Psyllids (seen hanging above) pick up or spread bacteria as they feed on tree sapFUNDECITRUS
In a destructive alliance, a group of bacteria and a group of insects—one causing and the other spreading citrus greening, one of the most devastating diseases in citrus farming—have continued to torment orange, tangerine, and lemon growers in Brazil. A combination of pest outbreaks, severe droughts, and erratic rainfall has stunted fruit growth and led to a 25% reduction in citrus output in São Paulo and Minas Gerais compared to 2023, according to a May report from the Brazilian Fund for Citrus Protection (FUNDECITRUS). As a consequence, orange prices have surged by an average of 40% in markets and produce stands.
Since the disease was first detected in 2004 in São Paulo—and later in Minas Gerais, Paraná, Mato Grosso do Sul, Santa Catarina, and most recently in Goiás this June—citrus greening has resulted in the removal of approximately 60 million trees, which represents 23% of the 260 million orange and other citrus trees grown in the country. Most of these are concentrated in São Paulo, which accounts for about 75% of the country’s citrus output.
In Brazil, citrus greening is caused by two species of bacteria: Candidatus and Liberibacter. Small, grayish insects up to 2 millimeters long, known as Asian citrus psyllids (Diaphorina citri), pick up the bacteria while feeding on sap from infected plants and spread it to healthy ones. The bacteria can infest the phloem (the vascular tissue that transports nutrients, such as amino acids and sugars) of all citrus species (including oranges, tangerines, mandarins, limes, and lemons) and even other plants, like orange jasmine (Murraya paniculata), which is popular in landscaping. Following their discovery in 1942 in Brazil, psyllids were initially considered a minor and mostly harmless citrus pest—until the arrival of the bacteria responsible for citrus greening.
Also known as huanglongbing (HLB), meaning “yellow dragon disease” in Chinese because of the yellow leaves on infected branches, citrus greening has proven even harder to fight than the previous major citrus pest, citrus variegated chlorosis (CVC), caused by the bacterium Xylella fastidiosa—the landmark genome sequencing of the Xylella bacterium kickstarted the FAPESP Genome Program in 1997 (see Pesquisa FAPESP issue n° 184). Xylella spreads slowly in the xylem (the tissue responsible for transporting water and nutrients, located closer to the outer layers of the plant than the phloem), and its vectors, the glassy-winged sharpshooters, spread less aggressively than psyllids do.
CVC has now been brought under control. “We developed a system for growing seedlings in screened nurseries, implemented new disease control methods and vector management strategies, and saw the incidence rate drop from 40% in the early 2000s to less than 0.5% today,” explains Juliano Ayres, a crop scientist and general manager at FUNDECITRUS. When citrus greening arrived in Brazil, growers tried to use the same tactics that worked against CVC—controlling the insect vectors and removing diseased plants and contaminated seedlings. However, these methods were only partially successful in containing greening disease.
The results from recently introduced crop management techniques suggest that the fight against greening is not lost, but is far from over. Farmers are employing a combination of strategies: using healthy seedlings grown in screened nurseries, planting in rows running parallel to the orchard edges with higher tree density per hectare, increasing fertilization, applying insecticides more frequently, and eliminating psyllids and infected plants.
Despite these efforts, citrus greening has continued to spread—and not just in Brazil. The number of affected countries has jumped from 40 in 2006 to 126 today, where the disease causes orange and lemon trees to produce fruits that are fewer in number, smaller, more acidic, and drop prematurely.
“This is a serious problem,” says José Roberto Postali Parra, a professor of crop science at the Luiz de Queiroz School of Agriculture (ESALQ), University of São Paulo (USP). “We need to ramp up efforts against citrus greening, with stricter enforcement of laws requiring the removal of infected plants, even though they remain productive, albeit at reduced levels.” Parra has participated in discussions with experts, and some have even suggested eliminating orange jasmine entirely.
Carlos Alberto Lucato, chairman of the Brazilian Table Citrus Association and co-owner of Citrícola Lucato, a citrus fruit company based in Limeira, São Paulo, has also been actively involved in meetings with officials from the São Paulo government and other states, where he has provided input on policies to combat citrus greening. “If we fail to take stricter action, citrus yields in São Paulo could drop even further in the long run, and consumer prices will skyrocket,” he warns.
Growers in São Paulo are increasingly relocating to regions with lower rates of greening disease in neighboring states. Eighteen years ago, Citrícola Lucato stopped cultivating oranges in Limeira and shifted focus to its 320-hectare orchards in the Jales region, in northwestern São Paulo, and to its 1,000-hectare orchards in the municipalities of Madre de Deus de Minas and Piedade do Rio Grande, in southern Minas Gerais. “If greening spreads to these regions, we’ll now know what measures to take, unlike 20 years ago when much of São Paulo wasn’t prepared,” Lucato says.
An infected plant with yellowing leaves and significant fruit dropFUNDECITRUS
In April, Citrosuco, a leading orange juice exporter, announced the purchase of its 26th farm, also located in southern Minas Gerais. A month earlier, Cutrale, another major juice processor, revealed a R$500 million investment to establish a 5,000-hectare orchard in Sidrolândia, Mato Grosso do Sul.
Zeroing in on the edges
During Expocitros, a citrus trade fair held in June in Cordeirópolis, São Paulo, crop scientist Franklin Behlau of FUNDECITRUS described the severity of the problem using Pera sweet orange orchards as an example. When 25% of a tree is infested, its yield drops by about 20%. If up to 50% of the tree is affected, fruit yield decreases by 40%, and in the most advanced stages, with the entire tree infected by the bacteria, the harvest can shrink by as much as 70%.
In the early 2000s, in an effort to deter the loss of orange groves in the United States, research teams from the US Department of Agriculture, led by plant epidemiologist Timothy Gottwald, discovered that the rate of infestation decreases from the edges inward in citrus orchards. This finding was key in controlling the disease-spreading insects.
“Trees planted within 150 meters of the orchard’s outer boundary host 80% of the psyllids,” notes FUNDECITRUS crop scientist Renato Bassanezi. This suggested that concentrating psyllid traps and insecticide spraying along the orchard edges would be more effective. Planting rows parallel to the orchard edges has been shown to reduce the incidence of disease by 20%, while perpendicular rows facilitate the spread of insect vectors. This strategy was detailed in a May 2013 article in Plant Disease that laid out a blueprint for controlling citrus greening.
At Expocitros, Eduardo Girardi, a crop scientist with the Brazilian Agricultural Research Corporation’s (EMBRAPA) Cassava and Fruit unit, proposed another potential solution to help manage greening: the use of dwarfing rootstocks (onto which fruit-bearing varieties are grafted), which reduce tree size by around 50%.
“These dwarfing varieties, like others, are still susceptible to greening, but their smaller shoot size makes it easier to spray insecticides, which helps lower disease incidence,” he explained. In an experiment with 500 Valencia orange trees, the flying dragon rootstock, the only dwarfing variety among the 16 tested, showed the lowest incidence rate—17% after eight years since planting—while others saw rates as high as 48%.
Other strategies fell short. Pheromones—volatile chemical compounds that spread through the air and help animals of the same species communicate—worked well in lab tests to attract psyllids but failed in field conditions.
In 2019, one of the insecticides used against psyllids, dimethoate, was banned following demands from European buyers of Brazilian citrus over concerns about human health risks. Later, it was discovered that psyllids had developed resistance to other insecticides, which were applied more frequently and without proper rotation. As a result, greening infestation rates rose.
Researchers found an alternative: spraying with kaolin, a white powder made mainly of the mineral kaolinite. In field trials, a 2% dilution in water significantly reduced the number of psyllids landing on orange tree leaves, without apparent harm to the plants. “Growers are already using kaolin in commercial orchards,” says Marcelo Miranda, a crop scientist at FUNDECITRUS.
Another approach is the use of Tamarixia radiata, a natural enemy of psyllids, which destroys the developing pests. “We discovered the wasp in 2006 in orchards in Piracicaba and Jaboticabal,” says Parra (see Pesquisa FAPESP issue n° 261). The wasp is now being bred in two production units in São Paulo and should be released in abandoned orchards, isolated trees, or organic groves, where chemical pesticides cannot be used. According to Parra, combining three strategies—insecticide application, biological control, and early removal of infected plants—can cut disease incidence by 74%, based on a study published in May 2023 in the journal Entomologia Generalis.
In Florida, where the disease emerged in 2005 and citrus yields plummeted by over 80%, attempts to slow down greening by boosting plant nutrition have had little success. US experts are testing the effectiveness of injecting antibiotics into tree trunks to reduce greening symptoms. In areas where the disease is incipient, they focus on quickly identifying and removing infected plants. In California, they are even experimenting with dogs trained to detect the scent of infected trees before symptoms appear.
“We’re still fighting a war with no end in sight,” Girardi remarks. To be effective, controlling insect populations needs to be a collective effort, like government measures to control the mosquitoes that spread dengue fever. However, as he notes, “not all farmers are as willing or financially capable of properly managing their orchards.” Lucato witnessed this firsthand during a visit to Minas: “A fellow grower told me he wanted to renew his orchard, but it was no use because his neighbor wouldn’t remove the greening-infested trees from his.”
The story above was published with the title “The long battle against citrus greening” in issue 343 of September/2024.
Project
Measures for reducing primary infections through integrated management of Huanglongbing in the citrus belt of São Paulo: Technical and economic feasibility (nº 17/21460-0); Grant Mechanism Thematic Project; Principal Investigator Renato Beozzo Bassanezi (Fundecitros); Investment R$5,666,086.32.
Scientific articles
BASSANEZI, R. B. et al. Efficacy of area-wide inoculum reduction and vector control on temporal progress of huanglongbing in young sweet orange plantings. Plant Disease. Vol. 97, no. 6, pp. 789–96. May 14, 2013.
GARCIA, A. G. et al. The importance of Integrated Pest Management to flatten the huanglongbing (HLB) curve and limit its vector, the Asian citrus psyllid. Entomologia Generalis. Vol. 42, pp. 349–59. May 18, 2022.
RODRIGUES, J. D. et al. Huanglongbing incidence, canopy volume, and sprouting dynamics of “Valencia” sweet orange grafted onto 16 rootstocks. Tropical Plant Pathology. Vol. 45, pp. 611–19. Oct. 17, 2020.
