Scales

Scales are small insects (1.0 to 7 mm long), which resemble shells glued to the plant. There are many species (types) of scales on citrus, which vary in shape (round to oval) and colour according to the species.

There are two main groups: hard (armoured) and soft (naked). The armoured scales are the most serious pests.
The most important armoured scales attacking citrus are the red scale (Aonidiella aurantii), the mussel purple scale (Lepidosaphes beckii), and the circular scale (Chrysomphalus aonidum).
The most important soft scales are the soft brown scale (Coccus hesperidum) and the soft green scale (Coccus viridiis or C. alpinus).

Female scales have neither wings nor legs. Females lay eggs under their scale. Some species give birth to young scales directly. Once hatched, the tiny scales, known as crawlers, emerge from under the protective scale. They move in search of a feeding site and do not move afterwards. They suck sap on all plant parts above the ground. Their feeding may cause yellowing of leaves followed by leaf drop, poor growth, dieback of branches, fruit drop, and blemishes on fruits. Leaves may dry when heavily infested, and young trees may die.

Soft scales excrete honeydew, causing growth of sooty mould. In heavy infestations fruits and leaves are heavily coated with sooty mould turning black. Heavy coating with sooty mould reduces photosynthesis. Fruits contaminated with sooty mould loose market value. Ants are usually associated with soft scales. They feed on the honeydew excreted by soft scales, preventing a build-up in sooty moulds, but also protecting the scales from natural enemies.
Armoured scales do not excrete honeydew.

The citrus rust mite (Phyllocoptruta oleivora)

The yellow tiny citrus rust mite attacks mainly the fruit. Its feeding causes the rind of the fruit to turn silvery, reddish brown, or blackish. One result of mite damage is small fruit, which deteriorates rapidly. This damage lowers the market value of the fruit. Heavy populations of the rust mite cause bronzing of leaves and green twigs, and general loss of vitality of the whole tree. Warm and humid conditions favour the development of rust mite.

The citrus bud mite (Aceria sheldoni)

It is a tiny, worm-shaped, creamy white mite. It has only two pair of legs, and is hardly visibly without a magnifying glass. These mites occur in protected places such as under the bracts of buds. They attack the growing points of the twigs, causing malformation of the young leaves and flower buds. As a consequence, the growth of the trees is retarded.

The fruit set can be seriously reduced and infested fruit may be malformed. Bud mites are more abundant during the hot season. Commonly found in developing and leaf buds. Damage under the bracts causes the death of the buds. Flower bud development is reduced, growth is retarded, branches become stunted and deformed, and rosette-shaped leaves are formed. The fruits, particularly in lemons are deformed. Almost all deformed fruits fall off at an early stage of development. Even light infestations may cause damage and control measures should be applied on time and regularly. Spots decrease the market value of the fruit and provide entry for fungal infection.

Damage fruits loose moisture rapidly and do not keep well. Infestation on ripe fruits causes light yellow or silver discolouration. These mites attack all citrus species, but damage is usually worst in lemons. Damaged fruit could drop prematurely or assume abnormal shapes. The juice content of damaged fruit is significantly lower than that of normal fruit.

Mealybugs

Several species of mealybugs attack citrus. They suck sap from tender leaves, petioles and fruit. Feeding on the fruit results in discoloured, bumpy, and scarred fruit, with low market value, or unacceptable for the fresh fruit market. Mealybugs excrete honeydew, which leads to the growth of sooty mould on fruit and leaves. Fruit cover with sooty mould at harvest must be washed. The most important is the citrus mealybug (Planoccous citri).

Ants

Certain ants are major indirect pests in citrus orchards. Although they do not damage the trees, they are associated to honeydew-producing insects such as soft scales, aphids, whiteflies, blackflies and mealybugs.
Natural enemies often keep these insects under control; however, ants feeding on the honeydew give them indirect protection by disturbing natural enemies. As a result numbers of these honeydew producing insects, and indirectly other pests such as armoured scales, may rise to damaging levels.

Ant management does not imply eradication of all ants. There are many different types of ants in citrus orchards. Many of them are important predators of other insects, including pests of citrus. Some of the species that could be a problem due to their association with honeydew-producing insects (e.g. the big headed ant Pheidole megacephala and the pugnacious ant, Anoplolepis custodiens are also beneficial preying on a variety of insects, and are valuable predators on the ground. Therefore these ants should not be destroyed but kept off the trees.

Red fire ants or weaver ants (Oecophylla longinoda)

A particular case is that of the red fire ants or weaver ants which nest on citrus and other fruit trees (guava, soursop, cashewnuts, coconut palms among others). These ants are present in many countries in Africa. They are common in the coastal regions in East Africa.
They built nests on trees by joining leaves with silk produced by the larvae. These ants are very active moving on the trees and on the ground in search of food. They are highly voracious feeding on a large range of insects visiting the trees, and are important in controlling many insect pests in fruit trees and coconut palms. In spite of these benefits, weaver ants are considered by some as a pest due to their aggressiveness combined with painful bites, which makes fruit picking difficult, and to their association with honeydew-producing insects. They can foster the build-up of these insect pests, but it has been observed that they do kill some of them when the amount of honeydew produced by these insects is bigger than the amount required by the colony of weaver ants.

The benefits provided by predatory ants feeding or deterring insect pests must be outweighed against the damage they may cost indirectly. As a whole weaver ants are considered beneficial. They have been used actively in China for the control of citrus pests for centuries (Way and Khoo, 1992). Experienced farmers in Asia and Africa have developed their own methods to deal with the inconvenience of weaver ants during harvesting.

Nematodes

More than 40 nematode species have been associated with citrus worldwide. The economically important species are the citrus nematode (Tylenchulus semipenetrans) and the burrowing nematode (Radopholus similis).

1) The citrus nematode (T. semipenetrans)
It causes a slow decline of citrus trees. Affected trees show reduced vigour, small yellow leaves, defoliation, die-back of twigs, and small fruits. The citrus nematodes are ectoparasitic and sedentary. Only females are parasitic on roots. They are found on the surface of fibrous roots under debris-covered egg masses embedded in a gelatinous matrix. The life cycle, from egg to egg, is completed within 6-8 weeks at temperatures of 24-26° C. Optimal reproduction occurs at 28-31° C. Soil salinity increases the population density of citrus nematode. In affected orchards, populations of the nematode are concentrated in upper soil layers. Movement of plant material and soil is responsible for the spread of the nematode. Also agricultural implements and water (irrigation or rain) spread the nematode in a citrus orchard.

2) The "burrowing nematode" (Radopholus similis)
It is called "burrowing nematode" on account of the cavities and tunnels it produces in the root tissues. Symptoms are generally present on groups of trees that increase in number with time, hence, the name, spreading decline. Symptoms are much more severe than in the case of T. semipenetrans and the spread is much quicker. Affected trees show fewer and smaller leaves and an abundance of dead twigs and branches. Trees wilt during periods of lack of moisture but generally the trees are not killed. It is an endoparasitic and migratory. Two distinct races of the nematode are known: the banana and citrus race. The former is known to attack banana roots but not citrus. The citrus race attacks bananas and citrus. The life cycle requires 18-21 days at 24-26° C, the optimum temperature being 24° C. Burrowing nematodes migrate through roots and from root to root to feed. The nematodes are rarely found in the top 10 cm of the soil, highest populations being between 30 and 180 cm. Primary spread is thorough propagating infested seedlings.

The citrus woolly whitefly (Aleurothrixus floccosus)

The citrus woolly whitefly was reported for the first time in East and Central Africa in the early to mid 90s. Serious attacks on citrus were observed in Kenya, Malawi, Tanzania and Uganda. The adults of this whitefly resemble small white moths, covered with mealy white wax. Eggs are laid on the lower surface of young leaves. The young stages resemble soft scale insects and have a woolly appearance. They produce large quantity of honeydew that leads to the growth of sooty mould on the infested trees. This may cause defoliation, loss of fruits and dwarfing of trees. Small, mottled fruits are produced.

The citrus blackflies (Aleurocanthus woglumi and A. spiniferus)

Adults of the citrus blackflies resemble tiny (1.3 to1.7 mm in length) greyish moths. Eggs are usually laid in a spiral pattern on the lower surface of leaves. The immature stages are shiny black scale-like insects and are up to 1.2 mm in length. A white fringe of wax surrounds the body of older larvae and the pupae.
The insects are most noticeable as groups of very small, black spiny lumps on leaf undersides. They produce a large amount of honeydew, which accumulate on leaves and stems and usually develop black sooty mould fungus, which cover the leaves blackening the foliage and sometimes the whole plant. Ants may be attracted by the honeydew. Heavy infestation causes general weakening and eventual death of plants due to sap loss and the development of sooty mould on leaves. Infested leaves may be distorted.

Citrus aphids (Toxoptera citridus and T. aurantii)

They are small (1 to 3mm in length), brown to black in colour, and may be winged (having 2 pair of wings) or wingless. They feed by sucking on new growth and blossoms. High numbers are found on the leaf surfaces during the period of flushing (production of new shoots) and stems of attacked young shoots die back. Attacked leaves are curled and distorted. Flower buds are damaged or drop. Aphids excrete large amounts of honeydew. Leaves and fruits may turn black due to the growth of sooty mould. Symptoms can be severe on flush growth during dry periods following rainy spells.
Citrus aphids transmit tristeza and other virus diseases in citrus. The black citrus aphid T. citridus is the most efficient vector of the citrus tristeza virus.

The citrus leafminer (Phyllocnistis citrella)

The caterpillar of the citrus leafminer usually attacks young leaves and shoots. It mines the undersurface of young leaves, but it can attack both leaf surfaces, in heavy infestations, and occasionally the fruit. Its feeding causes serpentine mines that have a silvery appearance and reach a length of 5 to 10 cm. The middle of the mines is marked by a light or a dark coloured stripe, which consists of the excreta of the caterpillars. The caterpillars are greenish yellowish and are to 4 mm in length. Caterpillars pupate within the mine, near the leaf margin, under a slight curl of the leaf. The moths are tiny (2 to 3 mm long), greyish white in colour with fringed wings.

Eggs look like small dew drops and are usually laid on the underside of the leaves. Attacked young leaves are twisted, show brown patches of dead tissue and eventually fall off.

Heavy infestations can interfere with photosynthesis because of the reduction in leaf surface. This pest is especially troublesome in citrus nurseries. It can kill young nursery plants. This leafminer was a frequently observed pest during a survey of major citrus pests conducted in Kenya, Malawi, Uganda, Tanzania and Zambia in 1995 (B. Löhr, personal communication).

The African citrus psyllid (Trioza erytreae)

It prefers cool climates and it is found in Kenya only at elevations above 800 m. The adult is about 2 mm long, brownish yellow with long transparent wings with market veins. They resemble winged aphids. The adults jump and fly short distances when disturbed. When feeding, adults take up a distinctive position, with the abdomen raised. The orange-yellow eggs are laid on the edges of tender young leaves. They can be distinguished with the naked eye as a yellow fringe to the leaf. After hatching the nymph moves only a very short distance and settles down to feed on the underside of leaves. Once settled, it does not move again unless disturbed. They resemble small green or yellow scale insects, and are up about 1 mm long. Parasitised nymphs are dark brown to black in colour. Pit-like depressions are formed beneath the nymphs bodies. These depressions look like raised bumps on the upper side of the leaves, and remain even after the nymphs have become adults.

As result of these pock marks young leaves may be severely deformed, and flush growth depressed. They also cause damage by sucking sap from the leaves. However, in general, these types of damage do not seriously affect infested trees. The main damage caused by the citrus psyllid is as the vector of the greening disease, a major disease of citrus. A few psyllids in an orchard can spread the greening disease, but when high numbers are present, the spread is particularly rapid. It is therefore necessary to manage the citrus psyllids to retard the spread of the greening disease.

The citrus thrips (Scirtothrips aurantii)

Citrus thrips are tiny insects (0.7 to 1 mm in length), and orange yellow in colour. Young stages are wingless, but adults have 2 pairs of narrow wings. Damage is caused by larvae and adults feeding on young twigs, leaves and fruits. Thrips feeding produces brown blemishes on the rind. Typical damage is the presence of rings of brown russet marks around the stem of the fruit. The damage is cosmetic and does not affect eating quality. However, external fruit blemishes can be so severe that the fruits are unmarketable. New shoots can be severely damaged. If thrips are abundant on young twigs, their feeding causes deformation of the twigs, which become thickened and distorted. In severe infestations, the leaves are deformed; young leaves are underdeveloped and drop when touched.

The false codling moth (Cryptophlebia leucotreta)

It is small (wingspan of 16-20 mm), dark brown to grey in colour. The moths are active at night. Female moths lay single eggs on ripening citrus fruits. The young caterpillar mines just beneath the surface, or bores into the pith causing premature ripening of the fruit and fruit drop.
The initial symptom on the fruit is a yellowish round spot with a tiny dark centre where the insect entered the fruit. In a later stage brown patches appear on the skin, usually with a hole in the centre. The young caterpillar is creamy-white with a dark brownish head. With age the body turn pinkish red. The fully-grown caterpillar is 15 to 20 mm in length. When mature the caterpillar leaves the fruit and pupates in the soil or beneath surface debris. Navel oranges seem to be the most heavily attacked. Grapefruit is less susceptible. In lemons and limes larval development is rarely, if ever, completed.

Fruit flies (Bactrocera invadens, Ceratitis capitata and C. rosa)

Several species of fruit flies are pests of citrus in Africa. In East Africa the most important are B. invadens, a new species of fruit fly recently introduced in the region, and C. capitata (Sunday Ekesi, personal communication). The female fly lays eggs within the skin of ripening fruits. Spots develop on the skin where eggs were laid and the hatching larva enters the fruit. The attacked area becomes soft, turns brown and decays as a result of secondary infection.

The swallowtail butterfly (Papilio demodocus)

The caterpillars of the swallowtail butterfly are also known as "orange dog". The butterfly is black with yellow markings on the wings, and has a wingspan of about 10 cm. They are common during the rainy season. Female butterflies lay whitish, grey eggs mainly on the tender terminal twigs and leaves. The caterpillars are white-brown, or green in colour. Most spines disappear as the caterpillar grows. Young caterpillars are brownish with white patches and are spiny. They resemble fresh bird droppings. Older caterpillars are green with some light markings and two eye-like spots at both sides of the front part of the body. When disturbed caterpillars shoot out a fleshy, forked retractable organ, through a slit behind the head, which gives off a repulsive smell.

Fully grown caterpillars are about 5 cm long. Caterpillars feed specially on the new growth of citrus trees. They can cause extensive damage to young trees, especially in citrus nurseries where their feeding can cause complete defoliation of the plant.

Damping-off (Rhizoctoni solani) and Phytophthora spp.

Damping-off of citrus is most often caused by Rhizoctonia solanispp. Phytophthora spp. The typical symptom of damping-off is dying of seedlings just after emergence from the soil. However, damping-off fungi can also cause seed rot, resulting in sparse stands of seedlings in nursery beds.

Greening disease

It is caused by a bacterium (Candidatus Liberibacter africanus). The disease is transmitted by citrus psyllids (Trioza erytreae) and through use of budwood obtained from diseased trees. The disease is not soil-borne. It is not seed-borne and it is not mechanically transmitted.

Symptoms on the leaves show mottling, yellowing of veins or zinc defiency (i.e. small leaves, interveinal chlorosis and brush-like growth). Zinc deficiency induced by greening is confined to one or several branches within a tree (sectoral infection).
Trees infected by greening are distributed within the orchard randomly. Affected branches bear few fruits and in some cases do not fruit. The affected fruits are usually under-developed, reduced in size, lopsided, start to colour from the stem end instead of the stylar end as in the case with healthy fruits. Affected fruits drop prematurely. In seedy citrus varieties, seed abortion occurs. Severely diseased trees exhibit open growth, sparse chlorotic foliage, dieback of branches and severe fruit drop.

In Kenya, the disease is not found below 800 m above sea level because both the bacterium causing the disease and citrus psyllids are sensitive to high temperatures. Optimum temperature for symptom expression is 21 to 24°C; symptoms are masked above 26° C. The disease is especially destructive to sweet oranges and mandarins. It is less severe on lemon, grapefruit, citron and West Indian lime.
Rootstocks have no effect on greening disease.

Phaeoramularia fruit and leaf spot

The disease is caused by fungus Phaeoramularia angolensis. The disease is favoured by wet, cool conditions. On leaves, the fungus produces circular, mostly solitary (single) spots that are up to 10 mm in diameter with light brown or greyish centres. Each spot is usually surrounded by a yellow halo. Occasionally, the thin necrotic tissue in the centres of old spots falls out, creating a shot-hole effect. During rains, leaf spots on young leaves often join together ending in generalised chlorosis. Premature defoliation takes place when leaf petioles are infected. On fruit, the spots are circular to irregular in shape or joining together and surrounded by yellow halos. Most spots measure up to 8 mm in diameter. On young fruits, symptoms often start with nipple-like swellings without yellow halos.

Spots on mature fruits are normally flat, and often a dark brown to black sunken margin similar to anthracnose around the spots is observed. Fruits of more than 40 mm in diameter are somehow resistant to the disease. The disease has been observed on all citrus species including grapefruit, lemon, lime, mandarin, pummelo and orange. Grapefruit, mandarin, pummelo and orange are very susceptible. Lemon is less susceptible and lime is least susceptible. The disease can reduce yield by 50 to 100%.

Citrus tristeza virus (CTV)

It has been found in all citrus growing areas of the world. It is spread by infected propagative material and several species of aphids (Toxoptera citricidus, T. aurantii, Aphis gossypii, A. craccivora, A. spiraecola and Myzus persicae).
T. citricidus is the most efficient vector of CTV. The virus has also been transmitted from plant to plant by the use of dodder (Cuscuta americana and C. subinclusa). CTV is not transmitted through citrus seeds. Most species of Citrus are hosts for CTV. The virus has naturally occurring field strains, which vary considerably in their ability to cause symptoms on different host plants and in the intensity of the symptoms expressed.

Symptoms caused by these strains include:
Seedling yellows (SY): This symptom consists of leaf yellowing and stunting in sour orange, grapefruit and lemon seedlings. This is a field problem when trees infected with SY strains of CTV are top-worked with grapefruit or lemon.
Decline on sour orange: Sweet orange, grapefruit or tangerine scions on sour orange rootstock become dwarfed, yellow (chlorotic), and often die. The decline may occur over a period of several years or very rapidly (quick decline). Trees that decline slowly generally have a bulge (swelling) above the bud union, and honeycombing (many fine holes or pitting) is present on the inner face of bark flaps removed from the sour orange rootstock. When trees decline rapidly, honeycombing does not occur, but a brown line may be observed at the bud union after the bark is removed. When budwood infected with decline-inducing strains is propagated on sour orange seedlings, the trees produced are stunted and unthrifty.
Stem-pitting on limes, grapefruit and sweet orange. Severely affected trees are stunted and may have bushy appearance. Leaves are yellow, and the twigs are brittle and break easily when bent. When the bark is removed from the affected twigs, elongated pits are seen in the wood. Trees affected by stem pitting have reduced yield and fruit quality is poor. Some strains cause longitudinal pits in the trunk, resulting in ropey appearance, and when bark is removed from the depressed parts deep pits can be seen in the wood.

Phytophthora-induced diseases (Phytophthora spp.)

They cause the most serious soil-borne diseases of citrus. These fungi are worldwide in distribution and cause citrus production losses in irrigated, arid areas as well as in areas with high rainfall. Diseases caused by Phytophthora spp. include damping-off in seedbeds, gummosis and brown rot of fruits. The most widespread and important Phytophthora spp. are P. nicotianae and P. citrophthora. Others of lesser importance in the tropics are P. citricola, P. hibernalisand P. palmivora. The most serious disease caused by Phytophthora spp. is gummosis (also known as foot rot).

Gummosis: An early symptom of gummosis is gum oozing from small cracks in the infected bark around the bud-union giving the affected trees a bleeding appearance. Citrus gum, which is water soluble, disappears after heavy rains. Severely affected tress have yellow foliage that eventually drops and twigs die-back often with a crop of small-sized fruits still hanging from bare branches. The feeder roots are destroyed when the root cortex is attacked; turn soft and easily separate giving the root system a stringy appearance. In an advanced stage, the trunk becomes girdled (encircled) and the affected trees decline and eventually die.

Gummosis is favoured by high moisture in the soil. Infection of fruit by Phytophthora spp. produces brown rot. The affected area is light brown, leathery and not sunken compared with the adjacent rind. Under humid conditions, white fungal growth (mycelium) forms on the rind surface. In the orchard, fruits on or near the ground become infected when they are splashed with water or come in contact with soil that is infested by Phytophthora spp.

Most of the infected fruits drop, but those that are harvested may not show symptoms until after they have been held in storage for a few days. Brown rot epidemics are usually restricted to areas where rainfall coincides with early stages of fruit maturity. It is important to note that most Phytophthora spp. are seed-borne.

Anthracnose (Colletotrichum spp.)

There are 3 anthracnose diseases of citrus caused by Colletotrichum spp. Post-bloom fruit drop, which affects flowers of all citrus species and induces drop of fruitlets and is caused by C. acutatum. Lime anthracnose, which attacks all juvenile tissues of only Mexican lime, is also caused by this Colletotrichum species. C. gloeosporioides causes a rind blemish on fruit, especially grapefruit, in the field.

Post-bloom fruit drop
Description: C. acutatum infects petals and produces water-soaked lesions that eventually turn pink and then orange brown as the fungus sporulates. Infected fruitlets abscise at the base of the ovary, and the floral disk, calyx, and peduncle remain attached to the tree, forming structures commonly referred to as 'buttons'. Leaves surrounding an affected inflorescence are usually small, chlorotic, and twisted and have enlarged veins. Warm, wet weather favours disease development.

Lime anthracnose
Description: It affects only Mexican lime. It attacks flowers, young leaves, young shoots and fruits. Infected fruitlets abscise, and 'buttons' are produced as in postbloom fruit drop. In severe cases, young leaves become totally blighted and drop, and shoot tips die-back, producing wither tip symptoms. The fruit lesions are often large and deep, and cause fruit distortion. The disease is favoured by warm, wet weather.

Rind blemish on fruit
Description: The disease is caused by C. gloeosporioides. It is particularly severe on grapefruits. The blemish appears as a superficial, reddish brown discolouration, often in the form of tear stains, which usually appears following prolonged light rains in warm weather.