National Program for the Prevention of Huanglongbing (HLB - ex Greening) disease

Clara S. García Darderes, Agricultural Engineer – cdardere@senasa.gov.ar

What is Huanglongbing (HLB - ex Greening) disease?

Huanglongbing is one of the most destructive diseases of citrus trees. It is caused by Candidatus Liberibacter spp., a bacterium restricted to the vascular tissues and which is propagated by insects and infected buds (propagation material). The bacterium disperses very quickly and is very difficult to control. A consequence of its harmful activity is that the lifespan of the affected plant is rapidly reduced. Huanglongbing affects all young and adult citrus plants; however, it does not affect people’s or animals’ health.

Huanglongbing is a Chinese word meaning “yellow dragon disease”. It was first detected in China in 1919 and occurs in 40 countries in Asia, Africa and Oceania, as well as in the northern and southern regions of American countries.

HLB was detected in the state of Sao Paulo, Brazil in February 2004. In 2005, the United States Department of Agriculture confirmed that infected leaves and fruits were spotted in southern Florida and, later, in Louisiana. Nowadays, the disease can be found in Cuba (2007), Dominican Republic (2008) and, more recently, in Belize and Mexico, where the disease has been detected in insects (i.e. D. citri). In Mexico, the disease was detected in Tizimín, Yucatán (2009).

• Worldwide distribution of HLB disease (Spanish version available)

Origins:
The disease comes from two places: Africa and Asia. Candidus liberibacter (the causal bacterium) has two forms: asiaticus (Asia) and africanus (Africa). The form that is now affecting crops in Brazil is a more virulent variant of C. liberibacter asiaticus; it has therefore been proposed that such variant be named C. liberibacter americanus.

Means of dispersal
Huanglongbing is transmitted only by vector insects and by infected buds. The former include Trioza erytreae psyllids (i.e., Africa; it is usually able to adapt to colder environments) and Diaphorina citri Kuwayama (i.e., Asia; it is more widely distributed in South America). In Argentina, the virus is transmitted by the vector insect Diaphorina citri.

• Distribution of Diaphorina citri in Argentina (Spanish version available)
• Worldwide distribution of Diaphorina citri (Spanish version available)

How does Candidus liberibacter spp. affect citrus trees?

Candidus liberibacter spp. is a persistent, non-propagative bacterium. It reproduces within the insect; however, it is not transmitted to other generations of such insect. As it bites the plant, the insect introduces the bacterium which, when circulating in the phloem, blocks the phloem vessels and, consequently, the transport of nutrients. In the course of time, the plant, which has poor development, declines and finally dies.

Other hosts for HLB and its vector insect
D. citri has been detected in Murraya paniculata (L.) Jack (Rutaceae). It is an ornamental plant and an alternative host of this psyllid and of the causal bacterium. It is found in the north eastern region of Argentina (i.e., the provinces of Corrientes and Misiones), as well as in the north western region (i.e. Salta and Jujuy). This plant of the Rutaceae family is used as hedge in streets, squares and gardens.

• SENASA ruling Nbr. 447 – Murraya paniculata (L.) Jack (Spanish version available)

Characteristics of D. citri
• Order: Hemiptera
• Life cycle (from egg to adult): 20 to 40 days. Expected longevity: three to four months.
• Number of eggs: 800 per female (during its entire life cycle)
• The eggs are ovoid and have an extension at the tips. They are orange-yellow and measure approximately 0,2 millimeters. The eggs are laid at the tips of tender shoots and on and among unfolded tender leaves. A great number of eggs are often laid on a same twig. Oviposition will depend on the existence of tender shoots.
• The nymphs are flattened at the dorsal-ventral area; they are yellowish brown, with no abdominal spots and with bulging wing buds. There are filaments along the abdomen. There are five nymphal instars. The nymphs are sedentary: they settle on tender stems and petioles, in this way forming colonies whose number of individuals will vary from a few of them to hundreds. Fifth-instar nymphs produce adult specimens (both females and males).
• The adult specimen is brown, mottled and two to three millimeters long. The males are slightly smaller than the females. The tip of their abdomen is blunt, whereas that of the females is distinctly sharp. The adults are not able to fly for a long time. They leap as soon as they are disturbed.
• They acquire the bacterium during the fourth and fifth nymphal and adult stages.
• The disease is not transmitted to offspring; only the adult specimens transmit it until the end of their life cycle.

Diaphorina citri technical datasheet

Symptoms:
There is initial yellowing of one branch; this contrasts with the overall green color of the citrus plant. The disease affects the entire plant. The symptoms are more evident during the fall and winter, because yellowing and mottling are more frequent. Such yellowing, though, is not so conspicuous during the spring and summer.

In leaves, a pale yellow coloring with green, irregular areas (mottling) can be observed. There is also defoliation, thickening of veins (which also turn lighter in color). In the course of time, the veins acquire a corky appearance. There is also asymmetry and blurring of colors in veins and leaflets. Sometimes, such symptoms may be mistaken for those produced by a shortage of zinc and copper.

In branches, the disease evolves until the affected branches suffer heavy defoliation. The symptoms occur in other branches and may affect the entire tree top. The tips may also die or dry off.

In fruits, there may be defoliation and fruit fall.

• External symptoms: there may be deformities and asymmetry, as well as reduction of size. Round, light-green spots may appear; such spots contrast with the normal green color of the fruit. Deformities in fruits occur provided as long as the leaves show symptoms.
• Internal symptoms: maturation differences and seed abortion; axis deviation and yellowing of veins. The white region of the rind (albedo) is sometimes thicker than normal.

(Click on images to enlarge)

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Damage produced:
• death of plants;
• reduction of fruit weight;
• reduction of the level of sugars (this is a significant standard for industrial purposes);
• higher acidity levels;
• reduction of juice percentage;
• reduction of fruit size and change in color and shape;
• affected young plants will not bear fruit;
• the disease affects all graft variants regardless of rootstocks;
• the shape and organoleptic properties of the fruits are altered.

Prevention measures:

• propagation material should not be illegally introduced in the country (e.g. buds, grafts or seedlings)
• citrus propagation material of unknown origin should not be introduced in the fields;
• certified plants should be used;
• crops should be constantly inspected; in case of doubt, expert advice should be sought (e.g. National Institute for Agricultural Technology – INTA;  National Service for Agrifood Health and Quality – SENASA; universities);
• chemical control of the vector psyllid should be performed, i.e. systemic insecticides should be applied to young plants (two years old). Systemic insecticides should be applied in the spring/summer every 15 days; contact insecticides, in the fall/winter;
• alternative hosts of citrus greening (e.g. Murraya paniculata specimens) should be removed from orchards.

Reference material:

Alternative host plants