16

Current status in the management

of HLB - Brazilian Experience
S. A. Lopes, R. B. Bassanezi, J. Belasque Jr.
Fund for the Defense of the Citriculture (Fundecitrus)
Av. Adhemar Pereira de Barros, 201, CEP 14807-040,
Araraquara, SP, Brasil
slopes@fundecitrus.com.br

Resumen
La ocurrencia de varias plagas y enfermedades han incrementado notablemnte los
costos de produccin en ls ctricos de Brasil, particularmente en el estado de So Paulo
(SP). La enfermedad ms importante es el Huanglongbing (HLB), la cual esta asociada a
ls especies Candidatus Liberibacter (Ca. L) asitica y a Ca. L. americana y trasmitidas por
el insecto Diaphorina citri. Aunque el HLB fue reportada en el 2004, actualmente esta
presente en ms de 300 municipios de SP y asi como en los estados de Paran y Minas
Gerais. La enfermedad esta ms expandida em SP, donde el 53.4 % de las 96,000 parcelas
de ctricos y el 3.78 % de los 200 millones de rboles mostraron sintomas en el 2011.
Entre las medidas de control recomendadas se incluyen la eliminacin de rboles
sintomticos, la aplicacin de insecticidas contra el vector y la plantacin de rboles sanos
producidos en viveros cubiertos con malla. Tanto la eliminacin de rboles enfermos,
como el control del vector no han sido adoptados con el rigor y frecuencia necesarias en
todos los huertos . Como consecuencia,
la incidencia de HLB se ha incrementado
considerablemente en ese tipo de huertos, afectando la efectividad del control de la
enfermedad tambien en sus vecinos cercanos. Como resultado del largo periodo de
incubacin del patogeno y de la variacin estacional de la expresin de sntomas,
cualquier estratgia aplicada para controlar la enfermedad podra arrojar resultados
positivos solo despus de por l menos dos aos de una operacin rigurosa y continua.
Adicionalmente, debido a la distancia de diseminacin del patgeno es grande, se tienen
que aplicar estratgias de control en una extensa escala espacial, que que considere la
inclusin algunas huertas de ctricos adyacentes. Esto resulta claro de los anlisis de los
datos de seis aos de manejo de HLB en varias huertas, y de los anlisis de experimentos
conducidos en reas de alta y baja presin del inculo. En general el primer estdio
mostr mejores oportunidades de xito en huertos grandes con rboles adultos,
localizados cercanas a las huertas vecinas, que no practican el control de HLB. El segundo
estudio mostr una reduccin considerable del avance de la enfermedad en el rea de baja
presin de inoculo, lo cual apoya la necesidad de eliminar arboles sintomticos y
controlar por medios qumicos el insecto vector a escala regional. La adopcin del manejo
regional del HLB por parte de grupos de productores distribuidos en varias partes de SP,

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ha causado una declinacin de la incidencia de HLB, la cual actualmente es inferior al 1%,

en una rea equivalente a un tercio del total de plantaciones de ctricos en el estado de SP.
Abstract
In Brazil and, in particular, in the state of So Paulo (SPS), where most citrus fruits
are produced in the country, the occurrence of several citrus diseases and pests has
largely increased the costs of fruit production. Huanglongbing (HLB), associated to
Candidatus Liberibacter asiaticus and Ca. L. americanus and transmitted by the insect
Diaphorina citri, is currently the most important citrus disease. First reported in two
municipalities in 2004 it is now present in more than 300 municipalities of SPS and the
states of Minas Gerais and Paran. In SPS, where the disease is more widespread, 53.4% of
the more than 96 thousand citrus blocks and 3.78% of the ca. 200 million trees were
showing symptoms in 2011. Recommended control measures include the elimination of
symptomatic trees, insecticide application against the insect vector, and planting healthy
trees produced in screened nurseries. Tree elimination and vector control have not been
adopted in all farms with the rigor and frequencies necessary. As a consequence, in such
farms HLB incidence has increased considerably, affecting the effectiveness of disease
control also in their closer neighbors. As a result of the HLB long incubation period and
seasonal variation of symptom expression, a positive result of any applied strategy to
control the disease will appear only after at least two years of continuous and rigorous
operation. Additionally, due to the long distance of pathogen dissemination, the control
strategies have to be applied on a large spatial scale, involving several adjacent citrus
farms. This became clear from the analysis of data of six years of HLB management in
several farms, and from analysis of experiments conducted in areas of low and high
inoculum pressures. Overall, the first study showed better chances of success in larger
farms with old trees, located away from neighboring farms not practicing HLB control. The
second study showed a considerable reduction of disease progress in the area of low
inoculum pressure, supporting the necessity of eliminating symptomatic trees and
chemically controlling the insect vector in regional scales. The adoption of regional HLB
management by several groups of growers distributed in several parts of So Paulo has led
to a decline in HLB incidence which is now lower than one percent in an area equivalent to
one third of the entire citrus plantings in the state.
The Brazilian citriculture
In Brazil, citrus is commercially explored in all geographic regions but of major
importance are the states of So Paulo, Bahia, Sergipe, Minas Gerais and Paran located in
the southeast and north regions of the country. The total citrus area was estimated in 900
thousand hectares in 2007, with around 70% of this total planted in SPS (1), where most
of the estimated 200 million trees are of Valncia, Natal, Pra and Hamlin sweet
oranges. Close to 80% of all harvested fruits are destined to 4 major industries for the
production of 1.35 million tons of concentrated orange juice to be exported mainly to
European, North American and Asian countries, and the remaining 20% are sold in natura
mainly in the local markets (6). In 2007, the country was responsible, respectively, for
40% and 60% of all citrus fruits and orange juice produced in the world (19). The citrus
business has moved 5.6 billion dollars yearly and generated more than 4 hundred
thousand jobs.
Main citrus diseases and pests
The large spatial and long temporal continuities of susceptible tissues, and the low
genetic variability, have made the Sao Paulo Sate (SPS) citriculture vulnerable to the
appearance of new diseases and pests and to the occurrence of severe epidemics. The
necessity to implement disease preventing and contention measures, such as the

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production of new young trees in screened nurseries to avoid insect vectored diseases,
frequent orchard inspections for identification and elimination of disease affected trees,
and constant insecticide and fungicide applications, has increased production costs
considerably. Among the diseases that have caused severe losses historically are: (i) citrus
tristeza, caused by the Citrus tristeza virus, which led to the elimination of more than 9
million trees in the 1940s and replacement of the sour orange rootstock by Rangpur lime;
(ii) citrus leprosis, caused by the Citrus leprosis virus, which was first reported in 1933
and is today responsible for constant applications of costly miticides against the vector of
the pathogen; (iii) citrus canker, caused by the bacterium Xanthomonas citri subsp. citri,
which was first detected in 1957 and led, in the last 9 years only, to the elimination of
more than 7 million plants; (iv) citrus leafminer Phyllocnistis citrella, first reported in
1996, and responsible for leaf damage and for favoring infection by the canker bacterium;
(v) citrus black spot, caused by the fungus Guignardia citricarpa, and today present in
several locations where it induces early fruit drop and fruit depreciation; (vi) citrus
variegated chlorosis, reported in 1987 and in 2011 affecting around 80 million trees only
in SPS, (vii) citrus sudden death, a disease of unknown etiology, which has led to the
elimination of 4 million trees since 2001, when it was first reported; and (viii)
huanglongbing (HLB), caused by Candidatus Liberibacter (Ca. L.) americanus and Ca. L.
asiaticus, and responsible for the elimination of estimated 18 million trees since it was
first reported in 2004.
Huanglongbing
a. Two genetically similar but biologically distinct liberibacter species.
Huanglongbing was first reported in Brazil in March 2004 in 2 farms in two
municipalities in the geographic center of SPS. Currently the disease is present in most SPS
as well as in Minas Gerais and Paran states. The affected plants found at the beginning
showed the characteristic HLB symptoms observed in other countries, namely, yellow
shoots, blotchy-mottled leaves associated in most cases with strong zinc deficiencies,
lopsided fruit with aborted seeds, and shoot dieback. Initially, the use of PCR with primers
specific for Ca. L. asiaticus and Ca. L. africanus gave, however, negative results (20). Soon it
was shown that the reason was the occurrence of a distinct liberibacter, brought later to
species level and named Ca. L. americanus, which contains DNA sequence changes in the
16SDNA gene not fully recognized by the primer pairs used for the other two species. With
the description of the new species, primers were developed for routine pathogen
detection and disease diagnostics, crucial for the field surveys and researches that have
been carried out since 2004.
Soon after the discovery of Ca. L. americanus, Ca. L. asiaticus, known to
occur for over 100 years in China, was also shown to be present in SPS (8), but at a much
lower frequency than Ca. L. americanus. Ca. L. asiaticus frequency has however
dramatically increased over the years. Data analysis of the Fundecitrus diagnostic
laboratory has shown an increase in Ca. L. asiaticus from around 2% in 2004 to less than
over 99.5% in 2012 (14; Nelson Wulff, unpublished data). Concurrently, Ca. L. americanus
proportion decreased from 98% in 2004 to less than 0.5% in 2012. Experimental data
strongly suggest that this shift in liberibacter prevalence is associated to the different
abilities of these liberibacters in multiplying in citrus trees, where Ca. L. asiaticus reaches
higher bacterial titers than Ca. L. americanus (11). Higher titers would increase the
chances of pathogen acquisition and transmission by the insect vector, as has been
described, for example, for the xylem-limited bacterium Xylella fastidiosa in grapevines by
sharpshooters (10). In graft transmission experiments, in singly and co-inoculated trees,
Ca. L. asiaticus has invariably been transmitted at higher percentages than Ca. L.
americanus (11).
Ca. L. americanus and Ca. L. asiaticus also differ in their sensitivities to high
temperatures (12). When affected trees were maintained for 60 days at daily cycles of
27C-32C, or for 90 days at 24C-35C, a complete symptom remission in the new

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vegetative flushes was observed in Ca. L. americanus-, but not in Ca. L. asiaticus-affected
trees. Contrary to the Ca. L. asiaticus-affected trees, the pathogen was not detected in any
tree previously affected by Ca. L. americanus. Ca. L. asiaticus was however affected by the
24C-38C daily cycle, a temperature condition totally detrimental to Ca. L. americanus.
Liberibacter thermal sensitiveness might explain the irregular spatial progress of HLB in
SPS, which has moved to a less extent towards the north and northwest regions of the
state. These regions are characterized by prevalence of hotter summer days than the
center and south of SPS, where HLB may occur at high incidence levels.
b. Liberibacter transmission
Both liberibacters that occur in Brazil are transmitted by the psyllid Diaphorina
citri, shown early in 1967 for Ca. L. asiaticus (7), and 2006 for Ca. L. americanus (21).
Known to occur in Brazil since at least 1942 but not causing any visible damage to citrus
trees, D. citri remained practically unnoticed in citrus orchards until 2004, when it became
the most unwelcome insect in citrus farms requiring frequent insecticide applications in
attempts to keep its populations as low as possible. In the presence of new young flushes
that develop during the wet spring and summer months, or at any time of the year in
irrigated areas, D. citri may reach high populations. Literature reviews show that under
favorable conditions a female may lay up to 800 eggs during the three to four month life
span (9). It takes 15 to 30 days to become an adult after passing through five nymphal
stages. The duration of the egg and nymphal stages of D. citri in Brazil varied from 2.6 to
7.7 days and from 9.4 to 35.8 days, respectively, at temperatures from 18 to 32C (18).
Egg viability was higher than 81.6% at the 18C to 32C. Nymph viability was higher than
70% at the 18 to 30oC, but dramatically reduced at 32C. The lower temperature
development threshold (TT) and thermal constant (K) values were 12.0C and 52.6
degree-days (DD) for eggs, 13.9C and 156.9 DD for nymphs, and 13.5C and 210.9 DD for
the complete biological cycle (egg to adult). Minimum periods for pathogen acquisition
and transmission are under investigation.
The use of contaminated buds during the process of young nursery tree
production could be another means of pathogen transmission. In SPS, this kind of
dissemination is, however, unlikely to occur today since all nursery citrus buds and
rootstocks are produced under screen (see below). Nevertheless, it cannot be discarded
that, in the past, when young nursery trees were produced in open areas, some plants
might have been infested by psyllids, which then disseminated the pathogen over long
distances.
c. Orange jasmine as an alternative host of liberibacter
In Brazil, hosts of Liberibacters include all commercial citrus species and cultivars
(with sweet oranges and mandarins showing higher susceptibility levels than limes and
lemons), and orange jasmine (Murraya exotica, ex Huang, 1997), a very popular
ornamental tree (16,17). The first orange jasmine tree suspected to host Liberibacter was
found in October 2004, in the citrus farm most affected by HLB at that time. The tree was
showing yellow leaves and shoot dieback throughout the canopy. Leaves were collected
and adults of D. citri captured from two parts of the plant. The pathogen (Ca. L.
americanus) was detected by PCR in both leaf samples and in one of seven lots of 10
psyllids. In surveys conducted in 2005/2006 and in 2009, the Liberibacters were detected
in 91 of 786 sampled orange jasmine plants in 10 of 76 sampled locations (15). PCRpositive trees exhibited yellow shoots and/or dieback symptoms indistinguishable from
those on PCR-negative trees. Ca. L. americanus was more common in 2005/2006 (96.6%)
and Ca. L. asiaticus in 2009 (84.8%). rplJ nucleotide sequences were identical within all
populations of either species. Symptoms were mild and developed less rapidly in orange
jasmine than in citrus, probably as a result of lower liberibacter multiplication rates.
Respective titers of Ca. L. americanus and Ca. L. asiaticus in orange jasmine averaged 4.3
and 3.0 log cells per gram of tissue, compared with 5.5 and 7.3 in citrus. The results

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indicate that orange jasmine does not favor liberibacter multiplication as much as citrus.
However, its importance in HLB epidemics should not be underestimated as it is a
preferred host of D. citri and is not under any strict tree-eradication program or measures
for insect control.
d. HLB management practices
HLB management strategies include the elimination of symptomatic trees to
reduce inoculum sources, application of insecticides to reduce vector populations so as to
avoid pathogen dissemination, and production and planting healthy nursery trees.
Ineffectiveness of pruning and elimination of symptomatic trees. Shortly after
the confirmation of the presence of HLB in Brazil, it was believed that removing
symptomatic shoots of affected trees would be enough to remove the contaminated tissues
and cure the diseased tree. With this objective several trees were empirically pruned by
growers, but without success. A field experiment was conducted with 592, 3- to 16-year
old healthy or Ca. L. americanus-affected sweet orange trees (13). The trees were pruned
by removing only the symptomatic shoots (by cutting them at the trunk level), or by
removing the entire canopy (decapitation) (by cutting the trunk 15 to 20 cm above the
graft line). The experiment confirmed the pruning ineffectiveness found by the growers.
Mottled leaves reappeared on most symptomatic (69.2%) or appeared on some
asymptomatic (7.6%) pruned trees, regardless of age, variety, and pruning procedure. The
ineffectiveness of pruning reinforced the importance of symptomatic tree elimination in
HLB management. The elimination of the trees with symptoms is then necessary because
there is no cure for HLB. The identification of the trees to be eliminated requires correct
field detection. Since HLB symptom can be confused with those induced by other
pathogens or mineral deficiencies, in order to find most HLB affected trees in the field, it is
critical to constantly keep in the farms, motivated and well trained inspectors. The use of
platforms coupled to tractors, where the inspectors stay in a better position to look at the
tree canopies, also improves the quality and effectiveness of the inspection process (3,4,5).
In experimental comparisons of groups of 2 to 4 well trained inspectors, the percentage of
symptomatic trees detected increased from average 48% for ground inspections to 60%
for platform with 4 inspectors. As a result of a long and variable incubation period, in
order to find all infected trees, all blocks should be inspected at least four times a year, but
more frequently in the most affected areas in the State. All orange jasmine trees should
also be eliminated from citrus farms. Even if they are not infected with the HLB pathogen,
they may contribute to both disease and vector maintenance and spread.
Control of the insect vector. Reduction of vector populations from internal and
external sources is the second parallel measure. It is costly, as it requires frequent
applications of insecticides, mainly during the spring and summer months, when the
insect usually reaches high populations. To determine the exact time for chemical
applications, the presence of psyllids in the orchard should be monitored visually (from
three to five young shoots of at least 1% trees per block) and with the use of yellow sticky
traps. Due to the migrating behavior of adult psyllid visual scouting and traps should be
placed in the border of the farms or blocks to monitor vector presence. If present, the
grower can choose insecticides, systemic or contact, available in the market. The systemic
ones are the most effective, with residual periods of 60-80 days. They can be applied via
soil, trunk or drenching. They are also the most expensive and, for this reason, are applied
in young nursery trees (before leaving the nursery) and in field trees up to three years of
age. Product absorption and translocation are more effective during the rainy seasons. The
contact insecticides are cheaper but less effective, with residual periods of no longer than
20 days. They are sprayed on trees older than three years, as well as on younger trees
during the dry seasons and simultaneously with systemic at rainy season. To reduce the
operational costs, some growers apply contact insecticides combined with other chemicals
(miticides, fungicides) or micronutrients.

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Planting of healthy trees. The third HLB control measure is the use of certified
healthy young trees for new plantings. In SPS, there is a law since 2003 that determines
that all trees must be produced in screened nurseries protected from the access of D. citri,
aphids and sharpshooters, vectors of HLB, citrus-tristeza and citrus variegated chlorosis
pathogens.
f. Effectiveness of local versus regional HLB management
As a result of the HLB long incubation period and seasonal variation of symptom
expression, a positive result of any applied strategy to control the disease will appear only
after at least two years of continuous and rigorous operation. Additionally, due to the long
distance the pathogen can be disseminated by the insect vector, the recommended
management practices need to be applied on a large spatial scale involving several
adjacent citrus farms. This became clear from a study of cases (3,5) and from analysis of
experiments conducted in areas of low and high external inoculum pressures (2).
The study of cases included data of six years of HLB management from eighteen
farms located in distinct parts of SPS where the recommended measures had been applied
since 2004 or 2005. Overall, the study showed better chances of success in larger farms
with old trees, located away from neighboring farms not practicing HLB control (3,5). The
most important factor for successful management was the early and aggressive
implementation of HLB control practices when the disease incidence is still very low.
In other study two experiments were conducted with the objective to assess the
effectiveness of symptomatic tree removal and insecticide applications, at different
frequencies and combinations, on the temporal progress of the disease within young
sweet orange plots in a period of around five years (2). Experiment one was located in an
area of low external inoculum pressure, representative of a situation of effective HLB
management applied in a large area or entire region, and experiment two was located in
an area of high external inoculum pressure, representative of a deficient HLB management
applied in a small and delimited area. In experiment one symptomatic trees started to
appear 10 months later, and the rate of disease progress and cumulative HLB incidence
were, respectively, 75% and 91% lower than those found in experiment two, probably
because the total and infective psyllid numbers were, respectively 76% and 90% lower.
Also, these experiments showed that with regional management the cost of psyllid control
can be reduced by 50% or more not compromising the efficiency of disease control.
Perspectives of the Brazilian citriculture in the presence of huanglongbing
The presence of the disease in SPS, Paran and Minas Gerais has alarmed growers
from other states in Brazil and growers from the neighboring countries in South America
which are apparently free of HLB. There is no reason to believe that HLB will be confined
to the locations it occurs today. Free transit of people and lack of barriers favor disease
dissemination to short and long distances as well the natural movement of D. citri. The
importance of the disease in the new citrus areas still free of HLB will depend, ultimately,
on how fast and how rigorously the removal of the first affected trees will take place, and
how intense and effective will be the efforts to suppress disease spread. In SPS, despite the
intense work in calling attention to the importance of the disease, many growers have not
followed the recommended measures. As a consequence, HLB incidence has increased
considerably. In some farms, all citrus trees were replaced by sugarcane but in others
affected trees have been maintained in the field, especially the older ones in which the HLB
symptoms seems to progress at lower rates. Most importantly, however, these farms have
served as sources of inoculum and made very challenging to initiate new plantings and too
costly to suppress the disease in their closed neighbors.
Since the disease was first reported in SPS continuous improvements have been
made on the recommended management practices. With the aid of PCR, field inspectors
have become more and more qualified to identify the field symptoms associated to HLB.

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By reducing the energy spent during walking and placing the inspector in a better position
to observe the entire tree canopy, the use of platforms coupled to tractors facilitated
considerably the entire process of inspection reducing the amount of escapes and,
therefore, the sources of inoculum. Lower volumes of insecticide applications have proved
to be as effective as the high volumes applied initially, and aerial applications through
airplanes allow treatment citrus orchards in larger areas in a much shorter time as
compared to terrestrial applications, a very important tool for regional HLB management.
In the entire SPS, HLB has progressed over the years. But this tendency is not true
to all situations. In large farms a decline in HLB incidence has in fact been detected in the
last years. The improvements made in management practices, the constant elimination of
affected trees in large areas, and the increase in the number of organizing growers
adopting regional management practices explain this progress in suppressing HLB. This
interruption in the disease progress curve plus the fact that in one-third of all citrus trees
grown in SPS the HLB incidence is lower than one percent have created an optimism
among growers and all the personnel involved in the citrus business. Contrary to what was
initially predicted, effective HLB management is possible and has become a reality in
Brasil.
Parallel to all efforts made by growers to manage HLB, other management
strategies or improvements in the current ones are under investigation. They include (i)
the use of natural enemies to control D. citri, (ii) search for more effective ways to monitor
vector population, (iii) search for new diagnostic methods to detect infected trees in the
field and/or before they express the first symptoms, and (iv) assessment of the role of
climatic factors in all aspects involved in pathogen transmission and disease progression.
The information generated with such research will be of help but only genetic changes in
the citrus host, making it more resistant to liberibacter infection and multiplication, or less
attractive or repellent to D. citri, will bring the most promising solution to the HLB
problem.
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