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Citrus Disease Control in Brazil1

Antonio Juliano Ayres2


Citrus Canker

Citrus Variegated Chlorosis

Citrus Black Spots

Citrus Leprosis



Other Diseases



Brazil is the world's biggest producer of oranges, producing about 1/3 of the world's production, that is, approximately 455 million boxes of 40.8 Kg each (AGRIANUAL, 2001). Orange production, though, is not evenly distributed among the Brazilian states. It is estimated that 93.5% of the country's production is concentrated in the states of São Paulo (82.4%), Sergipe (4.7%), Bahia (3.7%) and Minas Gerais (2.7%) (NEVES & BOTEON, 1998). The state of São Paulo further consolidated its leadership in the production of oranges in the agricultural year of 1999/2000 by producing 355.93 million boxes of 40.8 Kg. (ABECITRUS, 2001).

Today, about 70% of the oranges produced in São Paulo are destined for the production of concentrated juice for export. It is estimated that, worldwide, eight out of ten glasses consumed of the internationally marketed concentrated orange juice are produced in the State of São Paulo, which is responsible for 98 % of the total Brazilian production and export of concentrated orange juice.

The natural production potential of oranges, and their market value has made this fruit the base of citrus cultivation in the state of São Paulo. Orange production in the state is 92% of the total citrus production, followed by tangerines (5%) and limes and lemons (3%). The main sweet orange varieties are: `Pera' (40%), `Natal' (24%), `Valência' (22%) and `Hamlin' (6%). `Pera' is the main variety cultivated due to the quality of the fruit, which is ideal either for `in natura' consumption or for processing. This mid-season variety has a peculiar characteristic - it blooms twice out of season. This out of season yield is strategic to marketing the product between regular crops when oranges are relatively scarce in the market.

To better understand the role of citrus production in the State of São Paulo, it must be taken into account that the orange producing and processing sectors alone are responsible for an annual domestic and export income of over US$2 billion. It is estimated that this sector generates about 400,000 direct and indirect jobs. In the State of São Paulo alone, citrus is produced in 330 cities and 29,000 farming sites.

An array of factors has made citrus cultivation in the State of São Paulo a world leader in orange production at the end of the 1980's. The state has maintained this position ever since. Among these factors we can cite:

The country's natural conditions, low cost land and labour, quality research technology, and appropriate infrastructure, are some of the factors which, added together, have made citrus production in Brazil one of the most efficient and low production cost crops in the world. Brazil's cost, for each 40.8 Kg box, delivered at the plant, of close to US$1.80 compares very favourably with that of the State of Florida (USA), Brazil's major competitor in citrus production, which has an average production cost of US$3.80 per box (40.8 Kg). Added to these factors, the concentrated juice industries in Brazil were able to open up new markets and to fill the market gap in the USA in the 1960's and in the 1980's when Florida's groves were severely damaged by frosts.

Concern with phyto-sanitary problems led to the implementation of a program for registering matrix plants from nucellar clones in the 60's, thus providing for a citrus culture free from viruses and viroids graft-transmitted, such as Psorosis, Exocortis, and Xiloporosis. Nevertheless, other diseases and pests are still a cause for concern today, such as Citrus Canker (Xanthomonas axonopodis pv. citri), Citrus Variegated Chlorosis (Xylella fastidiosa), Leprosis (Citrus Leprosis Virus), Black Spot (Guignardia citricarpa), Blight, Tristeza (Citrus Tristeza Virus), Citrus Leaf Miner (Phyllocnistis citrella) and Citrus Borer (Ecdytolopha aurantiana).

FUNDECITRUS (Fund for Citrus Plant Protection) was created in 1977 with contributions from citrus growers and industries to provide political and financial institutional support to the National Campaign to Eradicate Citrus Canker (Campanha Nacional de Erradicação do Cancro Cítrico -CANECC). This campaign is being carried out in the State of São Paulo with the effective participation of the Ministry of Agriculture and the Agriculture Secretariat of the State of São Paulo.

In 1995, as the number of problems caused by diseases and pests like CVC, Black Spot and Citrus Borer increased, FUNDECITRUS decided to expand its activities and to become a sponsoring institution for research and development.

Presently, 80% of the institution's annual budget of approximately US$18 million comes from citrus growers' and orange juice processing industries' contributions that collect US$0.04 for every processed orange box (40.8 Kg). They are each equally responsible for 50% of this amount. In the last few previous years, the remaining 20% of the institution's income were contributions from the Ministry of Agriculture. FUNDECITRUS employs 2,455 people and 80% of its budget is assigned to Citrus Canker eradication campaigns.

Citrus Canker, CVC, Leprosis, Black Spot, Citrus Leaf Miner and Citrus Borer are the FUNDECITRUS research department's main priorities. The institution has a team of 10 researchers and 50 collaborator researchers from the main research institutions in Brazil and abroad. These research projects are all partially sponsored by FUNDECITRUS. To optimize and better direct the use of the financial resources, FUNDECITRUS has coordinated and facilitated the contacts between the producers and research institutions with government research sponsoring agencies (FAPESP, CNPq, FINEP)3. This has made possible the development of more extensive projects in the last few years, in collaboration with FAPESP, as for example, the Genome of Xyllella fastidiosa (the causal agent of CVC) and the Genome of Xanthomonas axonopodis pv. citri (the causal agent of Citrus Canker). Other applied researches into Black Spot, Citrus Canker and CVC were conducted in collaboration with CNPq.

The present situation of the main diseases in citrus in Brazil (Citrus Canker, CVC, Leprosis, Black Spot, Tristeza, Blight), the resulting losses and control strategies will be detailed below.


In Brazil, Citrus Canker, caused by the bacteria Xanthomonas axonopodis pv. citri, was first detected in 1957 in a nursery in Presidente Prudente in the State of São Paulo (BITANCOURT, 1957). In 1958, this disease was detected in the states of Mato Grosso do Sul and Minas Gerais. Later it was also found in the states of Rio Grande do Sul, Santa Catarina and Minas Gerais, where it is still present. This disease was also found in the state of Goiás, but a successful eradication campaign has made this state disease free.

In the state of São Paulo, an eradication campaign was launched immediately after the detection of Citrus Canker. The infected areas were delimited, the diseased plants and the contaminated nurseries were eliminated, the transportation of citrus prohibited and new commercial groves were banned. This prohibition was soon extended to other cities where areas with the disease were detected. Because these eradication procedures had not been sufficient to eliminate the disease, in 1957 eradication of all citrus (both healthy and diseased) took place in the rural and urban areas of the delimited contaminated areas of 29 cities. By 1961, 1,2 million plants (contaminated or healthy) had been eliminated in 21 cities, putting an end to total eradication. From 1961 to 1979 only small areas adjacent to former contaminated areas, previously subjected to total eradication, showed signs of the presence of the disease. These small areas were also subjected to eradication. Each of these small contaminated areas were considered to be the centre of the adjacent farming areas within a range of 1 km, which were then also subjected to citrus eradication. In 1982, citrus growing in the formerly totally eradicated areas was allowed even though the bacteria had not been completely eliminated in the area.

In 1979, Citrus Canker was detected for the first time in a lime grove (Citrus aurantifolia, Swingle) in the northern area of the Tietê River, in the city of Monte Alto. This region, an export zone, is considered a prime area for citrus farming in São Paulo. This disease was later detected and eradicated in nine other cities in the area. In 1980, only the farming properties where Citrus Canker was detected were subjected to interdiction. The interdiction of entire cities was discontinued.

In 1987, eradication procedures were changed and only the diseased plants and the plants located within a range of 50 meters were eliminated. In 1995, eradication procedures were changed again and only plants located within a range of 30 meters of the diseased plants were eliminated.

Although the number of plants contaminated by Citrus Canker has increased steadily, the presence of the Citrus Leaf Miner (Phyllocnistis citrella, Staiton) has contributed to the occurrence of a greater number of cases in 1996. This insect feeds on young flushes, building mines on the leaves, which facilitates infection by X. axonopodis pv. citri and increases the potential inoculum of the bacteria, consequently increasing the speed of the epidemic process (GOTTWALD et al., 1997).

Table 1 summarizes the evolution of Citrus Canker from 1992 to 1998 in the FUNDECITRUS area of work. This area includes 330 cities. It encompasses three contiguous areas, as follows: 1) All of the area located in the state of São Paulo, on the north bank of the Tietê River; 2) A 60km strip of land located on the south bank of the river; and 3) A small area in the South of the State of Minas Gerais, bordering the State of São Paulo. This practically comprises the whole citrus area whose products are destined for export.


Table 1

Number of contaminated cities, detection, trees with symptoms of Citrus Canker in the FUNDECITRUS area of work from1992 to 1998.


Contaminated Cities


Diseased Trees

Eliminated Trees

Eliminated Young Trees











































1 Eliminated trees plants with symptoms, including trees located within a 50 meter range
2 Eliminated trees with symptoms, including trees located within a 30 meter range.


The records of the occurrence of Citrus Canker during 1992-1998 resulted from routine inspections, especially in areas where there was suspicion of the presence of the disease, and also from producers' reports. This data did not show the distribution and incidence of the disease so, in 1999, from March to April, a stratified sample survey was made. Five percent of the commercial plots (over 200 plants) in the citrus export zone in the state of São Paulo were surveyed. This showed an estimated 0.69% of the plots with the disease, which corresponds to 583 plots (BARBOSA & FERNANDES 1999). The same survey showed that the disease was more concentrated in certain areas. The southern zone, which comprises 25.66% of the citrus trees in the state, had an incidence rate of the disease below the limit of the detection method, indicating that it was quite low.

Based on the results of this survey, from May to November of 1999, all the groves in the FUNDECITRUS area of work were inspected (147,394,638 trees), excluding the southern zone. The disease was detected in the four main varieties of sweet oranges (`Pera', `Valencia', `Natal' and `Hamlin') in 130 cities, in a total of 702 contaminated commercial plots. 1,246,248 plants were eliminated. 2,988 non-commercial groves (groves with less than 200 plants) were also eliminated in the urban and rural areas included in the inspection.

Until 1997, the elimination of diseased plants and plants located within a 30 meter range of the diseased ones seemed to be quite effective in eradicating the disease. After 1997, with the presence of Citrus Leaf Miner, this procedure lost its efficacy for in 80% of the cases, the plots were still contaminated after eradication. This was probably due to the high number of contaminated plants located outside the 30 meter range that the inspection failed to detect. In August 1999, the eradication procedures were again changed. After three simultaneous inspections by three teams, the plots which had more than 0.5% of diseased plants would have all their trees eradicated. In plots where the rate of the disease is lower than 0.5%, the former procedure is still in effect: - the eradication of diseased plants and the plants located within a range of 30 meters of the diseased ones are eradicated.

Although the eradication campaign did not achieve its main objective, that is, to eliminate the bacteria or to prevent its spread to new areas, it can be said that it was, in a way, not completely unsuccessful. 42 years after the beginning of the disease, according to BARBOSA & FERNANDES (1999), 99.73% of the plots have been kept healthy. A new sampling survey, which took place from March to April, 2000 and inspected 10% of the plots, showed that the incidence the disease has decreased to 0.27% in commercial plots.

With the present level of disease incidence, a tight control of the disease with exclusion and eradication procedures is fully justified from an economic point of view. If these procedures are abandoned the disease could quickly spread to all groves and the losses and expenses of management of the diseased groves would be far higher than the cost of exclusion and eradication and its consequent loss of eliminated plants (estimated as US$ 50 millions/year).


CVC was first detected in Brazil in 1987, in the Northern area of the State of São Paulo and South of Minas Gerais (DE NEGRI, 1990). It has expanded since then to the whole Brazilian territory. Today CVC is found in several other states of Brazil, including Paraná, Santa Catarina, Rio Grande do Sul, Goiás, Distrito Federal and Sergipe. There are reports of presence of CVC in Paraguay , Argentina and Costa Rica as well.

This disease affects all the commercial varieties of oranges in different rootstocks and it is caused by Xylella fastidiosa which blocks the vessels of the xylem of the plant. It can be transmitted to other orange groves by contaminated young trees and sharpshooters. Twelve different species of sharpshooters have been identified so far.

The symptoms of CVC can be seen in the leaves, branches and fruits. The losses by CVC occur in the more advanced stages of the disease, and are caused by a reduction in the development of the plant, particularly in the fruit. Severely diseased plants frequently have protruding branches in the upper part of the crown which have small leaves and fruits and show defoliation in the terminal twigs. This causes, in the most serious cases, the economic death of the trees. In the year 2000, the estimated damaged caused by CVC in the State of São Paulo was approximately US$110 million (considering the loss of plants in terminal stage, decrease in the production and disease control costs).

Since detection of CVC, significant knowledge of the pathosystem has been acquired, due mainly to priority given to research in this area by research institutions, agencies (FAPESP, CNPq) and FUNDECITRUS.

A definite solution to CVC has not yet been found, but it is possible to obtain a "technological package" to manage the groves so as to control the disease. The control strategy is based on procedures such as: the use of young trees from protected nurseries (nurseries covered by plastic and laterally protected by screens), the pruning of branches which show initial symptoms of CVC, or the eradication of plants with advanced symptoms, and chemical control of sharpshooters.

In the last three years the production of young trees aiming at restricting contamination risk of infection by CVC and Citrus Canker has been subject to radical changes. From the total of 20 million young trees in the State of São Paulo, approximately 4 million are now produced in protected nurseries. A State law, which will be in effect in January 2003, forbids the production of young trees in open nurseries. We hope that in two or three years, this law might make possible the total production of young trees in protected nurseries.

The data obtained in CVC surveys carried out by FUNDECITRUS showed that the incidence of the disease increased from 22.09% to 34.03% between 1996 and 2000. An increase in the severity of the disease was also noted, i.e. plants showing symptoms in the fruits increased from 6.17% to 20.80% over this period. It is believed that the increase in the severity of the disease is related to the last two unusually dry years (FUNDECITRUS, 2001).

Even though the increase in severity of the disease is quite worrying, there is optimism for the future. The procedures taken to prevent and control the diseases have already shown their first good results. CVC surveys in the last years showed a decrease in CVC intensity in younger groves (0 - 2years) in the last year.


Citrus Black Spots, caused by the fungus Guignardia citricarpa Kiely [Phyllosticta citricarpa (McAlp.) van der Aa.], was first detected in Brazil in commercial groves in 1980 in the State of Rio de Janeiro. The disease is also found in the states of Rio Grande do Sul (reported in 1986) and in São Paulo (reported in 1992) (GOES & FEICHTENBERGER, 1993).

Black Spot attacks leaves, branches and particularly fruits of sweet oranges, lemons, grapefruits, some tangerines and several hybrids. Black Spot causes lesions on the fruit skin, which are not acceptable for consumption in the fresh fruit market. In areas where the incidence of the disease is high, it might cause fruit drop if not appropriately treated.

In areas where citrus is produced for processing, the disease control aims at reducing the source of inoculum, thus eliminating the possibility of premature drop of the fruits. The fruit produced in these areas, even the fruit with symptoms of the disease, are used for processing since this disease does not affect the internal characteristics of the fruit, thus does not affect the quality of the juice.

In these areas, the production cost of a citrus grove is increased by US$100 per hectare due to the need for fungicide spraying to control the Black Spot. This extra cost is the same for industrial processing or for the domestic fresh fruit market (AGRIANUAL, 2001).

The European Union is the biggest consumer of Brazil's exports of fresh citrus. Because this disease is non-existent in the member countries of the EU, the batches of exported fruits are selected from disease-free groves.

Once the pathogen is introduced into the grove, its eradication is almost impossible. Thus preventive measures are quite important to ensure that the disease does not spread to new areas. The recommended preventive measures are:

Chemical control has been the procedure most used after the disease is detected in the field, especially when the production is destined for the fresh fruit market. Sprayings with protective copper compounds or systemic fungicides especially the benzimidazoles are made to protect the newly formed fruits. Other procedures that might help control the disease in contaminated areas include:


Leprosis is caused by a virus, which produces local symptoms in the leaves, branches and fruit. It is transmitted by mites of the Brevipalpus genus.

In Brazil, the disease is found in the States of Rio Grande do Sul, Santa Cartarina, Paraná, São Paulo, Rio de Janeiro, Minas Gerais, Tocantins, Piauí, Pará, Rondônia and Distrito Federal. A survey conducted by FUNDECITRUS showed that the disease has spread out to all citrus areas of the State of São Paulo where 61% of the groves have an average of 26% of their plants with one or more leprosis mites (SALVA & MASSARI, 1995).

This disease has become a serious problem, and according to several researchers it is considered a major viral disease in Brazilian citrus farming. When the disease is severe it jeopardizes the plant and its life span. It causes lesions in the fruit skin, premature drop of leaves and fruits and twigs dieback, with the possible death of the tree. The damages to the branches can decrease the plant productivity after some years because the damaged branches prevent the normal flow of plant sap. After effective mite control, it might take two years for a citrus tree with severe leprosis to achieve full recovery. Damage by leprosis in plants and in orange production has caused an annual cost of approximately 90 million dollars for mitecides to control the disease (FERREIRA, 1999). This represents about 40% of fertilizer and pesticide expenses and about 16% of the total costs of a grove.

Leprosis is found mainly in sweet oranges (Citrus sinensis, Osb.). Sour oranges, tangerines and tangor are also susceptible to the disease but other citrus cultivars do not usually show conspicuous symptoms of the disease.

The mite alone has not caused heavy damage to citrus unless the mite population is extremely high. Dissemination of the disease occurs only when infected citrus trees and vectors are present.

In citrus, the population of the leprosis mite is low and usually occurs in clusters of trees, which should be monitored carefully. When the trees are contaminated with the leprosis virus, the number of diseased plants will increase as the contaminated mites disperse.

Leprosis control is based mainly on the elimination of the sources of inoculum by pruning the affected trees and by using mitecides to reduce the vector (CHAGAS, 2000). Additional control procedures are also recommended, such as:

Spraying of the plots with mitecides has been based on the incidence of the leprosis mite which is periodically checked. This has reduced the number of sprayings to 2 or 3 per year or even 1 or 2 per year, when rotation of the mitecides is made.


Tristeza was first detected in Brazil in 1937. Because of the generalized use of sour orange as rootstock, it caused the death of nine million orange trees (from a total of 11 million). With the substitution of the sour orange by Rangpur lime as rootstock, the disease appeared in its minor form in the more tolerant tree crowns. This disease was significant only in less tolerant varieties like `Pera' sweet orange and `Mexican lime'. For these varieties the problem was satisfactorily handled with a program of cross protection, which used mild strains of the virus.


Blight was first detected in Brazil in 1977, in the State of São Paulo. It was later detected in other states and today it is found in all the producing areas. It is the main cause of low longevity of the groves. It is estimated that 5 percent of the tree deaths annually are due to this disease. The high mortality rate is due to the use of Rangpur lime (highly susceptible to the disease) as rootstock in more than 90% of the groves.


Other diseases also occur, but without any generalized damage. These diseases might, though, in specific conditions acquire importance, such as Gummosis and Root rot (Phytophthora spp), Postbloom Fruit Drop (Colletotrichum acutatum), Scab (Elsinoe australis and E. fawcettii), Melanose and Stem-end Rot of Fruit (Diaporthe citri), Anthracnose (Glomerella cingulata), Pink Disease (Corticium salmonicolor), Greasy Spot Like Disease (Mycosphaerella citri), Blue Mold and Green Mold (Penicillium italicum and P. digitatum ) and Alternaria Leaf Spot (Alternaria citri).


ABECITRUS. Produção de laranja - série histórica. (, Ribeirão Preto, 2001.

AGRIANUAL. Custo de Produção - laranja. FNP Consultoria & Comércio, Ed. Argos, p.289, 2001.

BARBOSA, J.C., FERNANDES, N.G. Incidência e distribuição de cancro cítrico no Estado de São Paulo. Jaboticabal, FUNEP. 1999. 11p.

BITANCOURT, A.A. O cancro cítrico. O Biológico. São Paulo, p.101-123. 1957

CHAGAS, C.M. Leprosis and zonate chlorosis. In: Timmer, L.W.; Garnsey, S.M.; Graham, J.H. (ed.) Compendium of Citrus Diseases, 2nd ed. St.Paul, APS Press 2000. p.57-58.

DE NEGRI, J.D. Clorose Variegada dos Citros: nova anomalia afetando pomares em São Paulo e Minas Gerais. Campinas: CATI, 1990. 6p. (Comunicado Técnico, 82).

FERREIRA, C.R.R.P.T. Defensivos agrícolas. Informações Econômicas, v.29, n.9, p.43-45, 1999.

FUNDECITRUS. Estatística CVC (,Araraquara, 2001.

GOES, A. & FEICHTENBERGER, E. Ocorrência da mancha preta causada por Phyllosticta citricarpa (Guignardia citricarpa) em pomares cítricos do Estado de São Paulo. Fitopatologia Brasileira 15: 73-75, 1993.

GOTTWALD, T.R., GRAHAM, J.H., SCHUBERT, T.S. An epidemiological analysis of the spread of citrus canker in urban Miami, Florida, and synergistic interaction with the Asian citrus leafminer. Fruits, vol 52, p. 383-390. 1997.

NEVES, E.M., BOTEON, M. Impactos alocativos e distributivos na citricultura. Preços Agríc., Piracicaba, n.132, p.3- 6, 1998.

SALVA, R.A.; MASSARI, C.A. Situação do ácaro da leprose no Estado de São Paulo - Levantamento - Fundecitrus, agosto de 1995. In: Oliveira, C.A.L.; Donadio, L.C. (ed.). Leprose

1 FUNDECITRUS - Fund for Citurs Plant Protection

2 Scientific Manager - Av. Adhemar Pereira de Barros, 201, 14807-040, Araraquara, SP - Brazil
e-mail: [email protected]

3 FAPESP - The State of São Paulo Research Foundation CNPq - National Council of Scientific and Technologic Development FINEP - Financier of Studies and Projects

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