Figure 1. This citrus leaf shows symptoms of greening disease. It is not known yet (June 11, 1998) whether greening disease was brought into Florida with the citrus psyllid. (21 KB)
Marjorie A. Hoy
Entomology and Nematology Department
University of Florida
Ru Nguyen
Division of Plant Industry
Department of Agriculture and Consumer Services
Key Facts
In June 1998, the citrus psylla Diaphorina citri Kuwayama was found for the first time in southeastern Florida by personnel in the Division of Plant Industry, Florida Department of Agriculture and Consumer Services.
Diaphorina citri is one of two psyllid insect species found attacking citrus. D. citri originated in Asia while the other psyllid, Trioza erytreae (Del G.), originates from tropical Africa.
D. citri 's original range in Asia included Pakistan and India through southeast Asia to south China, the Philippines, and Indonesia. This species also is recorded in Saudi Arabia, Mauritius, and Reunion, presumably due to accidental introductions. In the western hemisphere, D. citri was found only in Brazil and Honduras until recently. How D. citri got to Florida and where it came from is currently unknown (June 11, 1998). A survey conducted in June 1998 by Division of Plant Industry personnel indicated that D. citri infests citrus in Palm Beach, Broward and Martin counties, and the Indian River citrus growing area. The full extent of the infestation is being determined. According to Connie Riherd, Division of Plant Industry, D. citri is too widespread for eradication efforts to be made. We will have to learn to live with this pest.
Citrus psylla is a serious pest of citrus.
Figure 1. This citrus leaf shows symptoms of greening disease. It is not known yet (June 11, 1998) whether greening disease was brought into Florida with the citrus psyllid. (21 KB)
D. citri can cause two types of damage to citrus: direct feeding damage and transmission of a serious disease (greening disease - Figure 1). It is difficult to separate the effects of feeding from the effects of the disease the psyllids transmit. High populations of D. citri cause feeding damage because they attack young tender growth (flush), causing leaf distortion and curling (Figure 2). D. citri also produce honeydew, which leads to sooty mold infestations, and badly-damaged leaves will die and fall off.
Figure 2. Feeding by citrus psylla (D. citri) on the young flush of citrus trees causes damage to leaves and shoots because the psyllid has a toxic saliva. (23 KB)
Citrus Psylla Facts
D. citri breeds exclusively on young flush and has a very high reproductive rate. Multiple, overlapping generations can lead to very high populations. Eggs of D. citri are laid in the spring on young leaves in the buds or in leaf axils. The egg stalk is forced into the leaf tissue by the ovipositor of the female. Each female may lay up to 800 eggs during her two-month lifespan. Nymphs hatch in about 5 days and feed. They go through several instars before becoming adults. The life cycle takes about 20-40 days and there may be up to 30 overlapping generations per year.
Figure 3. The nymph of citrus psylla feeds on leaves and shoots of citrus. (16 KB)
D. citri nymphs are typically flattened with distinctly flattened wing buds (Figure 3). Adults of D. citri are about the size of aphids (2.5 mm) but resemble small cicadas. The antennae are long, simple, and segmented. Adults of D. citri have pale brown wings with a broad pale stripe along the center. A common name for the adults is "jumping plant lice."
Four main environmental factors regulate citrus psyllid populations: flushing rhythm of the citrus, weather extremes, condition and nutritional status of flush, and natural enemies.
Eradication efforts were not attempted in Florida, because the pest was found to be widely distributed and abundant. The tools available for eradication are very limited for this pest.
D. citri is an efficient vector of greening disease, which is considered the most serious citrus disease in Asia.
If this psyllid species arrived in Florida carrying greening disease with them, the impact on our industry could be very serious. Tests are being conducted now to determine whether the psyllids arrived free of the disease.
Even if the psyllids don't have the disease at this time, a future introduction of the pathogen would result in effective transmission of the disease by the psyllids that are now here.
The citrus disease transmitted by D. citri is called various names, including "greening", "leaf mottling", or "die back". The literature is confusing; in some older papers the causal agent is reported to be a virus, in others it is described as a "mycoplasma-like" organism, More recently, it was identified as a gram-negative bacterium. The organism cannot be cultured in vitro, but they can be detected by use of the polymerase chain reaction (PCR) of 16S rDNA and by electron microscopy.
Greening symptoms include mottling and yellow veins on leaves, out-of-season flowering, out- of-season flush production, abnormal fruit drop, fruit lopsidedness, off-color fruit at harvest, and an unpleasant flavor in the juice. All species of citrus appear to be susceptible, but sweet orange, mandarin, and tangelo are most affected in Asia.
The effect of greening disease on citrus in Florida will influenced by temperature conditions; the Asian form of greening and the Asian psyllid do well at high temperatures, although very hot conditions are unfavorable.
Citrus Psylla Control: An Integrated Approach
Now that D. citri has invaded Florida, an important next step is to import natural enemies of the pest in a classical biological control program.
Certified clean budwood or nursery stock will have to be made available if the disease is found in Florida.
Spread of greening disease is by infected budwood or nursery plants, as well as by the psyllid. Greening disease is probably not seed-transmitted. D. citri can acquire the greening organism in a short period of feeding and remain infective for a long time. Disease transmission rates and economic injury levels will have to be investigated under Florida conditions and with Florida's citrus varieties if the disease is found in Florida.
Natural enemies already in Florida may provide some control of citrus psyllids.
Generalist predators such as lacewings, syrphid flies, lady beetles, and spiders attack psyllids. These native natural enemies are not expected to suppress the pest populations to a non-economic level, however.
A classical biological control program offers great promise for suppressing D. citri and has been initiated.
Classical biological control involves a series of steps, including collecting, importing, and evaluating natural enemies in quarantine. If permission is given by state and federal regulatory agencies for their release from quarantine facilities, the natural enemies are reared and released into the new environment. Ideally, the natural enemies are specific to the target pest and become permanently established in the new environment, helping to suppress the pest population below an economic level on a permanent basis. Classical biological control programs typically require several years to carry out, and additional time may be required before the effectiveness of the natural enemies can be determined.
Two parasitoids will be imported into Florida.
Fifteen species of parasitic wasps are known to be associated with D. citri in the Asia Pacific region, but only two, Diaphorencyrtus aligarhensis (Shafee, Alam and Agaral) [Encyrtidae] and Tamarixia radiata (Waterston) [Eulophidae], are recorded as primary (beneficial) parasitoids. The rest act as hyperparasites (parasites of parasitoids) and should not be imported into Florida.
These parasitoids can substantially reduce psyllid populations. In northern India one parasitoid is recorded as exerting up to 95% mortality of the pest. In Thailand and Vietnam, D. aligarhensis and T. radiata are known to be important parasitoids. Excellent biological control of the Asian citrus psyllid was achieved by the introduction of these two parasitoids into Reunion Island; the vectors were nearly eliminated and the disease was controlled.
The parasitoid Tamarixia radiata is a eulophid ectoparasitoid that parasitizes the third, fourth, and fifth instars (Figure 4) and also host feeds, causing additional mortality. Females of T. radiata lay an egg ventrally on the outside of the psyllid. After the parasitoid larva devours its host, it attaches itself to a leaf or twig and the adult emerges by cutting its way out of the pupal chamber.
Figure 4. Tamarixia radiata is an effective parasitoid of the citrus psylla in Asia. These psyllid nymphs have been killed by the feeding of the immatures of this eulophid ectoparasitoid. (17 KB)
The parasitoid Diaphorencyrtus aligharensis (Encyrtidae) (Figure 5) lays its egg inside the body of second, third, and fourth instar psyllid nymphs. Parasitized nymphs can be recognized because the dorsum of the fifth instar swells and their color changes from yellow to a brownish-red, forming a "mummy". The adult parasitoid cuts its exit hole through the dorsal abdomen of the mummy. Adult females of D. aligharensis also host feed, causing additional mortality of the pest.
Figure 5. This adult female of Diaphorencyrtus aligarhensis inserts an egg into the nymphs of citrus psylla. The parasitoid develops within its psyllid host, finally emerging as an adult to begin the cycle again. This encyrtid endoparasitoid is another effective natural enemy of the citrus psylla in Asia. (13 KB)
Marjorie Hoy (IFAS-University of Florida, Gainesville) and Ru Nguyen (DPI-Department of Agriculture and Consumer Services) already have permits to import parasitoids of D. citri into quarantine facilities in Florida for evaluation and possible release.
Now that D. citri is established in Florida....
They are likely to spread throughout Florida. Many backyard citrus trees could be affected. Homeowners and farmers may use more pesticides to try to save their citrus crops from this pest.
The psyllid also attacks landscape plants (jasmine orange, Murraya paniculata) and this host plant can act as a source of the pest in citrus.
Research Needs
Now that the pest has arrived, tests should be conducted to determine which pesticides can help suppress psyllids, yet do not disrupt natural enemies of citrus pests in Florida. In Asia, dimethoate and other pesticides are used to control citrus psylla, but they are very disruptive to natural enemies of citrus pests.
The use of oil is less disruptive and should be evaluated in Florida. Tests with petroleum oil sprays (0.25 to 1.0%) against citrus psylla in China indicated that oil was most toxic to first and second instar nymphs and provided good control if applied sufficiently frequently during the summer. Oil has a number of advantages over conventional pesticides because oil is less disruptive to natural enemies, insects do not develop resistance to oil, oil has a low toxicity to vertebrates, and oil breaks down readily in the environment.
D. citri is monitored throughout the year in Thailand using a Saturn yellow sticky trap, but no economic injury level has been established. Varietal differences in responses to D. citri should be investigated now that the pest has arrived. At this time, no true resistance is known for any variety.
Methods for certifying budwood and nursery trees free of greening should be developed for Florida's conditions.
The role of native natural enemies in suppressing the pest(s) should be evaluated.
The effectiveness of natural enemies introduced in the classical biological control project should be monitored. Even though hyperparasitoids will not be imported into Florida, there are native hyperparasitoid species (such as Tetrastichus species, Cheiloneurus species, and Pachyneuron species) that could attack the introduced natural enemies (T. radiata and D. aligarhensis). If high rates of mortality are exerted on T. radiata and D. aligarhensis by these native hyperparasitoids, then their effectiveness could be reduced.
Classical biological control projects typically take several years before natural enemies can be established and become effective.
We thank Dr. Rut Morakote, Department of Agriculture, Bangkok, Thailand, for the use of the photographs on this page.
Selected References