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Mealybug Descriptive Essay

Morton, J. 1987. Tamarind. p. 115–121. In: Fruits of warm climates. Julia F. Morton, Miami, FL.


Tamarindus indica

Of all the fruit trees of the tropics, none is more widely distributed nor more appreciated as an ornamental than the tamarind, Tamarindus indica L. (syns. T.occidentalis Gaertn.; T.officinalis Hook.), of the family Leguminosae. Most of its colloquial names are variations on the common English term. In Spanish and Portuguese, it is tamarindo; in French, tamarin, tamarinier, tamarinier des Indes, or tamarindier; in Dutch and German, tamarinde; in Italian, tamarandizio; in Papiamiento of the Lesser Antilles, tamarijn. In the Virgin Islands, it is sometimes called taman; in the Philippines, sampalok or various other dialectal names; in Malaya, asam jawa; in India, it is tamarind or ambli, imli, chinch, etc.; in Cambodia, it is ampil or khoua me; in Laos, mak kham; in Thailand, ma-kharm; in Vietnam, me. The name "tamarind" with a qualifying adjective is often applied to other members of the family Leguminosae having somewhat similar foliage.
DescriptionThe tamarind, a slow-growing, long-lived, massive tree reaches, under favorable conditions, a height of 80 or even 100 ft (24-30 m), and may attain a spread of 40 ft (12 m) and a trunk circumference of 25 ft (7.5 m). It is highly wind-resistant, with strong, supple branches, gracefully drooping at the ends, and has dark-gray, rough, fissured bark. The mass of bright-green, fine, feathery foliage is composed of pinnate leaves, 3 to 6 in (7.5-15 cm) in length, each having 10 to 20 pairs of oblong leaflets 1/2 to 1 in (1.25-2.5 cm) long and 1/5 to 1/4 in (5-6 mm) wide, which fold at night. The leaves are normally evergreen but may be shed briefly in very dry areas during the hot season. Inconspicuous, inch-wide flowers, borne in small racemes, are 5-petalled (2 reduced to bristles), yellow with orange or red streaks. The flowerbuds are distinctly pink due to the outer color of the 4 sepals which are shed when the flower opens.

The fruits, flattish, beanlike, irregularly curved and bulged pods, are borne in great abundance along the new branches and usually vary from 2 to 7 in long and from 3/4 to 1 1/4 in (2-3.2 cm) in diameter. Exceptionally large tamarinds have been found on individual trees. The pods may be cinnamon-brown or grayish-brown externally and, at first, are tender-skinned with green, highly acid flesh and soft, whitish, under-developed seeds. As they mature, the pods fill out somewhat and the juicy, acidulous pulp turns brown or reddish-brown. Thereafter, the skin becomes a brittle, easily-cracked shell and the pulp dehydrates naturally to a sticky paste enclosed by a few coarse strands of fiber extending lengthwise from the stalk. The 1 to 12 fully formed seeds are hard, glossy-brown, squarish in form, 1/8 to 1/2 in (1.1-1.25 cm) in diameter, and each is enclosed in a parchmentlike membrane.

Origin and DistributionNative to tropical Africa, the tree grows wild throughout the Sudan and was so long ago introduced into and adopted in India that it has often been reported as indigenous there also, and it was apparently from this Asiatic country that it reached the Persians and the Arabs who called it "tamar hindi" (Indian date, from the date-like appearance of the dried pulp), giving rise to both its common and generic names. Unfortunately, the specific name, "indica", also perpetuates the illusion of Indian origin. The fruit was well known to the ancient Egyptians and to the Greeks in the 4th Century B.C.

The tree has long been naturalized in the East Indies and the islands of the Pacific. One of the first tamarind trees in Hawaii was planted in 1797. The tamarind was certainly introduced into tropical America, Bermuda, the Bahamas, and the West Indies much earlier. In all tropical and near-tropical areas, including South Florida, it is grown as a shade and fruit tree, along roadsides and in dooryards and parks. Mexico has over 10,000 acres (4,440 ha) of tamarinds, mostly in the states of Chiapas, Colima, Guerrero, Jalisco, Oaxaca and Veracruz. In the lower Motagua Valley of Guatemala, there are so many large tamarind trees in one area that it is called "El Tamarindal". There are commercial plantings in Belize and other Central American countries and in northern Brazil. In India there are extensive tamarind orchards producing 275,500 tons (250,000 MT) annually. The pulp is marketed in northern Malaya and to some extent wherever the tree is found even if there are no plantations.

VarietiesIn some regions the type with reddish flesh is distinguished from the ordinary brown-fleshed type and regarded as superior in quality. There are types of tamarinds that are sweeter than most. One in Thailand is known as 'Makham waan'. One distributed by the United States Department of Agriculture's Subtropical Horticulture Research Unit, Miami, is known as 'Manila Sweet'.

ClimateVery young trees should be protected from cold but older trees are surprisingly hardy. Wilson Popenoe wrote that a large tree was killed on the west coast of Florida (about 7.5º lat. N) by a freeze in 1884. However, no cold damage was noted in South Florida following the low temperatures of the winter of 1957-1958 which had severe effects on many mango, avocado, lychee and lime trees. Dr. Henry Nehrling reported that a tamarind tree in his garden at Gotha, Florida, though damaged by freezes, always sprouted out again from the roots. In northwestern India, the tree grows well but the fruits do not ripen. Dry weather is important during the period of fruit development. In South Malaya, where there are frequent rains at this time, the tamarind does not bear.

SoilThe tree tolerates a great diversity of soil types, from deep alluvial soil to rocky land and porous, oolitic limestone. It withstands salt spray and can be planted fairly close to the seashore.

PropagationTamarind seeds remain viable for months, will germinate in a week after planting. In the past, propagation has been customarily by seed sown in position, with thorny branches protecting the young seedlings. However, today, young trees are usually grown in nurseries. And there is intensified interest in vegetative propagation of selected varieties because of the commercial potential of tamarind products. The tree can be grown easily from cuttings, or by shield-budding, side-veneer grafting, or air-layering.

CultureNursery-grown trees are usually transplanted during the early rainy season. If kept until the second rainy season, the plants must be cut back and the taproot trimmed. Spacing may be 33 to 65 ft (10-20 m) between trees each way, depending on the fertility of the soil. With sufficient water and regular weeding, the seedlings will reach 2 ft (60 cm) the first year and 4 ft (120 cm) by the second year.

In Madagascar, seedlings have begun to bear in the 4th year; in Mexico, usually in the 5th year; but in India, there may be a delay of 10 to 14 years before fruiting. The tree bears abundantly up to an age of 50-60 years or sometimes longer, then productivity declines, though it may live another 150 years.

SeasonMexican studies reveal that the fruits begin to dehydrate 203 days after fruit-set, losing approximately 1/2 moisture up to the stage of full ripeness, about 245 days from fruit-set. In Florida, Central America, and the West Indies, the flowers appear in summer, the green fruits are found in December and January and ripening takes place from April through June. In Hawaii the fruits ripen in late summer and fall.

HarvestingTamarinds may be left on the tree for as long as 6 months after maturity so that the moisture content will be reduced to 20% or lower. Fruits for immediate processing are often harvested by pulling the pod away from the stalk which is left with the long, longitudinal fibers attached. In India, harvesters may merely shake the branches to cause mature fruits to fall and they leave the remainder to fall naturally when ripe. Pickers are not allowed to knock the fruits off with poles as this would damage developing leaves and flowers. To keep the fruit intact for marketing fresh, the stalks must be clipped from the branches so as not to damage the shell,

YieldA mature tree may annually produce 330 to 500 lbs (150-225 kg) of fruits, of which the pulp may constitute 30 to 55%, the shells and fiber, 11 to 30 %, and the seeds, 33 to 40%.

Keeping QualityTo preserve tamarinds for future use, they may be merely shelled, layered with sugar in boxes or pressed into tight balls and covered with cloth and kept in a cool, dry place. For shipment to processors, tamarinds may be shelled, layered with sugar in barrels and covered with boiling sirup. East Indians shell the fruits and sprinkle them lightly with salt as a preservative. In Java, the salted pulp is rolled into balls, steamed and sun-dried, then exposed to dew for a week before being packed in stone jars. In India, the pulp, with or without seeds and fibers may be mixed with salt (10%), pounded into blocks, wrapped in palmleaf matting, and packed in burlap sacks for marketing. To store for long periods, the blocks of pulp may be first steamed or sun-dried for several days.

Pests and DiseasesOne of the major pests of the tamarind tree in India is the Oriental yellow scale, Aonidiella orientalis. Tamarind scale, A.tamarindi, and black, or olive, scale, Saissetia oleae, are also partial to tamarind but of less importance. Butani (1970) lists 8 other scale species that may be found on the tree, the young and adults sucking the sap of buds and flowers and accordingly reducing the crop.

The mealybug, Planococcus lilacinus, is a leading pest of tamarind in India, causing leaf-fall and sometimes shedding of young fruits. Another mealybug, Nipaecoccus viridis, is less of a menace except in South India where it is common on many fruit trees and ornamental plants. Chionaspis acuminata-atricolor and Aspidiotus spp., suck the sap of twigs and branches and the latter also feeds on young fruits. White grubs of Holotrichia insularis may feed on the roots of young seedlings. The nematodes, Xiphinema citri and Longidorus elongatus may affect the roots of older trees. Other predators attacking the leaves or flowers include the caterpillars, Thosea aperiens, Thalarsodes quadraria, Stauropus alternus, and Laspeyresia palamedes; the black citrus aphid, Toxoptera aurantii, the whitefly, Acaudaleyrodes rachispora; thrips, Ramaswamia hiella subnudula, Scirtothrips dorsalis, and Haplothrips ceylonicus; and cow bugs, Oxyrhachis tarandus, Otinotus onerotus, and Laptoentrus obliquis.Fruit borers include larvae of the cigarette beetle, Lasioderma serricorne, also of Virachola isocrates, Dichocrocis punctiferalis, Tribolium castaneum, Phycita orthoclina, Cryptophlebia (Argyroploca) illepide, Oecadarchis sp., Holocera pulverea, Assara albicostalis, Araecerus suturalis, Aephitobius laevigiatus, and Aphomia gularis. The latter infests ripening pods on the tree and persists in the stored fruits, as do the tamarind beetle, Pachymerus (Coryoborus) gonogra, and tamarind seed borer, Calandra (Sitophilus) linearis. The rice weevil, Sitophilus oryzae, the rice moth, Corcyra cepholonica, and the fig moth, Ephestia cautella, infest the fruits in storage. The lesser grain borer, Rhyzopertha dominica bores into stored seeds.

In India, a bacterial leaf-spot may occur. Sooty mold is caused by Meliola tamarindi. Rots attacking the tree include saprot, Xylaria euglossa, brownish saprot, Polyporus calcuttensis, and white rot, Trametes floccosa. The separated pulp has good keeping quality but is subject to various molds in refrigerated storage.

Food UsesThe food uses of the tamarind are many. The tender, immature, very sour pods are cooked as seasoning with rice, fish and meats in India. The fully-grown, but still unripe fruits, called "swells" in the Bahamas, are roasted in coals until they burst and the skin is then peeled back and the sizzling pulp dipped in wood ashes and eaten. The fully ripe, fresh fruit is relished out-of-hand by children and adults, alike. The dehydrated fruits are easily recognized when picking by their comparatively light weight, hollow sound when tapped and the cracking of the shell under gentle pressure. The shell lifts readily from the pulp and the lengthwise fibers are removed by holding the stem with one hand and slipping the pulp downward with the other. The pulp is made into a variety of products. It is an important ingredient in chutneys, curries and sauces, including some brands of Worcestershire and barbecue sauce, and in a special Indian seafood pickle called "tamarind fish". Sugared tamarind pulp is often prepared as a confection. For this purpose, it is desirable to separate the pulp from the seeds without using water. If ripe, fresh, undehydrated tamarinds are available, this may be done by pressing the shelled and defibered fruits through a colander while adding powdered sugar to the point where the pulp no longer sticks to the fingers. The seeded pulp is then shaped into balls and coated with powdered sugar. If the tamarinds are dehydrated, it is less laborious to layer the shelled fruits with granulated sugar in a stone crock and bake in a moderately warm oven for about 4 hours until the sugar is melted, then the mass is rubbed through a sieve, mixed with sugar to a stiff paste, and formed into patties. This sweetmeat is commonly found on the market in Jamaica, Cuba and the Dominican Republic. In Panama, the pulp may be sold in corn husks, palmleaf fiber baskets, or in plastic bags.

Tamarind ade has long been a popular drink in the Tropics and it is now bottled in carbonated form in Guatemala, Mexico, Puerto Rico and elsewhere. Formulas for the commercial production of spiced tamarind beverages have been developed by technologists in India. The simplest home method of preparing the ade is to shell the fruits, place 3 or 4 in a bottle of water, let stand for a short time, add a tablespoonful of sugar and shake vigorously. For a richer beverage, a quantity of shelled tamarinds may be covered with a hot sugar sirup and allowed to stand several days (with or without the addition of seasonings such as cloves, cinnamon, allspice, ginger, pepper or lime slices) and finally diluted as desired with ice water and strained.

In Brazil, a quantity of shelled fruits may be covered with cold water and allowed to stand 10 to 12 hours, the seeds are strained out, and a cup of sugar is added for every 2 cups of pulp; the mixture is boiled for 15 to 20 minutes and then put up in glass jars topped with paraffin. In another method, shelled tamarinds with an equal quantity of sugar may be covered with water and boiled for a few minutes until stirring shows that the pulp has loosened from the seeds, then pressed through a sieve. The strained pulp, much like apple butter in appearance, can be stored under refrigeration for use in cold drinks or as a sauce for meats and poultry, plain cakes or puddings. A foamy "tamarind shake" is made by stirring this sauce into an equal amount of dark-brown sugar and then adding a tablespoonful of the mixture to 8 ounces of a plain carbonated beverage and whipping it in an electric blender.

If twice as much water as tamarinds is used in cooking, the strained product will be a sirup rather than a sauce. Sometimes a little soda is added. Tamarind sirup is bottled for domestic use and export in Puerto Rico. In Mayaguez, street vendors sell cones of shaved ice saturated with tamarind sirup. Tamarind pulp can be made into a tart jelly, and tamarind jam is canned commercially in Costa Rica. Tamarind sherbet and ice cream are popular and refreshing. In making fruit preserves, tamarind is sometimes combined with guava, papaya or banana. Sometimes the fruit is made into wine.

Inasmuch as shelling by hand is laborious and requires 8 man-hours to produce 100 lbs (45 kg) of shelled fruits, food technologists at the University of Puerto Rico have developed a method of pulp extraction for industrial use. They found that shelling by mechanical means alone is impossible because of the high pectin and low moisture content of the pulp. Therefore, inspected and washed pods are passed through a shell-breaking grater, then fed into stainless steel tanks equipped with agitators. Water is added at the ratio of 1:1 1/2 or 1:2 pulp/water, and the fruits are agitated for 5 to 7 minutes. The resulting mash is then passed through a screen while nylon brushes separate the shells and seeds. Next the pulp is paddled through a finer screen, pasteurized, and canned.

Young leaves and very young seedlings and flowers are cooked and eaten as greens and in curries in India. In Zimbabwe, the leaves are added to soup and the flowers are an ingredient in salads.

Tamarind seeds have been used in a limited way as emergency food. They are roasted, soaked to remove the seedcoat, then boiled or fried, or ground to a flour or starch. Roasted seeds are ground and used as a substitute for, or adulterant of, coffee. In Thailand they are sold for this purpose. In the past, the great bulk of seeds available as a by-product of processing tamarinds, has gone to waste. In 1942, two Indian scientists, T. P. Ghose and S. Krishna, announced that the decorticated kernels contained 46 to 48% of a gel-forming substance. Dr. G. R. Savur of the Pectin Manufacturing Company, Bombay, patented a process for the production of a purified product, called "Jellose", "polyose", or "pectin", which has been found superior to fruit pectin in the manufacture of jellies, jams, and marmalades. It can be used in fruit preserving with or without acids and gelatinizes with sugar concentrates even in cold water or milk. It is recommended as a stabilizer in ice cream, mayonnaise and cheese and as an ingredient or agent in a number of pharmaceutical products.

Food Value Per 100 g of Edible Portion

Pulp (ripe) *Leaves (young)Flowers
Moisture28.2-52 g70.5 g80 g
Protein3.10 g5.8 g0.45 g
Fat0.1 g2.1 g1.54 g
Fiber5.6 g1.9 g1.5 g
Carbohydrates67.4 g18.2 g
Invert Sugars30-41 g
(70% glucose; 30% fructose)
Ash2.9 g1.5 g0.72 g
Calcium35-170 mg101 mg35.5 mg
Magnesium71 mg
Phosphorus54-110 mg140 mg45.6 mg
Iron1.3-10.9 mg5.2 mg1.5 mg
Copper2.09 mg
Chlorine94 mg
Sulfur63 mg
Sodium24 mg
Potassium375 mg
Vitamin A15 I.U.250 mcg0.31 mg
Thiamine0.16 mg0.24 mg0.072 mg
Riboflavin0.07 mg0.17 mg0.148 mg
Niacin0.6-0.7 mg4.1 mg1.14 mg
Ascorbic Acid0.7-3.0 mg3.0 mg13.8 mg
Oxalic Acid196 mg
Tartaric Acid8-23.8 mg
Oxalic Acidtrace only

*The pulp is considered a promising source of tartaric acid, alcohol (12% yield) and pectin (2 1/2% yield). The red pulp of some types contains the pigment, chrysanthemin.

Seeds contain approximately 63%starch, 14-18%albuminoids, and 4.5-6.5%of a semi-drying oil.

Food ValueAnalyses of the pulp are many and varied. Roughly, they show the pulp to be rich in calcium, phosphorus, iron, thiamine and riboflavin and a good source of niacin. Ascorbic acid content is low except in the peel of young green fruits.

Other Uses

Fruit pulp:

in West Africa, an infusion of the whole pods is added to the dye when coloring goat hides. The fruit pulp may be used as a fixative with turmeric or annatto in dyeing and has served to coagulate rubber latex. The pulp, mixed with sea water, cleans silver, copper and brass.

Leaves: The leaves are eaten by cattle and goats, and furnish fodder for silkworms–Anaphe sp. in India, Hypsoides vuilletii in West Africa. The fine silk is considered superior for embroidery.

Tamarind leaves and flowers are useful as mordants in dyeing. A yellow dye derived from the leaves colors wool red and turns indigo-dyed silk to green. Tamarind leaves in boiling water are employed to bleach the leaves of the buri palm (Corypha elata Roxb.) to prepare them for hat-making. The foliage is a common mulch for tobacco plantings.

Flowers: The flowers are rated as a good source of nectar for honeybees in South India. The honey is golden-yellow and slightly acid in flavor.

Seeds: The powder made from tamarind kernels has been adopted by the Indian textile industry as 300% more efficient and more economical than cornstarch for sizing and finishing cotton, jute and spun viscose, as well as having other technical advantages. It is commonly used for dressing homemade blankets. Other industrial uses include employment in color printing of textiles, paper sizing, leather treating, the manufacture of a structural plastic, a glue for wood, a stabilizer in bricks, a binder in sawdust briquettes, and a thickener in some explosives. It is exported to Japan, the United States, Canada and the United Kingdom.

Tamarind seeds yield an amber oil useful as an illuminant and as a varnish especially preferred for painting dolls and idols. The oil is said to be palatable and of culinary quality. The tannin-rich seedcoat (testa) is under investigation as having some utility as an adhesive for plywoods and in dyeing and tanning, though it is of inferior quality and gives a red hue to leather.

Wood: The sapwood of the tamarind tree is pale-yellow. The heartwood is rather small, dark purplish-brown, very hard, heavy, strong, durable and insect-resistant. It bends well and takes a good polish and, while hard to work, it is highly prized for furniture, panelling, wheels, axles, gears for mills, ploughs, planking for sides of boats, wells, mallets, knife and tool handles, rice pounders, mortars and pestles. It has at times been sold as "Madeira mahogany". Wide boards are rare, despite the trunk dimensions of old trees, since they tend to become hollow-centered. The wood is valued for fuel, especially for brick kilns, for it gives off an intense heat, and it also yields a charcoal for the manufacture of gun-powder. In Malaysia, even though the trees are seldom felled, they are frequently topped to obtain firewood. The wood ashes are employed in tanning and in de-hairing goatskins. Young stems and also slender roots of the tamarind tree are fashioned into walking-sticks.

Twigs and barks: Tamarind twigs are sometimes used as "chewsticks" and the bark of the tree as a masticatory, alone or in place of lime with betelnut. The bark contains up to 7% tannin and is often employed in tanning hides and in dyeing, and is burned to make an ink. Bark from young trees yields a low-quality fiber used for twine and string. Galls on the young branches are used in tanning.

Lac: The tamarind tree is a host for the lac insect, Kerria lacca, that deposits a resin on the twigs. The lac may be harvested and sold as stick-lac for the production of lacquers and varnish. If it is not seen as a useful byproduct, tamarind growers trim off the resinous twigs and discard them.

Medicinal Uses:Medicinal uses of the tamarind are uncountable. The pulp has been official in the British and American and most other pharmacopoeias and some 200,000 lbs (90,000 kg) of the shelled fruits have been annually imported into the United States for the drug trade, primarily from the Lesser Antilles and Mexico. The European supply has come largely from Calcutta, Egypt and the Greater Antilles. Tamarind preparations are universally recognized as refrigerants in fevers and as laxatives and carminatives. Alone, or in combination with lime juice, honey, milk, dates, spices or camphor, the pulp is considered effective as a digestive, even for elephants, and as a remedy for biliousness and bile disorders, and as an antiscorbutic. In native practice, the pulp is applied on inflammations, is used in a gargle for sore throat and, mixed with salt, as a liniment for rheumatism. It is, further, administered to alleviate sunstroke, Datura poisoning, and alcoholic intoxication. In Southeast Asia, the fruit is prescribed to counteract the ill effects of overdoses of false chaulmoogra, Hydnocarpus anthelmintica Pierre, given in leprosy. The pulp is said to aid the restoration of sensation in cases of paralysis. In Colombia, an ointment made of tamarind pulp, butter, and other ingredients is used to rid domestic animals of vermin.

Tamarind leaves and flowers, dried or boiled, are used as poultices for swollen joints, sprains and boils. Lotions and extracts made from them are used in treating conjunctivitis, as antiseptics, as vermifuges, treatments for dysentery, jaundice, erysipelas and hemorrhoids and various other ailments. The fruit shells are burned and reduced to an alkaline ash which enters into medicinal formulas. The bark of the tree is regarded as an effective astringent, tonic and febrifuge. Fried with salt and pulverized to an ash, it is given as a remedy for indigestion and colic. A decoction is used in cases of gingivitis and asthma and eye inflammations; and lotions and poultices made from the bark are applied on open sores and caterpillar rashes. The powdered seeds are made into a paste for drawing boils and, with or without cumin seeds and palm sugar, are prescribed for chronic diarrhea and dysentery. The seedcoat, too, is astringent, and it, also, is specified for the latter disorders. An infusion of the roots is believed to have curative value in chest complaints and is an ingredient in prescriptions for leprosy.

The leaves and roots contain the glycosides: vitexin, isovitexin, orientin and isoorientin. The bark yields the alkaloid, hordenine.

SuperstitionsFew plants will survive beneath a tamarind tree and there is a superstition that it is harmful to sleep or to tie a horse beneath one, probably because of the corrosive effect that fallen leaves have on fabrics in damp weather. Some African tribes venerate the tamarind tree as sacred. To certain Burmese, the tree represents the dwelling-place of the rain god and some hold the belief that the tree raises the temperature in its immediate vicinity. Hindus may marry a tamarind tree to a mango tree before eating the fruits of the latter. In Nyasaland, tamarind bark soaked with corn is given to domestic fowl in the belief that, if they stray or are stolen, it will cause them to return home. In Malaya, a little tamarind and coconut milk is placed in the mouth of an infant at birth, and the bark and fruit are given to elephants to make them wise.

1. Introduction

Exallomochlus hispidus Morrison (Hemiptera: Pseudococcidae) is a mealybug native to Southeast Asia [1]. It is known to be a polyphagous insect, and members of 25 plant families have been recorded as hosts [2]. Williams reported that the mealybug occurs on 41 host plants belonging to 30 families in the Southeast Asian region [1]. In Indonesia, E. hispidus attacks high-value fruit crops such as mangosteen (Garcinia mangostana L.), soursop (Annona muricata L.), guava (Psidium guajava L.), rambutan (Nephelium lappaceum L.), durian (Durio zibethinus Murray), and duku/langsat (Lansium domesticum Correa) [1]. Exallomochlus hispidus has become a serious quarantine because it is often carried on the mangosteen fruit, an important export fruit commodity for Indonesia [3].

There are no reports of actual economic losses associated with any reduction in yield of G. mangostana fruits because of E. hispidus infestation. However, this mealybug can reduce the performance of the plants because its sugary honeydew excretions on nearby plant surfaces serve as a growth medium for sooty mold fungi, impairing photosynthesis and blackening the fruits [1]. The mealybug colonies are often surrounded by ants, which could put off consumers, particularly when handling or eating the fruit. The primary problem encountered with mealybugs affecting the economic value of the mangosteen fruits is the strict phytosanitary requirements of importing countries, like Australia, the United States, and New Zealand [3]; for example, New Zealand includes E. hispidus among the listed quarantine pests from Indonesia [4].

Farmers in Indonesia usually cultivate G. mangostana by intercropping with other fruit plants, like banana (Musa paradisiaca L.), coconut palm (Cocos nucifera L.), duku/langsat, durian, guava, jackfruit (Artocarpus heterophyllus Lam.), soursop, and rambutan, among others [5]. The intercropped plants also serve as alternate hosts for E. hispidus, which infest mangosteen, and could influence its life cycle parameters. Past research has shown that the host plant species can have a significant effect on mealybug development and reproduction, for example in the mango mealybug (Rastrococcus iceryoides) [6], and biological parameters can be changed when insects are reared on alternative media in the laboratory. For example, kabocha squash (Cucurbita maxima L.) is commonly used as a medium for rearing mealybugs in the laboratory [6,7,8]. Research on the bionomics of E. hispidus on mangosteen and other hosts has not yet been reported. Therefore, this research aimed to investigate the development and reproduction of E. hispidus on mangosteen and some of the other fruits that are cultivated around it: kabocha, soursop, and guava. The host plants used in this research represent some of the economically important fruit and intercropping plants grown on mangosteen plantations in Indonesia.

2. Materials and Methods

2.1. The Preparation of Fruit Hosts and Rearing of Mealybug E. hispidus

The source used for E. hispidus colonies was infested G. mangostana fruits from Bogor, West Java, Indonesia. The mealybugs were reared on kabocha fruits in the laboratory for three generations before the start of the experiment. When the size of the E. hispidus colony reached the maximum or the kabocha fruits began to wilt, the kabocha was replaced with fresh fruit. The colony was maintained at room conditions (27 °C ± 1 °C, in 70% ± 10% relative humidity, and a photoperiod of 12 h light and 12 h dark).

The experimental host fruits were mangosteen, guava, kabocha, and soursop. Mature mangosteen and guava fruits were bought from a supermarket, while kabocha and soursop fruits were bought at Kramat Jati Central Market, Jakarta. Before this experiment was conducted, E. hispidus was reared on host fruits (mangosteen, guava, kabocha, and soursop) for one generation to adapt to the experimental host [6]. The experimental host fruits were first washed in a sodium hypochlorite (3% v/v) solution three times to avoid any mold contamination of the fruit surface, followed by air-drying before being placed individually in insect rearing cages. The mealybugs were transferred using a soft brush from the adaptation to the experimental fruits [6,7]. Each rearing cage was made from a plastic cylinder (17 cm bottom diameter and 21 cm top diameter × 20 cm height) and the top was covered with a fine screen cloth to prevent the crawlers from escaping. The experimental units were maintained at room conditions as describe above. The experimental fruits were replaced twice a week and mealybugs transferred to fresh fruits using a soft brush.

2.2. Morphometrics of Adult Female E. hispidus

Twenty crawlers of E. hispidus were isolated from each adaptation host fruit and transferred into rearing cages containing experimental host fruit: mangosteen, guava, kabocha, and soursop fruit. The colonies were maintained under ambient temperatures and humid room conditions. Each adult female mealybug, 3–4 days after molting to the adult stage, was used for morphometric study and prepared as a whole-body-slide-mounted specimen observed under a stereo microscope Motic SMZ-171 using the method described in William and Watson [9]. The body length (mm) was measured digitally along the dorsal midline from the front of the head to the tip of the abdomen, and the width (mm) measured transversely between the lateral margins of the metathorax. The measurement data of 20 individuals from each host were automatically recorded using the Motic Image Plus version 2.0 (Motic Incorporation Ltd, Causeway, Hongkong, China) program [10].

2.3. Growth, Development, and Reproduction of E. hispidus

Twenty crawlers of E. hispidus were isolated from the adaptation colony and separately maintained in rearing cages on the experimental host fruit (i.e., mangosteen, guava, kabocha, and soursop fruit) as described previously. The growth and development of 20 crawlers each host were monitored until their death. Record of mealybug development periods on each host fruit was recorded every day, including nymphal stadium, prebirthing, birthing, postbirthing, and adult longevity. Molting was determined by finding white exuviae in the cages. The life cycle of the mealybug was recorded as starting with nymphs being laid, and ended with adulthood at the beginning of the birthing period. The fecundity of emerging adults was observed by counting the progeny daily until reproduction ceased (the postbirthing period).

2.4. Water, Nitrogen, and Total Sugar Content of the Host Fruits

Variations in the levels of nutrient such as water, nitrogen, and sugar in each host play an important role in the viability, growth, and reproduction of the mealybugs. Measurements of water, nitrogen, and total sugar content were made for the whole fruits of soursop, kabocha, and guava, and for the rind of mangosteen. The water content analysis was based on the difference between wet and dry weights. The estimation of nitrogen and total sugar contents were made using the Kjeldahl and Anthrone methods, respectively [9].

2.5. Data Analysis

The data were analyzed through one-way analysis of variance using the SAS program [10]. The means were separated by Tukey’s test on α = 0.05. The daily fecundity was analyzed by descriptive analysis and was recorded as a daily fecundity figure.

3. Results

3.1. The Morphology of E. hispidus

Body length: mealybugs on the mangosteen fruit were the shortest (average length 2.03 mm) and were significantly different from the mealybugs reared on the other hosts (Figure 1). Mealybugs reared on kabocha were the longest (average length 2.33 mm), but not significantly different from those reared on soursop (average length 2.31 mm). The mealybugs reared on guava were shorter (average length 2.15 mm) than those on kabocha and soursop, but they were longer than on mangosteen (average length 2.03 mm); this difference was statistically significant. Body width: the mealybugs reared on mangosteen had the smallest width (average 1.68 mm), which was significantly different from that of mealybugs reared on the three other hosts (Figure 1). The widths of mealybugs reared on kabocha and soursop (average widths 1.89 and 1.88 mm, respectively) were larger that of those reared on mangosteen (average 1.68 mm) and guava (average 1.76 mm); these results were significantly different (Figure 1).

3.2. The Bionomics of E. hispidus

Female E. hispidus mealybugs pass through three instar nymphal stages before the adult stage. The overall duration of development of E. hispidus (from the birth of the first instar nymph to the final molt to the adult stage) varied significantly between host plants. The development of first-instar nymphs on kabocha and soursop took about 7.7 to 8.8 days, a significantly shorter time than the development on guava and mangosteen (about 8.8–9.1 days). The shortest development of the second and the third-instar nymphs on kabocha, at about 6.0 and 6.9 days, which differed significantly from the development on the three other hosts, soursop, guava, and mangosteen, (between 7.1, 7.3, 7.3 and 8.2, 8.2, 8.4 days, respectively). The shortest life cycle (about 32 days) occurred on kabocha, followed by soursop (about 35 days); the longest life cycle was on mangosteen and guava fruits (about 38 days on both hosts) (Table 1).

Starting as newly emerged adults, the female E. hispidus went through three periods of reproductive development before death. Table 2 shows that the prebirthing period of E. hispidus was about 13.5–14.0 days on mangosteen and guava host fruits, which was significantly longer than the approximately 11.8–12.0 days on kabocha and soursop. The shortest offspring production period, which is the middle stage of reproductive development, was about 6.2 days on mangosteen, similar to that on soursop (about 7.4 days) but significantly different from the longest periods, about 8.9 and 10.0 days, on kabocha and guava, respectively. At the end of reproductive development, the mealybug took a break in reproduction before dying. The postnatal period of E. hispidus on kabocha was about 0.6 days, which was significantly shorter than on guava (about 1.4 days) but not significantly different from that on mangosteen and guava (about 1.1–1.2 days). The longevity of adult females was not very variable between the four host fruits, although the total adult life stage on guava (about 25.3 days) was longer than on the three other hosts, mangosteen, kabocha, and soursop (about 20.7, 21.3 days).

3.3. The Reproduction of E. hispidus

The host plant used for rearing of E. hispidus mealybugs influenced the fecundity of the adults produced. Figure 2 shows that the lowest number of offspring was produced by adults fed on mangosteen followed by those reared on guava and soursop (about 33–72, 45–159, and 53–168, respectively), with averages values of 46, 72, and 90 nymphs, respectively. The highest numbers occurred on kabocha fruit, with between 72 and 203 nymphs and an average of 101 nymphs. The nymph production on mangosteen was significantly different from that on kabocha, soursop, and guava, while nymph production on kabocha was not significantly different from that on soursop but was still significantly more than that on guava fruits.

The nymphal production in the early birthing period was highest and declined over the period with time of reproduction. Production of nymphs was the greatest on the second day for all host fruits, except guava, for which the highest production was on the third day. The longest birthing period was on guava (17 days), while the shortest was on mangosteen (10 days) (Figure 3).

3.4. Water, Nitrogen, and Total Sugar Content in Host Fruits

The nutrient content differed according to the host fruit (Table 3). Relative to the other fruits, the water content was the highest in the kabocha fruit (93.8%) and the lowest in the mangosteen fruit (64.5%) (Table 3). The nitrogen content was also the highest in the kabocha (2.0%) and the lowest in the mangosteen fruit (0.4). The total sugar content was the highest in the guava fruit (10.5%) and the lowest in the mangosteen fruit (2.0%).

4. Discussion

The body of adult female of E. hispidus is oval, fairly flat, and light tan in color. The body of the first-instar nymph (crawler) is light tan in color and is covered with a thin layer of mealy white wax that becomes thicker as the nymph grows. The first-instar nymphs (or crawlers) walk about actively to disperse to other hosts, or are picked up and transferred by the wind [11]; so crawlers can move from mangosteen plants to other host plants in the surrounding area. The second and third-instar nymphs as well as the adults are largely sessile and live in a colony.

The E. hispidus reared on different hosts had different adult body sizes (Figure 1). Those fed on mangosteen and guava were smaller than those reared on kabocha and soursop. Differences in body size on different hosts also have been reported for Rastrococcus iceryoides (Green) reared on kabocha and mango (Mangifera indica L.), whose bodies were longer than those reared on coffee (Coffea arabica L.), and their width on kabocha, mango, Jerusalem thorn (Parkinsonia aculeata L.), and pigeon pea (Cajanus cajan (L.) Millspaugh) was greater than in those on weeping fig (Ficus benjamina L.) and arabica coffee [6]. Similarly, the body size of Dysmicoccus brevipes (Cockerell) fed on pineapple [Ananas comosus (L.) Merr.] was found to be larger than that of specimens reared on galangal/kencur (Kaempferia galanga L.) [12].

The period of nymphal development influences the fitness of the mealybug [6]. The development of E. hispidus on kabocha was the shortest, followed by that on soursop, guava, and mangosteen, respectively. These findings agree with a study by Tanga et al. [6], which reported the development time of mealybug R. iceryoides to be shortest when reared on kabocha. The fitness of E. hispidus fitness is important because it will determine whether the mealybug is likely to survive an export journey, and potentially survive on a new host in the destination country. The U.S. Quarantine Agency has found specimens of E. hispidus on soursop, durian, mangosteen, duku/langsat, and rambutan from Indonesia, Malaysia, the Philippines, Singapore, Thailand, and Vietnam at U.S. ports of entry [1].

Exallomochlus hispidus mealybugs developed more slowly on mangosteen than on other hosts; however, mangosteen was still able to support the development and reproduction of the insect. Insects select host plants or certain parts of a plant that provide sufficient nutrition as their hosts to fulfill their needs [13]. The extended nymphal period on D. brevipes recorded by Bertin et al. was caused by low nutrition [7]. Tanga et al. [6] reported that the development of R. iceryoides takes longer on weeping fig and arabica coffee and there are fewer survivors on these two hosts. Nevertheless, both these hosts do support the development of R. iceryoides. The slower development is suspected to be caused by constituent compounds and physiological barriers that lead to R. iceryoides eating less, which slows development and decreases the number of survivors to adulthood [6]. Another study mentions that the total development period of D. brevipes on pineapple was 32.1 days, which is shorter than its development on galangal, which was 35.6 days [14].

In the present study, the host fruits were replaced twice a week and mealybugs were transferred to the fresh fruit. In nature, mealybugs live on host fruit that has not been picked, so this substrate differs from the picked fruit used in the laboratory. Furthermore, after picking the mangosteen rind quickly hardens during storage, and the physiological changes in the fruit can be expected to affect the growth of mealybugs. Maharani et al. 2016 reported that Paracoccus marginatus maintained on cut leaves of papaya (Carica papaya L.) produced 29.3–79.1 fewer eggs than those reared on papaya seedlings, which produced 157.5–324.6 eggs [14].

The results of the present study indicate that the duration of mealybug development depends on the hosts (Table 1). All four hosts supported the development and reproduction of the E. hispidus mealybug, which agrees with results reported by Williams [1].

Exallomochlus hispidus

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