Mirid damage is one of the three most important scourges affecting cocoa in Ghana and other West African countries. The other two scourges are the cocoa swollen shoot virus disease transmitted by mealybugs, and the black pod disease caused by Phytophthora palmivora and the more virulent and recently introduced P. megakarya. The Ghana government spends billions of Cedis annually on the purchase of insecticides, which are highly subsidized for farmers for the control of capsids on cocoa. For example, in 1992, C 12,532,080,000.00 out of a total expenditure of C 19,696,760,000.00 was spent on spraying machines, insecticides and other chemicals. At the time the exchange rate was about C 800.00 to one US dollar (Ghana Cocoa Board 26th Annual Report, Page 30).
Taxonomy and nomenclature
All the forty or so species of capsids (Heteroptera: Miridae) feeding on cocoa worldwide belong to the mirid subfamily Bryocorinae. In the subfamily Bryocorinae, the mirids are separated into two tribes, Monaloniini or Odoniellini. The Monaloniini include the two genera, Helopeltis and Monalonion, whilst the Odoniellini include the eight genera Boxia, Boxiopsis, Bryocoropsis, Distantiella, Odoniella, Platyngomiriodes, Pseudodoniella and Sahlbergella (Entwistle 1972).
Two mirid species, Distantiella theobroma (Dist.), Sahlbergella singularis Hagl., occur commonly on cocoa in Ghana and other West African countries (Box 1944; Squire 1947; Taylor 1954; Youdeowei 1969). Other cocoa mirid species recorded in West Africa include Bryocoropsis laticollis Schum, Odoniella spp., one Boxia species and about ten species of the genus Helopeltis (China 1944; Lavabre et al. 1963; Squire 1947; Taylor 1954). The Helopeltis spp. include Helopeltis lalendei (Carayon), the most common Helopeltis species in Ghana which also attacks cocoa from Cote d'Ivoire and Nigeria. Other Helopeltis spp. of rather confused identity include H. begrothi which has positively been recorded only in the Cameroon; H. seredensis Schmitz is frequent in Cote d'Ivoire and probably also present in Ghana; H. corbisieri Schmitz is found in the humid forests of Central Africa and probably also occurs in Cote d'Ivoire; H. gerini Carayon common in Southern Cameroon; H. muyumbensis (Ghesq.) occurs in the north and east of Congo; H. poppiusi Schmitz occurs in small numbers only in Cote d'Ivoire, H. lemosi Ghesgue is restricted to and occurs commonly on the islands of San Thome and Principe; H. scheutedeni Reut (= sanguineus Popp.) is widespread in inter-tropical Africa, H. westwoodi (White)is widespread in West and Central Africa but only occurs small numbers, and an undetermined Helopeltis sp. attacks pods in Tanzania.
Symptoms and damage
Capsids are not particularly numerous and this adds to the difficulty in studying them. For example, an average of six capsids per ten trees are capable of causing very serious injury. They are sucking insects and they damage the soft young tissues of the tree by piercing the young shoots with their mouth parts, injecting poisonous saliva and then sucking liquid food out of the resulting wound. Feeding by mirids is characterized by dark markings known as lesions, on both pods and shoots, which result from the collapse of plant tissue caused by the toxic saliva (Entwistle 1965). The shape of the lesions is somewhat characteristic of the mirid species. For example, lesions resulting from the feeding of Helopeltis spp. are roundish whilst those by Distantiella and Sahlbergella tend to be elliptical with the long axis parallel with that of the stem. Secondary damage characterized by canker and dieback occurs when the feeding lesions are invaded by parasitic fungi notably Calonectria rigidiuscula Berk. and Br. (Sacc.) and Fusarium decemcellulare (Cotterell 1927; Crowdy 1947; Goodchild 1952; Williams 1953; Kay 1961; Entwistle 1972). Estimates of the extent of infection of lesions by Calonectria in Ghana vary from 80 % (Hammond 1957) while in Nigeria an overall estimate of 95% has been given (Kay 1957). However, Calonectria infection is not associated only with mirid attack, the fungus may enter through wounds of many kinds. Mirids need to feed on stems for only a few days to ensure infection of the tree with Calonectria. From the primary lesion the fungus invades the xylem, phloem and medullary rays but the mycelium may initially be largely confined to non-lignified tissue and is intracellular. Typically infected lesions heal by a growth of callus tissue from the edges which eventually occludes an area of severely damaged cells in the xylem (Crowdy 1947). The affected area can be recognized by the overlying bark being characteristically rough. The roughness persists for many years and Calonectria has been found occluded beneath as much as three inches of living tissue. The significance of Calonectria lies in the fact that it is a weak parasite which can be occluded by healthy trees where it can be dormant for may years only moving into active phase when the tree becomes weakened. Dieback consequent on mirid attack (Plates ... to...) occurs to an extent which is dependent on the joint severity of action of a umber of separate factors - the duration and intensity of mirid attack itself, the state of shade cover above the trees, and climatic factors (especially drought and edaphic factors).
Mirids can kill only young green shoots and such damage is restricted to periods of flush when this type of tissue is present. Young cocoa is particularly susceptible to mirid attack. Thus, capsids make cocoa difficult to establish and can delay the time for it to come into bearing by several years.
In Africa there are two predominant patterns of mirid attack known as the "capsid blast" (Plate....) and "capsid pockets". Both of these patterns lead indirectly to depression of the tree vigor, which greatly reduces yield. "Blast" is recognized by a concentration of attack on fan branches and results in their terminal death. The dead leaves, brown and withered, remain attached to the trees for some time and gives a characteristic scorched or blasted appearance, often very striking on account of the size of areas afflicted. In Ghana, blast is mostly a dry season phenomenon (January and February) and may have very little effect on the tree. In areas such as Western Nigeria, where the overhead shade is less dense, degradation of the cocoa canopy itself has more serious consequences.
"Pockets" occur when the canopy of more or less discrete groups of trees, up to around one hundred in number, is strongly degraded by intensive feeding on fan branches. If damage persists, trees in the pocket cease to yield and finally die. Williams (1953) found that "capsid pockets" were frequently initiated by shade trees falling and breaking the cocoa canopy. Chupon growth was thus encouraged, providing ideal conditions for rapid multiplication of mirids. Thus "pocket" attack is more frequent in shaded than in unshaded areas.
Two primary phases of tree deterioration are generally recognized as "stag-headed" trees and "bare poles". Stag-headed trees result from the death of the crown of trees following persistent mirid feeding on fans and regenerative shoots from Calonectria dieback, with largely dead canopy branches remaining. By total loss of even these poor canopy remnants, the bare pole stage is reached. The trunk of such trees may have many feeble regenerative shoots. Damage is not uniformly distributed and severely damaged and healthy trees may occur together.
Posnette (1943) found that certain trees appeared to be "immune" or susceptible" to mirid attack while others seemed "tolerant", but none of these selections maintained their field behavior under laboratory conditions.
Mirids on pods feed largely in the parenchymatous husk tissue but the depth of stylet penetration is not known. Cherelles may wilt, and pods less than three months old have very little chance of surviving, usually dying from mirid damage or from fungi entering the pods through the lesions (Gerard 1968). In West Africa crop losses resulting from this are believed to be negligible because the tree compensates by shedding fewer fruits by cherelle wilt. Well-grown pods seldom seem directly affected. A comparison between ripe pods that had been heavily attacked (more than half the surface blackened by feeding) by S. singularis in Nigeria and clean pods revealed no significant differences in dimensions, pod weight, number of beans or weight of peeled beans.
Host range
Distantiella theobroma and Sahlbergella singularis are indigenous to West Africa. Since cocoa is not indigenous to West Africa, it is believed that mirids were originally present in the West African forest and were feeding on native forest trees long before cocoa planting began in the area. With the introduction of cocoa which proved more nutritious, the mirids switched from the wild plants to cocoa (Leston 1970). Entwistle (1972) has listed some alternative host plants o Entwistle (1972) has also listed alternative host plants of other cocoa mirids including Monalonion, Bryocoropsis, Odoniella and Boxia spp. Because of the confused identity of Helopeltis spp., the host range of species within this genus is uncertain and there is the need of much careful recording to take advantage of the clarified taxonomic situation as revised by Schmitz (1968).
Geographical distribution- further information:
Entwistle (1972) gives a good account of the distribution of cocoa mirids, with distribution maps. Of the five mirid genera viz. Sahlbergella, Distantiella, Bryocoropsis, Odoniella and Helopeltis which attack cocoa in the Ethiopia region, the first four are endemic to and occur only in West and Central Africa.
The most widespread and generally more economically important mirid in Africa is Sahlbergella singularis Hagl. but in Ghana, D. theobroma is more common and predominant than S. singularis. S. singularis attacks cocoa from Sierra Leone, in West Africa, to the Congo Republic and Central African Republic in the east but probably does not extend beyond 90C, the approximate limit of the cocoa belt. It is also present in the island of Fernando Poo, 32 km from the mainland. A Sahlbergella sp., probably S. singularis, has been reported in Cabinda, a northern enclave of Angola embraced by the Atlantic and the Congo Republic, which together with Mayumbe in the Congo, must be the southernmost limit of the species on cocoa.
The second most important species is D. theobroma, which reaches its peak in Ghana. In Cote d'Ivoire, it forms only 5 to 15 per cent of the mirid population though varying regionally from 0.2 to 0.5 per cent in Zepreghe up to over 80 per cent in Olibribuo (Lavabre et al. 1963). In Nigeria, it constituted only 3 per cent of all mirids collected (ref) and is largely restricted to a area bounded by Ondo, Ife, Ilesha and Kabba (i.e. mainly in the Western Region) and occurs mostly above 800 ft (245 m) contour where it constituted 18.2 per cent of a total of 4,000 mirids collected and was at 43 out of 90 collection sites (Entwistle 1964). In Yaoude in the Cameroon (elevation 600 m or more) D. theobroma has been reported in the proportion of 1: 140 (D. theobroma: S. singularis) (Lavabre 1957) and at Ikiliwinde (elevation 245 to 360 m) it occurs sparingly on young cocoa. In the Central African Republic, it was collected sparingly at Salo (Boulard (1967).
A detailed account of the worldwide distribution of other mirid species is also in Entwistle (1972).
Natural Enemies:
Studies in West Africa (Lodos 1968; Entwistle 1972; King 1971and 1973) have shown that all developmental stages of the cocoa capsids Distantiella theobroma and Sahlbergella singularis, including the egg stage, are affected by parasitic organisms which are either hymenopterous parasitoids or nematodes.
Percentage parasitism has been generally lower in D. theobroma than in S. singularis. For D. theobroma which is parasitized mainly by nematodes the rate of parasitism in nymphs and adults never exceeded 4% (King 1971). Parasitism by the braconid Euphorus anates Nix, and an unidentified Euphorus species was even lower. Other parasites common to both capsid species include Euphorus sahlbergellae Wlk., Euphorus helopeltides Ferr. and Encyrtus cotterelli Watson (Hymenoptera: Encyrtidae). The highest level of parasitism (20-59.5%) has been recorded in 4th instar nymphs of S. singularis (King 1971). Ectoparasitic leptid mites occur occasionally on D. theobroma and S. singularis but appear unimportant (Entwistle 1972).
Parasitic mermithid nematodes in the abdomen of S. singularis, D. theobroma and Helopeltis in Africa have often been allocated to the genus Mermis (Entwistle 1972) but Hexamermis Imicro-amphidis Stein and Agamermis paradecaudata Stein were described from Helopeltis antonii in Java (Menzel 1923; Steiner 1925). Their incidence is generally low.
Egg parasitism by Telenomus, Pediobus and Trichogramma spp. was reported in all four capsid species at 10% for D. theobroma and S. singularis, 10-73% for H. begrothi and 25-66% for B. laticollis.
Mirid predators recorded in West Africa include several species of ants including Oecophylla longinoda Latr., salticid spiders, reduviids, mantids, Grillidae (grasshoppers and crickets) and Pentatomidae but most of these are not specific to capsids (Entwistle 1972; Marchart & Leston 1996). Marchart & Leston (1969) recorded 20 species of spiders, 14 of mantids and 25 of ants as predators of D. theobroma. The predatory ants fall into two main categories: canopy-nesting ants (Oecophylla, Crematagaster and Macromischoides) and ground or stump nesting ants (Pheidole and Platythyrea). Reduviid predators include Rhinocoris obtusus Beau. and R. carmelitis Stal. A salticid spider, Plexipus paykulli And. lived for 65 days in the laboratory killing an average of 2 D. theobroma a day. The mantids Panurgica compressicollis Saus and Pseudocrobotra ocellata P. also destroyed 10 and 60 mirid adults and nymphs a day. There is the need to search for more obligatory capsid predators for control purposes.
Pathogenic fungi recorded on cocoa capsids include fungi imperfecti of the genus Hirsutella which attack S. singularis in Ghana and Nigeria (Anon 1970) and a white unidentified fungus which was very destructive when introduced into cages of S. singularis. Elsewhere, Beauveria bassiana has been reported to be lethal to Helopeltis theobromae Miller in Malaysia. Other fungi associated with coca mirids in West Africa are Bacillus and Aspergillus species (Collingwood 1971). A spore-forming bacterium originally reported as pathogenic to S. singularis in Nigeria proved to be even more pathogenic to D. theobroma in Ghana but slightly less so to Helopeltis begrothi.
Like sex pheromones, some crop protection companies in Great Britain and USA are actively involved with the development of suitable formulations of pathogens such as that for Beauveria, is commercially available under the trade name Boverin and has been used successfully to control a number of insect pests including Cydia pomella, a pest of apple in Europe and America. The International Institute of Biological Control of UK based at Silwood Park in Ascot is currently conducting studies aimed at promoting the use of Beauveria and other pathogens in Africa.
Biology and ecology:
Research carried out shows that all mirids have similar biology (Cotterell 1926 1943; Entwistle 1965). Adult females, with their saw-like ovipositor, insert their eggs in pods and stems. Eggs are completely buried and hidden from sight except for two very fine terminal hair-like filaments that arise from the chorionic rim of the egg. Cobben (1968) considered the horns to be bundles of isolated aeropyles, which open individually to the outside in the apical part of the horn. Each horn presumably encloses a single micropyle. The function of the horns is uncertain but Squire (1947) said they draw moisture away from the operculum, thus presumably facilitating respiration. The oviposition site of D. theobroma and S. singularis coincide with their feeding sited.
Mating of both D. theobroma and S. singularis takes place readily in captivity and has been observed to last from one to two hours. The low numerical levels, even at peak mirid populations, suggest a chemical attractant to be involved. Indeed Cotterell (1926) observed in Ghana those adult males of D. theobroma assembled to cages containing females but not to cages containing both sexes. On the other hand, olfactometer studies with this species using laboratory virgin adults which had never flown showed no indication of sex attractants (Anon 1968). The possibility of using sex attractants as a bait for capturing males for control purposes is currently being investigated.
There are five juvenile stages called nymphs. During the last three stages, the wings do not fully develop until the adult stage. The incubation period seems to vary from 13-17 days whilst each of the nymphal stages may last from 3-6 days. Females begin to lay eggs about a week after emergence and may lay 30-40 eggs each. There are insufficient accurate data on the duration of adult longevity due largely to the difficulty of maintaining mirids in captivity. However, most sources seem to suggest that adults of both D. theobroma and S. singularis live for less than one month. On cut shoots of Ceiba pentandra in water, a mean adult longevity of 16.6 days and a mean fecundity of 100 eggs with a maximum of 276 has been recorded for D. theobroma in Ghana where for S. singularis on thick stems of cocoa in water, a mean of 57 and maximum of 179 have been noted (Anon 1969). If food is available and the climate is favorable, they breed throughout the year. Longevities have been recorded of 7-42 days (mean 24.5 days) and 24-32 days (mean 28.0 days) for male and female S. singularis on the fruit of Desplatsia dewevrei under ambient environmental conditions in the insectary.
Mirids do not feed during the heat of the day, but rest at the fork and branch unions on the underside of pod stalks and in other protected situations and are relatively inactive. Patterson (1914) stated that feeding does not begin until 5.30 p.m. unless conditions are dull and wet and if the morning is sunless they may feed to 10 a.m. Thus insecticide (DDT) application on young cocoa in the 1950s was targeted at branch unions where the resting insects picked up enough of the insecticide to kill them. The method was very simple but, unfortunately, could not be applied to mature trees where the branch unions were out of reach.
There are generally low population densities of mirids on cocoa but most are found after the abatement of the major rains. In West Africa it has been shown that mirids have a distinct population cycle with minimum numbers occurring in the periods February to July and maximum numbers from August to January, the position of the maxima and minima varying somewhat from year to year (Entwistle 1965). It has been suggested that humidity has a direct influence on population changes in West Africa and there is no doubt that predators and parasites together have some effect (Gibbs et. al. 1968). The preference of S. singularis fifth instar nymphs in laboratory experiments is for high humidity (90-95%) and a temperature (in saturated air) between 18.5-23.50C (Prins 1965; Youdeowei 1964). Complex choice experiments demonstrated the dominance of light response over that of humidity, dark situations being chosen irrespective of humidity levels. In view of the susceptibility of mirid nymphs to desiccation, this is a striking result and may well indicate that concealment from predators is of more importance than protection from desiccation (Etwistle 1972). Its bearing on aggregation of mirids on the tree is obvious but its significance, if any, to inter-tree distribution is uncertain.
Routine hand collection has given a maximum number of 1000-2000 capsids/ha. Although individual trees may develop high populations, capsids are highly aggregated and the majority of trees have no capsids. A count of 2-5 live capsids per tree represents a high and damaging population.
It is often a source of perplexity that such low numbers of mirids should be associated with so much damage (Entwistle 1965). This confusion arises partly because the damage is most impressive after peak numbers have passed and partly because peak numbers are genuinely small compared with many other types of insect pests. It has been estimated that 6 mirids per 10 trees of cocoa must be considered dangerously high.
Mirids are particularly night-feeders, but in dull weather, they may be seen feeding during the day (Van Hall 1932).
Economic impact:
Attempts to estimates losses due to mirids are always complicated by the inadequacy of records and the complexity of losses from other causes such as fungus and virus diseases and physiological dieback (Entwistle 1965 and 1972). However, Crop losses in Ghana were estimated at 60,000 to 80,000 tons of dry cocoa (i.e. about 25%) in 1957. More recent studies indicate that about 25-30 % of the national cocoa acreage in Ghana is badly attacked, with an annual crop loss of about 100,000 tons.
Control methods:
Biological control
The use of natural enemies for control of cocoa capsids has not been very encouraging (Entwistle 1972), nevertheless the search for more specific natural enemies has been revived in Ghana in present times.
Chemical control of mirids in Ghana:
The need for routine chemical control was first recognized by Dungeon in 1909 (Dungeon 1910) when he used kerosene/soap as stem paint. Cotterell (1943) tested nicotine sulfate, lime sulfur and Tropical Mortegg and found nicotine sulfate effective at 0.1 per cent while lime sulfur and Tropical Mortegg caused leaf scorch even at low concentrations. However, the use of nicotine sulfate was discontinued because it was found to be expensive and toxic to mammals. When DDT and Lindane (Gammalin) became available after the 2nd world war, they were tested for miricidal control. Lindane gave a better control of mirids than DDT and was subsequently recommended in 1957 at 280 g a.i/ha in 56 liters (1.2 liters/ha) was recommended by CRIG for mirid control, using the motorized knapsack sprayer (Hammond 1957).
Aldrin was recommended in 1959 but was withdrawn in 1960 due to phytotoxicity. The large-scale use of lindane had its adverse effect when in 1962, some populations of Distantiella were found to be resistant to it in the Pankese area (Dunn 1963). The search for substitutes to lindane was therefore directed towards the carbamate and organophosphorus insecticides and latter the pyrethroids. Comparative tests proved the carbamates more suitable for mirid control than the organophosphates and pyrethroids were found too expensive to use on cocoa. Since 1963, CRIG has tested over a hundred chemicals, most of them concentional insecticides, against cocoa mirids in the field.
Presently, spray treatments with Gammalin 20 (280g a.i./ha or 1.2 liters/ha) and Unden (210g a.i./ha or 1.1 liters/ha) are the only chemical protection measures recommended in Ghana. Gammalin 20 and Unden are alternated every two years so as to extend their useful lifetime by reducing the possibility of development of resistance to either chemical.
Application equipment and method:
The question of choice of a suitable spraying machinery and application method is very important since the efficacy of any pesticide depends, to a large extent, on the pesticide being effectively distributed in the actual places where the pest rests on the trees. The machine should be able to deliver the toxicant to achieve a very good coverage of the cocoa tree.
The standard method of pesticide application on mature cocoa in Ghana is by motorized knapsack mist-blowers. Two methods of application have been developed in Ghana; these are either to cover a tree thoroughly on one side from the trunk into the canopy (T1) or to cover both sides with the insecticide (T2).
In neighboring countries of Nigeria, Cote d' lvoire and Cameroon, emphasis is placed more on the hydraulic compression sprayer and other smaller hand-operated types. In Cameroon, hand-held fogging device (the swing fog) is used as the standard method and good mirid control is claimed. This method of application has the advantage of covering large areas quickly but all treatments should be applied in the early morning when the smoke is carried up evenly and held in the canopy for a sufficient length of time to give an effective kill. Presently, another fogging technique, the FUMIVAP that has been recommended in Cote d'Ivoire is being tested in Ghana.
Spray timing:
Early workers recommended two sprays in June/July followed by two additional sprays in November/December (Hammond 1957). Later trials conducted by a Canadian team demonstrated that plots having this recommended schedule had higher mirid population build-up between August and November than the series of plots where four sprays were applied between the period August and December. Presently, spraying is done from August to December leaving out November for pod harvesting. This recommendation is to ensure that treatment coincide with the main period of mirid population increase.
Side effects of toxic chemicals and the need to develop sound pests management strategies:
Concern is being expressed worldwide about the widespread use of poisonous chemicals. Some problems, which have become apparent with total reliance on broad-spectrum insecticides, include:
Recently, methods of reducing the number of spray frequency are being studied at CRIG. Efforts to develop safer and biodegradable alternatives to chemical insecticides have been concerned with behavior modifying compounds such as semiochemicals and the use of natural enemies. Insect growth regulators have given encouraging results for capsid control in the laboratory, but since they act on contact, are unlikely to be effective in the field where capsids are patchily distributed.
The leaves, fruits and the seeds of the neem tree, Azadirachta indica A. Juss: Meliaceae contain active triterpenoids including azadirachtin, Salannin, nimbin, deacetylnimbin and thionemone. Studies have been conducted at CRIG to test the crude seed extract and commercialized seed oil for capsid control.
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