Citrus Canker; Movement of Fruit From Quarantined Areas, 54431-54445 [E9-25328]

Agencies

• DEPARTMENT OF AGRICULTURE
• Animal and Plant Health Inspection Service

[Federal Register Volume 74, Number 203 (Thursday, October 22, 2009)]
[Rules and Regulations]
[Pages 54431-54445]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: E9-25328]



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Federal Register / Vol. 74, No. 203 / Thursday, October 22, 2009 / 
Rules and Regulations

[[Page 54431]]



DEPARTMENT OF AGRICULTURE

Animal and Plant Health Inspection Service

7 CFR Part 301

[Docket No. APHIS-2009-0023]
RIN 0579-AC96


Citrus Canker; Movement of Fruit From Quarantined Areas

AGENCY: Animal and Plant Health Inspection Service, USDA.

ACTION: Final rule.

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SUMMARY: We are amending the citrus canker regulations to modify the 
conditions under which fruit may be moved interstate from a quarantined 
area. We are eliminating the requirement that each lot of finished 
fruit be inspected at the packinghouse and found to be free of visible 
symptoms of citrus canker and removing the current prohibition on the 
movement of fruit from a quarantined area to commercial citrus-
producing States. We are continuing to require fruit moved interstate 
from a quarantined area to be treated with an approved disinfectant and 
to be packed in a commercial packinghouse that operates under a 
compliance agreement. These changes will relieve some restrictions on 
the interstate movement of fresh citrus fruit from quarantined areas 
while maintaining conditions that will prevent the artificial spread of 
citrus canker.

EFFECTIVE DATE: October 22, 2009.

FOR FURTHER INFORMATION CONTACT: Mr. Stephen Poe, Senior Operations 
Officer, Emergency and Domestic Programs, Plant Protection and 
Quarantine, APHIS, 4700 River Road Unit 137, Riverdale, MD 20737-1231; 
(301) 734-4387.

SUPPLEMENTARY INFORMATION:

Background

    Citrus canker is a plant disease caused by the bacterium 
Xanthomonas citri subsp. citri (referred to below as Xcc) that affects 
plants and plant parts, including fresh fruit, of citrus and citrus 
relatives (Family Rutaceae). Citrus canker can cause defoliation and 
other serious damage to the leaves and twigs of susceptible plants. It 
can also cause lesions on the fruit of infected plants, which render 
the fruit unmarketable, and cause infected fruit to drop from the trees 
before reaching maturity. The A (Asiatic) strain of citrus canker can 
infect susceptible plants rapidly and lead to extensive economic losses 
in commercial citrus-producing areas. Citrus canker is only known to be 
present in the United States in the State of Florida.
    The regulations to prevent the interstate spread of citrus canker 
are contained in ``Subpart-Citrus Canker'' (7 CFR 301.75-1 through 
301.75-14, referred to below as the regulations). The regulations 
restrict the interstate movement of regulated articles from and through 
areas quarantined because of citrus canker and provide, among other 
things, conditions under which regulated fruit may be moved into, 
through, and from quarantined areas for packing.
    On June 30, 2009, we published in the Federal Register (74 FR 
31201-31209, Docket No. APHIS-2009-0023) a proposal\1\  to amend the 
regulations to modify the conditions under which fruit may be moved 
interstate from a quarantined area. We proposed to eliminate the 
requirement that each lot of finished fruit be inspected at the 
packinghouse and found to be free of visible symptoms of citrus canker 
and to remove the current prohibition on the movement of fruit from a 
quarantined area to American Samoa, Arizona, California, Guam, Hawaii, 
Louisiana, Commonwealth of the Northern Mariana Islands, Puerto Rico, 
Texas, and the U.S. Virgin Islands. (These are the commercial citrus-
producing areas listed in Sec.  301.75-5; we refer to them in this 
document as commercial citrus-producing States.)
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    \1\ To view the proposed rule and the comments we received, go 
to (https://www.regulations.gov/fdmspublic/component/main?main=DocketDetail&d=APHIS-2009-0023).
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    We proposed to continue to require fruit moved interstate from a 
quarantined area to be treated with an approved disinfectant and to be 
packed in a commercial packinghouse that operates under a compliance 
agreement. We proposed these changes to relieve some restrictions on 
the interstate movement of fresh citrus fruit from quarantined areas 
while maintaining conditions that would prevent the artificial spread 
of citrus canker.
    We solicited comments concerning our proposal for 60 days ending 
August 31, 2009. We received 34 comments by that date. They were from 
citrus producers, citrus packers, industry organizations, researchers, 
and representatives of State and foreign governments. Twenty-three 
commenters supported the proposed rule. Two of these commenters also 
directly addressed issues raised in the remaining comments, which are 
discussed below by topic.

Selection of an Option for Mitigating the Risk Associated With the 
Interstate Movement of Regulated Fruit From a Quarantined Area

    In a final rule\2\  effective and published in the Federal Register 
on November 19, 2007 (72 FR 65172-65204, Docket No. APHIS-2007-0022), 
we amended the regulations to establish new conditions for the 
interstate movement of regulated fruit from an area quarantined for 
citrus canker. That final rule eliminated a requirement that the groves 
in which fruit to be moved interstate is produced be inspected and 
found free of citrus canker. Instead, we added the packinghouse 
inspection requirement mentioned earlier. We retained the other 
requirements that had been in the regulations, including the 
requirement that the fruit be treated with a surface disinfectant and 
the prohibition on the movement of fruit from a quarantined area into 
commercial citrus-producing States.
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    \2\ To view the November 2007 final rule, go to (https://www.regulations.gov/fdmspublic/component/main?main=DocketDetail&d=APHIS-2007-0022).
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    We established those conditions based on the conclusions of a pest 
risk assessment (PRA) and risk management analysis (RMA) prepared for 
the 2007 rulemaking. The PRA concluded that asymptomatic, commercially 
produced citrus fruit, treated with a disinfectant and subject to other 
mitigations, is not epidemiologically significant as a

[[Page 54432]]

pathway for the introduction and spread of citrus canker.
    The RMA examined the risks associated with both symptomatic and 
asymptomatic fruit and concluded that the introduction and spread of 
Xcc into other States through the movement of commercially packed fresh 
citrus fruit from quarantined areas is unlikely. In addition, the RMA 
concluded that a phytosanitary inspection would ensure, with high 
confidence, that few shipped fruit would have symptoms of citrus canker 
disease. However, the RMA also concluded that the evidence available at 
that time was not sufficient to support a determination that fresh 
citrus fruit produced in an Xcc-infested grove cannot serve as a 
pathway for the introduction of Xcc into new areas, thus necessitating 
the prohibition on movement of fruit into commercial citrus-producing 
States.
    In our responses to public comments in the Background section of 
the November 2007 final rule, we stated: ``If, in the future, evidence 
is developed to support a determination that commercially packed citrus 
fruit (both symptomatic and asymptomatic) is not an epidemiologically 
significant\3\  pathway for the introduction and spread of citrus 
canker, we would undertake rulemaking to amend our regulations 
accordingly.''
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    \3\ The term ``epidemiologically significant'' refers to the 
minimum conditions required for introduction of a disease into an 
unaffected area. Our judgment of whether fruit is an 
epidemiologically significant pathway for disease transmission is 
based on the likelihood that the fruit itself will be infected with 
the disease, that the infection will occur in a way or at a level 
sufficient for transmission of the disease, and that such an 
infected fruit will encounter the biological conditions required for 
transmission of the disease.
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    Since the publication of the November 2007 final rule, two 
publications have provided additional evidence regarding the potential 
of fruit to serve as a pathway for the introduction and spread of 
citrus canker. This new evidence addresses key uncertainties and caused 
us to revisit our previous findings. The first article, by Gottwald et 
al. (2009), documents research on the survival of Xcc on commercially 
produced and packed citrus fruit and the likelihood that such fruit 
could serve as a mechanism to spread the disease. The second article, 
by Shiotani et al. (2009), documents research on the survival of Xcc on 
commercially produced mandarin fruits and the likelihood of spread of 
Xcc to trees from harvested mandarins.
    Accordingly, we prepared updates to the PRA and RMA that had 
accompanied the November 2007 final rule. The updated PRA, titled ``An 
Updated Evaluation of Citrus Fruit (Citrus spp.) as a Pathway for the 
Introduction of Citrus Canker Disease (Xanthomonas citri subsp. 
citri)'' (March 2009), examines the information presented in Gottwald 
et al. (2009) and Shiotani et al. (2009) in the context of the earlier 
PRA. Based on the evidence presented in both the November 2007 PRA and 
the two new publications, the updated PRA concludes that asymptomatic 
fruit (treated or untreated) is not epidemiologically significant as a 
pathway for introducing citrus canker. It further concludes that 
symptomatic fruit subjected to a packinghouse process that includes 
washing with disinfectants is also not epidemiologically significant as 
a pathway for introducing citrus canker.
    These conclusions led us to prepare a supplemental RMA, titled 
``Movement of Commercially Packed Citrus Fruit from Citrus Canker 
Disease Quarantine Area; Supplemental Risk Management Analysis'' (May 
2009). The supplemental RMA takes into account the conclusions of the 
updated PRA as well as the evidence and discussion presented in the 
November 2007 RMA. Like the November 2007 RMA, the supplemental RMA was 
submitted for peer review, in accordance with the Office of Management 
and Budget's bulletin on peer review. All the materials associated with 
the peer review on the supplemental RMA, including the peer reviewers' 
comments and our responses, are available at (https://www.aphis.usda.gov/peer_review/peer_review_agenda.shtml). The peer 
reviewers' comments were considered in developing the supplemental RMA.
    The supplemental RMA concludes that multiple lines of evidence, 
including, but not limited to, evidence from the two recent studies and 
the November 2007 RMA, indicate that commercially packed and 
disinfected fresh citrus fruit is not an epidemiologically significant 
pathway for the introduction and spread of Xcc, i.e.:
     Disease management practices in the grove reduce, but do 
not eliminate, Xcc populations.
     Commercially produced fruit harvested in areas where Xcc 
exists may be visibly infected or the fruit may carry the pathogen 
either on its surface or in wounds.
     Citrus canker disease development between harvest and 
packinghouse, via wounding for example, is not likely.
     Procedures for cleaning and disinfecting fruit are 
routinely applied by packinghouses.
     The individual efficacy of these procedures for removing 
or destroying Xcc may not be known in detail, but the effect of 
packinghouse treatments reduces the prevalence of viable Xcc and 
therefore the level of inoculum associated with commercially packed 
fresh citrus fruit.
     Packinghouse processing that includes a disinfectant 
treatment further reduces amounts of Xcc inoculum on infected or 
contaminated fruit.
     The viability of bacteria on fruit and in lesions and 
wounds diminishes after the fruit is harvested.
     The viability of Xcc bacteria that survive the packing 
process will further diminish during shipping.
     Epiphytic populations of Xcc may aid in pathogen 
dispersal, but substantial evidence indicates that bacterial 
populations do not infect intact mature fruit.
     Evidence indicates that wounds on harvested fruit 
containing Xcc inoculum do not lead to citrus canker lesion 
development, and Xcc populations generally decline rapidly, although 
wounds might occasionally retain Xcc populations that decline more 
slowly.
     The cool temperatures at which citrus fruit are stored and 
shipped and the duration of storage reduce the ability of Xcc to 
reproduce and cause infection.
     As a condition for successful establishment, Xcc, in 
amounts sufficient to cause infection, must encounter not only an 
environment with a conducive temperature, relative humidity, moisture, 
and wind events for infection, but also must encounter host plant 
tissue that is either at a susceptible growth stage or is wounded and 
then must successfully enter this tissue.
     Despite substantial international trade between Xcc-
infected and noninfected countries, there is no authenticated record of 
movement of diseased fruit or seeds resulting in the introduction of 
Xcc to new areas.
    In light of this evidence, the supplemental RMA considered five 
risk management options for the interstate movement of commercially 
packed citrus fruit from areas quarantined for citrus canker:
     Option 1: Allow distribution of all types and varieties of 
commercially packed citrus fruit to all U.S. States, without 
packinghouse treatment with a disinfectant.
     Option 2: Allow distribution of all types and varieties of 
commercially packed citrus fruit to all U.S. States, subject to 
packinghouse treatment with an Animal and Plant Health Inspection 
Service (APHIS)-approved disinfectant,

[[Page 54433]]

but without the current inspection requirement.
     Option 3: Allow distribution of all types and varieties of 
commercially packed citrus fruit to all U.S. States except commercial 
citrus-producing States, subject to packinghouse treatment of citrus 
fruit with an APHIS-approved disinfectant treatment; and, allow 
distribution of all types and varieties of commercially packed citrus 
fruit to all U.S. States, including commercial citrus-producing States, 
subject to packinghouse treatment with an APHIS-approved disinfectant 
treatment and APHIS inspection for symptoms of citrus canker.
     Option 4: Allow distribution of all types and varieties of 
commercially packed citrus fruit to all U.S. States other than 
commercial citrus-producing States, subject to packinghouse treatment 
with an APHIS-approved disinfectant.
     Option 5: Leave the current regulations for the interstate 
movement of citrus fruit from areas quarantined for citrus canker 
unchanged.
    After considering the evidence presented in the updated PRA and the 
supplemental RMA and the conclusions of those documents, we determined 
that currently available scientific evidence provides additional 
certainty that commercially packed and disinfected fresh citrus fruit 
is not an epidemiologically significant pathway for the spread of Xcc. 
Therefore, no mitigations beyond treatment with an APHIS-approved 
disinfectant are necessary. Accordingly, we proposed to implement 
Option 2.
    Several commenters acknowledged that the risk associated with the 
interstate movement of regulated fruit from a quarantined area is low 
but stated that, if there is any risk associated with allowing fruit to 
move from areas quarantined for citrus canker into commercial citrus-
producing States, such movement should be prohibited. These commenters 
stated that citrus canker has been a destructive and costly disease in 
Florida, one which spurred an eradication attempt that was ultimately 
unsuccessful, and that other commercial citrus-producing States do not 
want to be at risk for the introduction and establishment of the 
disease. One commenter recommended that we err on the side of caution 
in making changes to the regulations and stated that further research 
should be done before fruit from quarantined areas is allowed into 
commercial citrus-producing States.
    Two of these commenters proposed additional risk mitigation 
measures to address the risk they perceived to be associated with fruit 
moved interstate from an area quarantined for citrus canker. Both 
stated that such fruit should not be allowed to move into the eight-
county Citrus Zone in south Texas. These commenters cited the 
suitability of Texas' climate to citrus canker establishment (as 
demonstrated by previous outbreaks of citrus canker in Texas), the 
susceptibility of grapefruit (a common citrus crop in Texas) to citrus 
canker, and citrus canker's effect on young citrus trees. One of these 
commenters additionally requested that fruit destined for Texas 
originate only from groves that have been certified as being free of 
citrus canker for more than a year, based on a survey.
    Another commenter, responding to some of these commenters, stated 
that no agricultural trade between States and countries anywhere in the 
world could be conducted if minimal risk is unacceptable and that the 
proposed rule would mitigate the risks to the point that risks are 
negligible.
    Our goal in restricting the interstate movement of plants, plant 
products, and other articles is not to achieve zero risk, which, as the 
last commenter noted, cannot be achieved in agricultural trade. Rather, 
we seek to impose restrictions on the interstate movement of such 
articles that are commensurate with the risk they pose and that 
mitigate the risk associated with their interstate movement. Based on 
all the available scientific evidence, the updated PRA and supplemental 
RMA concluded that commercially packed and disinfected fresh citrus 
fruit is not an epidemiologically significant pathway for the 
introduction and spread of Xcc. We received several comments on the two 
new publications that led us to prepare the updated PRA and 
supplemental RMA, as well as comments on the updated PRA and 
supplemental RMA themselves. These comments are discussed in further 
detail later in this document. However, they did not change our 
conclusion that commercially packed and disinfected fresh citrus fruit 
is not an epidemiologically significant pathway for the spread of Xcc. 
Accordingly, this final rule implements Option 2 as proposed.
    We are not retaining the current prohibition on the distribution of 
fruit from a quarantined area to commercial citrus-producing States, 
and we are not adding the additional mitigations requested by two of 
the commenters. Based on our determination that fruit is not an 
epidemiologically significant pathway, we have determined that those 
additional mitigations are unnecessary to prevent the spread of citrus 
canker via the interstate movement of fruit from quarantined areas. As 
noted, it is impossible to eliminate all risk associated with the 
interstate movement of fruit from quarantined areas; given the 
conclusions of the updated PRA and the supplemental RMA, following the 
recommendation that we prohibit the movement of fruit into commercial 
citrus-producing States unless all risk is eliminated would impose an 
unnecessary restriction on the movement of fruit.
    Under section 412(a) of the Plant Protection Act (7 U.S.C. Sec.  
7712), the Secretary of Agriculture may prohibit or restrict the 
interstate movement of any plant or plant product if the Secretary 
determines that the prohibition or restriction is necessary to prevent 
the dissemination within the United States of a plant pest or noxious 
weed. Based on our supplemental RMA, APHIS has concluded that 
commercially packed citrus fruit treated with an APHIS-approved 
disinfectant is not an epidemiologically significant pathway for the 
dissemination of citrus canker within the United States. Accordingly, 
APHIS has determined that it is not necessary to prohibit the 
interstate movement of regulated fruit that is commercially packed and 
treated with an APHIS-approved disinfectant from an area that is 
quarantined for citrus canker in order to prevent the dissemination 
within the United States of a plant pest. This determination is based 
on the findings of the updated PRA and the supplemental RMA referred to 
earlier in this document and our judgment that the application of the 
measures we proposed will prevent the dissemination of plant pests 
within the United States.
    One commenter who was opposed to allowing the interstate movement 
of citrus fruit from a quarantined area to commercial citrus-producing 
States stated that California, a commercial citrus-producing State, is 
the home of three of the most important resources of citrus germplasm 
in the United States: The National Clonal Germplasm Repository for 
Citrus and Dates (NCGRCD), a U.S. Department of Agriculture-
Agricultural Research Service (ARS) facility supplying budwood 
worldwide; the Citrus Clonal Protection Program, University of 
California-Riverside (UCR), the first citrus germplasm program in the 
world supplying budwood to California, Arizona, and Texas; and the UCR 
Citrus Variety Collection, perhaps the most diverse citrus collection 
in the world dating back to 1907. The commenter stated that certified 
disease-free budwood and a broad genetic basis for

[[Page 54434]]

variety development and improvement are the foundation of every 
successful, profitable, and sustainable citrus industry in the world 
and that those three germplasm resources are the only ones in the 
United States (if not the world) that have not been exposed to citrus 
canker or other devastating citrus diseases such as citrus greening. 
The commenter stated that taking a ``calculated'' risk to expose these 
invaluable resources to one of the worst citrus diseases in the world, 
citrus canker, based on limited field and packinghouse practices that 
will not be inspected for compliance is unacceptable. This commenter 
also stated that the Florida citrus industry funded a project to 
``rescue'' Florida citrus germplasm by moving it to citrus canker- and 
citrus greening-free California in the NCGRCD facilities.
    As we have determined that commercially packed and disinfected 
fresh citrus fruit is not an epidemiologically significant pathway for 
the introduction and spread of citrus canker, we do not expect that 
these facilities will be exposed to citrus canker as a result of the 
implementation of this final rule.
    However, it should be noted that germplasm facilities are devoted 
to the preservation of the germplasm within the facilities and thus are 
protected against potential sources of pest and disease introduction. 
Indeed, potentially infected germplasm from foreign countries is 
imported into these same facilities for screening purposes, which is a 
much more likely pathway for the introduction of diseases such as 
citrus canker than the interstate movement of regulated fruit from a 
quarantined area. Allowing citrus fruit to be moved interstate from 
quarantined areas into California will not decrease the efficacy of the 
biosecurity in place at these facilities.
    It should also be noted that, under this final rule, packinghouses 
will be inspected to ensure that they are complying with the 
requirements to treat regulated fruit with an APHIS-approved 
disinfectant and to ensure that the fruit is free of leaves, twigs, and 
other plant parts, except for stems that are less than 1 inch long and 
attached to the fruit. With regard to the other commercial fruit 
production practices described in the November 2007 RMA, we assume that 
commercial growers and packinghouses will continue to employ procedures 
that reduce the incidence of citrus canker in their fruit, as citrus 
canker lesions reduce the market value of infected fruit.

New Evidence We Considered in the Updated PRA and Supplemental RMA

    Several commenters generally addressed the Gottwald et al. (2009) 
and Shiotani et al. (2009) publications. We address these comments 
below.
    One commenter stated that the premise of both publications was to 
prove that citrus canker cannot be transmitted by infected or 
contaminated citrus fruit. The commenter stated that, scientifically, a 
negative premise cannot be proven, and the commenter cited this as one 
major flaw of these studies. Another commenter stated that Shiotani et 
al. (2009) did not demonstrate that Xcc cannot be transmitted from 
fruit to susceptible tissue, as it did not adequately resolve the 
ability of Xcc to spread from asymptomatic fruit.
    One commenter, responding to the first commenter, stated that the 
two publications never set out to prove that something cannot happen 
because, philosophically and scientifically, this is impossible. 
However, the commenter stated, both publications soundly proclaim that 
risks can very effectively, very simply, and very reliably be reduced 
below any reasonable and measurable risk of transmitting citrus canker 
disease.
    As the last commenter states, neither of the publications concluded 
that citrus canker cannot be spread by fruit. Gottwald et al. (2009) 
concluded that ``harvested and packinghouse-disinfested citrus fruit 
are extremely unlikely to be a pathway for Xcc to reach and infect 
susceptible citrus and become established in canker-free areas.'' 
Shiotani et al. (2009) concluded that ``there is a low risk [of] 
transmission'' of Xcc from fruit. These conclusions are consistent with 
the conclusions of the updated PRA and supplemental RMA, as described 
earlier.
    Two commenters stated that the research in the Gottwald et al. 
(2009) and Shiotani et al. (2009) publications should be tested and 
retested by others who were not involved in the original research 
before changing the conditions under which fruit is allowed to move 
from an area quarantined for citrus canker. Three commenters stated 
that a national task force consisting of scientists from citrus-
producing areas other than Florida (and besides ARS personnel) should 
be assembled to address any change in current quarantine regulations 
that might result in the introduction of known destructive pathogens 
from known infected areas to noninfected areas (i.e., California, 
Arizona, Texas, etc.).
    The Gottwald et al. (2009) and Shiotani et al. (2009) publications 
were produced independently, published in a peer-reviewed journal, and 
came to similar conclusions regarding the epidemiological significance 
of fruit as a pathway for the spread of citrus canker. Among other 
topics they address, these publications provide valuable evidence 
regarding the potential for Xcc to spread from infected fruit to host 
plants in the field; this evidence is what prompted us to prepare the 
updated PRA and supplemental RMA.
    However, the updated PRA and supplemental RMA considered all the 
available evidence regarding the potential of fruit to serve as an 
epidemiologically significant pathway for the introduction and spread 
of citrus canker, not just the evidence in those publications. The 
weight of all the available evidence is what led us to the conclusion 
that commercially packed and disinfected fresh citrus fruit is not an 
epidemiologically significant pathway for the introduction and spread 
of Xcc. We have determined that the evidence provides adequate 
certainty regarding this conclusion to remove some restrictions on the 
interstate movement of commercially packed and disinfected fresh citrus 
fruit from an area quarantined for citrus canker.
    The November 2007 PRA and RMA and the supplemental RMA prepared for 
this rulemaking were all submitted for peer review in accordance with 
the Office of Management and Budget's bulletin on peer review. The peer 
reviewers for the November 2007 PRA and RMA and the supplemental RMA 
were experts in plant pathology, phytobacteriology, and risk 
assessment. The comments we received from these peer reviewers 
indicated that our analysis of the available evidence regarding the 
risk associated with the movement of fruit from an area quarantined for 
citrus canker was sound.
    It should also be noted that the authors of the Shiotani et al. 
(2009) publication were not affiliated with the State of Florida in any 
way, and the experiments in the Gottwald et al. (2009) publication were 
conducted by an international consortium of scientists working 
cooperatively and reaching the same conclusion after conducting similar 
experiments in two different countries, with participants from 
Argentina as well as Florida.

Gottwald et al. (2009)

    We received several comments specifically addressing Gottwald et 
al. (2009).
    Some of the experiments included in Gottwald et al. (2009) examined 
the

[[Page 54435]]

effectiveness of treatment with a disinfectant at reducing Xcc 
populations on citrus fruit. One commenter stated that the disinfection 
procedures significantly reduced pathogen survival but did not 
completely eliminate it. The commenter stated that, considering the 
large amount of fruit being shipped, even a low survival rate of the 
pathogen poses a high risk for the introduction of Xcc to a disease-
free area.
    This commenter also stated that the limitation of treatments in 
disinfecting fruit with lesions or fruit wounds contaminated with 
inoculum of the pathogen is well known. Oxidizing agents cannot 
effectively remove or reduce inoculum to acceptable levels in wounded 
tissue because of the natural reducing agents that occur in fruit 
tissue. Furthermore, these treatments would have little or no effect on 
established fruit lesions that act as reservoirs of inoculum. Thus, the 
commenter stated, without any inspections, even a few lesions on fruit 
would pose a high risk because the pathogen could not be eliminated 
using existing disinfection practices.
    Another commenter stated that one cannot in a practical sense 
sterilize the surface of fruit; it would do more harm than good, and 
there is no biological reason to do so. The commenter stated that there 
is an inoculum threshold necessary to naturally establish citrus canker 
under even the most conducive conditions (10\5\ colony-forming units 
(cfu)/milliliter (ml) for intact tissue infection, 10\3\ cfu/ml for 
wounded) and that fruit disinfection easily achieves the low levels of 
inoculum necessary to avoid the risk of disease transmission. The 
commenter stated that the concern that inoculum in wounds on fruit 
could not be completely eliminated overlooks the fact that the bacteria 
do not even cause an infection at the wound site, let alone become 
liberated to possibly induce a lesion elsewhere.
    The November 2007 RMA and the supplemental RMA both acknowledge the 
fact that disinfection treatments are not completely effective against 
Xcc bacteria in lesions. However, as the November 2007 RMA stated, 
there is abundant evidence that shows that packinghouse disinfection 
treatments destroy surface bacteria and reduce the viability of all 
bacteria on fruit. We did not rely solely on the Gottwald et al. (2009) 
publication in making our determination that treatment with an APHIS-
approved disinfectant is an effective mitigation against the risk of 
spread of citrus canker; rather, we considered all the available 
evidence regarding the effectiveness of disinfectant treatments.
    In addition, other evidence indicates that bacteria that remain in 
lesions after disinfection are not epidemiologically significant. For 
example, Gottwald et al. (2009) provided additional evidence supporting 
the conclusion that the viability of bacteria on fruit and in lesions 
and wounds diminishes after the fruit is harvested and that the 
viability of Xcc bacteria which survive the packing process will 
further diminish during shipping.
    We disagree with the first commenter that the effectiveness of 
disinfectant treatment on bacteria in wounds is a concern. The second 
commenter is correct to note that Xcc bacteria in wounds do not cause 
infections at the wound site. As discussed in the supplemental RMA, 
evidence indicates that wounds on harvested fruit containing Xcc 
inoculum do not lead to citrus canker lesion development, and Xcc 
populations generally decline, although wounds might occasionally 
retain Xcc populations that decline more slowly.
    Finally, with respect to the first commenter's concern about 
elimination of bacteria, we acknowledge that the surface disinfectant 
treatments approved by APHIS reduce numbers of Xcc cells to low or 
undetectable levels, but do not necessarily provide complete 
eradication. As the second commenter notes, complete eradication would 
be impractical. In any case, it is not necessary to completely 
eradicate Xcc in order to ensure that disinfected fruit is not an 
epidemiologically significant pathway. While the updated PRA and 
supplemental RMA conclude specifically that commercially packed and 
disinfected fresh citrus fruit is not an epidemiologically significant 
pathway for the introduction and spread of Xcc, it is not just the 
disinfection process that makes fruit not an epidemiologically 
significant pathway for Xcc, but also the biology of Xcc and the 
conditions that must be fulfilled in order for Xcc transmission from 
infected fruit to a host plant to occur, among other factors.
    Some commenters addressed experiments in the Gottwald et al. (2009) 
publication that were designed to investigate the likelihood that 
citrus fruit disposed of by consumers may serve as a source of inoculum 
for nearby host material. Gottwald et al. (2009) studied the 
transmission of Xcc from unprocessed, infected `Ruby Red' grapefruit 
and `Lisbon' lemon and packinghouse-processed `Ruby Red' grapefruit in 
cull piles to `Duncan' grapefruit seedlings during natural weather 
events. During the course of the experiments, citrus canker lesions did 
not develop on the grapefruit seedlings (488 seedlings total) 
surrounding the diseased fruit, in spite of extensive leafminer damage 
present on some of the seedlings. Xcc bacteria were not detected in 
assays of the foliage.
    Gottwald et al. (2009) repeated the cull pile experiment to see if 
transmission of Xcc from infected, unprocessed `Ruby Red' grapefruit 
fruit is possible under simulated extreme wind and rain conditions. 
Infected fruit were either placed in a cull pile or suspended by 
vertical strings. One seedling 0 meters (m) downwind from the cull pile 
became infected when subjected to the highest wind speed (25 m per 
second (m/s)) and simulated rain, developing 1 lesion on a single leaf 
injured by the action of the high-speed fan. The other 191 plants in 
the study did not develop Xcc lesions. No Xcc lesions developed on the 
192 plants placed at the same distance and subjected to the same wind 
speed (0, 10, and 25 m/s with water) from Xcc-infected grapefruit 
suspended from string. Xcc was recovered from 1 collection screen set 
up 2 m from suspended fruit, but no Xcc was recovered from the other 
144 collection screens set up at various distances (0 to 10 m) from 
cull piles or suspended fruit. Gottwald et al. (2009) stated that this 
cull pile experiment was ``a highly contrived situation designed to 
provide every possible opportunity for dispersal of Xcc and would be 
unlikely to occur in most areas, except those locations where 
hurricanes or tropical storms are common occurrences.''
    One commenter noted that one plant surrounding infected fruit in 
cull piles did develop the disease in one of the simulated wind and 
rain experiments, indicating that this pathway of transmission is 
possible. The commenter stated that one might think that this level of 
transmission from an infected fruit to a healthy plant is very low, but 
this can be interpreted as very high under the set of conditions 
established for the experiments. The commenter stated that conducting 
these studies in regions where other environmental conditions exist and 
with a different group of scientists may lead to a different 
conclusion.
    A second commenter stated that both Gottwald et al. (2009) and 
Shiotani et al. (2009) demonstrate that transmission of the bacterium 
is a difficult process to replicate and expressed a view that the 
natural spread of the bacterium from infected fruit to host plants 
remains poorly understood. The commenter stated that the cull pile 
transmission experiments conducted by Gottwald et al. (2009) do not 
provide conclusive

[[Page 54436]]

evidence that the risk of fruit-to-tree transmission is insignificant. 
The commenter stated that these trials were conducted with little 
replication and did not adequately represent weather events that are 
conducive to the transmission of the bacterium, that the authors did 
not demonstrate that Xcc could initiate infections under the 
experimental conditions in positive controls, and that the employed 
diagnostic methods were not tested in positive controls.
    This commenter also noted that transmission of Xcc from infected 
fruit to host plants did occur, despite each wind speed treatment being 
applied for only 5 minutes. While APHIS concluded that the experimental 
conditions that produced this result were ``highly contrived,'' the 
commenter stated, due to the small-scale nature of this trial, small 
sample sizes, short exposure times, and lack of adequate controls, the 
risk of transmission under natural conditions remains feasible and 
significant. The commenter concluded that the experiments by Gottwald 
et al. (2009) demonstrated the ability of Xcc to be spread from 
symptomatic citrus fruit.
    A third commenter stated that the transmission of Xcc from infected 
fruit to host plants in the simulated extreme wind and rain conditions 
was probably because of mechanical contact and injury, not from 
anything most people would consider as a natural transmission event. 
This commenter also noted that the cull pile in that experiment was 
composed of freshly picked and heavily infected fruit, not fruit that 
had been graded and disinfected according to packinghouse protocol. The 
commenter stated that the value of this experiment is that it 
demonstrates the ``tipping point'' for canker infection from fruit. The 
commenter stated that if the other commenters envision a pile of 
freshly picked canker-infected grapefruit suddenly arriving in a 
grapefruit orchard in Australia, Arizona, or California immediately 
adjacent to susceptible plants and experiencing 25 m/s winds 
accompanied by rain, the scenario is excessively imaginary. The 
``tipping point,'' in this commenter's view, identifies the dangerous 
conditions for shipping fresh fruit from a canker endemic area so they 
can be completely avoided.
    We agree with the first two commenters that it would have been 
optimal to have additional replications of the experiment in which Xcc 
was transmitted from infected fruit to host plants, to better determine 
the rate at which transmission occurs in these conditions. However, as 
noted, the conditions in the experiment in which Xcc was successfully 
transmitted from infected fruit to host plants were extreme conditions, 
designed (as the third commenter states) to establish whether 
transmission of Xcc from infected fruit to host plants is possible, not 
whether it is likely. (As the third commenter notes, Gottwald et al. 
(2009) concluded that the lesion that resulted from the simulated wind 
and rain cull pile experiment ``was the result of a leaf wound.'')
    In the context of the other experiments Gottwald et al. (2009) 
performed to assess the likelihood of fruit-to-plant transmission, and 
in the context of the conditions of the experiment, including not only 
the simulated extreme wind and rain conditions but also the fact that 
the fruit were unprocessed and untreated and the placement of those 
fruit directly adjacent to host plants, we have determined that this 
one successful transmission is consistent with a determination that 
commercially packed and disinfected fresh citrus fruit is not an 
epidemiologically significant pathway for the introduction and spread 
of Xcc, given all the available evidence about the potential for fruit 
to serve as a pathway.
    Although the first commenter is correct that conducting the 
experiments in other environmental conditions and with another group of 
scientists might lead to a different conclusion, based on the available 
science regarding the transmission of citrus canker, the environmental 
conditions under which these experiments were conducted are extremely 
suitable to the potential transmission of citrus canker. Fruit that 
were specifically selected for their high level of infection and that 
were subjected to none of the packinghouse processes (including 
disinfection) that are known to reduce the viability of Xcc infection 
were used in attempts to infect highly susceptible grapefruit plants at 
the most susceptible stage of the plants'development. The one trap 
plant that was infected was placed immediately adjacent to the infected 
fruit and subjected to simulated extreme wind and rain conditions that 
are unlikely to occur in most areas. We have determined that it is 
unlikely that studies in other regions and under other environmental 
conditions would produce a greater level of transmission of the disease 
from infected fruit to host plants.
    We have determined that the Gottwald et al. (2009) experiments 
adequately represented weather events that are conducive to the 
transmission of Xcc and represented a range of weather conditions as 
well. The trials were conducted both in field conditions that were not 
conducive to the transmission of Xcc, in Argentina, and that were 
conducive, in Florida.
    It would be difficult to develop a positive control for the cull 
pile experiments, as a positive control would require the successful 
transmission of Xcc, which Gottwald et al. (2009) were only able to 
accomplish under conditions described in the publication as ``highly 
contrived.'' (It should be noted that this was not APHIS' description.) 
Nevertheless, it should be noted that the authors who performed the 
cull pile experiments have performed similar experiments using yard 
blowers, as documented in Bock et al. (2005) and Parker et al. (2005). 
These publications demonstrated that using a forced air source for wind 
and hose water for rain will elicit and spread Xcc from infected 
plants. In one experiment in Bock et al. (2005), the blower was run for 
5 minutes, the same duration as in the 25-m/s artificial wind and rain 
cull pile experiment, and bacteria were recovered from the water to 
which the infected plants were exposed. Different experiments in both 
papers using different durations produced the same results. We would 
presume that using similar techniques to elicit and spread Xcc from 
infected fruit would be effective, if fruit was an epidemiologically 
significant pathway.
    The commenter correctly notes that the Gottwald et al. (2009) 
publication did not describe any positive controls for the immunostrips 
used in the cull pile experiments to determine whether Xcc was present. 
However, a personal communication with one of the authors of that 
publication indicates that the experimenters did use positive controls 
to confirm that the immunostrips were working properly and thus would 
have indicated that Xcc was present if it had been present.
    We disagree with the second commenter that the exposure times in 
the cull pile experiments in Gottwald et al. (2009) were ``short.'' The 
5-minute exposure time in the 25-m/s artificial wind and rain 
experiment was sufficient to infect 1 test plant. The commenter also 
ignores the field cull pile experiments, which each took place for 
several weeks, at different times of year.
    Finally, it is important to note that our determination that 
commercially packed and disinfected fresh citrus fruit is not an 
epidemiologically significant pathway for the introduction and spread 
of Xcc does not rest solely upon the Gottwald et al. (2009) cull pile 
experiments, although they do provide

[[Page 54437]]

valuable evidence supporting that determination. Rather, that 
determination takes into account all the evidence considered in the 
November 2007 RMA, the updated PRA, and the supplemental RMA, including 
evidence about the biology of the disease, the effectiveness of 
disinfectant treatment, the conditions that must be fulfilled for 
disease transmission to occur, and the fact that the movement of 
commercial citrus fruit has not been associated with an outbreak of the 
disease anywhere in the world.

Shiotani et al. (2009)

    We also received several comments specifically addressing Shiotani 
et al. (2009).
    One commenter stated that, in Shiotani et al. (2009), proper 
positive controls proving that the polymerase chain reaction (PCR) 
detection technique is working were not included in one set of 
experiments. (We believe the commenter is referring to the examination 
of fruit collected from a diseased commercial orchard to investigate 
the survival of Xcc.)The commenter stated that the lack of controls 
casts doubts on the results of this research.
    The commenter correctly notes that there is no explicit discussion 
of controls in the ``Materials and Methods'' section of the paper. This 
does not mean that the proper controls were not used, but we cannot 
verify that they were. That said, the fact that isolations and 
bioassays made from the same material also yielded negative results 
supports the PCR results.
    One commenter stated that the Shiotani et al. (2009) experiments 
used a laboratory strain of Xcc that has not been shown to be 
pathogenic but, the publication stated, ``is believed to be as robust 
as the wild-type.'' The commenter stated that this demonstrates 
critical flaws in the experimental design and that the conclusions of 
Shiotani et al. (2009) can thus not be accepted without reasonable 
doubts.
    The commenter quotes from the ``Discussion'' section of the 
Shiotani et al. (2009) publication. In the ``Materials and Methods'' 
section, the authors discuss the laboratory strain in more detail: ``A 
marked strain of X. citri pv. citri (KC21Rif100) that is resistant to 
rifampicin was used as inoculum. This strain is a stable, spontaneously 
derived mutant from strain KC21 (Shiotani et al., 2008), which has been 
shown to be as pathogenic as other strains of X. citri pv. citri in 
infection studies.'' We believe this information addresses the 
commenter's concern.
    The Shiotani et al. (2009) publication included experiments 
designed to assess the potential for spread of Xcc from mature Satsuma 
mandarin fruit inoculated with the marked strain of Xcc mentioned above 
and suspended in polypropylene net bags in navel orange trees. One 
commenter noted that, in one of the four experiments conducted, citrus 
canker was transmitted from culled mandarin fruit to leaves of navel 
orange trees in an orchard.
    Another commenter, responding to the first commenter, noted that 
the infections in that experiment were not caused by the marked strain 
of Xcc but by the wild type. Citrus canker is endemic in the area where 
this study was done, so a tagged strain was used. That way, the 
commenter stated, the researchers have an idea where the inoculum is 
coming from. The commenter stated that the fact that wild-type canker 
bacteria occasionally are caught in traps or cause infection on plants 
in the experiment does not undermine the conclusion in any way; in 
fact, it demonstrates that conditions conducive to the transmission of 
canker existed, and the marked strain on and in fruit did not 
demonstrate any risks of disease transmission.
    We agree with the second commenter.
    One commenter stated that the Shiotani et al. (2009) publication 
does not provide a high degree of confidence that transmission of Xcc 
from contaminated fruit to host plants is not epidemiologically 
significant. Although no transmission of Xcc was observed, the 
commenter suggested that it is possible that this was due to 
unexplained variables. Rainfall data were provided but no information 
was provided on the growth stage of trap plants, insect presence in the 
orchard, potential wounds and insect damage, spray history within the 
orchard, or other significant wind and weather events. Because the 
experiments were conducted in a commercial orchard, the commenter 
stated, it would be expected that pest and disease management would 
have been practiced at some point prior to the study.
    As noted earlier, the Shiotani et al. (2009) experiments used a 
marked strain of Xcc because Xcc is endemic in the area where the 
experiments took place. The wild-type strain of Xcc occurred in the 
orchard where the experiments took place, throughout the experiments. 
This indicates that at least some plants in the orchard were at a 
susceptible growth stage, and in general the transmission of Xcc 
between trees in the orchard indicates that whatever unexplained 
variables may have been present did not impede the normal transmission 
of Xcc.
    In Shiotani et al. (2009), the authors state, for the initial assay 
of fruit from diseased orchards, ``No chemicals had been sprayed to 
control the disease,'' addressing the commenter's concern about the 
previous employment of disease control methods. Disease control is not 
addressed directly for the other experiments, including the experiments 
regarding the potential spread of Xcc from Satsuma mandarin fruits. 
However, other statements in the publication imply that no disease 
control techniques were employed in the orchard:

 In September 2006, the Satsuma mandarin orchard in Saga was damaged by 
typhoon No. 0613. The typhoon brought rain with strong southerly winds 
with maximum speeds of 50 m/s to the orchard, which is located on a 
south-facing hillside. The severe meteorological conditions of this 
typhoon strongly facilitated spread of citrus canker, leading to the 
highest incidence of the disease in the orchard in the last decade. ... 
It is most likely that small populations of the wild strain of X. citri 
pv. citri survived in the orchard. Citrus canker infection caused by 
the wild strain indicated that conditions were also conducive for the 
establishment and spread of the introduced KC21Rif100 strain. The 
KC21Rif100 strain did not exude from lesions on Satsuma mandarin fruits 
after they were discarded in an orchard in October 2006, although 
conditions were conducive for the spread of X. citri pv. citri.

    If disease control techniques had been employed in the orchard, we 
assume that the authors would not have described the conditions as 
conducive for the spread of Xcc.
    These statements also indicate that information on significant wind 
and water events was provided, specifically with regard to typhoon No. 
0613.
    Shiotani et al. (2009) did not provide any information on insect 
presence or pest control in the orchard. The citrus leafminer is known 
to occur in Japan, but we do not know whether it occurs in the orchard. 
However, it is important to note that insects themselves are not known 
to be vectors for Xcc; the presence of the citrus leafminer or another 
insect in the orchard might increase the severity of canker in the 
orchard, but it would not enable transmission of Xcc from infected 
fruit to host plants.
    The commenter stated it is likely that naturally infected tissues 
have a higher

[[Page 54438]]

ability to transmit the bacterium than artificially surface-inoculated 
fruit, which were used in Shiotani et al. (2009).
    Shiotani et al. (2009) determined that the bacteria in the lesions 
that resulted from the artificial inoculation were viable. We know of 
no evidence that suggests that bacteria in natural lesions are more 
effective than surface-inoculated bacteria in spreading Xcc, and the 
commenter did not supply any.
    The commenter stated that another limitation of the design of this 
experiment is that it did not include a control group to demonstrate 
tree-to-tree transmission under a similar set of conditions.
    Tree-to-tree transmission was demonstrated through the incidence of 
the wild-type strain of Xcc, which the publication discussed. In this 
case, the wild-type strain acted as a control to show that transmission 
of Xcc within the orchard was possible and did occur.
    The commenter also stated that the uncertainties cited by the 
commenter are acknowledged by the authors, who suggested that 
conditions may have been unfavorable for spread of the bacterium.
    The statement in Shiotani et al. (2009) that conditions may have 
been unfavorable for disease spread referred to one replication of the 
experiment. The publication goes on to note that disease spread 
occurred at high levels in a subsequent replication:

 In the experiments started in November 2005 and March 2006, no canker 
symptoms were observed on any branches beneath the discarded fruits. 
This may be because weather conditions were unfavourable for disease 
spread during this period. During the experiment started on May 2006, 
canker lesions were observed on leaves of navel oranges located beneath 
the discarded Satsuma mandarin fruits. [hellip]The severity of the 
disease was greater in 2006 than in 2005. The incidence of citrus 
canker in the orchard was 36.2 percent and severity was 18.0. The high 
incidence may be attributed to typhoon No. 0613 that occurred on 
September 17, 2006.

    In addition, it should be noted that our determination that 
commercially packed and disinfected fresh citrus fruit is not an 
epidemiologically significant pathway for the introduction and spread 
of Xcc does not rest solely on the experiments in Shiotani et al. 
(2009), although they do provide valuable evidence supporting that 
determination. Rather, that determination reflected our analysis of all 
the evidence considered in the November 2007 RMA, the updated PRA, and 
the supplemental RMA, as discussed earlier.
    Shiotani et al. (2009) also examined the survival of Xcc bacteria 
on the surface of artificially inoculated fruit that were retained for 
sampling. One commenter noted that viable Xcc was isolated from 3 
canker lesions from 2 out of 6 Satsuma mandarin fruit (a cultivar 
resistant to citrus canker), 3 months after inoculation. Given these 
results, the commenter concluded that symptomatic citrus fruit (treated 
or untreated) remain a potential source of inoculum.
    We agree with the commenter that some viable bacteria may remain in 
lesions of infected fruit. However, in those fruits, the strain 
KC21Rif100 was found in only 3 of 14 lesions andat a bacterial 
population lower than 3 x 10\3\ cfu per lesion. This is consistent with 
one of the findings of the November 2007 RMA and the supplemental RMA, 
which is that the viability of bacteria on fruit and in lesions and 
wounds diminishes after the fruit is harvested. Diminishing bacterial 
populations are less likely to provide adequate inoculum to incite 
infection.
    It should also be remembered that the fruit that were sampled and 
found to have viable bacteria had been stored in protected conditions. 
The fruit that were artificially inoculated and used in the experiment 
regarding the potential of spread of citrus canker did not serve as 
sources of citrus canker transmission, even when the lesions had just 
been formed and presumably contained high levels of inoculum. The rinds 
of the artificially inoculated fruits retrieved after 3 days in the 
orchard did not have any viable bacteria. Finally, as noted earlier in 
the discussion of Gottwald et al. (2009), other evidence indicates that 
bacteria that remain on the fruit in lesions and wounds after 
disinfection are not epidemiologically significant.
    The commenter is correct to note that Satsuma mandarin is a 
resistant variety of citrus. As noted in the supplemental RMA, the 
Gottwald et al. (2009) and Shiotani et al. (2009) publications used 
citrus cultivars that represented the extremes of susceptibility from 
highly susceptible (grapefruit) to less susceptible varieties (lemon, 
mandarins). APHIS assumes cultivars not specifically studied would fall 
within this range of susceptibility and the results are therefore 
applicable to all citrus cultivars. In any case, the supplemental RMA 
and November 2007 RMA consider many different sources of evidence in 
making the determination that the viability of bacteria on fruit and in 
lesions and wounds diminishes after the fruit is harvested, not just 
the Shiotani et al. (2009) publication.
    One commenter noted that the authors of Shiotani et al. (2009) 
state: ``It is possible that bacterial cells of KC21Rif100 strain could 
not grow and colonize the surface of the contaminated fruits due to 
lack of nutrients.'' The commenter stated that, considering that at 
least a small percentage of fruit is always decaying during shipment 
and marketing, this decayed fruit can contaminate other fruit with 
nutrients that will make survival of the bacteria more likely.
    The commenter provided no evidence suggesting that this would 
occur, and we are aware of none. The available evidence suggests that 
rotting fruit would not provide nutrients that would make survival of 
Xcc bacteria more likely. For example, Fulton and Bowman (1929) 
demonstrated that canker does not survive on rotting fruit. In 
addition, decaying fruit would be decaying due to the presence of other 
organisms, and Xcc does not compete well with other organisms, as 
described in Fulton and Bowman (1929) and Leite (1990).
    One commenter stated that, at the end of the Shiotani et al. (2009) 
publication, the authors indicate that navel oranges are more 
susceptible to canker than mandarins. The commenter stated that this 
indicates that their pathogen survival studies on mandarins will not 
reflect the true risk of transmission of the pathogen/disease. Two 
other commenters echoed this concern and stated that, because 
California's growing situation is quite different than those in the 
research areas, there are serious issues about the extrapolation of 
data from study of only a few varieties. Another commenter, approaching 
this issue differently, suggested that restrictions on the interstate 
movement of different varieties of citrus fruit could vary based on the 
variety's resistance to citrus canker.
    The Shiotani et al. (2009) publication does not actually state that 
Satsuma mandarins are more resistant to Xcc than navel oranges, 
although this is widely acknowledged to be true. In any case, as noted 
earlier, the Gottwald et al. (2009) and Shiotani et al. (2009) 
publications used citrus cultivars that represented the extremes of 
susceptibility from highly susceptible (grapefruit) to less susceptible 
varieties (lemon, mandarins). APHIS assumes cultivars not specifically 
studied would fall within this range of susceptibility and the results 
are therefore applicable to all citrus cultivars. The commenters did 
not provide any specific reasons to question this assumption.

[[Page 54439]]

    In general, although we recognize that there are limitations in 
extrapolating from results achieved with Satsuma mandarins, the 
Shiotani et al. (2009) provides valuable evidence supporting our 
determination that commercially packed and disinfected fresh citrus 
fruit is not an epidemiologically significant pathway for the 
introduction and spread of Xcc. We took this evidence into account 
along with the Gottwald et al. (2009) publication and the other 
evidence cited in the November 2007 RMA and the supplemental RMA in 
making this determination.

Other Issues in the Updated PRA and Supplemental RMA

    One of the conclusions in the updated PRA is that standard 
packinghouse procedures and post-harvest treatments will remove and/or 
devitalize epiphytic populations of Xcc. This conclusion is echoed in 
the supplemental RMA.
    One commenter stated that the conclusion in the updated PRA that 
Xcc has a low survival potential is in contrast to earlier research by 
Golmohammadi et al. (2007), who reported that Xcc was frequently 
detected on fruit with canker-like symptoms in commercial consignments 
of citrus from Uruguay and Argentina into Spain. These consignments 
were accompanied by phytosanitary certification stating that fruit had 
been treated with postharvest bactericides, including chlorine and 
sodium orthophenylphenate. The presence of Xcc on these samples was 
confirmed by molecular and pathogenicity testing. Pathogenicity assays 
on grapefruit leaves confirmed that Xcc cells remained viable and were 
able to produce symptoms despite the application of postharvest 
treatments and low temperature storage.
    Both the updated PRA and the supplemental RMA addressed 
Golmohammadi et al. (2007). The updated PRA and supplemental RMA state 
that the results in Golmohammadi et al. (2007) indicate that 
disinfection protocols are not 100 percent effective. Some samples were 
only positive by PCR protocols. The authors concluded this was probably 
due to the disinfection treatments, which would reduce bacterial 
populations, and may induce the noncultivable state in the analyzed 
lesions. They further suggested that the bacterial cells in the lesions 
could be stressed after the fruit treatments (washing, disinfection, 
chemical treatments, transport, and storage at low temperatures for 
variable periods of time). Pathogenicity tests were successfully 
conducted only by artificial laboratory inoculations; the 
epidemiological significance of these results was not evaluated.
    Pathogenicity tests of bacteria in the laboratory do not indicate 
whether the bacteria would actually be able to infect host plants in a 
field setting, where conditions are likely to be less favorable than in 
a laboratory. The fact that Golmohammadi et al. (2007) concluded that 
bacterial cells in the lesions could be stressed after the fruit 
treatments suggests that the bacteria would not have been able to do 
so, particularly given the results of the experiments Gottwald et al. 
(2009) and Shiotani et al. (2009) conducted that addressed the 
transmission of Xcc from infected fruit to host plants in the field. 
Since Gottwald et al. (2009) and Shiotani et al. (2009) both used 
untreated fruit in their experiments, and Golmohammadi et al. (2007) 
concluded that packinghouse processing and disinfection treatment 
further reduce the viability of the bacteria, we have determined that 
the results of Golmohammadi et al. (2007) are consistent with the 
determination that commercially packed and disinfected fresh citrus 
fruit is not an epidemiologically significant pathway for the 
introduction and spread of Xcc.
    One commenter, specifically noting the detections of Xcc on fruit 
with canker-like symptoms in commercial consignments of citrus from 
Uruguay and Argentina into Spain, stated that standard harvesting and 
packinghouse procedures may not effectively eliminate infected fruit 
from the export pathway.
    Both the November 2007 RMA and the supplemental RMA acknowledge 
this. However, these procedures do reduce the prevalence of viable Xcc 
in commercial consignments of fruit, thus bolstering the conclusion 
that commercially packed and disinfected fresh citrus fruit is not an 
epidemiologically significant pa