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[Federal Register Volume 76, Number 31 (Tuesday, February 15, 2011)]
[Rules and Regulations]
[Pages 8603-8605]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: 2011-3367]

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Rules and Regulations
                                                Federal Register
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This section of the FEDERAL REGISTER contains regulatory documents 
having general applicability and legal effect, most of which are keyed 
to and codified in the Code of Federal Regulations, which is published 
under 50 titles pursuant to 44 U.S.C. 1510.

The Code of Federal Regulations is sold by the Superintendent of Documents. 
Prices of new books are listed in the first FEDERAL REGISTER issue of each 
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Federal Register / Vol. 76, No. 31 / Tuesday, February 15, 2011 / 
Rules and Regulations

[[Page 8603]]

DEPARTMENT OF AGRICULTURE

Animal and Plant Health Inspection Service

7 CFR Part 319

[Docket No. APHIS-2008-0052]
RIN 0579-AD07

Citrus Seed Imports; Citrus Greening and Citrus Variegated 
Chlorosis

AGENCY: Animal and Plant Health Inspection Service, USDA.

ACTION: Affirmation of interim rule as final rule.

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SUMMARY: We are adopting as a final rule, without change, an interim 
rule that amended the regulations governing the importation of nursery 
stock to prohibit the importation of propagative seed of several 
Rutaceae (citrus family) genera from certain countries where citrus 
greening or citrus variegated chlorosis (CVC) is present. The interim 
rule also required propagative seed of these genera from all other 
countries to be accompanied by a phytosanitary certificate with an 
additional declaration that neither citrus greening nor CVC are known 
to occur in the country where the seed was produced. We took that 
action because scientific evidence indicated that seed of certain 
genera of the family Rutaceae may be a pathway for the introduction of 
those diseases. The interim rule was necessary in order to prevent the 
introduction or dissemination of citrus greening or CVC within the 
United States.

DATES: Effective on February 15, 2011, we are adopting as a final rule 
the interim rule published at 75 FR 17289-17295 on April 6, 2010.

FOR FURTHER INFORMATION CONTACT: Dr. Arnold Tschanz, Senior Plant 
Pathologist, Plant Health Programs, PPQ, APHIS, 4700 River Road Unit 
133, Riverdale, MD 20737-1231; (301) 734-0627.

SUPPLEMENTARY INFORMATION:

Background

    Citrus greening (known internationally as Huanglongbing disease of 
citrus and referred to below as HLB) is considered to be one of the 
most serious citrus diseases in the world. HLB is a bacterial disease 
caused by strains of the bacterial pathogens ``Candidatus Liberibacter 
asiaticus'', ``Candidatus Liberibacter africanus'', and ``Candidatus 
Liberibacter americanus'' that attack the vascular system of host 
plants. The pathogens are phloem-limited, inhabiting the food-
conducting tissue of the host plant, and causes yellow shoots, blotchy 
mottling and chlorosis, reduced foliage, and tip dieback of citrus 
plants. HLB greatly reduces production, destroys the economic value of 
the fruit, and can kill trees. Once a tree is infected, there is no 
cure for HLB. In areas of the world where the disease is endemic, 
citrus trees decline and die within a few years and may never produce 
usable fruit. HLB was first detected in the United States in Miami-Dade 
County, FL, in 2005, and is only known to be present in the United 
States in the States of Florida and Georgia, Puerto Rico, two parishes 
in Louisiana, and two counties in South Carolina.
    CVC is also a highly injurious disease of citrus. Caused by a 
strain of the bacterium Xylella fastidiosa, CVC causes severe chlorosis 
between veins on the leaves of affected plants. Leaves on affected 
plants frequently have discoloration of the upper leaf coupled with 
brown lesions underneath. CVC may reduce plant growth and lead to 
abnormal flowering and fruit production. CVC is currently not known to 
occur in the United States.
    The regulations in 7 CFR part 319, ``Foreign Quarantine Notices,'' 
prohibit or restrict the importation of certain plants and plant 
products to prevent the introduction or dissemination of plant pests 
and noxious weeds into the United States. The regulations in ``Subpart-
Nursery Stock, Plants, Roots, Bulbs, Seeds, and Other Plant Products,'' 
Sec. Sec.  319.37 through 319.37-14 (referred to below as the 
regulations), restrict, among other things, the importation of seeds 
for propagation.
    In an interim rule \1\ effective and published in the Federal 
Register on April 6, 2010 (75 FR 17289-17295, Docket No. APHIS-2008-
0052), we amended the regulations to prohibit the importation of 
propagative seed of several Rutaceae (citrus family) genera from 
certain countries where HLB or CVC is present, and to require 
propagative seed of these genera from all other countries to be 
accompanied by a phytosanitary certificate with an additional 
declaration that neither HLB nor CVC is known to occur in the country 
where the seed was produced.
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    \1\ To view the interim rule, its supporting and related 
materials, and the comments we received, go to http://www.regulations.gov/fdmspublic/component/main?main=DocketDetail&d=APHIS-2008-0052.
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    Comments on the interim rule were required to be received on or 
before June 7, 2010. We received three comments by that date, from a 
citrus nursery, a company engaged in the commercial production, 
packing, and shipping of citrus products, and a State department of 
agriculture. The comments are addressed below, by topic.

General Comments on the Interim Rule

    One commenter stated that countries in which HLB or CVC is present 
would respond to the prohibitions of the interim rule by in turn 
prohibiting the importation of citrus articles from the United States. 
Because the loss of foreign markets would adversely impact the U.S. 
citrus industry, the commenter stated that the rule should be 
withdrawn.
    On September 19, 2005, the Animal and Plant Health Inspection 
Service (APHIS) of the United States Department of Agriculture (USDA) 
reported the first two confirmed detections of HLB within the United 
States to the International Plant Protection Convention. Since that 
time, it has been at the discretion of foreign countries to promulgate 
regulations prohibiting or restricting the importation of host articles 
of HLB from the United States, based on an assessment of the potential 
risk to plants, plant parts, and plant products within those countries 
that could be associated with the introduction or dissemination of the 
disease. We note, however, that countries that are members of the World 
Trade Organization have committed

[[Page 8604]]

themselves to basing prohibitions or restrictions on the importation of 
articles (such as, in this case, citrus from the United States) on 
scientific evidence and risk assessment.

Comments Regarding Transmission of HLB Through Propagative Seed

    In the interim rule, our stated rationale for imposing prohibitions 
on the importation of seed of genera that are hosts of HLB was that 
emerging evidence suggested that such seed could transmit the disease. 
To that end, we cited a peer-reviewed article by Susan Halbert and 
Keremane Manjunath that detailed that, when seedlings are generated 
from seed that is infected with HLB, a small percentage of those 
seedlings have been found to be infected with HLB.\2\
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    \2\ Halbert, Susan and Keremane L. Manjunath. Asian Citrus 
Psyllids (Sternorrhyncha: Psyllidae) and Greening Disease of Citrus: 
A Literature Review and Assessment of Risk in Florida. Found at 
http://www.bioone.org/doi/pdf/10.1653/0015-4040(2004)087[0330:ACPSPA]2.0.CO;2.
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    All three commenters stated that the Halbert and Manjunath article 
did not provide an adequate scientific basis for considering seed to be 
a pathway for the transmission of HLB. Two of the commenters pointed 
out that Halbert and Manjunath did not conduct original research 
regarding seed transmission, but instead referenced a 1981 study. The 
same commenters also pointed out that researchers in the 1981 study 
collected only a small number of seeds, and did not test the seedlings 
derived from this seed for the disease, but rather determined them to 
have the same stunted, chlorotic appearance as infected plants. Both 
commenters concluded by citing Halbert and Manjunath's assessment that 
the 1981 experiment ``bears repeating'' as evidence that Halbert and 
Manjunath themselves had concerns about the study's findings. Finally, 
one commenter cited two more recent studies, published in 2009, that 
the commenter asserted conclude that HLB is not seed-borne. All three 
commenters stated that we should amend the interim rule to allow the 
importation of propagative seed from countries where only HLB is 
present.
    We disagree with the commenters' interpretation of Halbert and 
Manjunath's assessment of the 1981 experiment; stating that an 
experiment bears repeating is not tantamount to stating that one has 
concerns with its findings, and is, in fact, consistent with the basic 
elements of the scientific method.
    Moreover, the Halbert and Manjunath article was not our sole basis 
for taking regulatory action; we referenced it in order to illustrate 
some of the information that factored into our determination. We 
considered other evidence. For example, as we mentioned in an interim 
rule that established domestic quarantine regulations for HLB and that 
was published in the Federal Register and effective on June 17, 2010 
(75 FR 34322-34336, Docket No. APHIS-2008-0015), researchers at USDA's 
Agricultural Research Service (ARS) and APHIS' Center for Plant Health 
Science and Technology (CPHST) have recently undertaken extensive 
studies to determine the likelihood of seed transmission of HLB. Both 
the ARS and CPHST studies found that a percentage of seedlings from 
infected seed tested positive for HLB via polymerase chain reaction 
(PCR) analysis; in the ARS study, the infection rate varied, but was as 
great as 78.5 percent in certain instances.\3\ ARS researchers did 
note, however, that the bacterium causing HLB remained at a very low 
titer in affected plants, and that most infected seedlings remained 
largely or entirely asymptomatic several years after testing positive 
for the disease.
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    \3\ Benyon, L.S., et al. Transmission of `Candidatus 
Liberibacter asiaticus' from seeds to seedlings in citrus along with 
a low bacterial tier and atypical HLB symptoms. Available by 
contacting the individual listed under FOR FURTHER INFORMATION 
CONTACT.
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    One of the 2009 articles \4\ referenced by the commenter does not 
contradict, and in fact is generally consistent with, the findings of 
the ARS study. The article details a 2007 study, conducted by Ute 
Albrecht and Kim Bowman, in which more than 15,000 seeds were obtained 
from symptomatic trees of the following species: Citrus macrophylla 
Webster, Citrus vangasay bojer, X Poncirus trifoliata, Citrus 
reticulata Blanco, Citrus aurantium L., and Citrus sinensis. Of the 
seedlings grown from these seeds, 769 were tested for HLB via PCR 
analysis at time periods ranging from 7 weeks to 9 months after sowing. 
Five of these 769 seedlings tested positive for the disease. However, 
titer levels of the bacterium were low, and the plants remained 
asymptomatic. In addition, repeated retesting of the positive plants 
several months after the initial test yielded negative PCR results.
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    \4\ Albrect, Ute and Kim D. Bowman. 2009. Canidatus Liberibacter 
asiaticus and Huanglongbing Effects on Citrus Seeds and Seedlings. 
HortScience 44: 1967-1973. Available at http://ddr.nal.usda.gov/bitstream/10113/38868/1/IND44303043.pdf.
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    The other article \5\ referenced by the commenter details an 
experiment that Hajivand Shokrollah conducted in order to determine the 
transmissibility of HLB through seed obtained from infected Citrus 
reticulata plants. As part of the experiment, Shokrollah tested 20 
seedlings grown from such seed by using PCR analysis. While each 
seedling tested negative for HLB, we do not consider 20 plants, all of 
the same species, to be a large enough or varied enough sample size to 
yield conclusive results regarding disease transmission.
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    \5\ Shokrollah, Hajivand, et al. Determination of the Presence 
of Huanglongbing in Seeds and Movement of the Pathogen in Citrus 
reticulata. American Journal of Applied Sciences 6: 60: 1180-1185. 
Available at http://www.allbusiness.com/medicine-health/disease-agents-vectors/13080162-1.html.
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    We acknowledge that all the studies referenced above suggest that 
the transmission of HLB via propagative seed is fundamentally different 
than its transmission via other vectors, such as budwood or Asian 
citrus psyllid: The bacterium is present in infected seedlings at low 
concentration levels, plants remain largely asymptomatic, and plants 
may test negative for the disease after initially testing positive. 
However, it is well-documented that the bacterium associated with HLB 
may be unevenly distributed throughout an infected plant, that the 
latency period for expression of symptoms may be pronounced, and that 
the manner in which those symptoms are expressed is influenced by a 
multitude of factors. Accordingly, because of the severity of HLB, in 
order for us to deregulate propagative seed as a host of the disease, 
we would need clear evidence that the disease cannot be transmitted via 
propagative seed or that infected seedlings cannot serve as vectors of 
the disease. Such evidence does not currently exist. Hence we are 
making no change to the interim rule in response to these comments.
    One commenter stated that hot water dips are effective in treating 
seed for HLB. However, the commenter failed to provide any evidence in 
support of this assertion.

Comments Regarding CVC Transmission Through Propagative Seed

    In the preamble of the interim rule, our stated rationale for 
imposing prohibitions on the importation of seed of genera that are 
hosts of CVC was that there was also emerging evidence that propagative 
seed could transmit this disease. To that end, we cited a 2003 study 
\6\ by W.B. Li et al. (referred to below as Li et al.).
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    \6\ Li, W.B., W.D. Pria, Jr., P.M. Lacava, et al. Presence of 
Xylella fastidiosa in Sweet Orange Fruit and Seeds and Its 
Transmission to Seedlings. Phytopathology (Vol. 93, No. 8) 2003, 
953-958.
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    One commenter pointed out that Li et al. was conducted only on 
three

[[Page 8605]]

subspecies of sweet oranges, did not evaluate disease transmission from 
seeds taken from asymptomatic fruit, and was aborted before conclusive 
findings could be drawn. The commenter therefore asserted that seed 
should not be regulated as a host of CVC until further research is 
conducted.
    The commenter is right in pointing out that Li et al. was aborted 
abruptly, because of a hurricane, and that only a study on three 
subspecies of sweet oranges was concluded by that time. However, CVC 
seed infection rates were greater than 22 percent for one subspecies 
evaluated in that study, and the transmission from seeds to seedlings 
was determined to be ``efficient.'' Moreover, research had begun on 
several other species, and was tending towards the results of the sweet 
orange study. Finally, we note that no studies have been conducted 
since 2003 that call into question the findings of Li et al. For these 
reasons, we have determined that Li et al.'s conclusion, that the study 
``demonstrated that [CVC] can be transmitted through seed to 
seedlings,'' is correct, and constitutes a sufficient basis for the 
prohibitions in the interim rule.
    Therefore, for the reasons given in the interim rule and in this 
document, we are adopting the interim rule as a final rule, without 
change.
    This action also affirms the information contained in the interim 
rule concerning Executive Order 12988 and the Paperwork Reduction Act.
    Further, this action has been determined to be not significant for 
the purposes of Executive Order 12866 and, therefore, has not been 
reviewed by the Office of Management and Budget.

Regulatory Flexibility Act

    This rule affirms an interim rule that amended the regulations 
governing the importation of nursery stock to prohibit the importation 
of propagative seed of several Rutaceae (citrus family) genera from 
certain countries where citrus greening or citrus variegated chlorosis 
(CVC) is present. The interim rule also required propagative seed of 
these genera from all other countries to be accompanied by a 
phytosanitary certificate with an additional declaration that neither 
citrus greening nor CVC are known to occur in the country where the 
seed was produced. The action was necessary in order to prevent the 
introduction or dissemination of citrus greening or CVC within the 
United States.
    We have prepared a final regulatory flexibility analysis addressing 
the economic effects of the interim rule on small entities, as required 
by the Regulatory Flexibility Act. The analysis identifies importers of 
citrus seed as entities potentially affected by the interim rule. The 
full analysis may be viewed on the Regulations.gov Web site (see 
ADDRESSES above for instructions for accessing Regulations.gov) or 
obtained from the person listed under FOR FURTHER INFORMATION CONTACT.

List of Subjects in 7 CFR Part 319

    Coffee, Cotton, Fruits, Imports, Logs, Nursery stock, Plant 
diseases and pests, Quarantine, Reporting and recordkeeping 
requirements, Rice, Vegetables.

PART 319--FOREIGN QUARANTINE NOTICES

    Accordingly, we are adopting as a final rule, without change, the 
interim rule that amended 7 CFR part 319 and that was published at 75 
FR 17289-17295 on April 6, 2010.

    Done in Washington, DC, this 9th day of February 2011.
Kevin Shea,
Acting Administrator, Animal and Plant Health Inspection Service.
[FR Doc. 2011-3367 Filed 2-14-11; 8:45 am]
BILLING CODE 3410-34-P
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