**Recovery Plan**

**for**

**Huanglongbing (HLB) or Citrus Greening**

caused by

*"Candidatus"* Liberibacter africanus, L. asiaticus, and L. americanus

October 17, 2006

Contents page

\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\-\--

Executive Summary 1

Contributors and Reviewer 2

I. Introduction 2

II\. Symptoms 3

III\. Spread 5

IV\. Monitoring and Detection 7

V. Response 8

VI\. USDA Pathogen Permits 9

VII\. Economic Impact and Compensation 10

VIII\. Mitigation and Disease Management 11

IX\. Infrastructure and Experts 15

X. Research, Extension, and Education Priorities 16

References 18

Web Resources 20

This recovery plan is one of several disease-specific documents produced
as part of the National Plant Disease Recovery System (NPDRS) called for
in Homeland Security Presidential Directive Number 9 (HSPD-9). The
purpose of the NPDRS is to insure that the tools, infrastructure,
communication networks, and capacity required to mitigate the impact of
high consequence plant disease outbreaks are such that a reasonable
level of crop production is maintained.

Each disease-specific plan is intended to provide a brief primer on the
disease, assess the status of critical recovery components, and identify
disease management research, extension, and education needs. These
documents are not intended to be stand-alone documents that address all
of the many and varied aspects of plant disease outbreak and all of the
decisions that must be made and actions taken to achieve effective
response and recovery. They are, however, documents that will help USDA
guide further efforts directed toward plant disease recovery.

Executive Summary

Huanglongbing (HLB) of citrus, also known as citrus greening is
recognized as a major threat to citrus production around the world. In
the United States, the harvested citrus acreage has averaged about one
million acres in the past 10 years. This includes oranges, grapefruit,
lemons, tangelos, tangerines and temples. In 2004, citrus production
yielded 16.4 million tons of fruit valued at 2.35 billion dollars. U.S.
production is expected to be seriously affected by HLB.

HLB was detected on two homeowner trees in South Florida on August 23
and confirmed on September 2, 2005. The Florida Department of
Agriculture and the USDA Animal Plant Health Inspection Service are
conducting an extensive survey in Florida and other regions of the
country. HLB appears well established in Florida. The State of Florida
feels eradication is no longer possible and that we must shift gears to
disease management.

Because of the discovery of HLB in Florida, there can be no doubt that
the citrus industry in the United States is threatened. This disease
effectively reduces the quantity and quality of citrus fruits,
eventually rendering infected trees useless. In areas of the world
affected by HLB the average productive lifespan of citrus trees has
dropped from 50 or more years to 15 or less. This is an especially
insidious disease because it displays few symptoms in its early stages
and may escape detection by our current diagnostic methods. The arrival
of the insect vector of HLB, the Asian citrus psyllid, in 1998, made it
inevitable that the HLB pathogens would spread if they were introduced.
It is feared that this vector, now in the presence of the HLB, has
spread HLB beyond our detection capabilities and therefore the ability
to practice effective eradication.

Improvement of survey methods is a key component of this recovery
strategy. A basic limitation of current surveys for HLB is the lack of
accurate and rapid detection techniques. Other critical research needed
to effectively confront HLB includes: determining the host range of the
HLB pathogens, clarifying vector-plant interactions, producing resistant
citrus by transgenic or other means, developing the capacity to culture
the pathogens of HLB, and clarifying our understanding of the basic
biology of the Asian citrus psyllid, the disease vector.

Insecticides have been the first line of defense to manage the vectors
of HLB. Unfortunately, while this strategy may be effective, we do not
know how effective it is; at what rate and how often to apply
insecticides; or which insecticides to apply (we do have some
preliminary data). This is complicated in the U.S. by the lack of
specific pesticide labeling for the Asian citrus psyllid, a situation
currently being addressed by several pesticide companies.

We will depend on the effective use of disease-free nursery plants
coupled with vector management and cultural controls. Citrus production
areas outside of Florida will be protected by quarantines, vector
control and early detection. Surveys will play an important role in
managing this disease and its vector.

**Huanglongbing (HLB) or Citrus Greening**

**(caused by *"Candidatus"* Liberibacter africanus,**

**L. asiaticus, and L. americanus)**

Contributors: John Bash and Rick Melnicoe of University of California;
Kathy Kosta, Magally Luque-Williams, Marylou Polek, and Dale Woods of
California Dept Food & Agriculture; Ron Brlansky, Fred Gmitter, Mark
Mossler, and Michael Rogers of University of Florida; Wayne Dixon, Susan
Halbert, Dennis Howard, and Tim Schubert of Florida Dept Agriculture;
Chung-Jan Chang of University of Georgia; Townsend Peterson of
University of Kansas; Cary Hamilton of New Mexico Dept Ag; Jacque
Fletcher of Oklahoma State University; John DaGraca of Texas A&M
University; Ed Gage of Texas Dept Agriculture; Rick Bennett, Jianchi
Chen, Ed Civerolo, Harold Coble, Vern Damsteegt, Tim Gottwald, David
Hall, John Hartung, Allen Jennings, Keremane Manjunath, Richard Lee,
Doug Luster, Norm Schaad, Kent Smith and Raymond Yokomi of USDA/ARS; Ted
Boratynski, Larry Brown, Russ Bulluck, Gwendolyn Burnett, Osama
El-Lissy, Joel Floyd, Dave Kaplan, Conrad Krass, Coanne O\'Hern, Matt
Royer and Eduardo Varona of USDA/APHIS; Kitty Cardwell of USDA/CSREES;
Dave Bell of USDA/RMA; and Jay Ellenberger, Tara Chand-goyal and Dan
Rosenblatt of USEPA

Reviewer: The American Phytopathological Society

I. Introduction

Huanglongbing (HLB) is the recognized common name adopted by the
International Organization of Citrus Virologists (Da Graca and Korsten,
2004) and the American Phytopathological Society (Timmer et al., 2000).
It was first described in 1956 in Chinese and described in English as
the \"yellow shoot disease\" (Lin, 1956). It has also been called citrus
greening and yellow dragon disease. HLB is probably the most serious
disease of citrus worldwide. Many authors suggest that HLB originated in
China or India in the late 1800s (Bove, 2006; Da Graca and Korsten,
2004; Gottwald et al., 1989; Halbert and Keremane, 2004; Timmer et al.,
2000). HLB seriously affects production of citrus in India, Asia,
Southeast Asia, the Arabian Peninsula, and Africa. In countries where
the disease is endemic, infected citrus seedlings decline within 5 to 8
years after planting and rarely bear usable fruit. Other names for HLB
are likubin in Taiwan, leaf mottling in the Philippines, and vein-phloem
degeneration in Indonesia.

The current range of HLB is in Africa (Burundi, Cameroon, Central
African Republic, Ethiopia, Kenya, Madagascar, Malawi, Mauritius,
Nigeria, Reunion, Rwanda, Somalia, South Africa, Swaziland, Tanzania,
and Zimbabwe), Asia (Bangladesh, Bhutan, Cambodia, China, East Timor,
India, Indonesia, Japan, Laos, Malaysia, Myanmar, Nepal, Pakistan, Papua
New Guinea, Philippines, Saudi Arabia, Taiwan, Thailand, Vietnam, and
Yemen) (Appel, 2004; Bove, 2006; CAB, 2003; Halbert and Keremane, 2004).
In 2004, HLB was detected in South America in Brazil (Bove, 2006;
Coletta Filho et al., 2004; Lopes et al., 2005; Teixeira et al., 2005)
and recently, in 2005, North America in the United States (Bove, 2006;
USDA/APHIS, 2005).

The pathogen that causes HLB is a non-culturable, phloem-inhabiting,
Gram-negative bacterium. Three very similar pathogens have been
described that cause HLB, one each from Africa, Asia and Brazil. They
have been separated into three species: *"Candidatus"* Liberibacter
africanus, *"Candidatus"* Liberibacter asiaticus, and *"Candidatus"*
Liberibacter americanus, named for the continent on which they were
first found.

In Florida, the Asian species of HLB was identified in August 2005. The
Asian citrus psyllid (*Diaphorina citri*) has been present in Florida
since 1998 and is believed to be the primary means by which HLB is
transmitted there (Appel, 2004; Bove, 2006; Coletta Filho et al., 2004;
Halbert and Keremane, 2004; Teixeira et al., 2005; USDA/APHIS, 2005).
The Florida Department of Agriculture and the USDA Animal Plant Health
Inspection Service are conducting an extensive survey throughout Florida
and in other citrus states. At least 652 trees in 12 counties in Florida
have proven positive by PCR tests (DNA identification of the HLB
pathogen). Most of the positive trees are in dooryards (557) but
commercial plantings (95) also are involved (USDA/APHIS, 2006). A team
of state and federal scientists will continue to monitor the incidence
of HLB in Florida and develop an integrated strategy to manage this
disease. Eradication of HLB is not seen as a possibility (University of
Florida, 2006).

The Asiatic and African forms of the disease have indistinguishable
symptoms. However, the African form develops only under cool
temperatures of 20-25ºC, while the Asian form develops under cool and
warm temperatures (20-35ºC). Information on the newly discovered form of
the disease in Brazil is preliminary, but the pathogen appears to be
more closely related to *"Candidatus"* L. asiaticus than to
*Candidatus"* L. africanus. This newly discovered pathogen is not
recognized by primers (DNA probes) specific to either of the previously
described species (Teixeira et al., 2005).

All citrus plants are potential hosts. Historically, the most
susceptible hosts are sweet oranges, tangelos, and mandarins. Moderately
susceptible hosts have been grapefruits, lemons, Rangpur lime,
calamondins, and pummelos. Mexican limes and trifoliate orange have been
more tolerant. Non-citrus species, such as *Murraya paniculata*, may
also serve as hosts of the HLB pathogens (Appel, 2004; Bove, 2006; Da
Graca and Korsten, 2004; Halbert and Keremane, 2004; Lopes et al., 2005;
Timmer et al., 2000).

II\. Symptoms

Symptoms alone are not diagnostic because many plant pathogens or
cultural conditions (fertility, weather, etc.) cause similar symptoms
(Appel, 2004; Bove, 2006). Hence, caution is needed in concluding that a
plant with the symptoms shown below is infected with one of the three
*Candidatus* Liberibacter species.

The initial symptoms are frequently the appearance of yellow shoots or
mottled leaves on a tree (Figure 1). As the bacteria move within the
tree, the entire canopy progressively develops a yellow color, retarded
growth and tip necrosis (Bove, 2006; Da Graca and Korsten, 2004; Halbert
and Keremane, 2004; Timmer et al., 2000).

The most characteristic symptoms of HLB are a blotchy leaf mottle and
vein yellowing that develop on leaves attached to shoots showing the
overall yellow appearance (Figure 2). These foliar symptoms may resemble
other diseases or a zinc deficiency although the green and yellow
contrast is not as vivid with HLB as it is with zinc deficiency. Leaves
with HLB have a mottled appearance that differs from nutrition related
mottling in that HLB-induced

mottling usually crosses leaf veins. Nutrition related mottles usually
are found between or

![](media/image1.jpeg){width="5.25in" height="3.4375in"}Figure 1.
Yellowing of a citrus shoots, on left, caused by HLB; healthy trees on
right. Photo courtesy Stephen M. Garnsey.

![](media/image2.jpeg){width="5.334027777777778in"
height="3.6368055555555556in"}

Figure 2. Leaf mottling caused by HLB. Photo courtesy J.M. Bové and M.
Garnier. Reprinted from Timmer, L.W., Garnsey, S.M., and Graham, J.H.
2000, Compendium of Citrus Diseases, Second Edition, American
Phytopathological Society, St. Paul, MN.

![](media/image3.jpeg){width="4.145138888888889in"
height="2.839583333333333in"}

Figure 3. Misshapen and greenish fruit of citrus affected with HLB
compared to healthy fruit shown in the lower left. Photo courtesy P.
Broadbent. Reprinted from Timmer, L.W., Garnsey, S.M., and Graham, J.H.
2000, Compendium of Citrus Diseases, Second Edition, American
Phytopathological Society, St. Paul, MN.

along leaf veins. Also, HLB-infected leaves may be small and upright
(Halbert and Keremane, 2004).

Fruit from diseased trees are small, often misshapen, and typically some
green color remains on ripened fruit (Figure 3). This is a key symptom,
especially in the presence of aborted seeds, and is the origin of the
common name "greening." The preferred name is currently huanglongbing or
HLB. Yields are almost non-existent, and the remaining fruit are
rendered worthless due to small size, poor color, and bad taste (Bove,
2006; Halbert and Keremane, 2004; Timmer et al., 2000).

HLB is an especially insidious disease because it displays few symptoms
in its early stages, may escape detection with our current diagnostic
methods, and may be vectored over a wide area before detection occurs.
If this disease has entered the U.S. prior to the introduction of the
citrus psyllid, the HLB vector, simple removal of unproductive trees
probably eliminated the pathogens of HLB before they spread. After the
discovery in 1998 in the U.S. of the citrus psyllid (Halbert and
Keremane, 2004), it is feared that this vector, in the presence of the
HLB, spread HLB beyond our detection capabilities and therefore the
ability to practice effective eradication.

III\. Spread

Long distance spread of HLB occurs by grafting with diseased budwood.
Local spread of the disease may be due to grafting but is also
attributed to two species of citrus psyllids. *Diaphorina citri* is the
primary carrier for the Asian form of the disease and presumably the
American form of the disease. *Trioza erytreae* is the primary vector
for the African form. However, both psyllids can transmit the Asian and
African species that cause HLB, at least experimentally (Halbert and
Keremane, 2004).

The Asian citrus psyllid (*Diaphorina citri*) is found only on citrus
(crops and ornamentals) and closely related Rutaceae (citrus family). A
preferred host is *Murraya paniculata*, an ornamental Rutaceaous plant
called jasmine orange that is often planted in the Southern United
States from California to Florida. It is utilized in hedges and as
Bonsai. A closely allied species, *Bergera koenigii*, is used as a
backyard spice plant and is also a potential host. The Asian citrus
psyllid was introduced, probably in early 1998, and spread to most
citrus growing areas in Florida (Da Graca and Korsten, 2004; Halbert and
Keremane, 2004). However, the bacteria that cause HLB have not been
reported in the U.S. until very recently (Bove, 2006; USDA/APHIS, 2005).
It has been noted that elsewhere in the world, when the vector appears,
it is a matter of only a few years until HLB also appears (Appel, 2004).

Adult Asian citrus psyllids are small (3 to 4 mm) with mottled brown
wings (Figure 4). Adults are active, jumping insects. Eggs are bright
orange and deposited on newly emerging citrus tissue. Nymphs are green
or dull orange, and feed on leaves and stems where they are difficult to
see. The Asian citrus psyllid is most likely to be found on new shoots,
and population increases occur during periods of active plant growth
(Appel, 2004; Halbert and Keremane, 2004).

![](media/image4.png){width="3.8756944444444446in"
height="3.308333333333333in"}

Figure 4. Adult female and nymphal instars of Asiatic citrus psyllid.
Drawing courtesy of Frank Mead, Florida Department of Agriculture and
Consumer Services. Reprinted from Catling, H.D., 1970, Distribution of
the psyllid vectors of citrus greening disease, with notes on the
biology and bionomics of *Diaphorina citri*, FAO Plant Protection
Bulletin 18(1):8-15.

The interactions between the vectors and the pathogens are poorly
understood. Acquisition times of between 30 minutes and 24 hours have
been reported. The pathogen also may multiply in the vector. Adults and
fourth and fifth instar Asian citrus psyllid nymphs can transmit L.
asiaticus after 8-12 days. A shorter latent period of 1 day is reported
for the African psyllid (Halbert and Keremane, 2004).

The African citrus psyllid and HLB are found in Africa, the Saudi
Arabian Peninsula, and several islands in the Indian Ocean. The Asian
citrus psyllid and HLB are found throughout Asia, in the Saudi Arabian
Peninsula, and in the same islands in the Indian Ocean. The Asian citrus
psyllid also occurs in several South American and Caribbean countries,
as well as in Florida and Texas in the U.S. The Asian citrus psyllid is
very likely to be a vector of *"Candidatus"* L. americanus as well as
*"Candidatus"* L. asiaticus in Brazil (Appel, 2004; Halbert and
Keremane, 2004).

IV\. Monitoring and Detection

[Current Surveys]{.underline}

Presently, several states are conducting surveys for HLB or the psyllid
vector of HLB.

*Alabama* -- Currently Alabama is surveying for HLB in any area that has
citrus, including ornamentals.

*Arizona* -- The Arizona Department of Agriculture has a survey for HLB
at the present time.

*California* --California has been conducting a citrus canker survey
every spring that considers HLB. The survey is performed in a four‑year
cycle, with the intent to survey approximately 25% of the acreage each
year. The State is divided into three geographical survey districts:
Northern, Central and Southern and each district pathologist coordinates
the survey within their district overseen by a state coordinator. In
addition to surveying for citrus canker symptoms, crews are also trained
in the identification of the psyllid *Diaphorina citri* (vector of HLB).

*Florida* -- Beginning in the spring of 2004 the Florida Cooperative
Agricultural Pest Survey (CAPS) team began an ongoing systematic survey
for HLB in select areas within the state. Areas surveyed were chosen
based on the expectation of HLB. Citrus plant samples collected in the
field by inspectors were screened by departmental experts and highly
suspect samples were tested by the PCR method (see the Detection and
Diagnosis section below). Six rounds of the survey were completed:
spring 2004, fall 2004, and spring 2005 in the greater Orlando area and
the Tampa/St Petersburg area. In addition to CAPS, the Florida Division
of Plant Industry completed an HLB survey from July 2004 to April 2005.
Despite these extensive surveys, HLB was not found until a CAPS survey
targeted likely farms in Homestead, Florida.

HLB was detected on two homeowner trees in South Florida on August 23
and confirmed on September 2, 2005 (USDA/APHIS, 2005). The Florida
Department of Agriculture and the USDA Animal Plant Health Inspection
Service are conducting an extensive survey throughout Florida and in
other citrus states. At least 652 trees in 12 counties in Florida have
proven positive by PCR tests (DNA identification of the HLB pathogen).
Most of the positive trees are in dooryards (557) but commercial
plantings (95) also are involved (USDA/APHIS, 2006). Southeast Florida
is heavily infested, while southwest and south central Florida has a
lighter infestation of HLB. A team of state and federal scientists will
continue to monitor the incidence of HLB in Florida and develop an
integrated strategy to manage this disease. APHIS and the State of
Florida have instituted quarantines to limit the spread of HLB within
Florida and to other states. Eradication of HLB is no longer seen as a
possibility (University of Florida, 2006).

*Louisiana* -- Currently surveying for HLB in any area that has citrus
or its relatives, including ornamentals.

*Texas* -- Texas is conducting surveys. The Texas Department of
Agriculture inspectors are being trained to recognize HLB-like symptoms.

*Quarantine interceptions at ports of entry* -- More than 400 seizures
of citrus plants, leaves and budwood have occurred from passenger
baggage since 1985. Many of those interceptions originated from
countries known to have HLB. Therefore, routine passenger entry is a
likely means by which HLB entered Florida.

[Detection and Diagnosis]{.underline}

After the collection of suspect samples by surveyors, they are examined
by specialists within each state or the National Plant Diagnostic
Network (NPDN) labs. Any likely samples are tested by polymerase chain
reaction (PCR), a DNA probe, for molecular identification of the HLB
pathogens. However, the PCR primers may miss some HLB pathogens leading
to false negatives. Also, the inability to culture the pathogens of HLB
has limited detection capabilities. New methods of identification are
being developed (Bove, 2006; Da Graca and Korsten, 2004).

The ultimate authority for confirming a diagnosis of HLB, since it is a
select agent and exotic pest, rests with the Plant Protection and
Quarantine (PPQ) division of USDA/APHIS. See the following section on
USDA Pathogen Permits or the APHIS web site at
<http://www.aphis.usda.gov/ppq>.

Biological indexing, electron microscopy, serology or some other
technique is needed to provide a more robust general detection of HLB
(Okuda et al., 2005). A purely molecular approach to diagnosis is not
wise, since primers for *"Candidatus"* Liberibacter africanus and
*"Candidatus"* Liberibacter asiaticus did not detect the new
*"Candidatus"* Liberibacter americanus pathotype. A primer set specific
for it has been prepared; however, the precedent is now established that
other *"Candidatus"* Liberibacter variants may exist which would not be
detected by any of the 3 probes.

[Future Surveys]{.underline}

Surveys for HLB are hampered and rendered questionable by two important
detection and sampling limitations. First, simple observations of the
symptoms of HLB are often confused with others diseases and conditions.
Second, citrus plants infected by the HLB pathogens may not show
symptoms for years following infection. During this latent phase of HLB
the

detection technique, PCR, is ineffective.

The most likely route of HLB introduction into Florida was probably via
smuggled HLB-infected plant material. For instance, in California citrus
tristeza virus (CTV) was discovered in a young commercial grove in
Fresno County in 1999. An investigation concluded that budwood infected
with CTV was smuggled into California from Japan. Based on this
experience and others, future movement of HLB by this route is a likely
possibility.

In the future, surveys may be worthwhile on other hosts of the psyllid
vectors of HLB, especially if those hosts are moved across state lines
as are many ornamentals such as *Murraya* spp.

V. Response

While this plan is focused primarily on recovery, certain facets of the
response to a new detection involve aspects of recovery with a continuum
of activities from response to recovery. The response is under USDA,
APHIS, Plant Protection and Quarantine's authority delegated from the
Secretary under the Plant Protection Act of 2000.

Generally, after a detection has been confirmed by a USDA, APHIS, PPQ
recognized authority, APHIS, in cooperation with the State Department of
Agriculture, is responsible for the response. The response is immediate
in the form of advance assessment teams of experts and survey personnel
sent to the site of initial detection to place holds, conduct
investigations, and initiate delimiting surveys. Actions that may be
taken include regulatory measures to quarantine infected or potentially
infected production areas, stop the movement of infected or potentially
infected articles in commerce, and control measures which may include
host removal and destruction, and/or insuring adherence to required
sanitary practices. APHIS imposes quarantines and regulatory
requirements to control and prevent the interstate movement of
quarantine-significant diseases or regulated articles, and works in
conjunction with states to impose these actions parallel to state
regulatory actions which restrict intrastate movement.

Huanglongbing is now considered established in Florida and is under
management as part of the Citrus Health Response Plan. Once an HLB
sample in another citrus growing state is confirmed positive by an APHIS
recognized authority, an advanced technical team may be sent to the site
as the first step in a response. A larger team would then be deployed
consisting of state and federal regulatory personnel operating under a
unified command within the Incident Command System. Survey teams will
conduct delimiting surveys in the area using trace back and trace
forward information and with various appropriate stratified delimiting
sampling schemes for surveys in the area of detection. It is important
as part of the response to control the movement of disease host and
vector host nursery stock out of infested counties since this may serve
as an avenue to infect other citrus production areas.

After the results of delimiting survey are known, if the disease is
considered generally distributed through commercial and residential
plant hosts in an area, options for control are very limited. In areas
where the vector is present, such as in citrus growing areas of Texas,
because of the lack of information about dispersal distance of the
vector and what an appropriate buffer distance for tree removal around
infected trees is, the response will likely be a long-term management
strategy similar to the Citrus Health Response Plan in Florida. If the
disease is isolated as it may be in an area where vectors are not
present, there is a good chance for eradication by destroying all
infected trees and any trees propagated from infected trees.

The "HLB New Pest Response Guidelines" document gives details of the
response options discussed above. For more information, see the link to
these guidelines at:
<http://www.aphis.usda.gov/ppq/ep/citrus_greening/index.html>

VI\. USDA Pathogen Permits

USDA/APHIS/PPQ permit and registration requirements for plant diseases
and laboratories fall under two authorities, the Plant Protection Act (7
CFR Part 330) and the Agricultural Bioterrorism Protection Act of 2002
(7 CFR Part 331). Laboratories receiving suspect infected plant material
or cultures are required to have PPQ permits. Laboratories possessing,
using, or transferring select agents such as \"*Candidatus*\"
Liberibacter spp., the causal agents of HLB, are required to be
registered, however diagnostic laboratories that identify select agents
are exempt from this requirement as long as they complete an APHIS/CDC
Form 4 and destroy the culture within 7 days.

The Plant Protection Act permit requirements apply to all plant pests.
This includes arthropod vectors of plant pathogens, such as the Asian
citrus psyllid (*Diaphorina citri*) and infected plant material,
including diagnostic samples, regardless of their quarantine status,
shipped interstate and require that the receiving laboratory have a
permit. For further guidance on permitting of plant pest material,
consult the PPQ permit website at:
<http://www.aphis.usda.gov/ppq/permits/> or contact PPQ Permit Services
at (301) 734-8758.

The Agricultural Bioterrorism Protection Act of 2002 (7 CFR Part 331)
specifies requirements for possession, use, and transfer of organisms
listed as select agents as are the HLB pathogens. Once an unregistered
diagnostic laboratory identifies a select agent, they must immediately
notify the APHIS Select Agent Program, complete an APHIS/CDC Form 4
within 7 days and either destroy or transfer the agent to a registered
entity within 7 days. In compliance with this Act, if a diagnostic
laboratory held back part of a screened sample or culture for voucher
purposes and that sample forwarded to the USDA Beltsville Laboratory
came back as positive for a select agent, the diagnostic laboratory is
required to notify the APHIS Select Agent Program immediately. This must
take place within seven (7) days of results notification and a PPQ
Officer must have the opportunity to witness the destruction of the
sample or culture within that time period. Clarification of this and
other information related to adherence to the select agent regulations
is available on the following APHIS website:
<http://www.aphis.usda.gov/programs/ag_selectagent/index.html>, or call
(301) 734-5960.

Researchers in the U.S. wishing to work with foreign plant pathogens
that are not select agents should review the websites listed above and
contact the PPQ permit unit to understand how best to comply with the
permit requirements\.... How to, limitations, any special
considerations?

VII\. Economic Impact and Compensation

Severe yield losses result from HLB infections of citrus trees. Trees in
the orchards usually die in about 3-8 years after becoming infected and
require removal and replanting. An 8-year survey conducted on Reunion
Island (France: Indian Ocean) in the 1980s and 90s determined that 65%
of the citrus trees were infected and unproductive within 7 years of
planting (Gottwald et al., 1989). Healthy citrus trees must live 5 to 10
years to make a profit. An infected tree produces misshapen fruit that
is bitter and generally unsuitable for sale as fresh fruit or for juice
(Appel, 2004; Bove, 2006; Da Graca and Korsten, 2004; Halbert and
Keremane, 2004; Roistacher, 1996).

A study was undertaken in the late 1990\'s to ascertain the number of
HLB-infected trees worldwide. It was estimated that 53 million trees
were infected in Asia and 10 million in Africa. A decade earlier HLB
infection resulted in the destruction of 30 million trees in Indonesia
alone. Four million citrus trees infected by HLB were destroyed on the
island of Bali in Indonesia over the period of 1986-88 and replanted
with mandarins in 1991. Of that new planting, 40% of the trees were
infected by 1993 and 90% showed symptoms by 1996. These examples explain
why HLB is held responsible for the marked decline in the citrus
industry in many countries (Bove, 2006; Da Graca and Korsten, 2004;
Halbert and Keremane, 2004).

Harvested citrus acreage in the United States has averaged one million
acres in the past 10 years. This includes oranges, grapefruit, lemons,
tangelos, tangerines and temples. In 2004, citrus production yielded
16.4 million tons of fruit valued at 2.35 billion dollars (Appel, 2004;
USDA/NASS, 2005). Production efficiency is expected to be seriously
compromised by HLB.

The reaction of the Risk Management Agency (RMA) to a loss caused by a
disease of this sort is straightforward. Under the Florida Fruit Tree
Pilot Crop Provisions, disease coverage is provided only for
specifically listed diseases. Currently, "Asiatic Citrus Canker" is the
only disease for which insurance coverage is provided.

The Florida Citrus Fruit Crop Provisions do not list loss of marketable
fruit due to disease as an insurable cause of loss.

Disease is an insurable cause of loss under the Pilot California Citrus
Dollar Crop Provisions, the Arizona-California Citrus Crop Provisions,
and the Texas Citrus Fruit Crop Provisions. However, disease will only
be an insured cause of loss if there are no effective control
mechanisms. The loss of marketable fruit will generally be a covered
cause of loss only for the first-year of occurrence.

Under the Nursery Crop Provisions, disease is a covered cause of loss if
there are no effective control mechanisms. To be insured, nursery trees
and plants must be shown on the approved plant listing for the area. In
Florida, listed plants may include citrus trees and ornamental host
plants grown by commercial nurseries. Disease coverage is provided only
for the insured trees and plants exhibiting damage. Coverage is not
provided for ordered, recommended or other voluntary removal of any
neighboring insured nursery trees or plants that may have been exposed
and do not exhibit the disease symptoms.

RMA expects producers to implement recommended disease control measures
for subsequent crop years to maintain insurance coverage.

VIII\. Mitigation and Disease Management

[Production of clean nursery stock]{.underline}

The first step in successful management of HLB is the production of
clean nursery stock. Without a clean start, there is no hope of an
economic return. Best management practices (BMP) for nurseries endorsed
by state and federal authorities include certification of stock,
inspection, physical and chemical protection for scion trees, liners and
propagations, location requirements such that nurseries are not in the
immediate vicinity of concentrations of citrus, and routine testing of
stock plants. Citrus nurseries should propagate trees from sources that
have been certified as \"pathogen free\" of HLB. A program similar to
that in California for citrus tristeza virus may be prudent. In that
program, testing of registered nursery source trees is mandatory (Appel,
2004).

[Chemical management of vectors]{.underline}

In countries where HLB exists, insecticides are the first line of
defense to manage the psyllid vector, thereby reducing the spread of the
HLB pathogens. Applying insecticide sprays at critical flushing periods
in order to kill psyllid nymphs may be an effective method of HLB
management. Unfortunately, we do not know how effective it is or at what
rate and frequency to apply insecticides. We are not even sure about
which insecticides to apply, although some preliminary data is
available. The following materials in Table 1 are registered in the U.S.
(availability may vary by state) for psyllid control on citrus and have
some efficacy. The materials listed in Table 2 are either of unknown
efficacy or not registered for use on citrus. Imidacloprid,
fenpropathrin, aldicarb, dimethoate, and thiamethoxam have been shown to
be effective insecticides for psyllid management on citrus (Rogers,
2005).

Table 1. Insecticides registered on citrus and have efficacy for psyllid
management.

+-----------+------------+-----+-------+-----------------+----------+
| **Common  | **Trade    | *   |       | **Labeled       | **Effica |
| Name**    | Names**    | *Re |       | Pest(s) on      | cy\*\*** |
|           |            | gis |       | Citrus**        |          |
|           |            | ter |       |                 | **on     |
|           |            | ed\ |       |                 | Ps       |
|           |            | *** |       |                 | yllids** |
+-----------+------------+-----+-------+-----------------+----------+
|           |            | *   | **On  |                 |          |
|           |            | *In | Cit   |                 |          |
|           |            | U.S | rus** |                 |          |
|           |            | .** |       |                 |          |
+-----------+------------+-----+-------+-----------------+----------+
| aldicarb  | Temik      | Yes | FL    | Asian citrus    | \+       |
|           |            |     |       | psyllid         |          |
+-----------+------------+-----+-------+-----------------+----------+
| chl       | Lorsban    | Yes | Yes   | Mites, aphids,  | \+       |
| orpyrifos |            |     |       | thrips, flies,  |          |
|           |            |     |       | scale, etc.     |          |
+-----------+------------+-----+-------+-----------------+----------+
| c         | Baythroid  | Yes | CA &  | Sharpshooter,   | \+       |
| yfluthrin |            |     | AZ    | thrips,         |          |
|           |            |     |       | grasshopper,    |          |
|           |            |     |       | etc.            |          |
+-----------+------------+-----+-------+-----------------+----------+
| d         | Dimate     | Yes | Yes   | Aphids, mites,  | \+       |
| imethoate |            |     |       | scales, thrips, |          |
|           |            |     |       | etc.            |          |
+-----------+------------+-----+-------+-----------------+----------+
| fenp      | Danitol    | Yes | Yes   | Psyllids        | \+       |
| ropathrin |            |     |       | (knock-down)    |          |
+-----------+------------+-----+-------+-----------------+----------+
| hort      | several    | Yes | Yes   | Psyllids        | \+       |
| icultural |            |     |       | (suppression)   |          |
| mineral   |            |     |       |                 |          |
| oils      |            |     |       |                 |          |
+-----------+------------+-----+-------+-----------------+----------+
| imi       | Admire -   | Yes | Yes   | Asian citrus    | \+       |
| dacloprid | soil       |     |       | psyllid         |          |
|           |            |     |       | (prophylaxis)   |          |
+-----------+------------+-----+-------+-----------------+----------+
|           | Provado -  |     |       |                 | \+       |
|           | foliar     |     |       |                 |          |
+-----------+------------+-----+-------+-----------------+----------+

\* Consult your state\'s pesticide regulatory agency to confirm
registration status.

\*\* Efficacy based on published (Rogers, 2005) and unpublished data by
Michael E. Rogers.

Table 2. Insecticides of uncertain efficacy for psyllid control and/or
not registered on citrus.

+-----------+-----------+-------+-------+-----------------+----------+
| **Common  | **Trade   | *     |       | **Labeled       | **Effica |
| Name**    | Names**   | *Regi |       | Pest(s)**       | cy\*\*** |
|           |           | stere |       |                 |          |
|           |           | d\*** |       | **on Citrus**   | **on     |
|           |           |       |       |                 | Ps       |
|           |           |       |       |                 | yllids** |
+-----------+-----------+-------+-------+-----------------+----------+
|           |           | **In  | **On  |                 |          |
|           |           | U     | Cit   |                 |          |
|           |           | .S.** | rus** |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| ac        | Actigard  | Yes   | No    | N/A (plant      | ?        |
| ibenzolar |           |       |       | activator       |          |
| -S-methyl |           |       |       | against         |          |
|           |           |       |       | bacteria)       |          |
+-----------+-----------+-------+-------+-----------------+----------+
| *         | Mycotrol, | Yes   | Yes   | Psyllids        | ?        |
| Beauveria | B         |       |       |                 |          |
| bassiana* | otaniGard |       |       |                 |          |
| GHA       |           |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| b         | Applaud   | Yes   | Yes   | Scales          | ?        |
| uprofezin |           |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| capsaicin | Super     | Yes   | Yes   | Aphids, mites,  | ?        |
|           | Pepper    |       |       | scale, thrips   |          |
|           | Guard     |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| carbaryl  | Sevin     | Yes   | Yes   | Leafrollers,    | ?        |
|           |           |       |       | mites, plant    |          |
|           |           |       |       | bugs, scales    |          |
+-----------+-----------+-------+-------+-----------------+----------+
| fenp      | FujiMite  | Yes   | No    | N/A             | ?        |
| yroximate |           |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| kaolin    | Surround  | Yes   | Yes   | Psyllids        | ?        |
+-----------+-----------+-------+-------+-----------------+----------+
| malathion | many      | Yes   | No    | N/A             | ?        |
+-----------+-----------+-------+-------+-----------------+----------+
| piperonyl | Pyrenone  | Yes   | Yes   | Psyllids        | ?        |
| b         |           |       |       |                 |          |
| utoxide + |           |       |       |                 |          |
| pyrethins |           |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| p         | MGK       | Yes   | Yes   | Psyllids        | ?        |
| yrethrins |           |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| pyr       | Knack     | Yes   | Yes   | Scales, flies,  | ?        |
| iproxyfen |           |       |       | leafminer       |          |
+-----------+-----------+-------+-------+-----------------+----------+
| spir      | Envidor   | Yes   | Yes   | Mites           | ?        |
| odiclofen |           |       |       |                 |          |
+-----------+-----------+-------+-------+-----------------+----------+
| spi       | Oberon,   | Yes   | Yes   | Mites           | ?        |
| romesifen | Forbid    |       |       | (non-bearing    |          |
|           |           |       |       | fruit trees     |          |
|           |           |       |       | only)           |          |
+-----------+-----------+-------+-------+-----------------+----------+
| thi       | Actara    | Yes   | No    | N/A             | \+       |
| amethoxam |           |       |       | (registration   |          |
|           |           |       |       | sought)         |          |
+-----------+-----------+-------+-------+-----------------+----------+

\* Consult your state\'s pesticide regulatory agency to confirm
registration status.

\*\* Efficacy based on published (Rogers, 2005) and unpublished data by
Michael E. Rogers.

N/A = not applicable because there are no U.S. labels for citrus use.

[Biological control]{.underline}

Biological control should be considered in any pest management program.
However, in this case little success has been experienced from
biological control programs. The population fluctuations inherent in the
biological system of a perennial crop diminish the effectiveness of
biological control for long term management of citrus psyllids.
Biological control of the two psyllid vectors of HLB apparently was
achieved on Reunion Island (France: Indian Ocean) with hymenopteran
psyllid parasites: *Tamarixia radiata* introduced from India against
*Diaphorina citri*, and *Tamarixia dryi*, from South Africa against
*Trioza erytreae* (Gottwald et al., 1989). The unparalleled success on
Reunion Island is thought to be related to the fact Reunion has an
unbuffered, closed island ecosystem. However, this remarkable result was
not achieved anywhere else. In contrast, the parasites have been present
in other locations such as India, Taiwan, Brazil, and Miami, Florida
where HLB continues to spread unabated. The two parasites specific to
*D. citri* were introduced into Florida in 1999, but only one, *T.
radiata*, is established (Appel, 2004; Michaud, 2004).

Lady beetles, the native *Olla v-nigrum* and the exotic *Harmonia
axyridis*, provide the best suppression of *D. citri* populations in
Florida (Michaud, 2004). Biological control of *D. citri* may suppress
vector populations in residential areas if no pesticides are used, but
reliance on biological control for commercial production probably is
impossible.

Biological control is expected to play a greater role in residential
planting (dooryards). Dooryard plantings do not employ the management
methods of commercial plantings such as insecticides and removal after
PCR detection methods. They will rely heavily on biological and cultural
tools that are inexpensive and more readily available to homeowners.

[Cultural control]{.underline}

The use of cultural methods for control of HLB has had some limited
success. In South Africa, removal of infected branches and trees,
removal of neglected trees, and the use of HLB-free planting material
are used to reduce the impact of HLB. In this regard, clean nursery
programs are essential. These methods must be combined with removal of
nearby ornamental citrus species that may act as a reservoir of the HLB
vectors and possibly HLB (Halbert and Keremane, 2004). Reservoir species
that may be especially troublesome are orange jasmine and Chinese box
orange.

Severe pruning of infected trees, partially successful in South Africa,
has not been useful in Brazil. After three months, 100% of pruned plants
were PCR positive for HLB. Brazil now recommends that infected trees be
removed within 48 hours of confirmation.

[Education]{.underline}

Education of homeowners and the citrus community is key to recovery from
this disease. Informal surveys by these groups may very well help
identify infected plants. Also, if the public and citrus producing
communities are educated about the threat posed by HLB, they are much
more likely to support management measures. Cooperative Extension plays
a key role in developing this component. There is an increased need for
broadly-trained personnel to educate the citrus industry and the public
about IPM and related issues.

[Eradication]{.underline}

Early detection and removal of infected trees should be the most
effective way of eradicating HLB after introduction. However, the
success of such an eradication strategy depends heavily on how early
identification and destruction of infected trees. Detection tools are
inadequate in this regard. By the time HLB is detected by visual
symptoms and confirmed by PCR, it has been resident in the infected
trees for years and when a vector is present has likely spread to other
trees. For this reason, identification in Florida was after the early
detection phase of this disease and eradication of HLB is no longer
considered a possibility in the State of Florida (University of Florida,
2006).

[Exclusion]{.underline}

Propagating material and plants are the primary means by which HLB is
spread over long distances (Appel, 2004). Regulatory restrictions on the
movement of both budwood and plants are crucial, especially if HLB
vectors are present (Bove, 2006; Timmer et al., 2000). The USDA APHIS
has restrictions in place for the importation of citrus germplasm
(budwood, plants, etc.) into the United States. Since the outbreak of
HLB in Florida, the USDA has imposed additional restrictions on the
export of citrus, citrus relatives, and other host species (e.g.
Murraya) from infested areas to other areas of Florida and other
citrus‑producing states.

Citrus seeds are imported routinely without any restrictions. This
avenue of HLB entrance is controversial (CAB, 2003; Halbert and
Keremane, 2004) and should be further investigated in order to exclude
the possibility of the entrance of HLB by this route.

Another exclusionary technique would be the removal of HLB and psyllid
hosts, say a mile around commercial fields, to limit transmission of HLB
by psyllids.

[Germplasm]{.underline}

Citrus germplasm is not rated routinely for resistance to the HLB
pathogens, although it is routinely screened for the presence of any
pathogens, such as those causing HLB. There are, however, differences in
susceptibility among citrus species, although all citrus species are
potential hosts. Historically, the most susceptible hosts are sweet
oranges, tangelos, and mandarins. Moderately susceptible hosts reported
include grapefruits, lemons, Rangpur lime, calamondins, and pummelos.
Mexican limes, and trifoliate orange have been reported as the most
tolerant. Surprisingly, the Florida isolates that cause HLB are
especially hard on pummelos, limes and grapefruit. While conventional
breeding techniques may yield resistant varieties, efficient genetic
transformation (biotech) techniques, already developed for citrus, may
yield results sooner (Yang et al., 2001).

[Other controls]{.underline}

The combination of shoot tip grafting, heat therapy and indexing is an
effective way to clean up infected propagation material. Heat therapy is
expensive, but it is used on high value material such as \"Foundation\"
nursery plant material. The effectiveness of heat therapy on a
large-scale has been variable between the Asian and African HLB likely
due to their different temperature regimes.

Other possible management techniques worthy of consideration are the use
of mild strains of HLB for cross protection. This and a wide variety of
other innovative management methods are discussed in the Proceedings of
2nd International Citrus Canker and Huanglongbing Research Workshop held
in November 2005 (LaVigne et al., 2005).

[Integration of Mitigation and Disease Management
Strategies]{.underline}

An integrated disease management strategy is needed to limit the spread
of HLB. Clean nursery programs that provide disease-free citrus are
imperative in concert with the destruction of infected trees and the
judicious use of insecticides to manage the psyllid vector. This
includes the removal of nearby ornamental citrus relatives that may act
as reservoirs of the HLB vector and possibly the pathogens. Use of
vector parasites and planting in areas free of vectors also should be
considered. Of course, effective scouting by well-trained personnel with
practical and interdisciplinary pest biology backgrounds will be
essential. Grove self-inspection should be a goal of Cooperative
Education programs.

These measures should be supported by research that enhances our
understanding and advances our management of this disease but they must
be used in concert -- individually they will have little effect. Results
will be realized much sooner if a source of resistance can be identified
(Appel, 2004; Bove, 2006; Da Graca and Korsten, 2004; Halbert and
Keremane, 2004; Timmer et al., 2000).

IX\. Infrastructure and Experts

A citrus research infrastructure exists to study citrus diseases. That
infrastructure could be directed to answer several important issues of
HLB listed in the next section on research priorities. If permitted,
most of that research probably would be limited to Florida, where the
current infestation has been found, due to quarantine concerns. However,
in some instances there will be good reason to conduct research in
locations that lack all three components: citrus, psyllids, and the
pathogens of HLB. In Florida, the primary centers of citrus research are
at the University of Florida\'s Citrus Research and Education Center at
Lake Alfred and Ft. Myers as well as at the USDA/ARS facility at Ft.
Pierce.

Research projects concerning HLB are active at the University of Florida
in Ft. Myers, Gainesville and Lake Alfred; USDA-ARS facilities in Ft.
Detrick Maryland, Riverside California, Ft. Pierce Florida, and
Beltsville Maryland; and the U.S. Department of Energy\'s Los Alamos
National Laboratory in New Mexico. According to the USDA/CSREES Current
Research Information System, \$15 million dollars were allocated for HLB
related research from 2001 to 2005. Of this amount, slightly less than
\$500 thousand were spent on research projects directed specifically at
HLB or its vector.

The following experts on HLB have been identified (Appel, 2004):

Joseph Bove -- expert on all phases of HLB

(retired) Lab Biol Cell Mol, Inst Biol Vegetale Mol, INRS, BP 81,
F-33883 Villenave d\'Ornon Cedex, France,+33-5-57-122369,
joseph.bove@wanadoo.fr

Ron Brlansky -- expert on identification and management of HLB and
vector transmission

Univ of Florida, Citrus Research and Education Center, 700 Experiment
Station Rd, Lake Alfred, FL 33850, 863-956-1151 ex 1300, fax
863-956-4631, rhby@ufl.edu

Russ Bulluck -- expert on biology and response to HLB

USDA, APHIS, PPQ, Center for Plant Health Science and Technology, 1730
Varsity Drive, Raleigh, NC 27607, 919-855-7646, fax 919-855-7480,
russ.bulluck@aphis.usda.gov

Joel Floyd (Contact), USDA Animal and Plant Health Inspection Service --
experts on biology and response to HLB, USDA, APHIS, PPQ, 4700
Riverdale, MD 20737, 301-734-4396, joel.p.floyd@aphis.usda.gov

Tim Gottwald -- expert on incidence and spread of HLB (epidemiology)

USDA, ARS, US Horticultural Research Laboratory, 2001 South Rock Road,
Ft. Pierce, FL 34945-3030, 772-462-5883, fax 772-462-5983,
tgottwald@ushrl.ars.usda.gov

John da Graca -- expert in all phases of HLB

Texas A&M University-Kingsville, Citrus Center, P.O. Box 1150, Weslaco,
TX 78599-1150, 956-968-2132, FAX: 956-969-0649, j-dagraca@tamu.edu

Susan Halbert -- expert on biology and management of HLB vectors and
field survey for HLB

Florida Department of Agriculture and Consumer Services, Division of
Plant Industry, PO Box 147100, Gainesville, FL 32614-7100, 352-372-3505
ex 185, halbers@doacs.state.fl.us

John Hartung -- expert in genomics of citrus and HLB

USDA, ARS, Fruit Laboratory, 10300 Baltimore Ave, Bldg 010a Barc-West,
Beltsville, MD, 20705-2350, 301-504-6571, fax 301-504-5062,
hartungj@ba.ars.usda.gov

Manjunath Keremane -- expert on detection of HLB in psyllid vectors

USDA, ARS, NCGRCD, 1060 Martin Luther King Blvd., Riverside, CA 92507,
951-827-4399, rivmk@ars-grin.gov

J.P. Michaud -- expert in biological control of HLB vectors

Kansas State University, Agricultural Research Center -- Hays, 1232
240th Ave., Hays, KS 67601, 785-625-3425 ex 212, fax 785-623-4369,
jpmi@ksu.edu

Michael Rogers -- expert on biology and management of HLB vectors

University of Florida, Citrus Research and Education Center, Lake
Alfred, FL, 863-956-1151, mrogers@crec.ifas.ufl.edu

Jim Stack (Director), National Plant Diagnostic Network -- experts in
diagnosis and detection of HLB, Kansas State University, 4024
Throckmorton Hall, Manhattan, KS 66506-5502, 785-532-1388, fax
785-532-5692, jstack@ksu.edu

Hong-Ji Su -- expert on detection, biology, and management of HLB

National Taiwan University, Taipei, Taiwan, 886-2-23625717,
hjsu@ntu.edu.tw

X. Research, Extension, and Education Priorities

[Research Priorities]{.underline}

The following lines of research are needed to enhance detection and
management of HLB. They would improve our ability to block the entrance,
detect the presence, and help manage the impact of HLB. The research
priorities listed below are broken into three groups based on relative
importance. Priorities within groups are considered equal. The top group
is listed as Most Important, the second group is Highly Important, and
the last group is Needs Evaluation -- important but less so than the
first two groups.

Research is active in several areas, including: biological control and
IPM techniques, germplasm development, molecular approaches such as DNA
probes, improved assays, maintenance of pathogen collections, and
epidemiology and genetic diversity. Specifics about this research can be
obtained from the USDA/CSREES Current Research Information System
website at: <http://cris.csrees.usda.gov/>. The future of research on
HLB was discussed in detail and a research priority list was constructed
at an international meeting held in 2005 in Orlando Florida (LaVigne et
al., 2005).

[Most Important]{.underline}

**▪** Develop **survey technique** for the HLB pathogens that is quick
and inexpensive -- The method should allow fast and efficient survey and
detection using serology or better and cheaper PCR primers. This should
help explain disease epidemiology leading to better management.

**▪** Determine **host range** of Liberibacter spp. and Asian citrus
psyllid -- Survey design will be impacted and improved by knowledge of
the host range. Hosts known to harbor the HLB vector should receive
first priority. Liberibacter populations in hosts should be determined.

**▪** Investigate **seed transmission** of Liberibacter spp. -- Current
open policy on international trade in citrus seeds may be allowing a
potential hazard that quarantine regulations could help resolve.
Determine seed and graft transmission from asymptomatic plants.

[Highly Important]{.underline}

▪ Develop **transgenic citrus varieties** with resistance to
Liberibacter spp. and a rapid screening method for resistant cultivars
-- Resistant varieties are a preferred means of management and probably
the most promising long‑term solution to HLB.

▪ New and/or improved **sampling and diagnosis**; sample twigs or
psyllids; determine preferred sector of tree -- This will enhance
effectiveness and minimize cost of surveys and allow the development of
a national survey standard to improve ability to compare states.

**▪** Develop a **survey technique** for the HLB pathogens that is more
accurate -- Should allow recognition of all strains thereby reducing the
number of false negatives and positives during survey and detection.

**▪** Evaluate **insecticide efficacy** on psyllids -- Should guide
selection of insecticides from regular registrations and for Section 18
requests.

**▪ Culture** Liberibacter spp. -- This is an important tool for
research in many areas. Plant and insect tissue should be investigated
as culture media. Successful culturing will lead to serological tests --
important survey tools.

▪ Determine complete **genomic sequence** of HLB pathogens -- Serve as a
basis for other HLB research and foster a forensic approach to determine
fine differences among strains or isolates.

▪ Investigate how **host‑pathogen interactions** affect disease severity
and epidemiology -- This area has great potential for enhancing
management.

[Needs Evaluation]{.underline}

▪ Evaluate psyllid and HLB **invasive potential** -- Determine the
potential range of the Asian citrus psyllid and HLB in the U.S. and the
expected severity of disease.

**▪** Determine the impact of the **vector and pathogen** on each other
-- Culturing Liberibacter spp. may be more successful with insect
medium. The potential impact of the pathogen on vector biology may
explain disease patterns and control.

**▪** Determine benefit of **psyllid control** -- This is currently
undetermined and is needed to justify psyllid management. Determining
the importance of adults vs. nymphs as vectors is also important.

**▪** Evaluate time and parameters required for **psyllid transmission**
-- This will help in developing effective disease management strategies
based on psyllid biology and disease epidemiology.

▪ Determine threat of **fruit-mediated transmission** of psyllids and/or
HLB -- Evaluate possibility that HLB could travel in fruit shipments
either in fruit or psyllids.

▪ **Economic impact** of HLB on the U.S. citrus industry -- Communicate
importance of HLB to the citrus industry to justify research priorities.

▪ Determine differences in **symptoms** of infected residential citrus
trees vs. those infected in the field and nursery; determine factors
that affect symptom expression; determine symptoms on non‑citrus hosts
-- This should improve detection and therefore management.

[Extension Priorities]{.underline}

*The following items need development:*

▪ Develop plans to test citrus propagation material to ensure that it is
free of HLB;

▪ Survey citrus and alternate host growing areas and greenhouse areas in
the U.S. with previous citrus history, including soil, water, crops and
weed samples;

▪ Encourage the development of culture and germplasm collections and
foster international cooperation on collections and research;

▪ Develop centers for the production of clean plant material using shoot
tip grafting, heat therapy, and other methods; and

▪ Determine the differences in symptoms of infected residential citrus
trees, commercial groves, and commercial nurseries. Also, determine
factors that affect symptom expression and symptoms on non-citrus hosts.

[Education Priorities]{.underline}

*The following items need development:*

▪ Educate a new cadre of plant pathologists in the epidemiology and
management of bacterial diseases;

▪ Develop training courses on detection, monitoring, and management of
HLB;

▪ Educate county extension, growers and crop advisors in sampling,
monitoring and management of related diseases and in the utility of
map-based tracking and information systems such as the Pest Information
Platform for Education and Extension (PIPE);

▪ Provide standard HLB sampling procedures and training materials for
all citrus-producing states, especially for high risk urban areas (most
likely sites for initial establishment) and nurseries (potential
distribution centers for infected trees), administered through CAPS
citrus commodity surveys; and

▪ Target outreach to homeowners, growers, and pest management
specialists through cooperative extension programs and the NPDN.

References

Appel, D.N. 2004. Huanglongbing of citrus; pathway analysis: intentional
introduction of Candidatus Liberobacter africanus and Candidatus
Liberobacter asiaticus. Special report by the National Agricultural
Biosecurity Center Consortium for the USDA Animal and Plant Health
Inspection Service, 35 pages.

Bove, J.M. 2006. Huanglongbing: a destructive, newly‑emerging,
century‑old

disease of citrus. Journal of Plant Pathology 88:7‑37.

CAB International. 2003. Crop Protection Compendium. CAB International,
Wallingford, UK.

Coletta Filho, H.D., Targon, M.L.P.N., Takita, M.A., DeNegi, J.D.,
Pompeu, Jr., J., Machado, M.A., do Amaral, A.M., and Muller, G.W. 2004.
First report of the causal agent of Huanglongbing, *"Candidatus"*
Liberibacter asiaticus in Brazil. Plant Dis 88(12):1382.

Da Graça, J.V. and Korsten, L. 2004. Citrus huanglongbing: review,
present status and future strategies. Diseases of Fruits and Vegetables,
Volume I, pages 229-245.

Gottwald, T.R., Aubert, B., and Xue-Yaun, Z. 1989. Preliminary analysis
of citrus greening (Huanglungbin) epidemics in the People\'s Republic of
China and French Reunion Island. Phytopathology 79(6):687-693.

Halbert, S.E. and Keremane, M.L. 2004. Asian citrus psyllids
(Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature
review and assessment of risk in Florida. Florida Entomologist
87(3):330-353.

LaVigne, A., Gottwald, T., Graham, J., Berger, P., and Dixon, W. 2005.
Proceedings of 2nd International Citrus Canker and Huanglongbing
Research Workshop, November 7-11, 2005, 87 pages.

Lin, Kung-Hsiang. 1956. Observations on yellow shoot of citrus. Acta
Phytopathologica Sinica 2(2):1-10.

Lopes, S.A., Martins, E.C., and Frare, G.F. 2005. DETECÇÃO DE Candidatus
Liberibacter americanus EM Murraya paniculata (Detection of Ca. L.
americanus in M. paniculata). Summa Phytopathologica 31:48‑49.

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2005. Characterization of the tufB-secE-nusG-rplKAJL-rpoB gene cluster
of the citrus greening organism and detection by loop-mediated
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Web resources

APHIS website:
<http://www.aphis.usda.gov/ppq/ep/citrus_greening/index.html>

APS website: <http://www.apsnet.org/media/hottopics.asp>

CREC: <http://www.lal.ufl.edu/extension/greening/index.htm>

Florida Dept Agriculture:
<http://www.doacs.state.fl.us/pi/chrp/greening/citrusgreening.html>

University of Florida:
<http://ipm.ifas.ufl.edu/agricultural/fruit/citrus/ASP-hoy.htm>

USDA initial report:
<http://www.aphis.usda.gov/lpa/news/2005/09/greening_ppq.html>