# Citrus Canker; Movement of Fruit From Quarantined Areas

> Briefs, arguments, decisions, and more.

URL: https://www.frixlaw.com/law-library/documents/fr%3AE7-22549

## Record

- **Collection:** Federal Register
- **Document type:** Rule
- **Published:** November 19, 2007
- **Citation:** 72 FR 65172

## Text

DEPARTMENT OF AGRICULTURE
Animal and Plant Health Inspection Service
7 CFR Parts 301 and 305
[Docket No. APHIS-2007-0022]
RIN 0579-AC34
Citrus Canker; Movement of Fruit From Quarantined Areas

AGENCY:

Animal and Plant Health Inspection Service, USDA.

ACTION:

Final rule.

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 the groves in which the fruit is produced be inspected and found free of citrus canker, and instead are requiring that every lot of fruit produced in the quarantined area be inspected by the Animal and Plant Health Inspection Service at a packinghouse operating under a compliance agreement and found to be free of visible symptoms of citrus canker. We are retaining 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. These changes will relieve some restrictions on the interstate movement of fresh citrus fruit from Florida while maintaining conditions that will help prevent the artificial spread of citrus canker.

DATES:

Effective Date:
November 19, 2007.

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 axonopodis
pv.
citri
(referred to below as
Xac
) 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 aggressive 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 §§ 301.75-1 through 301.75-14 of “Subpart—Citrus Canker” (7 CFR 301.75-1 through 301.75-17, 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. These regulations are promulgated pursuant to the Plant Protection Act (7 U.S.C. 7701
et seq.
).

On June 21, 2007, we published in the
Federal Register
(72 FR 34180-34191, Docket No. APHIS-2007-0022) a proposal
1

to amend the citrus canker regulations by modifying the conditions under which fruit may be moved interstate from quarantined areas. We proposed to eliminate the requirement that the groves in which the fruit is produced be inspected and found free of citrus canker, and instead proposed to require that every lot of fruit produced in the quarantined area be inspected by the Animal and Plant Health Inspection Service (APHIS) at a packinghouse operating under a compliance agreement and found to be free of visible symptoms of citrus canker. We proposed to retain 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.

1
To view the proposed rule, the supporting analyses, and the comments we received, go to
http://www.regulations.gov/fdmspublic/component/main?main=DocketDetail&d=APHIS-2007-0022
.

We solicited comments concerning our proposal for 30 days ending July 23, 2007. We subsequently reopened and extended the deadline for comments until August 7, 2007, in a document published in the
Federal Register
on July 27, 2007 (Docket No. APHIS-2007-0022, 72 FR 41239). We received 72 comments by the close of the comment period. They were from producers, exporters, researchers, and representatives of State governments. They are discussed below by topic.

Pest Risk Assessment and Risk Management Analysis

To inform the deliberations that led to the proposed rule, we prepared two documents that addressed the risk associated with the interstate movement of citrus fruit from a quarantined area: A pest risk assessment (PRA) and a risk management analysis (RMA). The PRA, which was titled “Evaluation of asymptomatic citrus fruit (
Citrus
spp.) as a pathway for the introduction of citrus canker disease (
Xanthomonas axonopodis pv.

citri
),” considered all available evidence associated with asymptomatic citrus fruit as a pathway for the introduction of citrus canker. The PRA concluded that asymptomatic, commercially produced citrus fruit treated with a surface disinfectant and subject to other mitigations is not epidemiologically significant
2

as a pathway for the introduction and spread of citrus canker. We first made this document available for comment on April 6, 2006, when we published a notice in the
Federal Register
(71 FR 17434-17435, Docket No. APHIS-2006-0045), announcing its availability for comment for 60 days; the comment period was subsequently extended to 90 days. We also submitted it for peer review in accordance with the U.S. Department of Agriculture (USDA) guidelines for peer review developed in response to the Office of Management and Budget's peer review bulletin. We received 19 comments by the end of the comment period, which we also submitted to the peer review panel members for their consideration.
3

We carefully considered the comments of the public and peer reviewers, and made revisions to the analysis based on concerns they raised. The revisions did not change the conclusions of the PRA; the revised version of the PRA was provided with the proposed rule.

2
We use the term “epidemiologically significant” to refer to minimum conditions required for disease transmission.

3
The original PRA and the comments we received on it can be viewed at
http://www.regulations.gov/fdmspublic/component/main?main=DocketDetail&d=APHIS-2006-0045
.

In light of the comments by the public and peer reviewers, it became clear that additional analysis was necessary to apply the conclusions of the PRA to the situation in Florida. In order to apply the conclusions of the PRA, we needed to extend its application to evaluate methods by which fruit
4

could be produced, treated, inspected, packaged, and shipped without resulting in the

spread of citrus canker to commercial citrus-producing areas. (Commercial citrus-producing areas are listed in § 301.75-5 of the regulations and are referred to in this document as commercial citrus-producing States. Those States, listed in § 301.75-5(a), are: American Samoa, Arizona, California, Florida, Guam, Hawaii, Louisiana, Northern Mariana Islands, Puerto Rico, Texas, and the U.S. Virgin Islands.)

4
Given the practical difficulties in ensuring that only asymptomatic fruit enters interstate commerce under any regulatory strategy, we refer here to host fruit in general.

To address the considerations described above, APHIS prepared the RMA, which was titled “Movement of commercially packed fresh citrus fruit (
Citrus
spp.) from citrus canker (
Xanthomonas axonopodis
pv.
citri
) disease quarantine areas, March 2007.” We made the RMA available for comment along with the proposed rule.
5

The RMA was also submitted for peer review, which occurred concurrently with the public comment period for the proposed rule.
6

The RMA analyzed the potential of fresh commercially packed citrus fruit and associated packing material to serve as a pathway for the introduction and spread of citrus canker into new areas. It also identified and evaluated options for regulating the interstate movement of citrus fruit from quarantined areas with the goal of reducing the potential for citrus canker introduction and spread. The recommendations in the RMA served as the basis for the proposed rule.

5
The RMA is available on the Regulations.gov Web site and in our reading room (see
ADDRESSES
above) and may be obtained from the person listed under
FOR FURTHER INFORMATION CONTACT
.

6
The peer review materials for the RMA may be viewed at
http://www.aphis.usda.gov/peer_review/peer_review_agenda.shtml
.

To develop the RMA, we reviewed available evidence regarding the biology and epidemiology of
Xac
and the management of citrus canker disease. The RMA concluded that the introduction and spread of
Xac
into other commercial citrus-producing States through the movement of commercially packed fresh citrus fruit from quarantined areas is unlikely because:

• Fresh citrus fruit is produced and harvested using techniques that reduce the prevalence of
Xac
-infected fruit;

• Citrus fruit is commercially packed using techniques that reduce the prevalence of infected or contaminated fruit, including disinfectant treatment for epiphytic contamination;

• For a successful
Xac
infection that results in disease outbreaks to occur, an unlikely sequence of events would have to occur;

• Reports of citrus canker disease outbreaks linked to fresh fruit are absent; and

• Large quantities of fresh citrus fruit shipped from regions with
Xac
have not resulted in any known outbreaks of citrus canker disease.

Nevertheless, the RMA concluded that the evidence is not currently sufficient to support a determination that fresh citrus fruit produced in a
Xac
-infested grove cannot serve as a pathway for the introduction of
Xac
into new areas. Therefore, the RMA evaluated several packinghouse-centered risk management options for the interstate movement of fresh commercially packed citrus fruit from regions infested with citrus canker to regions without the disease. These packinghouse-centered risk management options were evaluated to determine whether they provide an appropriate level of phytosanitary protection without the resource constraints and other practical considerations that make it difficult to maintain the grove-centered regulatory approach in Florida. The risk management options evaluated were:

•
Option 1:
Allow unrestricted distribution of all types and varieties of commercially packed citrus fruit to all U.S. States.

•
Option 2:
Allow distribution of all types and varieties of commercially packed citrus fruit to all U.S. States, subject to packinghouse treatment with APHIS-approved disinfectant and APHIS inspection of finished fruit that has completed the packinghouse culling, washing, disinfection, and grading processes.

•
Option 3:
Allow distribution of all types and varieties of commercially packed citrus fruit (except tangerines) in U.S. States except commercial citrus-producing States. Allow distribution of commercially packed tangerines to all U.S. States, including commercial citrus-producing States. Require packinghouse treatment of all such citrus fruit with APHIS-approved disinfectant and APHIS inspection of finished fruit (all types and varieties) for citrus canker disease symptoms.

•
Option 4:
Allow distribution of all types and varieties of commercially packed citrus fruit in U.S. States except commercial citrus-producing States and require packinghouse treatment of citrus fruit with APHIS-approved disinfectant and APHIS inspection of finished fruit (all types and varieties) for citrus canker disease symptoms.

•
Option 5:
Leave the current regulations for the interstate movement of citrus fruit from citrus canker quarantined areas in place and unchanged.

We proposed to implement Option 4. This option would have limited distribution of all types and varieties of citrus fruit to States other than commercial citrus-producing States, with mitigations conducted at packinghouses operating under compliance agreements. Those mitigations are the use of an approved disinfectant for all fruit and APHIS phytosanitary inspection.

We received several comments on the overall level of risk associated with the movement of commercially packed citrus from a citrus canker quarantined area, as well as our selection of Option 4. These comments have not led us to change our determination that Option 4 is the most appropriate option to implement. The RMA that we are making available with this final rule contains revisions based on the comments we received on the proposed rule and the comments we received through the peer review process, but its overall conclusion is the same. Accordingly, this final rule implements Option 4. (We are making some changes to the regulatory requirements associated with the implementation of Option 4. These changes are discussed later in this document.)

Some commenters believed that the evidence presented in the RMA warranted the selection of Option 2, which would have allowed the distribution of citrus fruit to all States, subject to packinghouse treatment with APHIS-approved disinfectant and APHIS inspection of finished fruit. These commenters stated that it was extremely unlikely that the circumstances necessary for the movement of commercially packed fresh citrus fruit to result in the introduction and spread of
Xac
into other commercial citrus-producing States would ever occur.

One commenter stated that the decision to allow the movement of regulated fruit from a citrus canker quarantined area only into States other than commercial citrus-producing States, rather than into all States, was based on politics rather than on science.

One commenter stated that no Florida citrus fruit infected with citrus canker has ever been found in a commercial citrus-producing State under the current regulations and that, at the commenter's packinghouse, not a single piece of fruit with citrus canker had been found by any inspectors or employees during the last growing season.

One commenter noted more generally that citrus canker has not been found outside Florida since the disease was first detected there, and stated that more certainty than uncertainty exists regarding the risk of commercially

packed citrus fruit as a viable pathway for citrus canker.

Another commenter noted that the PRA stated the following in its executive summary: “The combination of conditions necessary for introduction are so difficult to achieve that the likelihood of such occurrence is greater than the baseline exposure represented by unregulated pathways. The conclusions of the evaluation are reinforced by a strong record of empirical data from experience and interceptions.”

We acknowledge the efforts of the Florida citrus industry to put safeguards in place against citrus canker infestation. The proposed rule recognized the effectiveness of those safeguards by providing for the interstate movement to States other than commercial citrus-producing States of any lot of citrus fruit that is commercially packed, treated with APHIS-approved disinfectant, and inspected by APHIS and found to be free of visible canker lesions.

The RMA concludes that commercially packed fresh citrus fruit is an unlikely pathway for the introduction and spread of
Xac
and that a phytosanitary inspection ensures, with high confidence, that few shipped fruit would have symptoms of citrus canker disease. However, the model in Appendix 1 to the RMA indicates the potential for some commercially packed fruit with visible canker lesions to be shipped to commercial citrus-producing States. That potential for such fruit to reach commercial citrus-producing States, coupled with the aforementioned uncertainty regarding fruit as a pathway, led to the determination that the additional mitigation of prohibiting distribution to commercial citrus-producing States was required. 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 pathway for the introduction and spread of citrus canker, we would undertake rulemaking to amend our regulations accordingly.

Under section 412(a) of the Plant Protection Act (7 U.S.C. 7712(a)), the Secretary of Agriculture may prohibit or restrict the movement in interstate commerce of any plant or plant product if the Secretary determines that the prohibition or restriction is necessary to prevent the dissemination of a plant pest or noxious weed within the United States. Based on information provided in the PRA and RMA, we have determined that it is not necessary to prohibit the interstate movement of citrus fruit from a quarantined area into States other than commercial citrus-producing States under the conditions described in the proposed rule. While APHIS has concluded that commercially packed citrus fruit is an unlikely pathway for the introduction and spread of citrus canker, the remaining uncertainty about the level of risk associated with the movement of citrus fruit from a quarantined area has led us to maintain the prohibition on the movement of citrus fruit into commercial citrus-producing States.

One commenter supplied a report that provided initial data demonstrating that transmission of
Xac
from infected fruit placed directly under highly susceptible grapefruit seedlings does not occur.

The research (which can be viewed at
http://www.regulations.gov/fdmspublic/component/main?main=DocumentDetail&d=APHIS-2007-0022-0053
) is suggestive; when it is completed, it will help better determine whether citrus fruit can serve as a pathway for the introduction of citrus canker to commercial citrus-producing States outside the quarantined area. We encourage interested parties to make research on this issue available to us.

Two commenters stated that APHIS' treatment of the risk associated with citrus canker was inconsistent with its treatment of the risk associated with other plant pests. For example, one of the commenters stated, the evidence is clear that the interstate movement of nursery stock is a pathway for the long-distance spread of
P. ramorum
, but APHIS' regulations continue to allow high-risk nursery stock to move to all States, under specified conditions. The commenter cited APHIS' actions with respect to the light brown apple moth as another example.

The provisions governing the movement of regulated articles for each pest for which APHIS maintains quarantine requirements are the result of separate considerations of the available science and the risk posed by the plant pest in question. We make our determinations of risk based on, among other things, the likelihood that a pest will follow a specific pathway, the economic and environmental value of resources that could be damaged by the pest, and the likelihood of introduction of the pest into an unaffected area. Our choice of regulatory approach is based on, among other things, the likelihood that the mitigations available to us will be sufficient to prevent the introduction or spread of a plant pest. We have determined that the level of protection against the interstate spread of citrus canker that will be provided by the regulations as amended by this final rule is appropriate.

One commenter asked why APHIS allows fruit to be exported from the quarantined area into the citrus-producing areas of Europe, given that we proposed to prohibit the distribution of fruit from quarantined areas into commercial citrus-producing States. Other commenters asked that we allow the interstate movement of fruit from quarantined areas into commercial citrus-producing States under conditions similar to those required by the European Union (EU) for the importation of citrus fruit into the EU.

APHIS certifies U.S. plant products for export according to the conditions set by the importing country for the exportation of those products from the United States. The EU's requirements for the importation of citrus fruit apply to all areas where citrus canker is present, not just in the United States but in other countries whose citrus production areas are affected by citrus canker.

The EU import requirements involve certification of grove freedom from citrus canker and are similar to, but less restrictive than, the requirements that were in the regulations before the publication of this final rule. For reasons discussed in the RMA, we do not consider these requirements to be sufficient to allow the movement of fruit from citrus canker quarantined areas into commercial citrus-producing States at this time. We will continue to review the available science and will update the regulations if necessary.

Two commenters stated that Option 3, which would have allowed the unlimited distribution of tangerines subject to treatment and APHIS inspection, should be implemented. One commenter stated that canker finds have been few and far between, if the disease has been found at all, on some varieties of tangerine. Another stated that mandarin varieties are the least susceptible to citrus canker, and that the commercial citrus-producing States of California and Texas are important markets for producers of this fruit.

Tangerines are generally grouped in the species
Citrus reticulata
and are widely regarded as less susceptible to citrus canker disease than other commercially grown
Citrus
species. But many of the “tangerine” varieties grown in Florida are hybrids of
C. reticulata
with other more susceptible
Citrus
species. Clearly, tangerines in Florida are not immune to citrus canker, as APHIS records indicate that, during the 2005-2006 growing season grove surveys,
Xac
was detected on 274 samples from tangerine, tangor, and tangelo groves. APHIS pest interception data indicate that between 1985 and

2006,
Xac
was intercepted 632 times on
C. reticulata fruit
. The level of susceptibility was expressed as a continuum across “tangerine” varieties rather than as a discrete immunity for all varieties. This creates a regulatory problem when an overlap occurs in the level of susceptibility expressed by, for example, a more susceptible tangerine variety and a more resistant nontangerine citrus variety. Sufficient evidence does not exist to exclude tangerines from regulations applicable to other Florida citrus varieties. We are making no changes to the proposed rule in response to these comments.

Several commenters supported Option 4 but asked APHIS to continue to examine the scientific evidence with a view toward allowing unlimited distribution of fruit moved interstate from areas quarantined for citrus canker at some future time.

We will continue to examine scientific evidence regarding whether commercially packed citrus fruit (both with and without visible canker lesions) is an epidemiologically significant pathway for the introduction and spread of citrus canker. If, in the future, evidence is developed to support a determination that commercially packed citrus fruit is not an epidemiologically significant pathway for the introduction and spread of citrus canker, we would undertake rulemaking to amend our regulations accordingly.

Some commenters proposed other options to allow the movement of fruit from quarantined areas. One commenter stated that fruit from groves that are free of citrus canker and that are 1,500 feet or farther from an affected grove should be allowed to move fruit to commercial citrus-producing States.

It has been our experience in the State of Florida that citrus canker can spread more than 1,500 feet in stormy conditions. We recognize that citrus canker-free areas may exist adjacent to infected areas, but implementing the commenter's suggestion would require grove certification programs similar to those in place prior to the publication of this final rule. We have determined that certification of fruit for interstate movement at the packinghouse level rather than at the grove level will ensure an appropriate level of phytosanitary security; would be more reliable and less easily circumvented than the preharvest grove survey required by Option 5; would be consistent with the risk associated with citrus canker and commercially packed fruit from Florida; and would be easier and potentially less costly to implement and enforce than a grove-centered system of mitigations.

Some commenters disagreed with our determination that prohibiting the distribution of citrus fruit from a quarantined area into commercial citrus-producing States would be an effective mitigation. Commenters holding this view stated that the illegal movement of citrus fruit harboring citrus canker from a quarantined area to a commercial citrus-producing State may be expected through current commercial channels; they cited the movement of Spanish clementines from Georgia to Florida through retailer distribution when such movement was prohibited as one example of the potential for incorrect distribution. Another commenter cited the discovery of Florida fruit in commercial citrus-producing States as a result of distribution mistakes.

These commenters also stated that the potential for the movement of Florida citrus by tourists and visitors from nearby States into commercial citrus-producing States should also be taken into account, and that excluding shipments to buffer States would reduce the risk that this movement poses to commercial citrus-producing States. One commenter stated that the history of citrus disease movement such as citrus canker and citrus greening into Florida shows the high risk of movement by plant or by fruit from other citrus-growing countries. In these cases the initial infections were in urban areas, but movement to production areas was undetected until an epidemic was finally observed.

One commenter also stated that we had not addressed mail-order shipment or gift-pack movement of citrus from Florida.

These commenters proposed that we limit the distribution of fruit from citrus canker quarantined areas to other States in addition to the commercial citrus-producing States, thus creating a “buffer zone” around the commercial citrus-producing States. The buffer zones proposed by the commenters varied:

• One commenter suggested that only States east of the Mississippi River should be eligible to receive fruit moved interstate from quarantined areas.

• Two commenters suggested that only States in the northern tier of the United States and east of the Mississippi River should be eligible to receive such fruit.

• Two others suggested a buffer zone of all the States surrounding the commercial citrus-producing States.

We do not agree that a buffer zone, such as these commenters suggest, is appropriate or necessary. Due to the geographic separation between Florida and other commercial citrus-producing States, citrus canker is not likely to spread through natural means (such as through storms) from Florida to a State that is not a commercial citrus-producing State and then to a commercial citrus-producing State. While it is correct that the movement of plants for planting presents a high risk of spreading citrus canker from a quarantined area, the regulations already contain a prohibition on the movement of plants for planting; currently, only calamondin and kumquat plants are allowed to move interstate from the quarantined area, and those plants must be produced under conditions designed to prevent their infection with citrus canker. As mentioned earlier, we have determined that it is unlikely that the movement of commercially packed citrus fruit is an epidemiologically significant pathway for the spread of citrus canker.

The proposed rule included requirements that boxes or other containers of fruit moving interstate from a quarantined area include a limited permit mark as well as the statement indicating that the fruit is not to be distributed into a commercial citrus-producing State. This requirement (which applies to mail-order and gift-pack shipments as well as truck shipments) will help to prevent inadvertent movement of citrus from quarantined areas into a commercial citrus-producing State. To strengthen the protection provided by the limited permit requirement, we are also adding a requirement in this final rule that the limited permit mark and the distribution statement appear on any shipping documents accompanying boxes or other containers in which fruit is moved interstate.

To ensure that regulated parties comply with distribution restrictions, APHIS routinely monitors wholesalers and fresh fruit markets in commercial citrus-producing States and monitors distribution routes that are bound for commercial citrus-producing States to ensure that Florida citrus fruit does not unlawfully enter those States. This monitoring is conducted primarily by APHIS' Smuggling, Interdiction, and Trade Compliance program.

If we find Florida citrus in a commercial citrus-producing State, we will trace the product back to its distributor and its origin in Florida. We will investigate violations (through APHIS' Investigative and Enforcement Services) and may seek penalties against any distributor that moves Florida citrus to commercial citrus-producing States. We may seize the prohibited products and destroy them or ensure they are moved from the area of concern. We

will conduct surveillance on other methods of sale such as Internet sales and gift-pack shipments to ensure that the fruit is not advertised as being available for delivery to commercial citrus-producing States. We will also provide outreach to retailers and wholesalers who are moving products to help prevent any inadvertent movement of citrus from a quarantined area into a commercial citrus-producing State.

The packinghouse measures of disinfection and APHIS inspection ensure that even if a given shipment were illegally moved to a commercial citrus-producing State, the shipment would have a low likelihood of containing fruit with the potential to cause an outbreak of citrus canker disease.

As mentioned earlier, the RMA examined four options for allowing the interstate movement of citrus fruit from a citrus canker quarantined area under a packinghouse-centered approach. Of those four options, we determined that Option 4 was most appropriate, based on the available scientific evidence, which indicates that fruit subject to commercial packing, treatment, and APHIS inspection will be unlikely to serve as a pathway for the introduction or spread of citrus canker.

We recognize that individual consumers may move fruit from Florida into States other than commercial citrus-producing States and then subsequently move that fruit into commercial citrus-producing States. However, such movement could have occurred under the regulations in place before the publication of this final rule as well; APHIS does not have the regulatory infrastructure to monitor interstate movement of fruit by individual consumers. Additionally, even with a buffer zone in place, tourists and visitors would often travel across multiple States to reach their destinations, meaning that a buffer zone would not be highly effective at eliminating this consumer movement. For tourists and visitors, as well as for local residents who routinely move between commercial citrus-producing States and other States, the distance between the borders of commercial citrus-producing States and the citrus-producing areas within those States acts as a buffer as well, further decreasing the risk associated with such movement. Finally, the volume of such movement is extremely low when compared with the volume of commercial movement of fruit, making the risk of citrus canker establishment in commercial citrus-producing States through this scenario highly unlikely. These factors, combined with our determination that the introduction and spread of
Xac
into other commercial citrus-producing States through the movement of commercially packed fresh citrus fruit is unlikely and that the mitigations of treatment and APHIS inspection are highly effective, have led us to determine that a buffer zone to address such movement is unnecessary.

Scientific Evidence Used in the PRA and RMA

We received several general comments on the scientific evidence we used to make our determinations in the PRA and RMA. One commenter stated that the conclusion reached by the RMA is in part based on the lack of evidence that citrus fruit could play a role in the introduction of citrus canker in new areas, but that this lack of evidence is a consequence of the lack of scientific studies and is not based on scientific data; this commenter suggested that we evaluate the risks further using fruit produced subject to the regulations that were in place before the publication of this final rule. Another commenter suggested an extensive list of experimental data that the commenter believed were necessary to prove that the introduction and spread of
Xac
into other commercial citrus-producing States through the interstate movement of commercially packed fresh citrus fruit from a quarantined area is unlikely. One commenter stated that this program, which the commenter characterized as precedent-setting, requires a much more solid foundation of science and process affirmation than has been developed to date. Other commenters stated that not enough of the evidence we used in developing the RMA had been published in peer-reviewed scientific journals and that we had relied too much on preliminary research in making our determinations.

We used the best scientific evidence available to develop the PRA and the RMA, and we have detailed extensively how this evidence supports the conclusions we present in those documents. It is important to note that, based on the available evidence, we did not conclude that commercially packed citrus fruit could not serve as a pathway for the introduction and spread of
Xac
, but rather that it was unlikely that commercially packed citrus fruit serves as an epidemiologically significant pathway. That is why this final rule prohibits the distribution of such fruit to commercial citrus-producing States.

The Plant Protection Act charges us with ensuring that our decisions affecting imports, exports, and interstate movement of plants and plant products that we regulate under the Act are based on sound science. To fulfill this mission, we use all the scientific evidence that may be brought to bear on an issue, not just studies published in peer-reviewed journals. Observations based on APHIS' experience, survey and pest detection data, and preliminary experimental results can all provide valuable information to inform a regulatory decision, and we have used them in the PRA and RMA when appropriate. Having said that, the vast majority of the sources cited in the PRA and RMA have been peer-reviewed, as have both the PRA and RMA themselves.

Comments on specific studies we cited in the RMA and PRA are discussed later in this document.

The peer review for the RMA was conducted concurrently with the comment period for the proposed rule. One commenter stated that stakeholders should have the opportunity to review the peer reviewers' comments when submitting their own comments on this document.

We appreciate the commenter's concerns. APHIS had already provided for peer review of and public comment on the PRA, which informed the development of the RMA. In accordance with the Office of Management and Budget's bulletin on peer review, we are also making all the materials associated with the peer review, including the peer reviewers' comments, available at
http://www.aphis.usda.gov/peer_review/peer_review_agenda.shtml
. The conclusion of the RMA did not change as a result of the peer review, which was generally favorable.

One commenter included a late comment on the PRA as a reference, stating that APHIS had not made appropriate changes to the PRA based on the comment.

We reviewed the comment that the commenter included when we developed the revised version of the PRA. We addressed all the substantive points raised by that comment in the revised version of the PRA published with the proposed rule. Many of the points raised by that comment had been previously raised in other comments submitted on the PRA during the comment period.

As discussed earlier, the PRA concluded that asymptomatic, commercially produced citrus fruit treated with a surface disinfectant and subject to other mitigations is not epidemiologically significant as a pathway for the introduction and spread of citrus canker. However, in order to apply the conclusions of the PRA, we determined that we needed to extend its application to evaluate methods by

which fruit could be produced, treated, inspected, packaged, and shipped without resulting in the spread of citrus canker to commercial citrus-producing areas. Accordingly, the RMA addresses the risk associated with all commercially packed fruit; the RMA's recommendations have served as the basis for the Secretary's determination that it is not necessary to prohibit the interstate movement of citrus fruit from a quarantined area into States other than commercial citrus-producing States under the conditions described in the proposed rule. Therefore, specifically addressing comments on the PRA is unnecessary for the purposes of this rulemaking.

The Packinghouse-Centered Approach and the Current Regulations

In evaluating the risk associated with asymptomatic fruit, the PRA assumed that the citrus fruit in question was commercially produced under a specific set of pest management measures. The RMA, while recognizing that effective pest management measures for
Xac
are available to private and commercial growers and are normal production practices for many of these growers, does not assume that measures in the grove are mandatory. Instead, the RMA focuses on treatment with an APHIS-approved disinfectant at the packinghouse and APHIS inspection of fruit to be moved interstate. The recommendations in the RMA served as the basis for the proposed rule.

The regulations in place at the time the proposed rule was published required that fruit moved interstate originate in a grove that was found by an inspector to be free of citrus canker no more than 30 days before harvest (with additional requirements for limes), in addition to treatment of vehicles, equipment, and other articles that are used on the grove and treatment of the fruit itself.

Several commenters objected to APHIS moving away from the grove inspection approach and to the fact that we did not propose to require the use of the commercial production practices described in both the PRA and the RMA. These commenters stated that, under the proposed rule, measures such as copper sprays, designation and exclusion of infected trees, field culling of fruit, and packinghouse culling of fruit were all voluntary, and their effectiveness was unknown. The commenters expressed concern that not requiring these measures would increase the risk associated with citrus fruit moved interstate from a quarantined area.

One commenter stated that in other countries such as Argentina that ship fruit to citrus-producing countries in Europe, strict guidelines are followed that include field inspections and the planting of wind breaks between orchards that minimize wind velocity and subsequent dispersal of inoculum. The commenter stated that these countries realize that inspection of “finished” fruit in the packinghouse alone is not enough to guarantee the shipment of disease-free fruit.

One commenter stated that the objective of a rule addressing Florida's situation should be to prevent citrus canker from being introduced into disease-free areas in the United States; such a rule should not be designed with the primary objective of allowing shipments of fresh fruit from canker-affected areas. This commenter stated that the building blocks of premises and assumptions set forth in the proposed rule and the RMA create risk rather than develop protective barriers.

The regulations promulgated in this final rule include protective barriers against the introduction of citrus canker into other citrus-producing areas: Treatment with a surface disinfectant, APHIS inspection, and a prohibition of the movement of citrus fruit from a quarantined area into commercial citrus-producing States. We have determined that these barriers provide an appropriate level of protection with regard to the movement of citrus fruit from areas quarantined for citrus canker.

The grove certification requirement in place prior to the publication of this final rule and the APHIS packinghouse inspection required under this final rule are not dissimilar in their approach to preventing the interstate movement of fruit with visible canker lesions. Under the regulations in place before the publication of this final rule, none of the grove-centered measures cited by the commenters (copper sprays, designation and exclusion of infected trees, and field culling of fruit) were required. Rather, growers were required to demonstrate that their groves were free from citrus canker, on the basis of an inspection. In order to be found free from citrus canker, and thus have fruit from their groves be eligible for the interstate market, growers had incentives to employ the grove-centered measures described in the PRA and RMA and mentioned by the commenters.

Instead of a grove inspection, this final rule requires an inspection of the finished fruit at the packinghouse, which must operate under a compliance agreement and treat fruit with an approved surface disinfectant. Every lot of fruit must be inspected by an APHIS inspector for visible canker lesions. While growers are not required to practice measures that would reduce the prevalence of citrus canker in their fruit, and packinghouses are not required to perform their own culling process to remove fruit with visible canker lesions, the regulations promulgated in this final rule still provide them with a strong incentive to do so, since lots of fruit that fail APHIS inspection will not be eligible for interstate movement. Additionally, packinghouse culling for blemished fruit of any kind is already a standard business practice, and field management programs that include the use of copper sprays and field sanitation are already available to producers.

The purpose of the APHIS inspection at the packinghouses is to ensure that fruit moved interstate is free of visible canker lesions, and to prohibit the interstate movement of fruit that is not free of those lesions. From each lot of fruit intended for interstate movement, APHIS will inspect a quantity that is sufficient to detect, with a 95 percent level of confidence, any lot of fruit containing 0.38 percent or more fruit with visible canker lesions. Lots of fruit that fail inspection will not be allowed to enter interstate commerce.

A packinghouse-based inspection can ensure an appropriate level of phytosanitary security and will be easier to implement and enforce than the grove certification system in place before the publication of this final rule. Because it focuses on the end product, a packinghouse-based inspection will be more reliable and less easily circumvented than the preharvest grove survey that has been required in the regulations. A packinghouse-based inspection is also consistent with the risk associated with citrus canker and commercially packed fruit from Florida. In addition, a phytosanitary packinghouse inspection creates a performance standard for packed fruit that allows citrus producers greater flexibility to determine the most efficient and effective means of producing a compliant product.

Our choice of a packinghouse-based APHIS inspection as a means to prevent fruit with visible canker lesions from being moved interstate, rather than requiring specific grove and packinghouse practices to ensure the production of fruit free of visible canker lesions, is consistent with the recommendations of the 1997 Presidential/Congressional Commission on Risk Assessment and Risk Management. The commission recommended that agencies use alternatives to command-and-control

measures that dictate the use of specific technologies, where applicable (CRARM 1997), in order to encourage flexibility in the choice of risk management alternatives.

One commenter characterized the approach of the proposed rule as a control point approach, and stated that in the past APHIS has applied control point approaches only to quarantine treatments that are able to demonstrate a probit 9 level of effectiveness.

The probit 9 standard (99.997 percent mortality) applies to treatments for insect pests such as fruit flies, not to treatment of pathogens. In any case, the probit 9 standard is not applicable for the surface disinfectant treatment and packinghouse-based APHIS inspection that we are requiring. Scientific evidence indicates that both of these measures are highly effective.

One commenter stated that the PRA and RMA appeared to imply that packinghouse studies conducted to date were based upon fruit with known levels of contamination with
Xac.
The commenter asked how the packinghouse inspection process would achieve the results described in the RMA without grove inspections and without the ability to determine the infection pressure. The commenter also asked how the proposed measures can be effective without knowing the magnitude of the hazard, as expressed by the proportion of infected fruit.

Both of the packinghouse measures that we are requiring in this final rule are effective regardless of infection pressure. The surface disinfectant treatments approved by APHIS reduce numbers of
Xac
cells to low or undetectable levels. The APHIS packinghouse-based inspection is sufficient to detect, with a 95 percent level of confidence, any lot of fruit containing 0.38 percent or more fruit with visible canker lesions. In other words, if the infection pressure is higher than 0.38 percent of the fruit, it is 95 percent likely that the lot will be rejected from interstate commerce.

Two commenters cited findings of canker symptoms on fruit exported from Argentina and Uruguay to Spain in stating that symptomatic fruit will often pass through the packinghouse process. These commenters stated that the price growers and packers are receiving for citrus is what drives the quality of the citrus shipped, and that with low prices, low-quality fruit, such as those with canker, are more likely to be introduced into distribution channels.

We agree that, in general, price helps to determine the quality of fruit supplied. However, under the regulations established by this final rule, the fruit will be subject to an additional APHIS inspection separate from any field inspection and culling or packinghouse culling that may occur. Any lot that fails APHIS inspection will not be approved to move for interstate commerce. Given that, if there is a financial advantage to being able to supply fresh citrus to the interstate market, producers and packinghouses in quarantined areas are likely to employ measures and processes that will allow them to supply fruit free of visible canker lesions for APHIS inspection.

Treatments and Surface Contamination With
Xac

The regulations require all fruit moved interstate from an area quarantined for citrus canker to be treated in accordance with § 301.75-11(a). This paragraph has included two treatments: Thorough wetting for at least 2 minutes with a solution containing 200 parts per million (ppm) sodium hypochlorite, with the solution maintained at a pH of 6.0 to 7.5; or thorough wetting with a solution containing sodium-o-phenyl phenate (SOPP) at a concentration of 1.86 to 2.0 percent of the total solution, for 45 seconds if the solution has sufficient soap or detergent to cause a visible foaming action or for 1 minute if the solution does not contain sufficient soap to cause a visible foaming action.

One commenter noted that disinfectants are only effective if the active ingredient is not degraded. The commenter gave the example that sodium hypochlorite is degraded by sunlight and organic matter.

We agree with the commenter's point that it is important to ensure that the treatment is conducted properly. APHIS regularly monitors the treatment of fruit to ensure that the disinfectant agent is at the proper concentration and, in the case of sodium hypochlorite, pH, thus ensuring the effectiveness of the treatment. Under this final rule, we will conduct monitoring under conditions specified in the compliance agreements with packinghouses.

In this final rule, we are amending the treatment regulations to require fruit to be treated at a commercial packinghouse whose owner operates under a compliance agreement. Previously, the regulations had required that treatment be performed either in the presence of an inspector or at a facility whose owner operates under a compliance agreement under § 301.75-7(a)(2); this change will reflect the fact that all fruit intended for interstate movement must be treated at a commercial packinghouse under this final rule.

Several commenters stated that these surface disinfectant treatments may not be 100 percent effective, citing various reports that indicated that bacteria could be recovered from citrus fruit that had been treated with sodium hypochlorite or SOPP, including reports by Verdier (2006) and Golmohammadi (2007) and a newspaper article reporting on a lecture by Gottwald in which he presented unpublished preliminary results. With regard to the last of these, two commenters requested that we provide information about the followup studies mentioned in the article.

As stated in the RMA, the surface disinfectant treatments approved by APHIS reduce numbers of
Xac
cells to low or undetectable levels, but do not necessarily provide complete eradication. The evidence cited by the RMA does demonstrate that the treatments allowed under the rule substantially reduce bacterial populations, including
Xac
, found on the surface of citrus fruit to the extent practicable using surface disinfectant treatments currently registered for use in the United States on raw fruits and vegetables.

Recovery of
Xac
from fruit after surface disinfectant treatment does not demonstrate that the treatment is ineffective. Microbial detection or recovery tests simply measure the presence or absence of the organism in a sample and do not enumerate or measure the difference between the pre- and post-treatment bacteria population levels or infectivity. The treatments in the regulations are consistently reported as dramatically reducing
Xac
populations on the surface of fruit, if not eliminating them entirely. For example, Verdier (2006), cited by the commenters, measured the pre- and post-treatment levels in the wash solution and found that the bacteria population level was reduced 99.8 percent from an average of 39.4 colony-forming units (cfu)/mL on untreated controls to an average of 0.06 cfu/mL on treated fruit.

The information from Gottwald (2006) the commenters cite has not been published, and the followup studies referred to in news reports are currently being completed. We are not able to obtain the unpublished data that have been collected to this point. We will review the Gottwald information when it becomes available in final form. It is important to note again that the recovery of some bacteria after treatment is not inconsistent with treatment being highly effective at reducing
Xac
population levels, as described earlier.

Another commenter, referring to a study by Brown and Schubert (1987)

that the RMA cited, stated that the study's use of
Xanthomonas campestris
pv.
vesicatoria
as a proxy for
X. axonopodis
pv.
citri
in assessing the efficacy of SOPP was not appropriate, because the behavior of closely related bacteria may be very different.

The use of a proxy in efficacy testing is not unusual; for example, the Environmental Protection Agency (EPA) requirements for testing the efficacy of disinfectants allow the use of a proxy. A proxy organism was used in this study because the study was conducted in a model packinghouse. It is difficult to experiment with quarantine plant pathogens in the field because of the need to provide safeguards against their spread. While the bacteria in question are not identical, SOPP has a broad range of efficacy; there is no reason to believe that some feature of
Xac
would defeat the mechanism of SOPP. In addition, the RMA cited other studies establishing the efficacy of SOPP as a treatment against
Xac
itself.

The PRA contained the following statement regarding treatment effectiveness: “Studies performed in Argentina on the effectiveness of sodium hypochlorite on mature symptomless fruit artificially contaminated with
Xac
showed that sodium hypochlorite levels as low as 8 ppm were effective in eliminating epiphytic or surface bacteria from the fruit (Canteros, undated).” One commenter stated that there were no references about the viability of the bacteria, which is an important factor for risk assessment.

This particular study was one of many studies cited in the PRA and RMA establishing the effectiveness of sodium hypochlorite as a treatment. Other studies we cited included references about the viability of the bacteria.

Related to the presence of bacteria on the surface of treated fruit (also referred to as epiphytic bacteria or contamination), several commenters stated that fruit with such populations pose a risk of spreading citrus canker that was not addressed by the measures recommended in the RMA.

While surface populations of
Xac
undoubtedly exist on some citrus fruit that is packed in a quarantined area, and commenters cited scientific evidence establishing this point, substantial evidence indicates that surface bacterial populations do not infect mature fruit or survive on mature fruit long enough to infect other hosts. The evidence cited in the RMA regarding epiphytic survival indicates that epiphytic populations on harvested, mature fruit decline rapidly. For example, researchers in Brazil sprayed asymptomatic fruit, picked from trees, with a bacterial suspension of 10
6
cfu/mL; no bacteria were recovered after 5 days at room temperature under laboratory conditions (Belasque and Rodriguez Neto 2000). Epiphytic bacteria do not multiply in water on leaf surfaces or on dry leaves (Timmer
et al.
1996). Graham
et al.
(2000) found that
Xac
survived for 48 to 72 hours on a variety of inanimate surfaces in sun or shade, respectively. Additionally, there is no authenticated record of movement of diseased fruit as the origin for a citrus canker disease outbreak, which is especially suggestive given the brisk global trade in such fruit and the likely presence of some level of epiphytic bacteria on many fruit that is exported from citrus canker-affected areas.

Commenting on the PRA, one commenter noted that a low concentration of 8 cfu/mL (cited as a result of treatment by one study) may mean very high numbers of bacteria in tons of fruit.

The commenter's assertion is correct. However, shipments of fruit are commercially packed in boxes or other approved containers and are dispersed through market channels all over the United States, greatly diluting the concentration of bacteria which are at the same time experiencing rapid mortality. Therefore, such bacterial concentrations would not occur in the real world. In any case, for the reasons stated above, we have determined that fruit with epiphytic bacterial populations is not an epidemiologically significant pathway for the spread of citrus canker.

Some commenters were also concerned about the possible presence of
Xac
on other materials, citing reports of
Xac
survival for various periods on media like clean microscopic slides; leaf surfaces, plastic, wood, and other materials; cloth, sawdust and shavings, dried herbarium tissue, and sterile soil; and non-host weeds.

While
Xac
undoubtedly persists on a number of surfaces, it does not multiply outside of hosts. Under the regulations, the interstate movement of any regulated article other than fruit, calamondin and kumquat plants, and seed is prohibited. Regulated articles include leaves and grass clippings. In addition, under paragraph (c) of § 301.75-3, an inspector may designate any other product, article, or means of conveyance, of any character whatsoever as a regulated article when it is determined by an inspector that it presents a risk of spread of citrus canker and the person in possession thereof has actual notice that the product, article, or means of conveyance is subject to the provisions of this subpart. We do not typically regulate the movement of the other articles cited by the commenters under the current regulations because populations of
Xac
on such articles are very unlikely to infect mature citrus fruit.

Two commenters were concerned about the possibility that canker-infected fruit could contaminate packinghouse equipment with
Xac.
One commenter stated that packinghouse equipment needs to be disinfected if citrus canker is found in a lot run on that equipment. The other expressed a specific concern about contamination of existing wounds in fruit and stated that surface disinfestation cannot be continuously done during the commercial packing of fruit where both diseased and healthy fruit are being packed. This commenter suggested that we amend the regulations to exclude fruit from being packed from orchards or harvested fruit lots with an incidence of citrus canker above some established threshold, in order to minimize contamination of packing lines.

We acknowledge that infected fruit in a lot could contaminate the packing line with
Xac,
but, as stated above, substantial evidence indicates that the epiphytic bacterial populations that could be transferred from the packing line to the fruit do not infect mature fruit or survive on mature fruit long enough to infect other hosts. For that reason, we have determined that grove inspections are not necessary to mitigate the risk associated with such contamination, nor is disinfection of the packing line equipment necessary if canker is found during the inspection of a lot of fruit.

The RMA stated that “Bacteria within lesions may be more protected from the detrimental effects of washing, disinfection and drying. Viable
Xac
has been recovered by APHIS pathologists from citrus canker lesions on fruit culled from packinghouse lines after postharvest treatments (Riley 2007).” A few commenters expressed concern relating to this statement. One stated that chlorine is well known as a surface sanitizer but has no ability to penetrate beyond the surface—for example, into lesions. Another commenter noted that none of the experiments mentioned in the PRA or RMA evaluate the effect of disinfectants on
Xac
within the fruit, either in visible lesions (of any size) or in circumstances where the effects of
Xac
are not visible to the naked eye. The third, reacting to the statement about recovery of viable
Xac
by APHIS pathologists after postharvest treatments, asked what treatment had been performed, what level of recovery

had occurred, what preharvest management the fruits were subject to, why the fruits were not culled on the packing line before treatment, and whether the postharvest treatment included wax.

As stated earlier, the surface disinfectant treatments required in this final rule reduce numbers of
Xac
cells to low or undetectable levels. The RMA acknowledges that treatment with surface disinfectants is not effective on canker lesions, which is why this final rule also requires an APHIS inspection of each lot of fruit for canker lesions.

The canker lesions referred to in Riley (2007) occurred in fruit produced under the regulations that were in place before the publication of this final rule, i.e., with certification of grove freedom and with surface disinfectant treatment. As the regulations in place before the publication of this final rule did not require specific canker management measures, we do not have records of what canker management measures the fruit may have been subject to beyond the measures required by the regulations.

Addition of Peroxyacetic Acid Treatment

We proposed to add a new surface disinfectant treatment using peroxyacetic acid (PAA). The proposed rule would have required the regulated fruit to be thoroughly wetted for at least 1 minute with a solution containing 85 ppm peroxyacetic acid. At the request of growers in Florida, we evaluated the efficacy of this treatment and determined that the disinfectant is at least as efficacious as a surface disinfectant treatment as the currently approved disinfectants listed in the regulations. In the RMA, we described the tests that had been performed to confirm the efficacy of PAA. These tests were conducted on
X. axonopodis
pv.
citrumelo
(
Xa citrumelo)
, which was used as a surrogate for
X
.
axonopodis
pv.
citri
(i.e.,
Xac
).

Two commenters stated that PAA should be tested on
Xac
itself rather than on a surrogate. One stated that
Xa citrumelo
does not infect fruit and does not survive in orchards, making it a poor surrogate, and asked that we make the data referred to in the RMA publicly available. Another stated that, while it seems highly likely that PAA may be effective against
Xac
, to allow its use without any testing against the particular organism of concern appears to be unnecessarily optimistic. The commenter recommended testing in field conditions for this application or at least to demand post-introduction testing to demonstrate efficacy in the field.

We are making the data on PAA testing available on the Regulations.gov Web site with this final rule (see footnote 1 at the beginning of this final rule) or from the person listed under
FOR FURTHER INFORMATION CONTACT
.

As noted earlier in this document, the use of a proxy or surrogate is not unusual when testing a treatment's efficacy on a quarantine pathogen. The EPA label for PAA, which states the approved instructions for use and applicability of the disinfectant, acknowledges that it was tested on
Xa citrumelo
as a surrogate for
Xac
.

X. axonopodis
pv.
citrumelo
and
X. axonopodis
pv.
citri
differ primarily in the hosts they infect. (“pv.” stands for “pathovar,” which distinguishes strains or subspecies of the same bacteria based on their ability to only infect specific hosts.)
X. axonopodis
pv.
citrumelo
is generally considered to be more resistant to disinfection than
X. axonopodis
pv.
citri
, making the former a suitable surrogate for the latter.

In addition, PAA is an oxidizing agent whose mode of action has been shown to be effective on many bacteria, including
Bacillus cereus, B. subtilis, B. stearothermophilus, Clostridium botulinum, C. butyricum, C. sporogenes, Ditylenchus dipsaci, Enterococcus faecium, Escherichia coli
(including
E. coli
O157:H7),
Fusarium oxysporum, Gluconobacter oxydans, Lactobacillus plantarum, L. thermophilus, Leuconostoc mesenteroides, Listeria monocytogenes, Pseudomonas aeruginosa, P. fluorescens, Saccharomyces cerevisiae, Salmonella typhimurium, Staphylococcus aureus, Streptococcus delbreuckii
subsp.
bulgaricus
, and
Yersinia enterocolitica
. Based on PAA's characteristics as a general disinfectant and the results of the testing on
Xa citrumelo
, we have determined that PAA will be effective on
Xac
as well, and we are adding PAA as a surface disinfectant treatment for fruit in this final rule.

We are making three other changes related to PAA. While paragraph (a) of § 301.75-11 sets out treatments for fruit, paragraph (d) of that section sets out requirements for treatment of vehicles, equipment, and other articles. A solution of 85 ppm of PAA is also effective when used on vehicles, equipment, and other articles, and the availability of PAA as a treatment for packing line equipment would be useful for packinghouses in the quarantined area to fulfill the requirements in § 301.75-7(c)(2)(iv) for disinfection of packing equipment between packing lots of regulated fruit produced in a quarantined area and packing lots of fruit not produced in a quarantined area. Therefore, this final rule also adds PAA, when used indoors, as an approved treatment for vehicles, equipment, and other articles in paragraph (d) of § 301.75-11. We may decide to add PAA as a treatment for outdoor use in a separate rulemaking if we receive requests to do so.

The proposed rule would have added PAA as a fruit treatment in a new paragraph (a)(4) in § 301.75-11. Paragraphs (a)(1) and (a)(2) authorize the use of sodium hypochlorite and SOPP, respectively, as treatments for fruit; paragraph (a)(3) requires that these two surface disinfectants be applied in accordance with label directions. Instead of adding PAA in a new paragraph (a)(4), we have redesignated paragraph (a)(3) as (a)(4), added PAA in paragraph (a)(3), and amended paragraph (a)(4) to indicate that PAA must be applied in accordance with label directions as well.

The regulations in 7 CFR part 305 set out the requirements for phytosanitary treatments. Section 305.11 contains the two treatments that have been authorized for citrus fruit moved from a citrus canker quarantined area. Accordingly, in this final rule, we are amending that section to add PAA as a treatment for fruit.

Inspection and Potential for Mature Fruit Without Visible Lesions To Serve as Pathway for Infection

As mentioned earlier in this document, the PRA examined the risks associated with asymptomatic fruit. The PRA used the term “asymptomatic” to refer to the lack of visible signs or symptoms of citrus canker. The RMA examined the risks associated with all fruit that has been commercially packed, regardless of its disease status. We also prepared a quantitative model (Appendix 1 to the RMA) based on Florida production and shipping data to evaluate the efficacy of three levels of phytosanitary inspection in ensuring that symptomatic fruit does not enter commercial citrus-producing States. In the qualitative model, we defined “symptomatic” as meaning that the fruit have visible
Xac
lesions 1 millimeter (mm) in diameter and greater. One commenter pointed out that these terms were used inconsistently in the PRA and the RMA.

We appreciate the comment. In the version of the RMA that accompanies this final rule, Appendix 1 refers to fruit that have visible canker lesions and fruit that do not, rather than to symptomatic and asymptomatic fruit.

This commenter further stated that the proposed APHIS inspections of fruit target only relatively large symptoms readily visible to the naked eye, not whether any bacteria are present on the fruit. While the APHIS inspection is probably fairly effective at limiting the occurrence of larger
Xac
lesions in marketed fruit, the commenter stated, inspection is totally ineffective at detecting and limiting lesions smaller than 1 mm or at detecting
Xac
-infected fruit that have no visible lesions at the time of inspection. This commenter and other commenters also addressed surface populations of bacteria, stating that focusing inspection efforts on visible lesions ignores risk associated with bacteria.

We addressed the risk associated with epiphytic bacterial populations earlier in this document. We have determined that the other situations described by these commenters are unlikely to occur outside of an experimental setting. The reasoning behind this determination is discussed below.

Small lesions (less than 1 mm).
Commenters cited Koizumi (1972), in which Satsuma mandarin were either prick inoculated with
Xac
or naturally infected. The experimenter found that, in addition to lesions greater than 1 mm, lesions referred to as “late detection (small)” of a size of 0.1 to 0.15 mm also occurred. This would be below what we have determined to be the size threshold for a detectable lesion, as defined in Appendix 1 to the RMA. Besides stating that the existence of such lesions indicates that fresh fruit could be a pathway for the introduction or spread of citrus canker, the commenter also stated that it is possible that disinfecting the surface of the fruit might exacerbate the subsequent infectivity of
Xac
exuding from small lesions, by removing other (e.g., rot-provoking) organisms that might directly or indirectly accelerate the decline of
Xac
after harvesting.

As discussed in the RMA, in the field, immature citrus is most susceptible to infection with
Xac
and lesion development. Mature citrus fruit have natural wax layers on their surface, decreasing susceptibility by reducing access to natural openings, such as stomata. In addition, mature (not expanding) asymptomatic fruit without injuries or blemishes are not known to develop symptoms in the field. In the Koizumi (1972) study, mature fruit were experimentally inoculated while the fruit was still attached to the tree; equivalent conditions are extremely unlikely to occur naturally.

The lesions Koizumi observed resulted from a combination of artificial (prick) inoculations and natural infections and therefore provide little information about how the ratio of typical to atypical lesions on fruit varies under natural conditions. Koizumi's results varied greatly over the several years he conducted these experiments; the commenters cite results from the year with the highest incidence of infection, which coincided with unusually high temperatures and two typhoons (hurricanes). Koizumi speculated that the atypical lesions were the result of restricted expansion brought on by physiological changes in the maturing fruit and lower ambient temperatures. As noted by Graham
et al.
(1992b), the small late season lesions were characterized by a “lack of bacterial proliferation.” Lesions without proliferation would not provide an epidemiologically significant source of inoculum for
Xac
infections.

While other studies have conducted similar inoculation tests on fruit before (Fulton and Bowman 1929) and after (Graham
et al.
1992b; Verniere
et al.
2003), Koizumi (1972) remains the only paper to describe this type of lesion. Fulton and Bowman noted that if one was not careful to avoid oil glands when making puncture inoculations, the released oils cause injuries to the adjacent tissue. One could speculate that at least some of Koizumi's atypical lesions might, in fact, be injuries. We have no evidence that the lesions described by Koizumi (1972) occur in nature and therefore cannot agree that they would occur at the rates cited by the commenters.

Nevertheless, conditions could exist in which small
Xac
lesions occur. However, as noted above, immature fruit are most susceptible to
Xac
infection, and
Xac
lesions grow as the fruit matures; the growth of the lesions slows as the fruit reaches maturity. Picking mature fruit from the tree causes senescence of the fruit and further inhibits lesion development. Therefore, while small lesions might occur on immature fruit, they would typically grow into larger lesions as the fruit matures; if there were small lesions present on such fruit, it would be likely that lesions larger than 1 mm would be present as well. In general, APHIS inspectors do not see fruit with only lesions smaller than 1 mm; small lesions occur in association with larger lesions (Riley 2007).

The packinghouse culling and grading procedures are designed to remove fruit with visible lesions and would result in removal of the fruits likely to harbor the highest pathogen loads, and therefore present the greatest risk of disease transmission. The APHIS inspection after the packing process is completed will result in the rejection of any lot of fruit that has visible canker lesions and will prevent that lot from moving in interstate commerce.

Wounded fruit.
One commenter cited Fulton and Bowman (1929), who inoculated a mature grapefruit from the market and 75 days later tested the grapefruit. The test indicated that there were “something like 32,000 bacteria per puncture,” although the fruit had not developed external lesions. Another commenter stated that a general principle of postharvest pathology is that surface disinfestation of fruit with standard oxidizing chlorine washes will inactivate most microorganisms from the surface of non-wounded fruit, but not from fruit wounds.

The grapefruit described in Fulton and Bowman (1929) was one of a number of market fruit that were inoculated in this way, the rest of which either rotted after inoculation or supported bacterial populations that did not multiply. All these fruits were kept in moist laboratory conditions designed to facilitate the development of
Xac
bacteria.

Regarding the grapefruit, Fulton and Bowman stated the following in their 1929 study: “There is apparently a very marked difference in the behavior of the canker organism following inoculations in the peel of mature fruit after removal from the tree as compared with its behavior in the peel of mature fruit still on the tree. Possibly changes in the physiological condition of the fruit resulting from its removal from the tree are responsible for the difference * * * senescent changes in the peel favor the development of fungi having saprophytic tendencies; it is not inconsistent to presume these changes would in equal degree hinder the development of an organism having definitely parasitic habits like
Pseudomonas citri
[
Xac
].” This is consistent with a determination that infected wounds would occur extremely rarely in real-world conditions.

Fulton and Bowman also reported that infection only occurred if the wound stayed moist until the time of inoculation. Wounds that were allowed to dry and were inoculated after 26 hours did not result in infection. That is, infections occurred only when oil glands were avoided and inoculum was applied within 26 hours of wounding (Fulton and Bowman 1929). Verniere
et al.
(2003) reported a disease incidence of zero when inoculating mature fruit either by pin prick or spray inoculation.

As noted above, the conditions that would allow citrus canker to develop in wounds in the field are unlikely to

occur. In addition, any fruit with wounds would likely be culled in the field or by the packinghouse before it could be submitted for APHIS inspection.

Based on this evidence, we have determined that fruit with small lesions or infected wounds would occur extremely rarely and are not likely to be epidemiologically significant when they do appear. Therefore, it is appropriate to focus our inspection efforts on detecting lesions 1 mm or greater.

The RMA stated that APHIS plant pathologists have intercepted fruit in final packed cartons with lesions in the 2-3 mm range and have observed that the majority of the symptomatic fruit that APHIS inspectors intercepted after passing through the packing line undetected by graders have only one lesion (Riley 2007). Two commenters addressed this statement. Both asked for data on interceptions in Florida fruit, with one asking for information on how many fruit were detected and what varieties were found to be infected.

These data are available from the person listed under
FOR FURTHER INFORMATION CONTACT
.

One commenter stated that the fact that APHIS inspectors intercepted fruit with lesions did not substantiate the statement made later in the RMA that grading and inspection procedures are effective in removing fruit with visible lesions. Another commenter stated that all canker infections cannot be detected in packinghouses without knowing whether the fruit originates from a canker-free grove, or at least a grove with a very low level of canker infection. The commenter stated that it is very difficult, if not impossible, to distinguish canker blemishes from numerous other blemishes, especially in the growing conditions that prevail in Florida, where many blemishes appear on fruit.

One commenter cited the example of citrus affected by septoria, a fungus, that are exported to Korea. This commenter stated that the California citrus industry conducts vigorous training programs for line employees to identify and eliminate fruit with distinguishable symptoms and that this culling is then augmented by laboratory analysis. The commenter stated that lab analysis has always detected symptoms on a small percentage of fruit missed by highly trained employees.

We appreciate the opportunity to clarify this point. Various evidence, as cited in the RMA, indicates that packinghouse grading and inspection procedures are effective in removing fruit with visible lesions. Packinghouse graders and inspectors in Florida also receive training provided by the State in identifying canker lesions. The phytosanitary inspection that will be performed by APHIS in this final rule will provide another layer of inspection protection. We provided evidence supporting these points in the RMA, including detailed evidence about the efficacy of APHIS' inspection process. Scientific evidence indicates that these measures are highly effective, but since uncertainty remains about the epidemiological significance of symptomatic fruit, we are prohibiting the distribution of fruit moved interstate to commercial citrus-producing States.

As discussed earlier in this document, the APHIS packinghouse-based inspection is sufficient to detect, with a 95 percent level of confidence, any lot of fruit containing 0.38 percent or more fruit with visible canker lesions. In other words, if the infection pressure is higher than 0.38 percent of the fruit, it is extremely likely that the lot will be rejected from interstate commerce. APHIS inspection is thus effective regardless of infection pressure.

One commenter, responding to both the evidence presented for APHIS inspectors' detection efficacy in the qualitative portion of the RMA and in the model in Appendix 1, stated that none of the evidence provided for APHIS inspectors' detection efficacy corresponds to field conditions for detection of lesions. The commenter noted that the cited figures for refresher training correspond to identification within 40 seconds of a lesion presented to the inspector, which the commenter stated was inconsistent with location of a rare lesion on a fruit in a continuous search of 1,000 fruit samples within an average of 5 seconds, an estimate we presented in the Regulatory Impact Analysis for the proposed rule in the context of describing the proposal's potential impact on packinghouse operations. The commenter stated that evaluation of enzyme-linked immunosorbent assay (ELISA) Dip Stick tools and the evaluation of a diagnostic tool (if that is a separate exercise from the ELISA Dip Stick tool) also corresponded to classification of already-detected lesions.

We appreciate the opportunity to clarify the evidence presented in the RMA on the APHIS phytosanitary inspection. The evidence provided in the RMA is consistent with the proposed rule's approach of using inspection to detect lesions in the packinghouse. The training for phytosanitary inspectors was done in packinghouse conditions, using culled fruit for the test sample. Both in training and testing and in the packinghouse, inspection is performed on fruit that has been removed from the packing line.

Under packinghouse conditions, there is no time limit for fruit inspection once the fruit is randomly sampled. This can be accomplished because the fruit is inspected individually, away from the packing line. The 40-second time limit during training is a performance requirement for training, not a packinghouse inspection requirement. The estimate that the packinghouse inspection would require 5 seconds per fruit is also not an APHIS packinghouse inspection requirement; rather, this figure was cited in the context of the potential economic impact of the lot inspection on the packinghouse, and specifically in discussing possible delays associated with inspection. Inspectors who see questionable lesions will be able to take whatever time is necessary to determine whether those lesions are canker lesions.

The ELISA Dip Stick test did correspond to already detected lesions. The results of the ELISA Dip Stick test were cited in the RMA to provide empirical data on the size of lesions that can be detected by inspectors. The ELISA Dip Stick test is not part of the detection system that will be used in commercial packinghouses under this final rule; it will be used only for confirmation of lesions found by inspectors.

One commenter disagreed with the idea that only “finished” fruit would be inspected for citrus canker in the packinghouse. The commenter stated that citrus canker is more easily detected on fruit that has not been through the packing process. Brushing of fruit on the packing line may remove diseased tissue, the commenter stated, and waxing of the fruit will make the disease harder to diagnose.

Inspection of fruit before they go through the packing process would not allow the packinghouses themselves to cull canker-infected fruit prior to packing. In the RMA, we described in detail the efficacy of inspection of finished fruit for citrus canker, as discussed earlier.

Our experience indicates that washing fruit will make it easier to detect citrus canker lesions. Citrus fruit that comes directly from the field is often covered in dirt, sooty mold, and other debris and material that could obscure citrus canker lesions. Washing the fruit removes some of this material. Because citrus canker lesions occur within the peel of the fruit, they would not be brushed off during finishing. Additionally, the wax used on fruit is transparent, which means it would not impede disease detection.

Potential Pathways for Spread of Citrus Canker Through Movement of Fruit

As mentioned earlier, the RMA that was made available with the proposed rule concluded that the introduction and spread of
Xac
into other commercial citrus-producing States through the movement of commercially packed fresh citrus fruit is unlikely because:

• Fresh citrus fruit is produced and harvested using techniques that reduce the prevalence of
Xac
-infected fruit;

• Citrus fruit is commercially packed using techniques that reduce the prevalence of infected or contaminated fruit, including disinfectant treatment for epiphytic contamination;

• For a successful
Xac
infection that results in disease outbreaks to occur an unlikely sequence of events would have to occur;

• Reports of citrus canker disease outbreaks linked to fresh fruit are absent; and

• Large quantities of fresh citrus fruit shipped from regions with
Xac
have not resulted in any known outbreaks of citrus canker disease.

One commenter stated that we did not enumerate any complete pathways for transmission and so did not evaluate the scientific evidence in such a way as to evaluate the possibility or likelihood for transmission along such pathways. The commenter also stated that there are pathways (including illegal diversion of fruit and perfectly legal amateur grower activities) from every part of the country that may lead to infection of commercial citrus areas and that have not been evaluated. This commenter and another commenter suggested several potential pathways that we had not addressed in the RMA.

In general, it is difficult to examine quantitatively the pathways by which infected fruit could theoretically spread citrus canker. Those pathways are dependent on consumer behaviors and biological events for which we lack data that we could use to quantify them, and no such data were provided by the commenters. This lack of data is one reason we have determined that it is appropriate to prohibit distribution of fruit moved interstate from a quarantined area to commercial citrus-producing States. As discussed earlier, such a prohibition, combined with the monitoring and enforcement efforts APHIS will use to ensure that the prohibition is adhered to, is effective at preventing the illegal movement of fruit.

We discuss the specific pathways brought up by the commenters below.

One commenter suggested that citrus canker could be spread through long-distance movement due to storm or cyclone activity.

The available evidence indicates that the maximum range for spread of citrus canker through storm activity would not be sufficient to spread citrus canker from Florida to another commercial citrus-producing State.

One commenter suggested that citrus canker could be spread through movement on workers' clothes and picking bags.

As discussed earlier, while
Xac
can persist on a number of surfaces, its infectivity outside lesions is unknown. We do not agree that it is likely that workers will move between Florida and other commercial citrus-producing States without laundering their clothes and while carrying their own picking bags. The commenter provides no evidence that could be used to empirically estimate the frequency of such behavior, and APHIS is unaware of any such evidence.

Two commenters suggested that citrus canker could be spread if fruit or peel from citrus fruit infected with
Xac
is placed in or around susceptible host plants, after which a water event moves the bacterium from the fruit or peel to the host plant. One commenter cited Koizumi (1972) as evidence that
Xac
could be recovered from fruit peel for months if the peel was placed in physiological solution for 2 hours. This commenter stated that only one bacterium is required to cause infection. Another commenter cited fruit with live
Xac
cells that are thrown into a compost pile or bin under a backyard citrus tree, after which a splash or water movement occurs. Once a backyard citrus plant was infected, these commenters stated, rain or storm events could spread the bacterium to commercial citrus groves.

The Koizumi (1972) study recovered bacteria using physiological solution, a buffered saline solution that ensures optimal conditions for bacterial recovery. Analogous conditions do not occur in nature. Additionally, for this scenario to occur, citrus fruit that is infected would have to have been moved from a quarantined area into a commercial citrus-producing State—movement that is prohibited by the regulations. As discussed earlier, we are increasing monitoring and disease surveillance activities and making changes to the regulations in order to help prevent the illegal or inadvertent movement of fruit from quarantined areas into commercial citrus-producing States. If an infected fruit was illegally moved into a commercial citrus-producing State, it would have to be exposed to susceptible plants under very specific physical and environmental conditions for infection to occur.

While it is true that one bacterium is sufficient to cause infection, that one bacterium would have to encounter conditions that were appropriate for infection. There is a very low likelihood that any one bacterium will encounter conditions sufficient to cause infection; it is difficult to create these conditions even in a laboratory setting. Under natural conditions, it would require thousands if not millions of tries for one bacterium to cause infection. Gottwald and Graham (1992) estimated that as few as 2.4
Xac
bacteria forced into a water congested stomatal cavity of a susceptible plant were sufficient to cause a lesion. However, they also determined that the minimum concentration of bacteria in the inoculum needed to produce an infection, and presumably to place the estimated 2.4 bacteria in a stomatal cavity, was 10
5
cfu/mL. Thus, although it may take only 2.4 infective bacteria in the right place to cause infection, it takes exponentially greater numbers of bacteria in the inoculum for those 2.4 bacteria to occur in the right place at the right time.

The data submitted by one commenter (see
http://www.regulations.gov/fdmspublic/component/main?main=DocumentDetail&d=APHIS-2007-0022-0053
), in which infected fruit were placed next to grapefruit seedlings in natural conditions for 2 months without infection of the seedlings, suggests that the likelihood of such an occurrence may be low.

Finally, for this pathway to occur, rain or storm conditions would have to prevail that could spread the bacterium over long distances, but Borchert
et al.
(2007) concluded that such conditions are unlikely to prevail outside Florida, the State that is currently quarantined for citrus canker.

We acknowledge that it is possible that all of these circumstances could prevail, but such a “perfect risk” scenario would be an extremely rare event. The commenter provides no evidence that could be used to empirically estimate the frequency of this behavior, and APHIS is unaware of any such evidence.

One commenter suggested a fruit-to-human-to-plant pathway for the introduction of citrus canker into a commercial citrus-producing State. A hobbyist who cultivates citrus in a State other than a commercial citrus-producing State could handle infective citrus from the quarantined area, then infect the plants the hobbyist is cultivating. The hobbyist might not notice the canker infection and could

subsequently move the infected plants into a commercial citrus-producing State.

We acknowledge that such an occurrence is possible, but such a “perfect risk” scenario would be an extremely rare event. The commenter provides no evidence that could be used to empirically estimate the frequency of such amateur citrus grower behavior, and APHIS is unaware of any such evidence.

None of the pathway scenarios suggested by the commenters have changed the RMA's conclusion that an unlikely sequence of epidemiological events would have to occur for a successful
Xac
infection that results in disease outbreaks to occur as a result of the movement of commercially packed, treated, and APHIS-inspected fruit to States other than commercial citrus-producing States.

Potential for Citrus Canker Establishment in Commercial Citrus-Producing Areas

The RMA included a discussion of the susceptibility of commercial citrus-producing areas that are not currently quarantined for citrus canker to the spread of the disease. This discussion included a reference to a study by Borchert
et al.
(2007) that developed a citrus canker spread model using the North Carolina State University APHIS Plant Pest Forecast System to identify areas where citrus canker could become established in the major citrus-producing regions of the United States.

Two commenters stated that modeling of pathogen establishment, infection, and disease severity should be an essential component of the risk assessment for each citrus-producing State and region within the State, adding that the Borchert project results should be made publicly available.

We disagree that modeling of pathogen establishment, infection, and disease severity in commercial citrus-producing States is a necessary component of the risk assessment. The RMA concluded that the introduction and spread of
Xac
into other commercial citrus-producing States through the movement of commercially packed fresh citrus fruit from quarantined areas is unlikely. Nevertheless, because the RMA concluded that the evidence is not currently sufficient to support a determination that fresh citrus fruit produced in a
Xac
-infested grove cannot serve as a pathway for the introduction of
Xac
into new areas, we are prohibiting the interstate movement of fruit from a quarantined area into commercial citrus-producing States. This measure makes modeling of pathogen establishment, infection, and disease severity in commercial citrus-producing States unnecessary.

The Borchert
et al.
(2007) study is an internal APHIS document. We made the study available to commenters who requested it during the comment period, and it is available from the person listed under
FOR FURTHER INFORMATION CONTACT
. The Borchert
et al.
(2007) study provides the modeling requested by the commenters.

Some commenters addressed the risk citrus canker posed to specific States. One commenter stated that California is a fresh citrus State with more than 200,000 acres dedicated to the fresh market production of oranges, lemons, grapefruit, mandarins, and other citrus varieties. Although the majority of the oranges are grown in arid areas, many of the lemons and some of the grapefruit are produced in climates with higher humidity and rainfall. The commenter stated that the survival of canker in these areas would be expected; the survival of canker in the more arid areas is less certain, but canker's potential impact cannot be ignored based on survival reports from other arid lands. Another commenter, addressing the suitability of California's climate for development of citrus canker, stated that Dalla Pria
et al.
(2006) stated that the greatest severity of canker occurred at 24 hours of leaf wetness, with 4 hours of wetness being the minimum duration sufficient to cause 100 percent incidence at optimal temperatures of 25 °C to 35 °C.

Another commenter stated that when Texas had citrus canker, it was in southeast Texas, which has higher rainfall than the Rio Grande Valley. The Rio Grande Valley generally has high relative humidity, although the commenter stated that there is tremendous variability in Texas' weather patterns; for example, July 2007 has been very wet. The commenter stated that canker would be able to thrive in the conditions present in the commercial growing area of South Texas. Surveys for citrus greening, the commenter stated, have revealed that Texas has substantial amounts of citrus in an area approximately 100 miles north of the Gulf of Mexico from Brownsville to Houston. The commenter noted that the challenges of eradicating canker in the urban areas of Florida contributed to the failure of the eradication program and anticipated that many of those same difficulties would be experienced in Texas if citrus canker appeared in urban areas.

We agree with these commenters that citrus canker could be introduced to California and Texas. The RMA cited Peltier and Frederich (1926) as indicating that the disease “could develop in all of the citrus regions of the world
sometime
over the growing season.” These facts do not change our conclusions that (1) only a small portion of each commercial citrus-producing State actually produces citrus, and an even smaller portion has a climate suitable for canker disease development; and (2) the climate in Florida is the most favorable of any State for the development of citrus canker, and it would be more difficult for citrus canker to be introduced into and subsequently become established in any other State. Regardless, the remaining uncertainty about the level of risk associated with the movement of citrus fruit from a quarantined area has led us to maintain the current prohibition on the movement of citrus fruit into commercial citrus-producing States.

Two commenters urged APHIS to address the risk of spreading citrus canker to other potential host areas, which may not be areas where citrus is commercially produced. One commenter stated that citrus (not just fruit-bearing trees) can be and is grown in other areas of the United States, and those areas are also at risk of citrus canker. The commenter noted that during the initial outbreak of citrus canker in the mainland United States, disease outbreaks were also recorded in Alabama, Mississippi, South Carolina, and Georgia. The commenter also noted that Borchert
et al.
(2007) were tasked “to identify areas where citrus canker could become established in the major citrus producing regions of the United States,” rather than all the areas in the United States in which citrus canker could become established.

These commenters recommended that the RMA and the proposed rule take account not only of current commercial citrus-producing areas, but also areas where citrus currently grows (even if it is not commercially grown) and areas where citrus could grow, but does not currently. These commenters stated that establishment of citrus canker in any such area might subsequently lead to establishment in commercial areas, since many of these areas are contiguous with commercial areas, and long-distance transport now appears to be more likely than historically, presumably due to the presence of the Asian leafminer (
Phyllocnistis citrella
Stainton) in Florida. These commenters also stated that citrus canker establishment in areas where citrus is not commercially produced would lead to other pathways for establishment in areas where it is.

The focus of the citrus canker program has been on commercial citrus-producing States because these States present the highest likelihood for introduction of the disease, due to the density of citrus plantings in those States. Prohibiting the movement of fruit from areas quarantined for citrus canker to States other than commercial citrus-producing States would be overly restrictive.

We acknowledge that dooryard plantings of citrus exist outside of commercial citrus-producing States. However, while canker infection in a State other than a commercial citrus-producing State could serve as a pathway for introduction into a commercial citrus-producing State, as discussed earlier under the heading “Potential Pathways for Spread of Citrus Canker Through Movement of Fruit,” an unlikely sequence of epidemiological events would have to occur in order for citrus canker to be introduced and established through the movement of citrus fruit from a quarantined area.

If, in the future, commercial quantities of citrus are planted in a State that is not currently designated as a commercial citrus-producing State, we will designate that State as a commercial citrus-producing State in § 301.75-5.

As discussed in the RMA, injuries caused by the Asian leafminer can produce wounds that serve as infection courts in leaves and, to a lesser extent, fruit, but the leafminer itself is not a vector for the spread of citrus canker.

Potential Application of the Packinghouse-Based APHIS Inspection System to Imported Citrus

The regulations in 7 CFR 319.28 prohibit the importation of citrus fruit from areas where citrus canker is present, except for Unshu oranges from Japan and Cheju Island, Republic of Korea, that are produced in accordance with the systems approach described in paragraph (b) of that section. The systems approach for Unshu oranges from Japan and Korea requires measures to ensure that the oranges are produced in an area free from citrus canker; for Unshu oranges from Japan, the systems approach requirements also address the citrus fruit fly.

Several commenters expressed concern that the proposed regulations, if implemented, could lead to requests from other citrus-producing countries to export citrus fruit under conditions similar to those we proposed for the interstate movement of fruit from citrus canker quarantined areas. The commenters noted that, under international trade agreements, APHIS has agreed not to impose conditions on the importation of commodities that are more restrictive than those we impose on the domestic movement of similar commodities. These commenters stated that the RMA should consider the risk associated not only with the interstate movement of citrus fruit from domestic quarantined areas but also the risk associated with potential imports from foreign citrus-producing areas affected with citrus canker.

One commenter who had expressed concern about illegal movement of Florida citrus into commercial citrus-producing States stated that this potential problem would only increase if citrus fruit was allowed to be imported from foreign areas affected with citrus canker.

Our analysis of the risk associated with the importation of citrus fruit from other countries where citrus canker exists under conditions similar to those in this final rule would be conducted separately from the analysis we conducted for this rulemaking. Before we would consider using an approach similar to that promulgated in this final rule to allow the importation of citrus fruit from canker-affected areas in another country, the national plant protection organization of such a country would need to submit a request that we do so. A country requesting to be able to use this framework to export citrus to us would have to demonstrate the ability to perform the required treatments and phytosanitary inspections; it would also be required to have a bilateral workplan in place with APHIS. Depending on the circumstances, we may allow imports only through a preclearance program staffed by APHIS inspectors whose salaries are funded by the exporting country. In addition, there may be other citrus pests in foreign citrus production areas whose risk would need to be mitigated separately from the risk posed by citrus canker. For these reasons, we have not amended the RMA that accompanies this final rule to discuss potential imports from other countries.

One commenter specifically noted that the requirements for Unshu oranges from Japan are not in harmony with the proposed rule.

The proposed rule and the risk management analysis are based on the most recent science and our determination of the appropriate level of protection for the citrus canker pathogen. We may reassess the risk associated with the importation of Unshu oranges from Japan in the future if Japan requests that we do so. If we reassess the risk associated with Unshu oranges from Japan, as discussed earlier, the assessment will take into account all relevant local conditions and all pests that are present in Japanese citrus production areas.

It is important to note that Unshu oranges from Japan, if they are fumigated for arthropod pests, are allowed to be imported into commercial citrus-producing States, because they are produced under a systems approach. Fruit moved interstate from citrus canker quarantined areas is not allowed to be moved into those States under this final rule.

One commenter noted that the term “commercially packed” can be interpreted in different ways. In South Korea, the commenter stated, one group of growers used a “commercial” packing shed that was no more than 75 meters by 50 meters and in which the post-harvest treatment with sodium hypochlorite was performed in a small bath. The commenter stated that it is important to recognize that different circumstances prevail in different countries when harmonizing domestic regulations with import regulations.

We fully agree with the commenter that the circumstances in a country would need to be assessed before we could allow the importation of citrus from a citrus canker-affected area under conditions similar to those under which we are allowing the movement of citrus from a citrus canker quarantined area.

With regard to the specific circumstance cited by the commenter, we have determined that it is necessary to define the term “commercial packinghouse” in this final rule, given that the PRA and RMA analyzed the risk associated with the interstate movement of commercially packed fruit. In this final rule, we are adding a definition of
commercial packinghouse
to the regulations. This definition reads: “An establishment in which space and equipment are maintained for the primary purpose of packing citrus fruit for commercial sale. A commercial packinghouse must be registered as a packinghouse with the State in which it operates or hold a business license for treating and packing fruit.” This definition will help to ensure that the packinghouses that pack fruit for interstate movement under this final rule have equipment and operating procedures that are consistent with those described in the PRA and RMA.

Because the PRA and RMA referred specifically to the risks associated with commercially packed fruit, we are amending the proposed regulations in § 301.75-7 to refer specifically to commercial packinghouses.

One commenter stated that implementation of the proposed rule

may also result in foreign countries requesting APHIS to consider a similar approach for fresh commodities other than citrus. The commenter stated that the approach described in the proposed rule could be applied in any number of other situations in which a systems approach is not operationally or financially feasible.

It is important to note in response to this comment that we determine what phytosanitary mitigations are appropriate for the importation or interstate movement of commodities based on our assessment of the risk their importation or interstate movement poses and the appropriate level of phytosanitary protection against that risk. If we determined that a set of mitigations was necessary to provide the appropriate level of protection for a commodity proposed for importation, but that set of mitigations was determined not to be operationally or financially feasible by the national plant protection organization of the exporting country, we would not allow the importation of that commodity.

We would only allow the importation of a commodity under an approach similar to the approach used in this final rule if we determined that this approach could provide the appropriate level of phytosanitary protection. In past cases where we have determined that inspection, treatment, and limited distribution mitigations similar to those implemented in this final rule can provide an appropriate level of protection against the introduction of plant pests by imported commodities, we have employed such mitigations. For example, litchi imported from Thailand are inspected for a fungal pathogen, irradiated for arthropod pests, and prohibited from being imported or moved into Florida due to the litchi rust mite.

In order for us to determine that a packinghouse-centered approach provided an appropriate level of phytosanitary protection, we would have to determine that the biology of the pest supported such an approach and that the pest in question could be effectively detected by inspection of the commodity. In addition, other considerations may apply based on the level of risk we determine importation of the commodity to pose.

Miscellaneous Comments on the RMA

One commenter noted that, since viable
Xac
have been found in fruits with canker lesions that are imported into Europe, it is clear that the importation of symptomless fruits from canker-infected areas has a risk of introducing the disease if all the control steps, carried out by many people at different times, are not always perfectly implemented.

The RMA concluded that the introduction and spread of
Xac
into other commercial citrus-producing States through the movement of commercially packed fresh citrus fruit from quarantined areas is unlikely. While fruit with visible canker lesions has likely been imported into the EU, the importation of citrus fruit from areas where citrus canker is present has not resulted in the introduction of the disease in the EU, despite the fact that all fruit imported into the EU is allowed to move to citrus-producing areas within the EU. (This is discussed in more detail in the RMA in Section 5.6.2, “International and Interstate Movement of Citrus Fruit.”) In addition, treatment and inspection will both serve as effective mitigations against the potential of fruit moved interstate to introduce citrus canker to other States. Nevertheless, the RMA concluded that the evidence is not currently sufficient to support a determination that fresh citrus fruit produced in a
Xac
-infested grove cannot serve as a pathway for the introduction of
Xac
into new areas. That is why this final rule prohibits the distribution of fruit moved interstate from quarantined areas to commercial citrus-producing States.

In the RMA, we stated that there is no authenticated record of the movement of fresh fruit infected with
Xac
being related to the epidemiology of citrus canker disease. One commenter stated that pest-free areas are now established on the basis of a pest being “known (as demonstrated by scientific evidence) not to occur” rather than “not known to occur,” and the same standard of evidence should apply to this statement; research should be conducted to establish this statement as fact.

We agree with the commenter's characterization of the process by which pest-free areas are established. Our statement was not meant to imply that we had positively established that fresh fruit infected with
Xac
has never served as a pathway for the transmission of citrus canker. Rather, it reflects the fact that no outbreaks of citrus canker have ever been attributed to the movement of infected fruit, despite the brisk global trade in such fruit. (The majority of outbreaks of citrus canker whose cause is known were caused by the movement of infected citrus nursery stock, rather than fruit.)

The RMA noted the Asian leafminer interacts with
Xac
by providing wounds that serve as infection courts in leaves and, to a lesser extent, fruit. Leafminer wounds create suitable microclimates for
Xac
development, and leafminer-damaged leaves have more and larger lesions. One commenter asked whether injuries from the peel miner, an insect present in California, could result in higher infection of fruits.

Injuries from the peel miner would be likely to increase the susceptibility of fruit to infection, and increase the severity of the infection if they became infected. In terms of overall spread of citrus canker, the peel miner would not likely be as epidemiologically significant as the Asian leafminer, since leaves of citrus trees and plants are more susceptible to citrus canker infection than the peels of citrus fruit.

One section of the RMA discussed the effect of shipping and storage temperatures on
Xac
populations, concluding that typical shipping and storage temperatures reduce such populations. One commenter noted that pathologists are able to keep
Xac
-infected samples in refrigerators at 2 °C to 4 °C and still isolate the bacterium. The commenter stated that the emphasis of this section should be on the survival of the bacterium.

We agree with the commenter that cool temperatures do not necessarily cause mortality for
Xac
, and the RMA noted accordingly that such temperatures influence survival rather than stating that they inactivate the bacteria. However, in the context of an analysis of the likelihood of citrus fruit serving as a pathway for the introduction or spread of citrus canker, it is important to note that shipping and storage temperatures reduce
Xac
populations. In addition, commercial refrigeration is also quite dry, and
Xac
is highly influenced by humidity, so the dryness of refrigeration is more likely to have mortality effects than the cold.

The RMA stated that fruit are susceptible to citrus canker infection from petal fall until they are around 6 cm in diameter, and are most susceptible at a fruit diameter of about 2-4 cm. One commenter stated that fruit size cannot be related to susceptibility unless the variety is indicated, as some varieties (such as grapefruit) are bigger than others (such as mandarins).

We agree with the commenter, and we have amended the discussion in the RMA to state that fruit are susceptible to natural (stomatal) infection from petal fall until they are fully expanded (around 6 cm in diameter for some varieties), and are most susceptible after stomata form and fruit is in a stage of rapid expansion, a period of about 90 to 120 days (at a fruit diameter of about 2-6 cm for some varieties).

In discussing the international and interstate movement of citrus fruit, the

RMA noted that in 2004, India (where
Xac
is reported) shipped 8 metric tons of citrus to Ghana and 2 metric tons to South Africa, and that no outbreaks of
Xac
have been reported in any of the recipient countries. One commenter stated that the shipment of citrus from India to South Africa seems a dubious record.

These data were drawn from the Food and Agriculture Organization's “World trade and crop production statistics” database at
http://faostat.fao.org
. The commenter provided no further information establishing these records as dubious.

We also discussed the movement of fresh citrus from Florida during
Xac
outbreaks. One commenter asked whether the earlier shipments of Florida fruit were from canker-free areas, or at least canker-free areas of production under official control.

We noted in the RMA that these shipments of Florida citrus may have originated in areas of low prevalence or free of
Xac
. These shipments were required to originate in groves that had been certified to be free of
Xac
based on an inspection.

Comments on the Model in Appendix 1 to the RMA

As mentioned earlier, to assist in evaluating the options we identified for packinghouse-centered risk management, we prepared a quantitative model (Appendix 1 to the RMA) based on Florida production and shipping data to evaluate the efficacy of three levels of phytosanitary inspection in ensuring that fruit with visible canker lesions does not enter commercial citrus-producing States. The three inspection levels were determined by preliminary estimates of the Plant Protection and Quarantine program's Citrus Health Response Program staff of inspection levels that might be operationally feasible. The three inspection levels evaluated were 500 fruit per lot, 1,000 fruit per lot, and 2,000 fruit per lot. Statistically, randomized inspection of 500, 1,000 fruit, or 2,000 fruit per lot will ensure, with 95 percent confidence, that the proportion of undetected fruit with visible canker lesions in a cleared lot is no more than 0.75, 0.38, and 0.19 percent, respectively.

The outputs of the quantitative model were probability distributions. The model determined, with 95 percent confidence, that the total number of citrus fruit shipped from Florida to 5 citrus-producing States (Arizona, California, Hawaii, Louisiana and Texas) over a single shipping season would be 181,283,744 or less if unlimited distribution is permitted. The model determined, with 95 percent confidence, that the number of
Xac
-symptomatic fruit reaching those 5 States in a single shipping season would be 633,152 or less at the 1,000 randomly sampled fruit inspection level. We anticipate that about double that number (approximately 1,266,304 or less) of
Xac
-symptomatic fruit would reach those States at the 500 fruit inspectional level. About half that number (approximately 316,576 or less) would reach those States at the 2,000 fruit inspectional level. The model further determined with 95 percent confidence that the number of symptomatic fruit reaching citrus-producing areas within those States in a single shipping season would be 2,135 or less at the 1,000 fruit inspectional level, about double that number (approximately 4,270 or less) at the 500 fruit inspectional level, and about half that number (approximately 1,067 or less) at the 2,000 fruit inspectional level. (As discussed in Section 9.3.3.4 of Appendix 1 to the RMA, the actual acreage on which citrus is produced within a citrus-producing State is a small fraction of the total acreage of that State.) The base level inspection of 1,000 randomly sampled fruit per lot was adopted because it is operationally feasible with small adjustments to the current phytosanitary inspection process in Florida.

The potential for fruit with visible canker lesions to reach commercial citrus-producing States, coupled with the aforementioned uncertainty regarding fruit as a pathway, led to the determination that additional mitigations were required.

We received several comments from one commenter addressing the model in Appendix 1 to the RMA.

The commenter stated that the model failed to take into account the increased numbers of fruit that would be moved interstate from Florida and imported from citrus canker-affected areas in other countries, and thus underestimated the number of potentially infected fruit that could reach commercial citrus-producing States. The commenter cited another comment that estimated that the spread of canker has resulted in an additional 20 percent of Florida's total fresh citrus groves becoming ineligible for interstate movement under the regulations that were in place before the publication of this final rule. That 20 percent, that commenter stated, represents approximately 8 million 4/5-bushel cartons or an approximately $80 million potential business opportunity under the proposal.

The comment estimating the potential increase in fruit moved interstate under this final rule is dealt with in more detail under the heading “Comments on the Preliminary Regulatory Impact Analysis and Initial Regulatory Flexibility Analysis” later in this document. We have concluded that the increase in the number of fruit that will be moved interstate under this final rule is likely much less than the commenter estimates, although we have been unable to quantify the probable increase.

This final rule does not change our requirements for the importation of citrus fruit from areas in other countries where citrus canker is present. Therefore, this final rule will not increase the amount of fruit imported from such areas. As stated earlier in this document under the heading “Potential Application of the Packinghouse-Based APHIS Inspection System to Imported Citrus,” our analysis of the risk associated with the importation of citrus fruit from other countries where citrus canker exists under conditions similar to those in this final rule would be conducted separately from the analysis we conducted for the proposal and this final rule.

In Section 9.3.3.1 of Appendix 1, we determined probability distributions for the number of
4/5
-bushel cartons shipped per growing season for each commercial citrus-producing State destination and variety of fruit. To determine the probability distributions, we used the minimum, average, and maximum values of the last 4 years (2003 through 2006) of historical data on citrus fruit shipping from Florida to other commercial citrus-producing States.

One commenter stated that the last 4 seasons of data have been strongly affected by both natural events (damage caused by hurricanes, tree destruction in an attempt to eradicate the canker outbreak) and imposed movement restrictions (due to the canker outbreak). The commenter noted that over the 10 years preceding the 2003 through 2006 data, the average domestic shipping quantity was 1.6 times higher than it was during those years. The commenter stated that the uncertainty in the expected average number of fruit that will be shipped from Florida is therefore considerably higher than would be expected from examination of just the last four seasons, unless APHIS considers that the decline in numbers is a permanent feature of the Florida industry and the last four seasons are typical.

The amount of citrus moved interstate has declined steadily since the 1996-97

season, with a larger decline in 2004-05, when fruit production was affected by hurricanes. (See figure 1.)

ER19NO07.000

The trends and changes occurring in the Florida citrus industry suggest that the last four seasons are typical. The 2006 Commercial Citrus Inventory for Florida (USDA-NASS 2007) states the following about the 2-year trend for Florida citrus fruit production: “Florida's citrus acreage peaked again at 857,687 in 1996 but has been declining ever since. The 2006 total is 621,373, down 17.0 percent in a 2-year period noted for hurricanes, diseases, and urban development. The net change, a loss of 127,182 acres, is the greatest in any non-freeze period and 2nd overall. The Indian River District bore one-third of this loss. Removals out-numbered new plantings by a ratio of more than 5:1. The 23,623 acres of new plantings are the least recorded in any two-year period since 1970-71.” The last two sentences are especially germane to this discussion, as any reboun

[Text truncated at 120,000 characters. The full text is on the page linked above.]

---

Source: Frix Law Library, https://www.frixlaw.com/law-library/documents/fr%3AE7-22549. Public record. Not legal advice.