Review
International
variation
in
phytosanitary
legislation
and
regulations
governing
importation
of
plants
for
planting
R.
Eschen
a,*
,
K.
Britton
b,
E.
Brockerhoff
c,
T.
Burgess
d,
V.
Dalley
e,
R.S.
Epanchin-Niell
f,
K.
Gupta
g,
G.
Hardy
d,
Y.
Huang
h,
M.
Kenis
a,
E.
Kimani
i,
H.-M.
Li
j,k,
S.
Olsen
e,
R.
Ormrod
l,
W.
Otieno
m,
C.
Sadof
n,
E.
Tadeu
o,
M.
Theyse
paCABI,Ruedesgrillons1,2800Dele´mont,Switzerland
bForestServiceResearch&Development,USDAForestService,1400IndependenceAveSW,Washington,DC20250,USA cScion(NewZealandForestResearchInstitute),POBox29237,Christchurch8540,NewZealand
dCentre for PhytophthoraScienceand Management,School ofVeterinaryand LifeSciences, MurdochUniversity,
Murdoch,WesternAustralia6150,Australia
ePlants,Food&EnvironmentDirectorate,MinistryforPrimaryIndustries,POBox2526,Wellington,NewZealand fResourcesfortheFuture,1616PStreetNW,Washington,DC20036,USA
gDivisionofPlantQuarantine,NationalBureauofPlantGeneticResources,NewDelhi110012,India
hPestRiskAnalysisGroup,InstituteofPlantQuarantine,ChineseAcademyofInspectionandQuarantine(CAIQ),Beijing,
China
iKenyanPlantHealthInspectorateService,POBox49592-00100,Nairobi,Kenya jMoA-CABIJointLabforBio-safety,InstituteofPlantProtection,Beijing100193,China kCABI,ZhongguancunNandajie12,InternalPostBox56,Beijing10080,China
lPlantHealthandBiosecurityPrograms,CanadianFoodInspectionAgency,1853BredinRoad,Kelowna,BCV1Y7S9,
Canada
mCABI,LimuruRoad,PlotNo9–CanaryBird,Muthaiga,Nairobi,Kenya
nDepartmentofEntomology,PurdueUniversity,SmithHall,901WestStateStreet,WestLafayette,IN47907-2089,USA oEmpresa BrasileiradePesquisa Agropecua´ria (Embrapa),Estrada daRibeira, Km 111Bairro Guaraituba,CEP:
83411-000Colombo,PR,Brazil
pFreshProduceImportersAssociation,POBox27019,Gezina0031,SouthAfrica
a
r
t
i
c
l
e
i
n
f
o
Keywords:
Internationaltrade Liveplants
Invasiveinvertebratepests andmicrobialpathogens
a
b
s
t
r
a
c
t
Thetradeinplantsforplanting(P4P)isoneofthemajorpathwaysfortheintroductionof pests.Thestrongincreaseinworldtradeinthepastdecadesappearstohaveledtoan increaseinintroductionsofspeciestransportedbythispathway,andhighlightstheneedfor effectivephytosanitarylegislationandmeasures.Thephytosanitaryregulationsinmost countriesarebasedontheInternationalPlantProtectionConventionandtheWorldTrade Organisation’sAgreement onSanitary andPhytosanitary Measures,but thereare large
*Correspondingauthor.Tel.:+41324214887;fax:+41324214871. E-mailaddress:[email protected](R.Eschen).
Available
online
at
www.sciencedirect.com
ScienceDirect
journalhomepage:www.elsevier.com/locate/envsci
http://dx.doi.org/10.1016/j.envsci.2015.04.021
1.
Introduction
There is increasing evidence that international trade, in particular the trade in live plants for planting (P4P, syn. nurserystock),isamajorpathwayfortheintroductionofalien plantpests(both arthropodpestsand microbialpathogens;
Worketal.,2005;Kenisetal.,2007;Liebholdetal.,2012;Santini etal.,2013).ThetradeinP4Pcontinuestoseeastrongincrease involume(Liebholdetal.,2012;Eschenetal.,2014),aswellas shifts in the origins of the plants, due to moving nursery operationstocountrieswhereproductioncostsarelowerand theimportationofretail-readyplants.Forexample,European importsofP4PfromChinahaveincreasedfivefoldoverthe pasttenyearsandarenowonaparwiththevolumeimported fromNorth America,which remained static(Eschenet al., 2014). Concomitant with increasing tradewill be a similar increaseininvertebrateplantpestsandinfectivepropagules ofplantpathogens(Liebholdet al.,2012;Brockerhoffetal., 2014).Thereis,therefore,anurgentneedtounderstandthe efficacyofexistingmeasuresandwhatmeasuresareneeded toreduceandmitigatetheriskofintroducingpeststhrough intercontinentaltradeinP4P.
National legislationand regulationsare fundamental to providingtheregulatoryframeworkforprotecting agricultur-al,forest andother plantresources fromalien pests,or to managesuchthreats.Thereareanumberofpossibilitiesto mitigatethe introduction of quarantine pestsvia trade by effective implementationof regulations, such as measures to ensure low pest prevalence in the exporting country, treatmentof consignments,importing dormant plantsand restrictingimporttospecificseasons,sizes,orplantcondition. Ifsuchmeasuresdonotreducetherisktoanacceptablelevel, importoftheaffectedcommoditiesisprohibited.Theseand other measureshave been adoptedin nationallegislations world-wide.Phytosanitarylegislationandregulationcanbe effectiveinreducingtherateofpestestablishments(Roques, 2010;Hlasny,2012),butthemeasuresprescribedinnational legislationsvaryand it wouldbevaluable toidentifythose partsoflegislationsandregulationsmosteffectiveinreducing risk.
The legislation concerning the management of risks associatedwiththeimportofP4Pandtheassociateddispersal of pests and diseases is, in most countries, based on
international treaties and conventions (MacLeod et al., 2010),inparticulartheInternationalPlantProtection Conven-tion (IPPC; FAO, 1997) and the WTO Agreement on the Application of Sanitary and Phytosanitary Measures (SPS Agreement; WTO, 1995). The IPPC stipulates the use of phytosanitarycertificatesandtherightofcountriestoregulate theimportofcertainplantspeciestoavoidentryofpests,to inspect or quarantine specific consignments and to define whichpestspeciesarenotallowedtoenterthecountry.The SPS Agreement stipulates that countries have the right to decide their own level of acceptable risk, and to apply phytosanitarymeasures asrequiredtoprotectplantlifeor health,aslongasthesedonotdiscriminateagainstcertain countries or foreign commodities and have the minimal necessaryimpactontrade.Moreover,anylimitsontradeset under the SPS Agreementhave to bebased on science or internationalstandards,suchastheInternationalStandards on Phytosanitary Measures (ISPMs) set bythe IPPC (except forprovisionalmeasures).
TheRegionalPlantProtectionOrganizations(RPPOs)were created as regional organisations of the IPPC and are a platform for regional collaboration and in some cases coordinateharmonisationonphytosanitaryissuesand devel-opscience-basedphytosanitarystandardsfortheirrespective regions.Ultimatelysomeregionalstandardsforphytosanitary measuresareadoptedbytheIPPCasISPMsandhaveaglobal reach.Forexample,ISPM36(Integratedmeasuresforplants forplanting,FAO,2012)wasinitiatedastheNorthAmerican PlantProtectionOrganization’sRegionalStandardfor Phyto-sanitary Measures 24 (Integrated Pest Risk Management Measures for the Importation of Plants for Planting into NAPPO Member Countries, NAPPO, 2013). Although ISPMs arenotlegallybindingundertheIPPC,WTOMembersshall basetheirsanitaryorphytosanitarymeasureson internation-al standards, guidelines or recommendations, where they exist(WTO,1995).
The majority of countries aremembers of the WTO or contractingpartiestotheIPPC,andcanbeexpectedtocomply withtheirrespectiveobligations,buttheyhaveverydifferent approaches to ensuring phytosanitary safety. A country’s regulatorydesignconsistsofaregulatoryframework (phyto-sanitary legislations, regulations and procedures) and a NationalPlantProtectionOrganisation(NPPO)thatis responsi-bleforoperatingtheregulation(FAO,2004b).Theinternational differences incountries’approaches tomanagingtheriskofintroducinginvasivealien species through international planttrade. We reviewed elements ofthe phytosanitary legislationsoftencountriesonallcontinentsandaimedtofindregulationsthatprevent biological invasions.We foundlargedifferencesincountries’phytosanitaryregulations. New Zealand and Australia have the strictest phytosanitary regulations, while Europe maintainsageneralauthorizationforP4Pimports.Theremainingcountrieshaveregulations betweentheseextremes.Theevidenceissparseregardingthequalityofimplementation andeffectiveness,andimpactofindividualphytosanitarymeasures.Werecommendthat NationalPlantProtectionOrganisationscollectdetailedinformationonP4Pimportsandthe effectivenessofphytosanitarymeasures.Suchinformationcouldprovideabasistoimprove acountry’sphytosanitaryregulatoryframeworkorcouldbeusedinriskassessments.
#2015ElsevierLtd.Allrightsreserved. Legislation
IPPC ISPM
differencesinregulatorydesignsresultfromdifferencesinthe regulatoryframeworkandapproachestoriskmanagement.As asimplification,countriescanbedividedintothosethatallow liveplantimportsuntilaknownpestthreatisidentifiedanda riskanalysisjustifiesregulation(‘‘blacklist’’)andcountriesthat onlyallowentryofcommoditiesthathavebeenassessedand areconsideredsafe(‘‘whitelist’’).Thisdividescountriesroughly into(1)thosemanagingtheriskofknownharmfulorganisms, byidentifyingblacklistsofrestrictedpeststhataredeemedso harmfulthattheymustnotenterthecountry,and(2)countries managingriskbyidentifyingsafe,authorizedcommoditiesor pathways,aswellastypicallylongerlistsofnon-authorized pests (Table1). Inother words, the distinction isbased on whethersomethingcannotbeimportedbecauseitisprohibited (basedonariskanalysis)orwhetheritisnotauthoriseduntil aprocessofevaluationcanbecompleted.
An internationalreview of approaches to phytosanitary safetymayinformthedevelopmentoflegislationandpolicy tohelpcountriesreducepestriskviaP4P,butweareunaware ofsuchreviewinpeer-reviewedliterature orreports. Here, weprovideanoverviewofmeasuresthatcanbeimplemented tolimittheintroductionofnon-nativepeststhroughtradein P4P and illustrate the measures with examples from the UnitedStatesofAmerica(USA),EuropeanUnion(EU),South Africa,India, NewZealand,Australia,Brazil,Canada,China and Kenya. The Electronic Supplement contains a list of consultednationalandinternationallegislativetexts.These
countries were selected to cover arange oforganisational complexity,theapproachtophytosanitarysafety,aswellas tocoverbothprimarilyimportingandexportingcountriesand torepresent allcontinents. Wedescribedifferences among countriesandtheapparentreasonsforinternationalvariation inphytosanitaryregulatorydesign.Wealsodiscussevidence for transport ofregulated organisms and the effectiveness of phytosanitarymeasuresto reducethe number of trans-portedpests.
1.1. Importpermits
Countries can issuea general authorisation forthe import of P4P or may demand an import permit with specific requirements orofficialconsent thatauthorisestheimport ofplantsofparticulargeneraororigins(FAO,2004b).TheIPPC encourages general authorisations to be developed when similar specific authorisationsare requiredfor many com-modities(FAO,2004b).However,theEUistheonlyregionin ourcomparisonthatmaintainsageneralauthorisationforP4P importsanddoesnotuseimportpermits(Table2).Mostother countries require individuals or companies that wish to importP4Ptoapplyforanimportpermit,oftenirrespective ofgeneraororigins.
Thepurpose,validityandcostofthepermitsvarywidely among countries. The application for import permits can provide useful information about the plants intended for
Table2–Summaryofthemeasuresstatedinregulations,arrangedbycountry.Thatameasureisrequiredforalllive plantsimportsisindicatedwith+andmeasuresthatarenotrequiredatallareindicatedwithS.Hashsigns(#)indicate
thatadditionalmeasuresarerequiredforspecificgenus–origincombinations.InEurope,pathwayriskanalysesare carriedoutinexceptionalcases,bytheEuropeanandMediterraneanPlantProtectionOrganisation.
New Zealand
Australia USA Canada India China Brazil Kenya South Africa
EU
Phytosanitarycertificate + + + + + + + + + +
Importpermit + + + + + + + + +
Importinspections + + + + + + + + + +
Pathwayriskanalysis + + # + + + + # #
Nocontaminants/soil # # # + # + + + # #
Pre-exporttreatments + + # # # # + # # #
Pestfreearea # # # # # # # # # #
Pestfreeproductionsite # # # # # # # # # #
Shippinginspecificseason # + # # #
Post-entryquarantine + + # # # # + # # #
Table1–Summaryofnumberofregulatedpestsindifferentcountries.Countriesareorderedalphabetically.Notethat KenyaandSouthAfricahavenotissuedalistofregulatedorganisms.AustraliaregulatesOrders,ratherthangeneraor speciesandinAustraliaandNewZealandinspectorsmusttreatunidentifiedorganismsasregulatedorganisms.Brazil includesphytoplasmasinprokaryotes.
Blacklist Whitelist
Brazil Canada China EU India USA Australia NewZealand
Arthropodsandnematodes 243 82 146 110 517 101 – 9,442
Molluscs 0 12 6 0 4 0 – 34
Prokaryotes 27 10 79 19 104 16 – 296
Fungi 110 46 125 37 281 56 – 4,232
Phytoplasmas 0 10 0 0 19 20 – 126
Virusesandviroids 43 63 40 67 226 83 – 820
Diseases 0 0 0 0 2 0 – 107
import.Thiscanmotivateregulatorstocarryoutapathway riskanalysis ifthe applicationconcerns anew commodity or pathway (e.g. genus–origin combination), to decide on whetheradditionalphytosanitarymeasuresforcommodities or consignments are necessary, or to prohibit import if deemednecessary.Anumberofcountries,includingChina, Canada, Kenya and Brazil perform pathway risk analyses whenimportersapplyforimportpermitsfornew commodi-ties. The USA uses import permits as a means to inform importers of regulations and requirements related to the importedcommodityandservesasabasisforlegalactionif regulationsarebreached.IntheUSA,permitsfortheimport ofplantsofaspecifiedspeciesfromoneoriginareissuedfora periodoffiveyearsandinCanadaforaperiodofthreeyearsin themajorityofcases.Thisdiffersfrommostothercountries, wherepermits areissued forindividualshipments. Permits areissuedfreeofcosttotheapplicantinChinaandtheUSA, butthecostofapermitisRs300inIndia(atthetimeofwriting ca.s3.5),KSH600inKenya(ca.s5),$166.62inNewZealand(ca. s102)and$185.00inAustralia(ca.s125).
1.2. Pestriskanalysisandpathwayriskanalysis
Theaimofriskanalyses,carriedoutonpestsorpathways,isto determinewhethertheriskposedbyapestorpathwayissuch that it requires regulation and what measures would be effectivetomitigatetheserisks(FAO,2004a,2007a,b). Such measuresmaythenbeprescribedinlegislation,regulations,or bilateralagreementsasaconditionforentryofacommodity orforapathway.Inthecasewherenomeasuresareidentified thatwouldensureanacceptablelevelofrisk,acountrymay decide to prohibit entry of the identified commodity. For example,the EU hasprohibited the importof Populusspp. plantswithleavesfromNorthAmericancountries(AnnexIII, partAinAnonymous,2000),Chinahasprohibitedtheimport ofPinusspp.fromDPRKorea,Japan,France,Canadaandthe USA(Anonymous,2007),andKenyahasprohibited importa-tion offruitsand fruittrees fromChina, Japan, Koreaand Manchuria(Anonymous,1961).
Pest risk analyses are a common basis for establishing quarantinepestlists,butincaseswheretheyareonlycarried outonorganismsthatareknownorsuspectedtobeharmful, theypoorlycontributetothemitigationoftheriskposedby unknown,poorlyknownorunderestimatedpests(Simberloff, 2005; Kenis et al., 2007). A good pest risk analysis should captureandhighlighttheuncertaintyassociatedwithpoorly knownorunderestimatedpestsandcanbeperformedwell, evenifbasedonlittleorunreliabledata(SequeiraandGriffin, 2014). Pathway risk analysis may be a more appropriate approachforimportedcommoditiessuchasP4Pthan pest-by-pestriskanalysis,asdifferentcommoditieswillhavedifferent risksforthesamepestsandasinglecommoditymaybea potentialpathwayformanypests(Evans,2010).
IntheEU,riskanalysesaregenerallybasedonsinglepests; oftenthosethathavejustenteredEUcountriesorareinvading other continents. In contrast, many other countries and regions carry out pathway risk analyses on all new plant commoditiesbeforeallowingtheirimportation (Table 2). In addition,somecountriescarryoutapreliminaryriskanalysis onunexpectedandunknownpestsfoundduringinspections
attheportofentry(POE)andcometoaquickdecisionabout thereleaseofaconsignmenttotheimporteroraboutrequired provisionalmeasures.Afullriskanalysismustbecarriedout at a later date to satisfy the requirements of the SPS Agreement. Thevariationinthenumber ofregulatedpests (Table1)mayinpartbeduetothisdifferenceinapproachto risk analysis, the national plant health regulations or the NPPO’sappetiteforrisk.
TheUSAhasrecentlyintroducedanewregulatorycategory forP4P,NotAuthorisedPendingPestRiskAnalysis(NAPPRA; Fed.Regist.319.37-2a)aspartofatransitionfromablacklist approachtoawhitelistapproachfornewcommodities:new pathwaysaresubjecttoriskanalysispriortoadecisionon whether to allow import and identification of additional importrequirements.Ineffect,anycountrythatrequiresrisk assessment prior to issuance of import permits for new pathwayshasNAPPRAinplace.
1.3. Pestfreeareaandpestfreeplacesorproductionsites
Ifapestdoesnotoccur,orisveryrareinaregionorproduction sitethenthechanceofaconsignmentbecominginfestedmay benegligible.However,ifapesthasbeenrecordedfrompart of a country, the importing country may require that the exporting countries provide evidence that the area of productionisfreeofthepestofconcern(FAO,1995).Excluding thepestofconcernfromtheproductionsitecaneffectively manage the risk of some pests through, for example implementationofscreensorotherphysicalbarriers,cultural methods,orgeneralsitehygiene(FAO,1999).Therecognition of pest free areas is an administrative process involving the exporting and importingcountry, but the NPPO of the exportingcountryisresponsibleformaintainingsurveillance ofpestfreeareas(FAO,2009b).Pestfreesitesofproduction areestablishedbyproducersincompliancewiththe require-mentsoftheexportingcountry’sNPPO.Thepest’sabsencecan bedemonstrated,forexample,throughtrappingorsurveys, forwhichtheNPPOisresponsible(FAO,1999).Manycountries usepestfreerequirementstomitigaterisksassociatedwith specificpathways,andthedifferencesdependontheoutcome ofriskanalyses.
1.4. Shippinginspecificseasonsorplantgrowthstages
Pests anddiseases havethe bestchances ofestablishment if the climates in the importing and exporting countries aresimilar and seasonallyaligned.Limiting importationto particularseasonsmaylimittheprevalenceofparticularpest types,suchasleaf-feedinginsectsorsomefoliarpathogens, ondormantplants.However,therisksmaybeloweror less-easilyidentifiableiftheseasonsinexportingandimporting countries areasynchronous, forexample if the plants are moved in spring or autumn between climatically similar regionsontheNorthernandSouthernhemispheres.
The EU requires that plants of certain genera, such as
growingmedia,allofwhichmustbegrownunderasystems approachanddonotincludedeciduousspeciesorspecieswith true dormancy, have been actively growing and protected frompeststhroughphysicalexclusionstructuresintheperiod priortoexport(7CFR319.37-8).Theaimofthisrequirement istoincreasethelikelihoodofdetectingpathogensandother inconspicuouspests.TheNewZealandStandardfor Importa-tion of Nursery Stock stipulates that the plants must be activelygrowingthroughoutthepost-entryquarantineperiod (Anonymous,2012),againaimedatoptimisingthechancesof detectingdiseasesymptoms,butsomehorticultural commod-ities, such as Malus, Prunus and Vitis, are required to be importedinadormantstate.KenyaandSouthAfricadonot have measures based on differences in growingseason or climate with exporting countries and restrictions on the seasonofimportisseldomusedinChinaasitisalargecountry witharangeofclimates.
1.5. Importofsoil
In a phytosanitary context, soil is considered a high risk because of the pathogens, cryptic insect life stages and nematodesthatitcancontain,butitmayalsocontainseeds or root fragments that may allow the establishment of unwanted plants and the presence of soil makes the inspectionofplantsmoredifficult.Mostcountriestherefore prohibittheimportofsoil,withpotentialexceptionsmadefor importsforscientificpurposes.Manycountriesalsoprohibit theimport ofplantswithsoilattached. Plants insterilized mediausuallyareacceptable.
The USA distinguishes soil from growing media and packing material. For instance, soilis not allowed (except fromCanada);rootedcuttings maybeshippedbarerootin sawdustasanapprovedpackingmaterialbut itbecomesa growingmedium and is regulated differentlyif the plants areestablishedinthesawdust.NewZealandrequireswhole plants(includingcuttings) that have been grownin soilto bedipped inFenamiphos prior toexport, or an additional declarationthatthewholeplantswereraisedforseed/cuttings insoil-lessmediaincontainersmaintainedourofcontactwith thesoil.TheEUandsomeother countries,includingIndia, allow enough soil to sustain the plants during transport. Moreover,thevolumeofsoilattachedtoimportedtreescan besubstantial,thusdramaticallyincreasingthechanceofit harbouringunwantedpestsorpathogens.InEurope,where thereisnolimitonthesizeofimportedplants,sometreesare importedwithmorethanahundredlitresofsoilandineffect anentireecosystemisbeingtransplanted.
1.6. Treatmentofplantspriortoexportoratentryinto theimportingcountry
Measuresaimedatreducingthepresenceandprevalenceof pestsonP4Pintheexportingcountry,i.e.preventingentryinto thepathway, aremoreeffectiveandprovide ahigherlevel of safety than management of pests that have arrived or established inthe importingcountry. Chemicalor physical treatmentsorcombinationsthereofcaneffectivelypreventor lowerthe risk ofinfestationofplants, but therearefewer options available for treating P4P once they are infected.
Fumigationandpesticidetreatmentscanandareapplied,but these may not be effective against pests living inside the plants.Heatorcoldtreatments,whichareusedtotreatother commoditiessuchasfruitsorwood,arenotassuitableasthey maydamagetheplants,inparticularsmallplants.
NewZealandrequireschemicaltreatmentofliveplantsin theexportingcountrypriortoshipping.Alllivenon-dormant plantsmustbesubmergedinabathcontainingtwoinsecticides andacaricideseachofdifferentchemicalclasses;fumigation (forexamplewithmethylbromide)isrequiredforsomespecies totargetscaleinsectsincaseswheredipshavebeenshownto notbeeffective.Treatmentwithfungicidesisprohibited,asthis canmerelysuppresssymptomsandmakeitmorelikelythat pathogensgounnoticedduringinspections,withtheexception ofsomemandatoryfungicidetreatmentsforrootrotsandrusts (e.g. Section2.2.1.8 ofAnonymous,2012).Australia requires fumigationofallliveplantsusingmethylbromidepriortoentry into the country, which is done after inspection. We are unawareofasimilarrequirementforchemicaltreatmentsof allP4Pelsewhere,althoughsomecountriesrequiretreatment forspecificpathways.
1.7. Phytosanitarycertificates
AcommonrequirementforimportofP4Pisaphytosanitary certificate, with which the NPPO of the exporting country certifiesthatinspectionpriortoexporthasestablishedthatall the requirements of the importing country are met and, optionally, thattheconsignmentispracticallyfreeofthose peststhatareregulatedbytheimportingcountry(FAO,2011). All countries in our comparison require shipments of live plantstobeaccompaniedbyaphytosanitarycertificate.
1.8. Post-entryquarantine
Phytosanitaryinspectionsarenot100%effectiveforfindingall harmfulorganisms inaconsignment,becauseofthesmall number of sampled plants and short time available for inspecting each plant (Work et al., 2005; Liebhold et al., 2012). Moreover, inconspicuous invertebrate pests with crypticlifestagesandplantpathogensaredifficulttodetect during visual inspections. Post-entry quarantine in the importing countryprovidesmoretimeforthedevelopment of pests and the expression of symptoms. During the quarantineperiod,thereareinspectionsbyofficialinspectors, in addition to regular checks by the quarantine facility operator. Ifharmfulorganismsarefound,the consignment may be treatedor destroyed.If no harmful organisms are found, theofficialinspectorreleases theconsignmentfrom post-entryquarantineandtheplantscanenterthecountry.
The period that plants must remain in a post-entry quarantine facility alsovaries, roughly fromthree months toseveralyears.InNewZealand,allP4P(exceptsometissue cultures,dormantbulbs,andPhalaenopsiswholeplantsfrom Taiwan)mustgointopost-entryquarantineforaminimumof three months,and up to three years.New Zealand allows horticulturalgermplasm(e.g.budwood)fromcertified facili-ties withreduced post-entry quarantine requirements (e.g. ninemonthsactivegrowthinsteadof24monthsforPrunus). Similarly,thepost-entryquarantineperiodinAustraliaranges frommonthstoyears,dependingonplantspecies.IntheUSA, mostimportedfruittreesgointo post-entryquarantinefor twoyears.Asanexception,PrunusfromEuropemustcome fromcertifiedfacilities,andimportfromothersources,except Canada, is prohibited. In the USA post-entry quarantine constitutes ofan open-field plantation, in which the trees areregularlyinspectedforpests.InBrazil,allnurserystock mustgoforthreemonthsintopost-entryquarantine,which canrangefromopenfieldtoclosedfacilities,dependingon perceivedrisk.IntheEU,plantsofonlyafewgenerarequire three months post-entry quarantine (for example dwarfed plants of Chamaecyparis, Juniperus and Pinus, originating in Japan:AnnexofAnonymous,2002).Indiarequirespost-entry quarantineforimportedcuttingsandplantsforpropagation, from45daystooneyear,dependingonthespeciesandthe pestriskinvolved.Kenyastipulates thatcertainshipments must go into quarantine before they areallowed into the country. The quarantine facilities often belong to the importers,allowingimportoflargernumbersofplantsand providingthebestcareforthequarantinedplants,whichare commonly imported for propagation. Ultimately, however, inspectionsarecarriedoutby governmentofficials.Finally, the post-entryquarantine period maystart only whenthe plantsareactivelygrowing(asinNewZealand),withtheaim ofincreasingthelikelihoodofdetectingpests.
1.9. Integratedmeasures(systemsapproaches)
Integratedmeasuresforthemanagementofharmful organ-ismsrequiretwoormorephytosanitarymeasures indepen-dent of each other (FAO, 2002). In some cases, integrated measures make it possible to meet the required level of protectionincaseswherenoadequatesingletreatmentexists. Inothercases,anintegratedmeasuremayprovideequivalent protectionagainstharmfulorganismsasanalternativesingle measureortreatment,butmaybelesstrade-restrictive.The implementation of effective integrated measures requires analysis ofthe pathway to identify critical points for pest reductionandmanagement.
ISPM36proposesintegratedmeasuresspecificallyaimedat P4P(FAO,2012).Thesemeasuresareallimplementedinthe exportingcountry,reducingthechanceofharmfulorganisms beingcarried onthe exportedplants. Only afew countries, particularly New Zealand and Australia, require integrated measuresfortheimportofliveplantsingeneral.Forimports intotheEU,specificplantgenera,oftenfromparticularorigins, mayrequireacombinationofspecifiedtreatments,suchasAcer
spp.fromChina.Otherexamplesaretheimportofplantsin growingmediatotheUSA,whichrequiresacomplexsystems approach(Federal Register,2012a),andthe importofwhole
Phalaenopsisplantsingrowingmediafrom TaiwanintoNew ZealandwithouttheneedforPEQ,asallrisksaremanaged pre-export.Thelimitednumberofcountriesdemandingintegrated measuresmaybeinpartduetotherelativelyrecentacceptance of such an approach towards phytosanitary security, as illustratedbytherecentadoptionofISPM36.
1.10. Pre-exportclearingprogrammes
Cooperative efforts between plant producers in exporting countriesandregulatoryagenciesprovideawaytoreducerisk ofmovingpestswhileallowingcontinuedtradeofproblematic P4P.Forexample,CostaRicanowexportsDracaenatotheUSA through a pre-export clearance program. Over 11,000 pest interceptionswererecordedonDracaenaspp.fromCostaRica from 1984 to 2011 (Colpetzeret al., 2011). In2006 aset of integratedpracticeswereimplementedinapilotprogramto reduce the numberof infested shipments into theUSA by participatingproducersthatsubstantiallyreducedpest inter-ceptions(Hidalgoetal.,2013).Theseincludepestmanagement practices for field production as well as plant inspection protocols for packing houses, worker training, minimum lightingrequirementsandphysicalscreenbarrierstoprotect clean inspectedplants.Asaresultofanauditable bilateral workplanacceptedbybothCostaRicaandtheUSAin2012 (Federal Register, 2012b), all Dracaena shipments require a phytosanitarycertificateincludingastatementthatspecified integrated practices have been followed. In addition to continuedaccesstotheUSAmarket,growersareinducedto participateinthisprogrambyachangeintherulesthatallows themtoselllargerandmorevaluableplants.
1.11. Inspectionsatthepointofentry
Whileseveralofthecomparisoncountriesdidnotprovide instructionsor guidelinesforinspectorsintheirlegislation, there are large differences in inspection practices across countries.Thesedifferencesresultinequallylargedifferences inthestatisticallikelihoodthatthelevelofinfestationisbelow alevel thatisdeemedacceptablebytheimportingcountry. Forexample,Australiastipulatesinspectionofallplantsina consignment.InNewZealandinspectorsinspectallplantsof eachspeciesorvarietyinaconsignmentupto600plants.The USAhashistoricallyfollowedasamplingguidelineof2%of theunitsinaconsignmentduringregularinspectionsandin Europesamplingintensityishighlyvariableamongcountries (Eschenetal., 2015).Thesampling intensityofinspections carriedoutaspartoftheAgriculturalQuarantineInspection MonitoringprogrammeintheUSA,whichisrestrictedtoafew selected genera, are based on hypergeometric statistics, meaning that the sample size is calculated based on the consignmentsize,acceptablelevelofrisk,andtherequired levelofconfidenceinthesamplingoutcome.Theconsignment size and all inspections outcomes are recorded, allowing calculation ofinfestation rates and various other analyses (Venette et al., 2002). In addition, the USA is piloting a programme to sample all genera using hypergeometric sampling,ratherthanthe2%guidance.
2.
Discussion
Our review illustrates that, despite the common basis in internationalstandards, therearelarge differences inhow countries regulateimports of P4P.In fact,only two ofthe measuresandproceduresdescribedherearerequiredbyall countries:phytosanitarycertificatesandimportinspections, buteventheimportinspectionsarenotcarriedoutwiththe sameintensityeverywhere.Allothermeasuresareeithernot required by all countries or apply only to specific genera, exporting countries or commodities. In addition, certain measuresmaynot bepracticalinsomecountries, such as season-dependentimportsintropicalorverylargecountries. Each country in this comparison applies a unique set of phytosanitarymeasures(Table2),whichreflectsvariationin approachestoriskanddifferencesinregulatorydesign.
Thelargestdifferencesarebetweenthecountrieswiththe strictestmeasuresandalltheothercountries.ThecurrentEU legislationappearstohavethemostopenapproach,asitis theonlyregioninthecomparisonwithgeneralauthorisation for P4P. Australia and New Zealand have the strictest legislations: no other countries have strictly white list approaches to regulation, or stipulate both pesticide treat-mentandpost-entryquarantineforallimportedP4P.Strict regulations presumably reduce the number of new pest entering the country or establishing, but there have been newpestsrecentlyestablishwhichhavenotbeentracedto imports of P4P (e.g. Pseudomonas syringae var. actinidae on kiwifruit;Anonymous,2011).
Because of the cost and practicalities of putting plants throughpost-entryquarantine,thismaybeprimarilysuitable forrelativelysmallconsignments.Asaconsequence, coun-trieswithstrictpost-entryquarantineregulationsmayimport mostly smaller volumes for breeding and propagation. In
addition,quarantinedplantsdonotenterthemarketofthe importingcountryimmediately.Thus,post-entryquarantine requirementsmayrestrictthetradeincertainplantspecies or types,in particularthose that areshort-lived.Countries wherethenursery industryreliesontheimportofnursery stock from warmer or cheaper-labour countries and that importbillionsofplantsperyear,suchastheNetherlandsand theUSA,arelogisticallyunabletoimplementstrictmeasures, suchaswideapplicationofpost-entryquarantine.
UndertheSPSAgreement,eachcountryhastherighttoset its ownlevelofrisk.NewZealandandAustraliabasesome of their nationalidentityon flora and fauna, which isnot routinelyfoundintherestoftheworld,andsupportastrong plant protection program and it is a priority of the two governmentstopreventfurtherintroductions.Countrieswith landbordersmayhavelesscontrolovertheestablishmentof peststhanislands,inparticular thosepeststhathavebeen introducedintoneighbouringcountriesandcontinue spread-ing naturally.This difference affects regulation, because it maybeimpossibletostopsecondaryspreadfromneighbours, andafocusonincreasedbiosecurityatsharedpointsofentry may be more effective than focussing on land crossings betweenindividualcountries.Forexample,thephytosanitary regulations ofSwitzerlandand EU arealmostfully harmo-nized,andtheregulationsofthreeEast-Africancountriesas well,withUgandaandRwandaacceptingimportof consign-mentsarrivingbyboatinMombasathathavecompliedwith the regulations of Kenya. Several countries, including the Netherlands,areglobaltradinghubsforP4P,whichmaybe particularlyexposedtopestsasaresultofthelargeimport volume anddiverse pathways,and itisimportant thatthe phytosanitary practicesin thesecountries meethigh stan-dardsinordertolimitthespreadofpeststhroughtrade.
National and international phytosanitary legislations in theirpresentformareoftenrelativelyrecentandsome less-developedcountrieshaveoutdatedlegislationthatdoesnot yetreflecttheSPSAgreementandtheupdatingoftheIPPC. One reason for the slow changes may be that changing legislation is time consuming as it has to be accepted by Parliament.Alackofphytosanitarycapacitymaybeanother reasonfortheslowuptakeoftheIPPCandSPSAgreement.The IPPCcapacitydevelopmentsectionprovidessupporttoupdate olderlegislations,buttheacceptanceofsuchrevised legisla-tionbyParliamentsmaystillbeaslowprocess.Intheshort term itmaybemosteffectivetointroduce regulationsand policythatamendexistinglegislation(SequeiraandGriffin, 2014)ortopromotegoodpracticeamongproducers.Ourstudy has likelymissedaspectsofsomecountries’phytosanitary policies because of our focus on legislation. For example, Canada’sPlantProtectionActandregulationsaremoreofa ‘‘toolbox’’ofpowersandadministrativeprocedures,whilethe detailsoftheplantprotectionprogramarefoundinpolicies anddatabases,suchaspolicydirectiveD-01-01‘‘Phytosanitary RequirementstoPreventtheEntryofPhytophthoraramorum’’. The USA lists plants, pests, origins and procedures in a number of places in legislation, particularly 7 CFR 319.37 (ForeignQuarantineNotices).
toensure market access. Implementation of phytosanitary regulations is part of the NPPOs tasks as set out in the legislation (Sequeira and Griffin, 2014), but application of phytosanitary measures and thus the primary mitigating actionsagainstquarantineisprimarilydonebyproducers.The engagementofproducersintheimplementationof phytosa-nitarymeasures througheducation and guidancefromthe NPPO is therefore of great importance. How the producer engagement isorganised in a countrymaydependon the phytosanitarydesign,aswellastheorganisationalcomplexity and capacity of the plant protection organisation. Thus it maydependonthelevelofdetailinlegislationorlower-level legislativetexts,asdiscussedinthepreviousparagraph,or ontherelative importanceofsub-nationalplantprotection organisations,whichisgreaterinfederalorlargestatesthan inunitarystates.Incaseswherethereisinsufficientcapacity within the exporting country, importing countries may providetechnicalsupportandcapacitybuildingtomeettheir requirements.Forexample,theNetherlandsandtheUSAoffer traininginphytosanitaryissuesforthebenefitof phytosani-taryservicesofpoorer tradingpartners,suchasKenyaand Ethiopia.Theeffectivenessofimplementationofregulations isparamounttobiosecurity,butthereislittleevidenceforhow goodimplementation,orhoweffectiveindividualmeasures are.InspectorsfromanNPPOmayvisittheirtradingpartners toaudittheNPPO andproducers.These auditsprovidethe importingcountrieswithsomeinformationaboutthequality and reliability of the implementation of measures in the exporting country. For example, the Food and Veterinary OfficeoftheEUperiodically auditscountriesthatexportto the EU and reports on its findings and recommendations (http://ec.europa.eu/food/fvo/).Countriesthatdonothavethe meansforsuchauditshavelessabilitytoidentifyproblems withtheimplementationofphytosanitarypractices.
Theremayalsobeadiscrepancybetweenregulationsand practice in importing countries, due to large numbers of importedP4Pandtechnicalcapacitylimitations.IntheEU,for example,allincomingconsignmentsmustbeinspectedatthe firstPOE,butthelargedifferencesinthevolumeofimported plantsinmemberstatesandthegenerallylimitednumberof inspectorsmayresultindifferencesinthewayinspectionsare carriedout.ThelargevolumeofimportedP4Pinpeakseasons mayalsoaffecttheabilityofinspectorsintheUSAtocarryout inspectionsasspecified(Liebholdetal.,2012).
Anyattempttoassesswhetherthedifferentapproachesto phytosanitarysafetyaffectthearrivalandestablishmentrates ofnewinvasivespeciesisdifficult,becausemostcountries lackdataforuseinsuchanassessment.Beyondinformation onarrivalratesandestablishments,importandinterception data could also facilitate hazard identification and the assessmentofrisk(SequeiraandGriffin,2014).Inparticular, collectionandanalysisofdataonP4Pimports,atthegenus levelandbyorigin,inconjunctionwithdataonintercepted harmful organisms and clean consignments, could enable analysisofpatternsandtrendsintheimportofliveplantsand theassociatedrisks.However,onlyafewcountriesappearto collectdataonthepestsfoundduringborderinspectionsand negativeobservationsareveryrarelyreported,whichprevents statisticallyrobustanalysesofinterceptiondata(Worketal., 2005;Kenisetal.,2007).Inaddition,detailedinformationon
importsofP4Palsoisrarelycollected,asmostcountriescollect tradeinformationprimarilyfortaxingpurposesandthelevel of detail then corresponds to the needs of the customs authority. The customs offices often use the Harmonised Systems codes,but thereare far toofewcategories inlive plantstocapturethediversityintradedP4P.Yet,thesedata arecritical forcomparing countries’regulatoryframeworks and theeffectofphytosanitarymeasures,asdifferencesin arrivalratesarelikelytodependontheintensity,originand typeoftrade.
Someoftheevidenceavailabletoassesstheeffectiveness ofphytosanitarymeasuresincludesreducedpest establish-mentratesintheUSAandCanadaaftertheenactmentofthe planthealthlegislations inthe 20thcentury(Roques,2010; Hlasny,2012)andlowpestinterceptionratesinNewZealand, eitherattheborderorinpost-entryquarantine(Tualauand Nair, 2008; Tualau et al., 2010), as the result of strict phytosanitaryregulationsthatmayhavetheeffectofreducing tradevolume.Recordsofconsignmentsfoundtobeinfested whileinpost-entryquarantineinNewZealandillustratesthat post-entryquarantinecanbeausefulmeasure.Astudyfor NewZealand’s MinistryofPrimaryIndustriesrevealedthat 14% of the consignments were infested (Tualau and Nair, 2008),despiteearlierclearanceduringinspectionsatthepoint of entry. The vast majority of these infestations were pathogens,possiblyduetothehigherlikelihoodthat patho-gensgounnoticedduringinspectionsatthepointofentryand becausepre-exportinsecticideandacaricidetreatmentsmay haveremovedmostarthropodpests.Thisisarareexample of a measurable effect of phytosanitary measures. More detaileddatacollectiononimports,interceptions,and estab-lishmentsovertimewouldenableevaluationofphytosanitary measuresandmoreaccurateandrapidriskassessment,thus improving phytosanitary safety throughimplementation of moreappropriate,evidence-basedmeasures.
Insightsintotherangeofphytosanitaryregulatory frame-worksemployedbyvariouscountriesmayhelpcountriesto identify additional or alternative measures that may be appropriate in their context. Our review of phytosanitary regulationsrevealedthatallcountriesregulateplantimports differentlyandmostrelyonmeasurestargetingspecificpests. Given the continuous increasein the number of newpest establishmentsinmanycountriesandbecausemanyofthose pestswereunknownornotknowntobeharmfulpriortotheir establishment, such targeted measures appear inadequate forthepreventionofnewpestintroductions.Incontrastto measuresforwoodpackaging materials(FAO,2009a),there existfewmeasuresthatcanbegenerallyappliedtoalltrade in P4P.Two exceptions maybefumigation aspracticed in Australiaandthetreatmentswithpesticidespriortoexportto NewZealand.However,itmaynotbepossibletoapplythese onalargerscale,forexampleincountriesthatimportlarge numbers of P4P,such asthe USA or the EU. Identification of other, particularly effective measures or regulations for reducingpestestablishmentrateswouldbeverybeneficial.
approach rates and may lead to some harmonisation of regulatoryframeworks.Thedevelopmentofanynewsystem of integrated measures requires, however, knowledge and capacitythatdependonresearchandexpertcommitteesto determinelikelypointsofsystemfailuresandhowtomonitor andmitigatesuchfailures.Thus,internationalcollaboration and assistance in capacity building may contributeto the wider implementation of integrated measures. Continued researchintogenerallyapplicable,singlemeasures nonethe-lessremainsnecessary,inparticularforthereplacementof methyl-bromide,whichisbeingphasedout.Wealso recom-mendthatdetaileddatacollectiontoassistwitheffectiveness evaluationsbeencouraged.
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Summary of the international agreements and national legislationsandregulationsinthecountriesthatwereused forthiscomparison.
Uncited
references
Anonymous(2008),Devorshak(2012)andParkeandGru¨nwald (2012).
Acknowledgements
WethankBobGriffin,BrianDoubleandBramdeHoopandan anonymousreviewerforcommentsonearlierversionsofthe manuscript.Partofthisworkwasdevelopedthroughworking group ‘Globalization of the Live Plant Trade: Informing Efficient Strategies for Reducing Non-Native Pest Invasion Risk’supportedbytheNationalSocio-Environmental Synthe-sisCenter(SESYNC)underfundingreceivedfromtheNational ScienceFoundationDBI-1052875.REwassupportedthrough agrantfromtheSwissSecretariatforScience,Educationand Researchtojointhe COSTActionPERMIT.Theinclusionof KenyainthestudygreatlybenefitedfromaCABIDevelopment Bursary,awardedtoRE.
Appendix
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Supplementary
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Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. envsci.2015.04.021.
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