management of the Cocoa Pod Borer, parasitoid, Trichogrammatoidea P. A. C. Ooi, et al. (Eds.). MAPPS, bactrae fumata Nagaraja for the control Kuala Lumpur, Malaysia. of cocoa pod borer, Conopomorpha
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cramerella (Snellen) in Malaysia. Paper Selangor, Malaysia, 18-19th March presented at 5th International 1999. Symposium of Trichogramma and Other Awang, A., Lamin, K. and Lee, M. T. Egg Parasitoid, Cali, Colombia. 4-7 1999b.Use of yeast as alternative March 1998. protein source in feed formulation for Awang, A. Hasim, S. and Kelvin Lamin, the rice moth eggs production. Paper 2003a. Optimum release density of egg presented at MCB-MAPPS Conference, parasitoid Trichogrammatoidea bactrae Kota Kinabalu, Sabah on 2-3 November fumata Nagaraja for controlling cocoa 1999. pod borer, Conopomorpha cramerella Awang, A., Lamin, K., Lee, M. T. and (Snellen) in Malaysia. Kertas kerja Sastroutomo, S. S. 1999c. Biological dibentangkan di Persidangan Pegawai control in the tropics: towards efficient Kanan Lembaga Koko Malaysia, Hotel biodiversity and bioresource Hilton, Kuching, Sarawak. 23-25 management for effective biological September 2003. control, pp. 48-51. In: Proceedings of Awang, A., Lamin, K. and Hasim, S. the Symposium on Biological Control in 2003b. Mass production and utilization the Tropics held at MARDI Training of egg parasitoid Trichogrammatoidea Centre, L. W. Hong (Ed.), from 18-19 bactrae fumata Nagaraja as an March, 1999, Serdang, Malaysia. alternative method for the control of Awang, A., Lamin,K., Lee, M. T. and cocoa pod borer, Conopomorpha Sulaiman Hashim, 1999d.Cocoa pod cramerella (Snellen) in Malaysia. Paper borer tolerance screening study on some presented at 14th International Cocoa commercial cocoa clones. Paper Research Conference, Ghana. 14-18 presented at MCB-MAPPS Conference, October 2003. Kota Kinabalu, Sabah, Malaysia on 2-3 Awang, A., Hasim, S. and Kelvin Lamin, November 1999. 2003c. Parasit telor, Pengeluaran dan Awang, A., Lamin, K. and Mohd Shakri, A. Kenerkesanannya di dalam kawalan ulat 2001. A preliminary results on the pengorek buah koko. Kertas kerja establishments of cocoa black cntas dibentangkan di Bengkel Perlindungan Dolichoderus spp. in Sabah Malaysia Tanaman Koko 2003, Hotel Emas, and their effect on cocoa pod borer Tawau, Sabah. 20-21 Oktober 2003. Conopomorpha cramerella damage. 4th Awang, A., Hasim, S. and Kelvin Lamin. Asia Pacifice Confeerence on 2004. Mass production of egg Entomology, Renaissance Kuala parasitoid. Paper presented at Lumpur Hotel. 14-17 Aug 2001. Commercilization Seminar, Marriot Awang, A., Lee, M. T. and Hasim, S. 1998a. Hotel Putrajaya, Kuala Lumpur, Effect of cold storage on the emergence Malaysia. of parasitised rice moth eggs. Poster Awang, A., Lamin, K. and Lee, M. T. Session at Malaysian International 1999a.The use of egg parasitoid, Cocoa Conference, Kuala Lumpur. 26- Trichogrammatoidea bactrae fumata 27th November 1998. Nagaraja for the control of cocoa pod Awang, A., Rita Muhamad and Chong, K. borer, Conopomorpha cramerella K. 1988b. Comparative merits of cocoa (Snellen) Research progress, constraints pod and shoot as food sources of mirid, and prospect. Paper presented at Helopeltis theobromae Miller. Planter Symposium on the Biological Control in 64(744): 100-104. the Tropics. Pusat Latihan MARDI,
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Awang, A., Lee, M. T., Lamin, K. and Azhar,I. 1986c. Pengorek buah koko Hasim, S. 2002. Optimum release Conopomorpha cramerella satu density of egg parasitoid ancaman terhadap koko di Trichogrammatoidea bactrae fumata Semenanjung Malaysia.Cocoa pod Nagaraja for controlling cocoa pod borer, a potential threat to Peninsular, borer, Conopomorpha cramerella Malaysia. Paper presented at Seminar Snellen in Malaysia. Paper presented at Teknologi Koko Masakini Kedua, 23 pp. 6th Egg Parasitoid Symposium, Italy. (In Bahasa Malaysia) (Mimeographed). 15-18 September 2002. Azhar, I. 1988a. Host plant resistance to Awang, A., Meriam, M. Y. and Hasim, S. cocoa pod borer - A research progress, 2000. Pengurusan Teknologi Serangga pp. 1-27. In: Proc. MARDI Senior Staff Perosak Koko yang efisien. Kertas kerja Conf., Kuala Lumpur, Malaysia. dibentangkan di Kursus Teknologi Azhar, I. 1988b. Mengenalpasti serangga Koko Lanjutan 2000. Beringgis Beach perosak koko melalui kesan dan Resort, Papar, Sabah. 12-15 November simptom serangan Identification of 2000, Hotel Rajah Court, Kuching, cocoa insect pests through damage and Sarawak. 22-25 Oktober 2000, Hotel attacked symptoms. Lapuran MARDI Residence, Bangi, Selangor. 25-27 No. 122, 26 pp. September 2000. Azhar, I. 1989. Towards the development of Awang, A., Sadao Wakamura and Tay, E. B. integrated pest management of 1995. Efficacy of mating distruption Helopeltis in Malaysia. MARDI Res. J. using synthetic sex pheromone for the 17: 55-68. management of cocoa pod borer. Paper presented at International Workshop of Azhar, I. 1990a. Postharvest management Cocoa Pod Borer, Sulawesi, Indonesia. of cocoa pod borer (Lepidoptera: 16-18 October 1995. Gracillariidae) MARDI Res. J. 18: 71- 80. Azhar, I. 1985a. Conopomorpha cramerella (Snellen), a new name for the cocoa pod Azhar, I. 1990b. Studies on sclerotic layer borer. MAPPS Newsl.9: 4. hardness of cocoa pod. MARDI Res. J. 18(1): 63-69. Azhar, I. 1985b. Natural and cultural control in the management of selected cocoa Azhar, I. 1992. Role of black ants in cocoa pests, pp. 225-267. In: Integrated pest pod borer natural control.MAPPS management in Malaysia, B. S. Lee, W. Newsl. 16(4): 36-37. H. Loke and K. L. Heong (Eds.). Azhar, I. 1994a. Ants mealybugs Malaysian Plant Protection Society, interactions in cocoa - Density Kuala Lumpur, Malaysia. dependent mutualism, pp. 88-89. Azhar, I. 1986a. Ancaman pengorek buah In: Proc. 4th Internat. Conf. Plant Prot. koko Conopomorpha cramerella Trop., Kuala Lumpur, Malaysia. Terhadap Industri holo de Malaysia. I. Azhar, I. 1994b. Fitting two empirical Perihal Biologi dan Keroskan in models to the dispersal of cocoa pod Malaysian. Teknol. Koko-Kelapa, Jil. 2, borer egg parasitoid after a release, pp. pp. 53-59. 336-338. In: Proc. 4th Internat. Conf. Azhar, I. 1986b. Ancaman pengorek buah Plant Prot. Trop., Kuala Lumpur, koko Conopomorpha cramerella Malaysia. Terhadap Industri Koko Ki Malaysia. Azhar, I. 2001a. Cocoa black ant (CBA) as a III. Pengurusan perosak ini in bioindicator of the cocoa and coconut Malaysian. Teknol. Koko-Kelapa, Jil. 2, agroecosystern health measured pp. 71-76.
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