Importation of dianthus (Dianthus spp.) for planting from Guatemala into the United States and Territories A Qualitative, Pathway-Initiated Pest ...
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Importation of dianthus (Dianthus spp.) for planting from Guatemala into the United States and Territories A Qualitative, Pathway-Initiated Pest Risk Assessment Agency Contact Plant Pest Risk Analysis (PPRA) Science and Technology (S&T) Plant Protection and Quarantine (PPQ) Animal and Plant Health Inspection Service (APHIS) United States Department of Agriculture (USDA) 1920 Main Campus Drive, Suite 400 Raleigh, NC 27606 August 17, 2021 Version 3
Executive Summary
The purpose of this report is to assess the pest risks associated with importing commercially
produced unrooted cuttings with foliage of dianthus, Dianthus spp. (Caryophyllaceae), from
Guatemala into the United States and Territories for planting.
Based on the market access request submitted by Guatemala, we considered the pathway to
include the following processes and conditions: unrooted cuttings with no more than 10 leaves,
to be imported year-round. The pest risk ratings depend on the application of all conditions of the
pathway as described in this document. Dianthus cuttings without roots produced under different
conditions were not evaluated and may pose a different pest risk.
We used scientific literature, port-of-entry pest interception data, and information from the
government of Guatemala to develop a list of pests with quarantine significance for the United
States and Territories. These are pests that occur in Guatemala on any host and are associated
with the commodity plant species anywhere in the world.
The following organisms are candidates for pest risk management because they have met the
threshold for unacceptable consequences of introduction.
Pest type Taxonomy Scientific name Likelihood of
Introduction
Arthropod Diptera: Agromyzidae Liriomyza huidobrensis Medium
(Blanchard)
Chromistan Pythiales: Pythiaceae Phytopythium vexans (de Bary) Medium
Abad, de Cock, Bala, Robideau,
Lodhi & Lévesque*
Virus Bunyavirales: Tospoviridae Orthotospovirus Impatiens Medium
necrotic spot virus**
* This organism is a quarantine pest for U.S. Territories, only.
** This organism is a quarantine pest for Hawaii and U.S. Territories, only.
Detailed examination and choice of appropriate phytosanitary measures to mitigate pest risk are
addressed separately from this document.Table of Contents 1. Introduction ............................................................................................................................... 1 1.1. Background .......................................................................................................................... 1 1.2. Initiating event...................................................................................................................... 1 1.3. Potential weediness of the commodity ................................................................................. 1 1.4. Description of the pathway................................................................................................... 1 2. Pest List and Pest Categorization ............................................................................................ 2 2.1. Pest list ................................................................................................................................. 2 2.2. Pests considered but not included on the pest list ................................................................ 4 2.3. Pests selected for further analysis or already regulated ....................................................... 5 3. Assessing Pest Risk Potential ................................................................................................... 5 3.1. Introduction .......................................................................................................................... 5 3.2. Assessment ........................................................................................................................... 6 4. Summary.................................................................................................................................. 17 5. Literature Cited ...................................................................................................................... 18 6. Appendix: Pests with non-quarantine status ........................................................................ 29
1. Introduction
1.1. Background
The purpose of this report is to assess the pest risk associated with the importation of
commercially produced, unrooted cuttings with no more than 10 leaves of Dianthus spp. for
planting from Guatemala (referred to as the export area) into the United States and Territories1
(referred to as the pest risk analysis or PRA area).
This is a qualitative risk assessment. The likelihood of pest introduction is expressed as a
qualitative rating rather than in numerical terms. This methodology is consistent with guidelines
provided by the International Plant Protection Convention (IPPC) in the International Standard
for Phytosanitary Measures (ISPM) No. 11, “Pest Risk Analysis for Quarantine Pests” (IPPC,
2017). The use of biological and phytosanitary terms is consistent with ISPM No. 5, “Glossary of
Phytosanitary Terms” (IPPC, 2018b; 2019).
As defined in ISPM No. 11, this document comprises Stage 1 (Initiation) and Stage 2 (Risk
Assessment) of risk analysis. Stage 3 (Risk Management) will be covered in a separate
document.
1.2. Initiating event
The importation of plants for planting into the United States is regulated under Title 7 of the
Code of Federal Regulation, Part 319 Subpart – Plants for Planting (7 CFR §319) and the Plants
for Planting Manual (USDA PPQ, 2020). Under this regulation, the entry of Dianthus spp. from
Guatemala into the PRA area is not authorized. This commodity risk assessment was initiated in
response to a request by the Vice Ministry of Animal and Plant Health and Regulations (VISAR)
to change the Federal Regulation to allow entry (Simao, 2019).
1.3. Potential weediness of the commodity
In some cases, an imported commodity could become invasive in the PRA area. If warranted, we
analyze the commodity for weed risk.
A weed risk analysis is not required when (a) the commodity is already enterable into the PRA
area from other countries, (b) the commodity plant species is widely established or cultivated in
the PRA area, or (c) the imported plant part(s) cannot easily propagate on its own or be
propagated. We determined that the weed risk of Dianthus spp. does not need to be analyzed
because this commodity is already enterable from other countries (USDA PPQ, 2020).
1.4. Description of the pathway
A pathway is “any means that allows the entry or spread of a pest” (IPPC, 2018b; 2019). In the
context of this document, the pathway is the commodity to be imported, together with all the
processes the commodity undergoes from production through importation and distribution. The
following description of this pathway focuses on the conditions and processes that may have an
1
The PRA area includes all 50 states, Guam, the Commonwealth of the Northern Mariana Islands, Puerto Rico, and
the U.S. Virgin Islands.
1impact on pest risk. Our assessment is therefore contingent on the application of all components of the pathway as described in this section. 1.4.1. Description of the commodity The specific pathway of concern is the importation of unrooted cuttings of Dianthus spp. for planting. The cuttings will have a maximum of ten (10) leaves. 1.4.2. Summary of the production, harvest, post-harvest, shipping, and storage conditions considered Production, harvesting, and post-harvesting procedures in the export area were not considered as part of this assessment. Shipping and storage conditions were also not evaluated as part of this assessment. 2. Pest List and Pest Categorization The pest list is a compilation of plant pests of quarantine significance to the United States and Territories. This includes pests that are present in Guatemala on any host and known to be associated with Dianthus spp. anywhere in the world. Pests are considered to be of quarantine significance if they (a) are not present in the PRA area, (b) are actionable at U.S. ports of entry, (c) are regulated non-quarantine pests, (d) are under federal official control, or (e) require evaluation for regulatory action. Consistent with ISPM No. 5, pests that meet any of these definitions are considered “quarantine pests” and are candidates for analysis. Species with a reasonable likelihood of following the pathway into the PRA area are analyzed to determine their pest risk potential. 2.1. Pest list We developed the pest list based on the scientific literature, port-of-entry pest interception data, and information provided by the government of Guatemala. We listed the pests that are of quarantine significance to the PRA area in Table 1. For each pest, we provided evidence of the pest’s presence in Guatemala and its association with Dianthus spp. We also indicated the plant parts with which the pest is generally associated and provided information about the pest’s distribution in the United States, if any. Pests that are likely to remain associated with the harvested commodity in a viable form are indicated by shaded rows and are listed separately in Table 2. Ver. 3 August 17, 2021 2
Table 1. List of quarantine pests associated with Dianthus spp. (in any country) and present in
Guatemala (on any host)
Pest name Presence in Host Plant part(s) 2 Considered further?3
Guatemala association
ARTHOPODS
Diptera: Agromyzidae
Liriomyza Weintraub et Weintraub et Leaf Yes
huidobrensis al., 2017 al., 2017 (Weintraub et al., This insect is a leaf
(Blanchard) 2017) miner.
Lepidoptera: Noctuidae
Copitarsia decolora Simmons and Pogue and Leaf No
(Guenée) Pogue, 2004 Simmons, 2008 (Cortés P et al., External feeder
1972)
FUNGI AND CHROMISTANS
Phytopythium vexans CABI, 2021; French, 1989; Roots, stems Yes
(de Bary) Abad, de Lodhi et al., Sharma and (Nakkeeran et al., This pest is present in the
Cock, Bala, 2020 Sharma, 2008 2018; Sharma and continental United States
Robideau, Lodhi & Sharma, 2008) (Hendrix and Campbell,
Lévesque syn.: 1970; Ivors et al., 2008;
Pythium vexans de Parkunan et al., 2014)
Bary and Hawaii (Kleijunas
and Ko, 1975; Raabe et
al., 1981). It may qualify
as a quarantine pest for
Puerto Rico as we found
no evidence of this pest
occurring there.
VIRUSES AND VIROIDS
Orthotospovirus Barriento Roggero et al., Leaves, stems Yes
Impatiens necrotic Equite, 2006; 1999; (Roggero et al., This pest is present in the
spot virus Barrios, 2006 Shahraeen et 1999) continental United States
al., 2002 (Kuo et al., 2014;
Tzanetakis et al., 2009).
However, it may qualify
as a quarantine pest for
Hawaii or Puerto Rico
because we found no
evidence of this pest
occurring there.
2
The plant part(s) listed are those for the plant species under analysis. If the information has been extrapolated, such
as from plant part association on other plant species, we note that.
3
“Yes” indicates simply that the pest has a reasonable likelihood of being associated with the harvested commodity;
the level of pest prevalence on the harvested commodity (low, medium, or high) is qualitatively assessed as part
of the Likelihood of Introduction assessment (section 3).
32.2. Pests considered but not included on the pest list
2.2.1. Organisms with non-quarantine status
We found evidence of organisms that are associated with Dianthus spp., and are present in the
export area, but are not of quarantine significance for the PRA area. These organisms are listed
in the Appendix.
2.2.2. Quarantine pests considered but not included on the pest list
We found a single, 35-year-old record of Eyrsiphe buhrii U. Braun (syn.: Oidium dianthi Jacz.)
in Guatemala and Erysiphe pisi var. pisi DC. [syn.: Eyrsiphe communis (Wallr.: Fr.) Schltdl.] on
Dianthus spp. (Amano (Hirata), 1986). As the author of these records stated they were
unreliable, we did not include them on the pest list.
2.3.3. Organisms identified only to the genus level
In commodity risk assessments, the taxonomic unit for pests selected for evaluation beyond the
pest categorization stage is usually the species (IPPC, 2013). Generally, we do not assess risk for
organisms identified only to the genus level, especially if the genus is reported in the PRA area.
Many genera contain multiple species, and we cannot know if the unidentified species occurs or
is regulated in the PRA area. Because the organism has not been fully identified, we cannot
properly assess the likelihood and consequences of its introduction. However, if the genus is
absent from the PRA area or is actionable at U.S. ports of entry, the genus can be regulated as a
quarantine pest.
There have been 50 interceptions of quarantine arthropod taxa on Dianthus from Guatemala
since 2016 (Table 2).
Table 2. Quarantine arthropods considered but not included on the pest list
Where Imported Number of
Material For Pest
Intercepted As Interceptions
Permit Cargo 38
Consumption Cut Flower 37
Frankliniella sp. (Thysanoptera: 12
Thripidae)
Noctuidae sp. (Lepidoptera) 7
Copitarsia sp. (Lepidoptera: 3
Noctuidae)
Phyllophaga sp. (Coleoptera: 3
Scarabaeidae)
Agromyzidae sp. (Diptera) 2
Thripidae sp. (Thysanoptera) 2
Tortricidae sp. (Lepidoptera) 2
Aphididae sp. (Hemiptera) 1
Helicoverpa sp. (Lepidoptera: 1
Noctuidae)
Hoplia sp. (Coleoptera: 1
Scarabaeidae)
Nodonota sp. (Coleoptera: 1
Chrysomelidae)
Ver. 3 August 17, 2021 4Platynota sp. (Lepidoptera: 1
Tortricidae)
Thysanoptera sp. 1
Propagation Cut Noctuidae sp. (Lepidoptera) 1
Flower
Baggage Consumption Cut 9
Flower
Noctuidae sp. (Lepidoptera) 5
Frankliniella sp. (Thysanoptera: 1
Thripidae)
Geometridae sp. (Lepidoptera) 1
Miridae sp. (Hemiptera) 1
Phlaeothripidae sp. 1
(Thysanoptera)
General Consumption Cut Frankliniella sp. (Thysanoptera: 3
Cargo Flower Thripidae)
We have provided basic information about the quarantine taxa identified to genus-level to help
risk managers determine if measures beyond those intended to mitigate fully identified pests are
warranted.
• Coleoptera: Chrysomelidae: Nodonota sp. infests fruit, leaves (Stear, 1920), and
flowers (Jolivet, 1987),
• Coleoptera: Scarabaeidae: Phyllophaga sp. and Hoplia sp. infest foliage, fruit,
and roots (CABI, 2021),
• Lepidoptera: Noctuidae: Copitarsia sp. infest flower, fruit, leaf (Díaz et al.,
2012), and Helicoverpa sp. infest buds, fruit, and foliage (CABI, 2021),
• Lepidoptera: Tortricidae: Platynota sp. infest foliage and fruit (CABI, 2021),
• Thysanoptera: Thripidae: Frankliniella sp. infest leaves and flowers (CABI,
2021).
2.3. Pests selected for further analysis or already regulated
We identified three quarantine pests for further analysis (Table 3).
Table 3. Pests selected for further analysis
Pest type Taxonomy Scientific name
Arthropod Diptera: Agromyzidae Liriomyza huidobrensis (Blanchard)
Chromistan Pythiales: Pythiaceae Phytopythium vexans (de Bary) Abad, de Cock, Bala,
Robideau, Lodhi & Lévesque
Virus Tospoviridae Orthotospovirus Impatiens necrotic spot virus
3. Assessing Pest Risk Potential
3.1. Introduction
We estimated the risk potential of each pest selected for further analysis. Risk is described by the
likelihood of an adverse event, the potential consequences, and the uncertainty associated with
these parameters. For each pest, we determined if an endangered area exists within the United
Ver. 3 August 17, 2021 5States and Territories. The endangered area is defined as the portion of the PRA area where
ecological factors favor the pest’s establishment and where the pest’s presence will likely result
in economically important impacts. If a pest causes an unacceptable impact (i.e., is a threshold
pest), this means it could adversely affect agricultural production by causing a yield loss of 10
percent or greater, by increasing U.S. production costs, or by impacting an environmentally
important host or international trade. After the endangered area is defined, we assessed the pest’s
likelihood of introduction into that area on the imported commodity.
The likelihood of introduction is based on the potential entry and establishment of a pest. We
qualitatively assess this risk using the ratings: Low, Medium, and High. The risk elements
comprising the likelihood of introduction are interdependent; therefore, the model is
multiplicative rather than additive. We defined the risk ratings as follows:
High: This outcome is highly likely to occur.
Medium: This outcome is possible; but for that to happen, the exact combination of
required events needs to occur.
Low: This outcome is unlikely to occur because one or more of the required events are
unlikely to happen, or because the full combination of required events is unlikely to align
properly in time and space.
We address uncertainty associated with each risk element as follows:
Negligible: Additional or more reliable evidence is very unlikely to change the rating.
Low: Additional or more reliable evidence probably will not change rating.
Moderate: Additional or more reliable evidence may or may not change rating.
High: Reliable evidence is not available.
3.2. Assessment
3.2.1. Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae)
Liriomyza huidobrensis is a polyphagous leafminer with multiple hosts, including greenhouse
ornamentals and field crops (Spencer, 1973). It is highly fecund, producing as many as 288 eggs
per female (Neder de Román and Arce de Hamity, 1984), and has four to five generations
annually (Serantes de Gonzalez, 1973). Adult flight capacity is limited; dispersal over long
distances is facilitated by the movement of propagative host material and cut flowers (Smith et
al., 1997).
The endangered area for Liriomyza huidobrensis within the United States and Territories
Climatic suitability Liriomyza huidobrensis has a broad geographic distribution. It has been
reported from Africa: Comoros, Democratic Republic of the Congo,
Kenya, Mauritius, Morocco, Réunion, Seychelles, South Africa, Uganda,
Zimbabwe; Asia: China (Beijing, Chongqing, Fujian, Gansu,
Guangdong, Guizhou, Hebei, Hubei, Nei Mongol, Shaanxi, Shandong,
Sichuan, Tibet, Xinjiang, Yunnan), Georgia, India (Manipur, Uttar
Ver. 3 August 17, 2021 6Pradesh), Indonesia (Java, Sulawesi, Sumatra), Israel, Japan (Aomori,
Hokkaido, Miyagi, Yamaguchi), Jordan, Lebanon, Malaysia (Peninsular),
North Korea, Philippines, Saudi Arabia, Singapore, South Korea, Sri
Lanka, Syria, Taiwan, Thailand, Turkey, Vietnam, Yemen; Europe:
Albania, Austria, Bulgaria, Croatia, Cyprus, Czech Republic, Finland,
France, Germany, Greece (including Crete), Hungary, Italy (Piedmont,
Liguria, Sicily), Malta, Montenegro, the Netherlands, Poland, Portugal,
Serbia, Spain, Switzerland; Caribbean: Guadeloupe; Central America:
Belize, Costa Rica, Dominican Republic, El Salvador, Guatemala,
Honduras, Nicaragua, Panama; North America: Canada (Ontario);
Oceania: Australia (New South Wales) Guam; South America:
Argentina, Brazil (Goiás, Minas Gerais, São Paulo), Chile (including
Easter Island), Colombia, Ecuador, French Guiana, Peru, Uruguay,
Venezuela (CABI, 2021, Glavendekic, 2012; Munyuli et al., 2017;
Okonya and Kroschel, 2016; Partsvaniya and Loladze, 2011; Spencer,
1973; Takano et al., 2008; Wang et al., 1998).
Thermotolerance plays an important role in determining seasonal
abundance and geographic distribution of L. huidobrensis. A temperature
range of 18° to 24°C is considered best for overall population growth and
optimal survival occurred at 20° to 25° (Mujica et al., 2017). Liriomyza
huidobrensis pupae can survive up to 30 frost days at minimum
temperatures of -11.5˚C in the Netherlands (van der Linden, 1993) and -
20.6˚C in China (Chen and Kang, 2004) and can survive at elevations of
up to 3200 meters (Chen and Kang, 2002). However, L. huidobrensis is
intolerant of high temperatures (Kang et al., 2009; Mujica et al., 2012)
with development compromised at temperatures above 28° to 29°C
(MacVean, 1999; Mujica et al., 2017; Rodríguez-Castañeda et al., 2017).
Based on these ecophysiological adaptations, the geographic distribution,
L. huidobrensis could potentially establish in the United States in Plant
Hardiness Zones 6 -12 (USDA ARS, 2012). We were able to refine the
Endangered Area using the niche modelling algorithm MaxEnt (version
3.4.1; Phillips et al., 2006) (Fig. 1). We considered the pest’s temperature
tolerances, its occurrence data found in the Global Biodiversity
Information Facility (GBIF) (http://data.gbif.org) and via Google Earth
Pro, along with 19 bioclimatic variables data layers acquired from the
WorldClim dataset (http://www.worldclim.org/) at 2.5 arc-minutes
spatial resolution.
Hosts in PRA area Hosts in the PRA area include Amaranthaceae: Amaranthus caudatus;
Apiaceae: Apium graveolens, Coriandrum sativum, Daucus carota,
Hydrocotyle ranunculoides; Asteraceae: Arctium lappa, Artemisia
annua, Bellis perennis, Bidens pilosa, Calendula officinalis, Callistephus
chinensis, Carduus nutans, Chrysanthemum × morifolium, Cichorium
intybus, Conyza bonariensis, Crepis pulchra, Cynara scolymus, Emilia
sonchifolia, Gerbera jamesonii, Helianthus annuus, Lactuca sativa,
Leucanthemum vulgare, Sonchus oleraceus, Taraxacum officinale,
Ver. 3 August 17, 2021 7Zinnia violacea; Brassicaceae: Brassica juncea, B. oleracea, B. rapa,
Capsella bursa-pastoris, Nasturtium officinale, Raphanus sativus;
Cannabaceae: Cannabis sativa, Humulus japonicus; Caryophyllaceae:
Gypsophila elegans; Chenopodiaceae: Beta vulgaris, Chenopodium
album, Dysphania ambrosioides, Spinacia oleracea; Convolvulaceae:
Ipomoea batatas; Cucurbitaceae: Citrullus lanatus, Cucumis melo, C.
sativus, Cucurbita maxima, C. moschata, C. pepo, Luffa aegyptiaca,
Momordica charantia; Euphorbiaceae: Euphorbia marginata;
Fabaceae: Cicer arietinum, Glycine max, Lablab purpureus, Lathyrus
latifolius, Medicago sativa, Phaseolus vulgaris, Pisum sativum, Trifolium
repens, Vicia faba; Liliaceae: Allium cepa, A. sativum, Asparagus
officinalis; Linaceae: Linum usitatissimum; Malvaceae: Abelmoschus
esculentus, Hibiscus trionum; Onagraceae: Clarkia amoena;
Papaveraceae: Papaver rhoeas; Plantaginaceae: Plantago major;
Poaceae: Hordeum vulgare, Setaria viridis, Triticum aestivum, Zea
mays; Polemoniaceae: Phlox drummondii; Portulacaceae: Portulaca
oleracea; Ranunculaceae: Ranunculus sceleratus; Solanaceae:
Capsicum annuum, Datura quercifolia, Nicotiana tabacum, Solanum
lycopersicum, S. melongena, S. tuberosum; Tropaeolaceae: Tropaeolum
majus; Violaceae: Viola tricolor (CABI, 2021; Larraín et al., 2013;
Spencer, 1973; USDA NRCS, 2021; Weintraub et al., 2017).
Economically Economically important hosts include Apium graveolens (celery),
important hosts at Daucus carota (carrot), Cynara scolymus (artichoke), Helianthus annuus
riska (sunflower), Lactuca sativa (lettuce), Brassica juncea (mustard), B.
oleracea (cabbage), Raphanus sativus (radish), Beta vulgaris (beet),
Spinacia oleracea (spinach), Ipomoea batatas (sweet potato), Citrullus
lanatus (watermelon), Cucumis melo (cantaloupe), C. sativus
(cucumber), Cucurbita pepo (squash), Glycine max (soybean), Medicago
sativa (alfalfa), Phaseolus vulgaris (bean), Vicia faba (fava bean), Pisum
sativum (pea), Allium cepa (onion), A. sativum (garlic), Asparagus
officinalis (asparagus), Hordeum vulgare (barley), Triticum aestivum
(wheat), Zea mays (maize), Capsicum annuum (bell pepper), Nicotiana
tabacum (tobacco), Solanum lycopersicum (tomato), S. melongena
(eggplant), and S. tuberosum (potato) (USDA-NASS, 2021).
Potential Liriomyza huidobrensis larvae feed within the leaf mesophyll, and adults
consequences on puncture leaves for feeding and oviposition. This damage can result in
economically leaf wilting and death (Smith et al., 1997; Weintraub et al., 2017).
important hosts at Liriomyza huidobrensis is a major pest of potato, fava bean, beet, and
risk garlic in South America (Spencer, 1973), and of chrysanthemums,
Primula, Verbena, lettuces, Phaseolus, cucumber, celery, and Cucurbita
pepo in the Europe (Smith et al., 1997). Yield losses may reach 70% or
higher in green bean and potato, and 70 to 100% in cucumber; economic
losses of 30% have been reported in flower production (Rauf et al.,
2000). Thus, this species has the potential to cause unacceptable
consequences if introduced into the United States.
Ver. 3 August 17, 2021 8Endangered Area The endangered area comprises those regions of the continental United
States, in which L. huidobrensis is able to survive outdoors (estimated to
be Plant Hardiness Zones 6-12) (Fig. 1). Cultivation of commercial hosts
in greenhouses could expand the endangered area into regions outside of
the projected Plant Hardiness Zones.
a
As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non-
market (environmental) plants (IPPC, 2017).
The likelihood of introduction of Liriomyza huidobrensis into the endangered area via
Dianthus spp. imported from Guatemala
Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Likelihood of
Entry
Pest prevalence on Medium Low Liriomyza huidobrensis has been reported to be
the harvested an economic pest of Dianthus in Norway
commodity (Weintraub et al., 2017), Netherlands (de
Goffau, 1991), Argentina (Salvo and
Valladares, 1997), Chile, China (Weintraub et
al., 2017), Greece (Roditakis, 1994), Indonesia
(Shepard and Braun, 1998), and Belgium (de
Clercq and Casteels, 1992). Because
L. huidobrensis larvae are leaf miners, there is a
possibility that the insect will remain with the
harvested commodity.
Likelihood of Low Low Adults puncture abaxial and adaxial leaf
surviving post- surfaces for feeding and oviposition, and larvae
harvest processing mine the leaf parenchyma tissues (Weintraub et
before shipment al., 2017), this damage can result in leaf wilting
and death (Smith et al., 1997; Weintraub et al.,
2017). Larval mines may coalesce to form
broad, blotch-like galleries are obvious (Alford,
2012). Infestations thus should be readily
detected and affected plants culled or treated.
However, eggs and small mines may not be
detected. The rating was reduced by one level.
Ver. 3 August 17, 2021 9Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Likelihood of Low Low Information supplied by the Guatemala
surviving transport Dirección de Sanidad Vegetal del
and storage Viceministerio de Sanidad Agropecuaria y
conditions of the Regulaciones stated that Dianthus will be grown
consignment in greenhouses, and that temperatures in the
production area range from 17.2°C to 26.5°C,
which is within the range considered optimal for
species survival (Mujica et al., 2017)).
Therefore, conditions under which the Dianthus
plants will be grown, stored, and transported
will permit survival of eggs or larvae infesting
plants that have escaped detection. Thus, the
rating did not change.
Overall Low
Likelihood of
Entry
Likelihood of High Negligible The commodity to be imported comprises
Establishment shipments of living unrooted cuttings of
Dianthus for propagation. We assumed these
cuttings will be sent to nurseries or greenhouses
where they will be grown until they are ready
for sale. The close proximity of other hosts
under such conditions and the fact that several
L. huidobrensis may be present in a single leaf
(Lopes et al., 2019), could facilitate mating and
oviposition and allow for pest establishment.
Additional pest hosts, such as artichoke,
sunflower, lettuce, mustard greens, spinach,
sweet potato, squash, onions, asparagus, garlic,
bell pepper, tobacco, tomato, and eggplant, are
widely grown as transplants for commercial
sale. Such garden plants would also serve as
colonization resources.
Likelihood of Medium
Introduction
(combined
likelihoods of entry
and establishment)
Ver. 3 August 17, 2021 10Fig. 1. Projected potential distribution based on climatic suitability for L. huidobrensis.
3.2.2. Phytopythium vexans (Peronosporales: Pythiaceae)
Phytopythium vexans is a soilborne pathogen (Scheck, 2014; Spies et al., 2011) that can
disseminate through irrigation water and crop residue (Nakkeeran et al., 2018; Redekar et al.,
2019). This pathogen causes diseases such as damping-off (Lodhi et al., 2020) and stem/root rot
(Tao et al., 2011; Yu et al., 2016).
The endangered area for Phytopythium vexans within Puerto Rico
Climatic suitability Phytopythium vexans is present in Africa: Comoros, Republic of the
Congo, Ivory Coast, Kenya, Liberia, Madagascar, Mauritius, Morocco,
Nigeria, Rwanda, South Africa, Tanzania, Tunisia, Uganda; Asia:
Brunei, Cambodia, China, India, Indonesia, Iran, Japan, Korea, Malaysia,
Pakistan, Sri Lanka, Thailand, Turkey, Vietnam; Europe: Bulgaria,
France, Germany, Greece, Ireland, Italy, Netherlands, Spain (Canary
Islands), United Kingdom; North America: Guatemala, Haiti, Jamaica,
Mexico, Panama, continental United States and Hawaii; Oceania:
Australia, Fiji, New Zealand, Papua New Guinea, Samoa, Solomon
Islands, Solomon Islands; South America: Argentina, Brazil, Venezuela
(Adhikari et al., 2013; Benfradj et al., 2017; Briard et al., 1995; CABI,
2021; Davidson et al., 2000; de Jesus et al., 2016; Dubey et al., 2020;
EPPO, 2021; Hernández et al., 2019; Hon-Hing et al., 2012; Jabiri et al.,
2020; Langenhoven et al., 2018; Le, 2016; Mbaka, 2011; Newhook and
Jackson, 1977; Noireung et al., 2020; Nzungize et al., 2011; Parkunan et
al., 2014; Polat et al., 2017; Rao, 1963; Robertson, 1980; Rodriguez-
Padron et al., 2018; Santoso et al., 2015; Steinrucken et al., 2017; Thao et
al., 2020; Watanabe, 1992; Yu et al., 2016). These locations include Plant
Ver. 3 August 17, 2021 11Hardiness Zones 12 – 14, which encompass Puerto Rico (Takeuchi et al.,
2018).
Hosts in PRA area Host plants of P. vexans that are present in Puerto Rico include Araceae:
Anthurium andraeanum (flamingo-lily), Colocasia esculenta (taro);
Chenopodiaceae: Spinacia oleracea (spinach); Euphorbiaceae: Hevea
brasiliensis (rubber); Fabaceae: Arachis hypogaea (peanut), Glycine
max (soybean), Medicago sativa (alfalfa), Parkinsonia aculeata
(Jerusalem thorn), Phaseolus vulgaris (kidney bean); Lauraceae: Persea
americana (avocado); Poaceae: Zea mays (corn); Proteaceae:
Macadamia integrifolia (macadamia nut); Rosaceae: Malus domestica
(apple); Rutaceae: Citrus reticulata (mandarin); Urticaceae: Boehmeria
nivea (ramie); Zingiberaceae: Zingiber officinale (ginger) (Dervis et al.,
2014; Feng et al., 2020; Hernández et al., 2019; Jabiri et al., 2020; Le,
2016; Mbaka, 2011; Munkvold and White, 2016; Noireung et al., 2020;
Nzungize et al., 2011; Park et al., 2019; Steinrucken et al., 2017; van der
Plaats-Niterink, 1981; Wheeler et al., 2005; Yu et al., 2016; Zeng et al.,
2005).
Economically Economically important hosts at risk in Puerto Rico include alfalfa,
important hosts at apple, avocado, corn, ginger, kidney bean, macadamia nut, mandarin,
riska peanut, ramie, rubber, soybean, spinach, and taro.
Potential Phytopythium vexans is likely to cause unacceptable consequences. This
consequences on pathogen can cause collar, corm, rhizome, root, and stem rot in many
economically hosts (Nakkeeran et al., 2018; Dervis et al., 2014; Dohroo ).
important hosts at Phytopythium vexans infection may lead to death and yield loss (Yu et
risk al., 2016). In rubber trees, P. vexans causes patch canker disease, which
is characterized by rotted bark wood and reduced latex flow (Zeng et al.,
2005).
Endangered Area The endangered area includes anywhere host plants are present in Puerto
Rico.
a
As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both
commercial and non-market (environmental) plants (IPPC, 2017).
The likelihood of introduction of Phytopythium vexans into the endangered area via
Dianthus spp. imported from Guatemala
Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Likelihood of
Entry
Ver. 3 August 17, 2021 12Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Pest prevalence on Medium High This pathogen is cosmopolitan (Lodhi et al.,
the harvested 2020) and listed under general references of
commodity carnation diseases (Nakkeeran et al., 2018;
Sharma and Sharma, 2008). We found one
reference of this pathogen’s presence in
Guatemala (Lodhi et al., 2020). In other areas,
P. vexans was isolated from 16.7 percent of
sampled field-grown grape (Spies et al., 2011)
and found in 100 percent and 20 percent of
durian and avocado farms surveyed,
respectively (Rodriguez-Padron et al., 2018;
Vawdrey et al., 2005).
Phytopythium vexans causes rot of carnation
stems near the soil line (Nakkeeran et al., 2018).
Because the exporter did not specify where on
the plant the cuttings would be collected from,
the cuttings may be taken from plants parts
containing the pathogen. Because of this and the
pathogen’s prevalence in other hosts, we began
with a risk rating of “Medium.”
Likelihood of Low Medium Infected cuttings may have discolored stems or
surviving post- wilted leaves (Nakkeeran et al., 2018), which
harvest processing would be visible. However, asymptomatic
before shipment infections occur in some hosts (Ivors et al.,
2008; Mircetich, 1971). The risk rating was
reduced by one level.
Likelihood of Low Negligible Transport and storage procedures in the
surviving transport exporting area are not being considered as part
and storage of this assessment. We did not change the
conditions of the previous risk rating.
consignment
Overall Low
Likelihood of
Entry
Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Ver. 3 August 17, 2021 13Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Likelihood of Medium If this pathogen were introduced to the area, it
Establishment would be able to spread to nearby hosts through
crop residues and through irrigation water
(Nakkeeran et al., 2018; Redekar et al., 2019).
Because of the presence of hosts in Puerto Rico
and ability to spread if introduced into the
environment, we chose a risk rating of
“Medium.”
Likelihood of Medium
Introduction
3.2.3. Impatiens necrotic spot virus (INSV) (Bunyavirales: Tospoviridae)
Impatiens necrotic spot virus is transmitted by thrips: Frankliniella occidentalis (western flower
thrips), F. fusca (tobacco thrips), and F. intonsa (Naidu et al., 2001; Sakurai et al., 2004;
Wijkamp and Peters, 1993). It has a wide host range encompassing both field and greenhouse
crops (Daughtrey et al., 1997).
The endangered area for Impatiens necrotic spot virus within Hawaii and Puerto Rico
Climatic Impatiens necrotic spot virus is present in Africa: Egypt, Uganda; Asia: China,
suitability Iran, Japan; Europe: Belgium, Bosnia and Herzegovina, Bulgaria, Czech
Republic, Finland, France, Germany, Greece, Hungary, Italy, Lithuania,
Netherlands, North Macedonia, Poland, Portugal, Serbian greenhouses, Slovenia,
United Kingdom; North America: Canada, Costa Rica, Mexico, continental
United States; Oceania: Australia, New Zealand nurseries; South America:
Chile, Colombia, Guatemala (Barriento Equite, 2006; Barrios, 2006; Beris et al.,
2020; Dejuk Protti, 2015; Ding et al., 2011; El-Deen Abd El-Wahab et al., 2011;
Elliott et al., 2009; EPPO, 2021; González-Pacheco and Silva-Rosales, 2013;
IPPC, 2018a; Kondo et al., 2011; Liu et al., 2010; Muwanika et al., 2013;
Sepúlveda et al., 2005; Shahraeen et al., 2002; Stanković et al., 2020; Tzanetakis
et al., 2009; Vásquez and Angarita, 1997; Veerakone et al., 2015). These
locations include Plant Hardiness Zones 11 - 13, which encompass Hawaii and
Puerto Rico (Takeuchi et al., 2018).
Hosts in PRA Host plants of INSV that are present in Hawaii and/or Puerto Rico include
area Amaryllidaceae: Hymenocallis littoralis (spiderlily); Apocynaceae: Vinca sp.
(periwinkle); Araceae: Spathiphyllum sp. (spathiphyllum), Zantedeschia
aethiopica (calla lily); Asteraceae: Cichorium intybus (chicory), Dahlia sp.
(dahlia), Lactuca sativa (lettuce), Tagetes sp. (marigold), Xerochrysum
bracteatum ( syn.: Bracteantha bracteata, Helichrysum bracteatum) (golden
everlasting); Balsaminaceae: Impatiens walleriana (buzzy lizzy); Brassicaceae:
Capsella bursa-pastoris (shepherd's purse); Cactaceae: Opuntia microdasys
(angel's-wings); Caryophyllaceae: Dianthus caryophyllus (carnation), D.
chinensis (pink); Cyperaceae: Cyperus esculentus (yellow nutsedge), C.
Ver. 3 August 17, 2021 14rotundus (purple nutsedge); Fabaceae: Arachis hypogaea (peanut), Vicia faba
(faba bean); Hydrangeaceae: Hydrangea macrophylla (hortensia); Lamiaceae:
Ocimum basilicum (basil), Salvia sp. (salvia); Liliaceae: Tulipa sp. (tulip);
Malvaceae: Hibiscus rosa-sinensis (China-rose), Malva parviflora (Egyptian
mallow); Orchidaceae: Dendrobium sp. (dendrobium), Phalaenopsis sp. (moth
orchid); Primulaceae: Lysimachia sp. (yellow loosestrife); Rosaceae: Schefflera
actinophylla (Australian cabbagetree); Rubiaceae: Gardenia jasminoides (Cape-
jessamine); Solanaceae: Capsicum annuum (pepper), Nicotiana tabacum
(tobacco), Physalis peruviana (Cape-gooseberry), P. philadelphica (syn.: P.
ixocarpa) (tomatillo), Solanum lycopersicum (tomato), S. tuberosum (potato)
(Beris et al., 2020; Blockley and Mumford, 2001; Eiras et al., 2012; Elliott et al.,
2009; González-Pacheco and Silva-Rosales, 2013; Kuo et al., 2014; Liu et al.,
2010; Louro, 1995; Martinez-Ochoa et al., 2003; Martinez-Ochoa et al., 2004;
Materazzi and Triolo, 2001; Pappu et al., 1999; Pourrahim et al., 2012; Roggero
et al., 1999; Rudzińska-Langwald and Kamińska, 1998; Stanković et al., 2020;
Zhang et al., 2010).
Economically Economically important hosts at risk in Hawaii and/or Puerto Rico include both
important agricultural and ornamental plants. Some agriculturally important crops include
a
hosts at risk basil, bell pepper, chicory, faba bean, lettuce, peanut, potato, tobacco, tomatillo,
and tomato. Ornamental plants include buzzy lizzy, calla lily, Cape-jessamine,
dendrobium, hortensia, moth orchid, shoeblackplant, and spider lily.
Potential INSV is likely to cause unacceptable consequences. INSV distorts foliage,
consequences produces yellowing and dead areas on plant tissue, and stunts plants (Beris et al.,
on 2020; Koike et al., 2008; Kuo et al., 2014). The virus can inhibit fruit production
economically in pepper and fruit that is produced ripens unevenly with dead, concentric green
important rings (Naidu et al., 2005). Severely infected basil and lettuce are unmarketable
hosts at risk due to leaf necrosis and stunting (Grausgruber-Gröger, 2012; Kuo et al., 2014).
Infected spinach also have malformed leaves which may affect marketability
(Liu et al., 2009). Disease incidence for INSV has been reported as 20 to 39
percent in field-grown spinach, 50 percent in greenhouse potato minitubers, 70
to 80 percent in greenhouse basil, and 40 percent for field-grown lettuce (Beris et
al., 2020; Kuo et al., 2014; Liu et al., 2009; Grausgruber-Gröger, 2012; Crosslin
and Hamlin, 2010).
Endangered The endangered area includes anywhere host plants are present in Hawaii and
Area Puerto Rico.
a
As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both
commercial and non-market (environmental) plants (IPPC, 2017).
The likelihood of introduction of Impatiens necrotic spot virus into the endangered area via
Dianthus spp. imported from Guatemala
Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Likelihood of
Entry
Ver. 3 August 17, 2021 15Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Pest prevalence on High Medium Dianthus caryophyllus and D. chinensis were
the harvested found infected with INSV (Roggero et al., 1999;
commodity Shahraeen et al., 2002). INSV has been reported
with an incidence of up to 40 percent in spinach
and 50 percent in greenhouse-grown potato
(Crosslin and Hamlin, 2010; Liu, 2009).
Because of the high incidence in these hosts, we
began with a risk rating of “High.”
Likelihood of Medium Medium INSV causes symptoms such as leaf
surviving post- malformation, necrosis, and ringspot in basil,
harvest processing lettuce, and spinach (Grausgruber-Gröger, 2012;
before shipment Kuo et al., 2014; Liu et al., 2009). While
symptomatic D. chinensis may be culled,
asymptomatic infections may also occur
(Roggero et al., 1999; Martinez-Ochoa et al.,
2003). We reduced the risk rating to “Medium.”
Likelihood of Medium Negligible Transport and storage procedures in the
surviving transport exporting area are not being considered as part
and storage of this assessment. We did not change the
conditions of the previous risk rating.
consignment
Overall Medium
Likelihood of
Entry
Risk Element Risk Uncertainty Evidence for rating (and other notes as
Rating Rating necessary)
Likelihood of High Low Hawaii and Puerto Rico have suitable hosts and
Establishment the vectors Frankliniella occidentalis and F.
fusca are present in both areas (Cho et al., 1987;
Feliciano et al., 2008; GBIF, 2021; POWO,
2021; USDA NRCS, 2021; Yudin et al., 1987).
Were INSV introduced to the area, it can spread
to nearby hosts.
Likelihood of Medium
Introduction
(combined
likelihoods of entry
and establishment)
Ver. 3 August 17, 2021 164. Summary
Of the organisms associated with Dianthus spp. in the export area and present worldwide, we
identified three that are quarantine pests for the United States and Territories. These pests are
likely to meet the threshold for unacceptable consequences in the PRA area (Table 3). Thus,
these also have a reasonable likelihood of following the commodity pathway (Table 3). Thus,
these pests are candidates for risk management. These results represent a baseline estimate of the
risks associated with the import commodity pathway as described in section 1.4.
Table 4. Summary of pests that met the threshold for unacceptable consequences of
introduction, have a reasonable likelihood of following the commodity pathway, and thus, are
candidates for risk management.
Pest type Scientific name Likelihood of Uncertainty
Introduction statement
(optional)a
Arthropod Liriomyza huidobrensis (Blanchard) Medium
Chromistan Phytopythium vexans (de Bary) Abad, de Cock, Bala, Medium*
Robideau, Lodhi & Lévesque
Virus Orthotospovirus Impatiens necrotic spot virus Medium**
a
The uncertainty statement, if included, identifies the most important source(s) of uncertainty.
* This organism is a quarantine pest for U.S. Territories only.
** This organism is a quarantine pest for Hawaii and U.S. Territories only.
Our assessment of risk is contingent on the application of all components of the pathway as
described in section 1.4. Appropriate phytosanitary measures to mitigate pest risk are addressed
in a separate document.
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