Australasian Plant Pathology, 2007, 36, 520–523 www.publish.csiro.au/journals/app

Managing plant diseases offshore

Jeanne M. VanDersal

USDA APHIS, Program Policy and Development, Risk Analysis Systems, Washington DC 20250, USA.Email: Jeanne.M.VanDersal@usda.gov

Presented as a Keynote Address at the 16th Biennial Conference of the Australasian Plant PathologySociety, 24–27 September 2007, Adelaide

Abstract. Managing exotic plant diseases and other potential pests imported into the United States (US) on incomingcargo is an on-going challenge for many countries including the US. The primary exclusionary strategy used by the USfor exotic pathogens is inspection of arriving cargo and passengers at ports of entry. In spite of these efforts, introductionsof many exotic pests have occurred through numerous ports of entry resulting in costly eradication efforts by Governmentand US industry. In an effort to moderate these risks, the US is focusing on offshore strategies. One offshore strategydeveloped first as a pilot project and currently as an ongoing project is known as the Offshore Pest Information System(OPIS). OPIS is a secure web-based information sharing tool that allows users to communicate in an organised mannerabout offshore plant and animal health events and issues. OPIS was designed to allow the US to quickly and effectivelyrespond to offshore plant pests that could potentially threaten the US.

Why was the Offshore Pest Information System (OPIS)developed?

Managing exotic plant diseases and other pests is an ongoingchallenge for many countries especially as international tradearound the world increases. In the past, the United States (US)has relied on inspection of arriving cargo and passengers atports of entry as a primary exclusionary strategy for exoticpathogens. However, international trade has been expandingat a more rapid rate than the human resources devoted toinspection at US ports of entry. Between 1998 and 2006,the US imported an average of nearly $47 billion worth ofagricultural products annually. The introduction of such pestsas Mediterranean fruit fly, citrus canker, Asian longhornedbeetle and other wood-boring insects and plant diseases throughnumerous ports of entry have resulted in costly eradicationefforts by Government and industry. Exclusion at the port ofentry is no longer sufficient to protect US plant resources. Aftera comprehensive review of the US plant and animal healthsafeguarding systems (USDA/APHIS/PPQ 1999), it was agreedthat in addition to our reliance on inspections at the port ofentry, the US could focus on offshore strategies such as: pestrisk mitigation in the areas of production; certification at thepoint of origin; preclearance activities at the port of export; andreliance on relevant information and other data on emerging andknown pest threats. The later offshore strategy, developed firstas a pilot project and currently as an ongoing project, is knownas the OPIS.

What is OPIS?

The OPIS project was designed to allow the Animal andPlant Health Inspection Service (APHIS) to quickly and

effectively respond to potential offshore plant pest threats.OPIS is a secure web-based information sharing tool thatallows users to communicate in an organised manner aboutoffshore plant and animal health events and issues. It isan effort to maintain a central repository where gatheredinformation about pest issues in foreign countries can bestored and reviewed by APHIS program officials (NAHSS2005). Access to this system is secured and primarily limitedto US government inspection entities; APHIS officials withinthe US and abroad, and program identifiers and researchers.OPIS is designed to allow the collection, reporting, analysisand communication of relevant offshore pest informationconcerning targeted pests that are not known to occur inthe US or are of limited distribution. There are four basicelements to this system: (i) collection of the information;(ii) reporting of the information to program officials;(iii) synthesis of the information; and (iv) communication ofthe information.

With the assistance of several professional scientific societiesand industry groups, APHIS has compiled an OPIS target pestlist. Approximately 100 of these pests have been identifiedas ‘priority’ targets and comprise insects, mites, pathogens,nematodes, molluscs and weeds that the cooperating groupsidentified as the most threatening to US plant and animal health.The OPIS pest list currently contains 17 diseases identified aspotentially dangerous to the US although they are not yet inthe country. They include: brown stripe downy mildew, citrusblack spot, citrus canker, Citrus greening, Citrus tristeza virus,downy mildew of corn, geminiviruses, Mal secco disease ofcitrus, Pierce’s disease, potato wart, rice bacterial leaf streak,southern bacterial wilt, sudden oak death, sweet orange scaband tospoviruses.

© Australasian Plant Pathology Society 2007 10.1071/AP07065 0815-3191/07/060520

Keynote Address CSIRO PUBLISHING

Managing plant diseases offshore Australasian Plant Pathology 521

APHIS already has a presence abroad in many countriesthrough International Services (IS), a unit of APHIS thatworks outside the US and plays a major role in ensuring theUS gathers and exchanges information on plant and animalhealth issues. IS has cooperated with foreign governments ina number of major surveillance and control programs in foreigncountries and has worked with these countries to establishpreclearance programs. Working with OPIS, IS-designatedemployees act as coordinators and play a more pronouncedrole overseas working cooperatively with foreign governmentsregarding information about geographic distribution of pestsabroad, new survey techniques, and control methods. Thesesafeguarding officers, called Animal, Plant Health Specialists(APHS), work collaboratively with local scientists, nationalplant protection personnel and others, to collect and shareinformation regarding the pest status of countries in their areaof responsibility. The program began as a pilot program in 2004and was implemented in three regions: Africa, South Americaand the Caribbean. These regions were chosen because oftheir proximity to the US, developing pest populations, andexistence of potential pathways identified by present or plannedtrading activities.

Foreign countries regularly collect information on thedensity and distribution of priority pests where they are knownto occur. Typically new detections of these organisms are alsomonitored and reported. Once this information is collected theinformation is communicated through the secure electronicsystem by APHIS safeguarding personnel. It is then evaluatedand reviewed by key scientists and policy making officialswithin APHIS to determine credibility of the information andits impact on American plant resources to determine necessarypest and disease risk management options. Working with theforeign government IS can assist the foreign country withpest and disease risk management options. These optionsmay include:

(1) initiating offshore pest management or risk mitigation,(2) organising early-detection surveys for these pests and

diseases in the US,(3) improving port-of entry inspection procedures, and(4) re-evaluating and/or revising existing phytosanitary

practices.

Who uses OPIS?

The information collected through OPIS can be utilised invarious capacities. US Custom and Border Protection inspectorsfrom the newly formed Department of Homeland Security, arecurrently performing the inspections at ports of entry in the USand they need to be aware of pest situations abroad in orderto focus their inspection activities on commodities entering theUS. State plant regulatory agencies also need similar informationto concentrate their domestic (in-country) pest surveys in areasmost at risk as identified by local pathway analyses. APHIS riskassessors and trade managers need to know what pest threatsexist offshore as they evaluate potential trade opportunities withcountries that may harbour pests of concern to the US. Whenadded to current practices, OPIS will strengthen ties with foreigngovernments and allow mitigative measures to be implementedquickly and more effectively in foreign countries, potentially

reducing costly shipping and other clearance delays for bothimporters and exporters.

One state within the US that is particularly vulnerable toexotic pathogens is our southern- most state of Florida becauseit has the most tropical climate of any state in the US. Thepopulation is ∼17 million with an estimated 1.25 million peopleworking in agricultural related jobs. These residents producebillions of market value of agricultural products or about 3–5%of the agricultural products of the US as a whole. Florida’stop commodities are: forestry products ($8 billion), greenhouseand nursery products ($1.6 billion), citrus ($1.17 billion), cane(for sugar) ($517 million), tomatoes ($508 million) and dairyproducts ($356 million). With 15 air and sea ports, Florida servesas the first point of entry to the US mainland for many productsand passengers from foreign countries. Once introduced, Floridais especially vulnerable to pest establishment because of itsfavourable year-round climate and abundance of horticulturalhosts. A recent study by Klassen et al. (2002) reported that from1986 through 2000, some 150 exotic arthropod species becameestablished in Florida.

Examples of exotic diseases introduced to Floridain recent years

Bean golden mosaic virus (BGMV), a whitefly-transmittedgeminivirus, was widespread throughout the Greater CaribbeanBasin by 1990 (Brunt et al. 1990). BGMV appeared in southFlorida immediately after the passage of Hurricane Andrew on24 August 1992. For several years, until control measures couldbe developed, the yields of entire fields of bush and pole beanswere lost to damage caused by this whitefly-transmitted virus.

Another disease that causes a reduction in yield as well aspostharvest damage to and loss of fruit is Black Sigatoka, adestructive foliar disease of banana. It is caused by a leaf spotfungus, Mycosphaerella fijiensis (anamorph: Paracercosporafijiensis). This pathogen was first described from Fiji in 1963,but by 1972 it had spread to the Western Hemisphere (Honduras)in the Caribbean Basin and subsequently throughout the entireCaribbean Basin. Black Sigatoka was first reported in the USin Florida in 1998 (Ploetz and Mourichon 1999). According toPloetz (2001), it is now estimated that about 25–40 fungicidesprays per season are needed to combat this disease in bananaproduction.

Examples of plant pathogens and/or diseaseson the current OPIS pest list

Citrus black spot is a citrus disease caused by the fungus,Guignardia citricarpa (anamorph: Phyllosticta citricarpa), andit is not present in the US. Previous records of occurrencesof Guignardia on citrus in some countries involved a non-pathogenic species of Guignardia. In 2003, this non-pathogenicstrain was confirmed as belonging to a distinct species,G. mangiferae. Therefore, records in many countries oncethought to have had this widely distributed pathogen werechanged to ‘absent, never occurred’ in CABI (CABI 2006).The current distribution lists G. citricarpa in five countries inAsia: Bhutan, China, Indonesia, Philippines and Singapore; twocountries in South America: Argentina and Brazil; three states inAustralia: New South Wales, Victoria and Queensland; and five

522 Australasian Plant Pathology J. M. VanDersal

countries in Africa: Kenya, Mozambique, Zambia, Zimbabweand South Africa (restricted distribution).

This pathogen usually first appears on, and is spread by, leafinfections. Young fruit are most susceptible, but usually do notshow symptoms at this stage. The fungus can remain dormant for4 or 5 months until the fruit matures before black spots actuallydevelop. It is sometimes difficult to identify G. citricarpa withcertainty unless pycnidia are present in the lesion. The diseasecauses external blemishes which make fruit unsuitable for thefresh fruit market. APHIS restricts the movement of fresh fruitin areas from countries where this pest occur.

Sweet orange scab is another citrus disease of concern to theUS caused by the fungus, Elsinoe australis. Symptoms of thisdisease are often confused with another scab, Sour orange scab,caused by E. fawcetti. Both of these scab diseases affect theexternal quality of fruit and are found only on young citrus fruit.E. australis does not infect the leaves of any citrus species andis found only affecting the fruit; typically when young and notmore than 20 mm across in size according to CABI. Sour orangescab, however, is often found infecting leaves and these leavesserve as a source of inoculum for future infestations. Inoculumfor new infections consists of conidia, and possibly ascospores,from scabs formed on fruits. Conidia are formed abundantlyon wet scabs, in a nearly saturated atmosphere, between20 and 28◦C.

The temperature range required for germination of conidiais narrow according to studies by Whiteside et al. (1988), andinfection does not take place below 14 or above 25◦C. Survivalof the pathogen occurs in scab pustules on fruits remainingon the tree, thus providing the inoculum for the next season.Dissemination of the pathogen is mostly by rain (or irrigationwater), although insects and, to a certain extent, wind-carriedwater droplets containing spores may contribute to the spreadof the pathogen. In international trade, the pathogen can becarried on infected nursery stock, ornamental citrus plants,and fruits.

CABI does not list this disease as occurring in China,although there have been about 20 interceptions of this diseasereported in the US on incoming cargo and/or baggage fromChina (probably on dried peel). Several Pacific Islands (TheCook Islands, Fiji, Niue and Samoa) are listed in CABI ashaving Sweet orange scab ‘present with no further details’. Itis also reported from Argentina and Brazil. APHIS restrictsthe movement of fresh fruit from areas in countries where thispest occur.

Ralstonia solanacearum race 3 biovar. 2 is a bacterialpathogen not known to occur in the US that causes the diseasein known as southern wilt, bacterial wilt and brown rot of potato(USDA/APHIS/PPQ 2003). This soilborne pathogen persists indeep, wet soils and reservoir plants. It causes a wilt disease inseveral important agricultural crops such as potatoes, tomatoes,peppers and eggplant. Its distribution in potato fields can bespotty, and it is commonly found in areas that have poor drainage.Potatoes are a sizeable economic crop for the US with productionin 36 out of 52 states; 20.7 billion kilograms per year with avalue over $2.6 billion. This disease is of special concern to thepotato industry in the US because race 3 is a cold-temperaturetolerant strain that has caused serious disease problems inpotato crops in other temperate countries around the world that

share a similar climate with parts of the US where potatoesare grown.

R. solanacearum race 3 biovar 2 can only be transmittedthrough irrigation water, contaminated soil, equipment, orpersonnel working with infected material. For example, it maybe spread by propagating infected plants, taking cuttings withoutdisinfecting cutting implements between plants, pinching budsof infected plants without hand sanitation, and especiallyby shared water irrigation systems. Therefore, the currentmitigation measures implemented in foreign countries where thisdisease is known to occur, address these specific pathways. Manyoffshore mitigation measures have been applied to greenhousesin countries where this disease is known to occur and products,particularly geraniums that could carry this pathogen, areexported to the US. Since there is no available treatmentfor plants infected with R. solanacearum race 3 biovar 2,infected geraniums must be destroyed to prevent the spread ofthe disease.

Introductions in greenhouse production geraniums occurredin several states within the US in 2003, introduced fromKenya, and 2004, introduced from Guatemala, but were bothsubsequently eradicated. Geranium imports into the US arecurrently allowed from foreign countries with this diseaseunder control and with the new implemented risk managementstrategies for this pathogen.

Bursaphelencus cocophilus, formerly known asRhadinaphelenchus cocophilus (red ring nematode) (Agrios1997), is vectored by the palm weevil, Rhynchophoruspalmarum, and causes the fatal disease known as Red ringdisease of coconut. Larvae of R. palmarum feed by burrowingthrough coconut stems and, when this occurs in trees which areinfected with B. cocophilus, the larvae can become inoculatedwith the nematode. Adult weevils emerging from trees infectedwith B. cocophilus carry the nematode to new sites.

B. cocophilus infestation occurs more commonly in trees2.5–10 years old, with greatest incidence in those 4–7 years old.Occasionally, a palm as young as 1.5 years or more than 20 yearsold may be attacked. The major palm hosts are Cocos nucifera(coconut palm) and Elaeis guineensis (African oil palm); theminor hosts are Phoenix canariensis (Canary Island palm),Phoenix dactylifera (date-palm) and Sabal palmetto (Cabbagepalm). B. cocophilus is a potential phytosanitary risk on coconutsin all tropical countries, especially where the palm weevil,R. palmatus, is known to occur.

Major crop losses of coconut plantations occur and youngcoconut palms easily succumb to B. cocophilus attack andinfestation by B. cocophilus. There is no record of any tree,once affected, having recovered. The disease is not recognisableexternally in its very early stages and the roots, stems and leafpetioles are already infested before the first external symptomsbecome visible. In young coconut plants, B. cocophilus has beenseen invading tissues in the roots, stems and leaves. At first, thenematodes occur as intercellular parasites but later they can befound both intercellularly and intracellularly in newly invadedtissue. In some cases, as many as 10 000 nematodes have beendiscovered in only 1 g of such tissue.

The Red ring nematode has been reported from areas inCentral America, South America, many Caribbean Islands andMexico. Although B. cocophilus and R. palmarum are not found

Managing plant diseases offshore Australasian Plant Pathology 523

in Florida, some other potential beetle vectors of the Red ringnematode – Metamasius hemipterus and R. cruentatus – arecommon in Florida. If this nematode were introduced to Florida,it could threaten the ornamental palm industry in Florida and is,therefore, a concern to APHIS.

Mutual benefits of this program

A vital component of the APHIS safeguarding mission isinfrastructure building through technical assistance. APHISis frequently asked to provide technical expertise at regionalworkshops. An important role of the APHS personnel is toassist the area office in supporting and coordinating trainingand lending other assistance that would strengthen safeguardingsystems and build plant and animal health awareness. Many ofthese activities are conducted in collaboration with internationalorganisations, other agencies of the US government, andlocal and US academic entities. APHIS experts impart ‘handson’ training to foreign counterparts ranging from conductingcommodity risk assessments which allow countries to makeregulatory decisions based on science to pest detection andsurvey activities such as fruit fly surveys. This enhancednetworking capability enables the APHS personnel to betterunderstand how countries manage surveillance and incursionresponses, and how key decisions are made in-country and bywhom.

In several countries resources are inadequate for screening oridentifying intercepted pests. Conducting research and trainingactivities in these foreign countries and sharing availableresources such as pest identification keys, data sheets, orother diagnostics assistance will help our foreign cooperatorsrecognise suspect organisms.

Summary

OPIS is a real-time web-based tool for gathering informationabout changing pest and pathway conditions. OPIS allows securereporting of plant health issues together with an ongoing analysisof developing situation in trading partner countries. It enablesthe US to work together with foreign countries to suppressoutbreaks, assist with research and develop strategies to betterdeal with potential plant pest issues while maintaining ongoingtrade. OPIS will assist in making operational, regulatory, andpolicy decisions about exotic pest issues.

The best way to limit the impact of invasive species and exoticpest and diseases is to prevent them from invading and becomingestablished in new areas. OPIS will enable APHIS to assistwith identifying emerging plant pest issues offshore before theybecome established in the US. In this complementary approachto exclusion, the identification and reporting of pests in thecountry of origin could become a standard operating procedure.The information assembled in the web-based system, known asOPIS includes the data gathered that provides information onpotential risks so that adequate resources can be focussed atspecific ports of entry and other vulnerable areas of concern,or that other mitigations can be evaluated and implementedin advance of arrival into the US. It is anticipated that suchan approach could ultimately reduce the likelihood of pestoutbreaks and establishments in the US.

References

Agrios GN (1997) ‘Plant pathology.’ 4th edn. (Academic Press: New York)Brunt A, Crabtree K, Gibbs A (eds) (1990) ‘Viruses of tropical plants.’ (CAB

International: Wallingford, UK)CABI (2006) ‘Crop protection compendium.’ (CAB International:

Wallingford, UK)Klassen W, Brodel CF, Fieselmann DA (2002) Exotic pests of plants: current

and future threats to horticultural production and trade in Florida and theCaribbean Basin. Micronesica 6(Suppl.), 5–27.

NAHSS (2005) National Animal Health Surveillance System (NAHSS)Outlook August. Available at http://nsu.aphis.usda.gov/outlook/[Verified 30 August 2007].

Ploetz RC (2001) The most important disease of a most important fruit.Available at http://www.apsnet.org/education/feature/banana/top.html[Verified 30 August 2007].

Ploetz RC, Mourichon X (1999) First report of black Sigatoka in Florida.Plant Disease 83, 300. doi: 10.1094/PDIS.1999.83.3.300C

USDA/APHIS/PPQ (1999) ‘Safeguarding American plant resources –a stakeholder review of the APHIS-PPQ safeguarding system.’ conductedby the National Plant Board at the request of USDA/APHIS/PPQ.

USDA/APHIS/PPQ (2003) Pest data sheet: Ralstonia solanacearumrace 3 biovar 2. Available at http://www.aphis.usda.gov/planthealth/plant pest info/ralstonia/index.shtml [Verified 4 October 2007].

Whiteside JO, Garnsey SM, Timmer LW (1988) ‘Compendium of citrusdiseases.’ (American Phytopathological Society: St Paul, MN)

Manuscript received 16 August 2007, accepted 27 August 2007

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