Pest Risk Assessment for Potential Invaders of Minnesota

Minnesota Invasive Terrestrial Plants & Pests Center New Species Evaluation

Globodera pallida (Stone 1973) (Pale cyst nematode)

Evaluated: A.C. Morey; Reviewed: R.C. Venette (1/15/20)

OVERVIEW:

Common names: pale cyst nematode (PCN), white potato cyst nematode, potato cyst nematode (also used for other Globodera spp.), potato root eelworm Synonyms: Heterodera pallida, Heterodera rostochiensis sensu lato

[from Moens et al. 2018, Jones 2017]

Of the eight genera of cyst nematodes, only two – Heterodera and Globodera – contain economically important species. Within Globodera, three species are of major importance: G. pallida, G. rostochiensis, and G. tabacum. All are found worldwide in temperate regions, with their economic damage restricted to hosts within Solanaceae.

Globodera pallida differs from G. rostochiensis because females lack the morphological “golden phase” of development. Globodera pallida was originally designated as a pathotype to G. rostochiensis (=Heterodera rostochiensis sensu lato) prior to description in 1973. Both species are considered native to Peru. There are few specific symptoms associated with G. pallida infection, and it is often confused with other stresses. Death of the plant from G. pallida infection is rare, but infection by the nematode can reduce plant productivity (e.g., potato) to the point of crop loss and make the plant more susceptible to fungal pathogens.

MAJOR KNOWLEDGE GAPS ASSOCIATED WITH ASSESSMENT:

 Climate tolerance  Natural dispersal capacity  Impact to native communities  Impact on ecosystem services

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ARRIVAL Proximity to Minnesota: MEDIUM

RANKING Very High Pest is known to occur in Minnesota Pest occurs in Wisconsin, Iowa, South Dakota, North Dakota, Manitoba or High Ontario Medium Pest occurs in North America Low Pest is not known to occur in North America

Globodera pallida does not currently occur in Minnesota (MDA 2019).

Globodera pallida was documented in the U.S. for the first time in 2006 during a routine survey of an Idaho potato field (Hafez et al. 2007). It has not yet been found anywhere else in the U.S. (CERIS 2019).

In Canada, its current distribution is limited to regions in Newfoundland (CABI 2019; Stone, Thompson, and Hopper 1977), with a putative record for Alberta (Mackesy, Molet, and Sullivan 2016).

The global distribution of G. pallida otherwise includes numerous countries in Europe, Asia, Africa, Central and South America, and New Zealand (CABI 2019; Ferris 2019; Zasada and Dandurand 2018).

Existence of Pathways: MEDIUM

RANKING High Pathways for arrival of the pest in Minnesota are known to occur Pathways for the arrival of the pest in Minnesota are conceivable, but not Medium known to occur Low Pathways for arrival of the pest in Minnesota are difficult to conceive

Globodera pallida does not currently occur in Minnesota (see Proximity to Minnesota), but it is currently federally regulated by the USDA to prevent spread from Idaho. No regulations in Minnesota exist, but negative survey results are required for export of seed potatoes from the state (MDA 2019).

Movement of soil from an area infected with G. pallida is considered the primary pathway of spread into new areas, such as soil adhere to farming equipment, seed potatoes, tare dirt, animals, and humans (Mackesy, Molet, and Sullivan 2016; USDA- APHIS 2015). Cysts can also be present in soil adhering to other plant materials and in water run-off (Moens, Perry, and Jones 2018). It is believed that G. pallida (and G. rostochiensis) were first introduced into Europe from potatoes originating from the nematodes’ native range in South America. Subsequent introductions to North

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America appear to have occurred from infested potato seed pieces coming from Europe (Mackesy, Molet, and Sullivan 2016).

Though the import of soil and potatoes is highly regulated, risk is still assumed through movement of soil and potato smuggling as well as different plant and non- plant material that may have minute amounts of infested soil present, such as second-hand vehicles (Mackesy, Molet, and Sullivan 2016).

Entry into Minnesota could also occur through the dispersal of cysts via wind, rain, and flood or irrigation water (Mackesy, Molet, and Sullivan 2016; Ferris 2019), though this is unlikely at present given the lack of nearby infestations to the state (see Proximity to Minnesota).

Innate Dispersal Capacity: MODERATELY LOW

RANKING Maximum recorded dispersal >500 km per year (or moves in low level Very High jets/ upper atmosphere) High Maximum recorded dispersal 500-250 km per year Moderate Maximum recorded dispersal 100-250 km per year Maximum recorded dispersal 1-100 km per year (wind dispersal; flowing Moderately Low water) Maximum recorded dispersal <1 km per year (movement through soil; Low splash dispersal)

Like other cyst forming nematodes G. pallida has sedentary endoparasitic habits; it has no stage for active long-distance dispersal (USDA-APHIS 2015; Ferris 2019) Juveniles and males disperse through the soil to neighboring roots to feed and mate, respectively, though such movement is only a maximum of 1 m (Mackesy, Molet, and Sullivan 2016). Once formed, cysts can stay attached to roots or break off and are free in the soil, persisting for many years (Mackesy, Molet, and Sullivan 2016). In the absence of a host, viable cysts have been recorded to persist in the soil for 20-30 years (Zasada and Dandurand 2018; USDA-APHIS 2015; Christoforou et al. 2014).

Passive transport of cysts can also occur via wind (i.e., blown in soil), rain, and other water sources (Mackesy, Molet, and Sullivan 2016). Specific estimates for passive dispersal could not be found.

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ESTABLISHMENT AND PERSISTENCE

Suitability of Minnesota Climate: HIGH

RANKING High >40% of Minnesota is predicted to be suitable Medium >20 to 40% of Minnesota is predicted to be suitable Low >0 to 20% of Minnesota is predicted to be suitable Negligible No part of Minnesota is suitable

The counties in Idaho where G. pallida has been found (Bingham and Bonneville) (Hafez et al. 2007; Mackesy, Molet, and Sullivan 2016) have regions of USDA Zone 4b or warmer (USDA-ARS 2012). Similarly, regions in Newfoundland, Canada (Manuels and Botwood) (Stone, Thompson, and Hopper 1977) where G. pallida occurs are equivalent to Zones 4b or warmer (NRC 2014).

Description of extreme climate tolerance for G. pallida could not be found, but a study of G. rostochiensis found that both hatched and unhatched juveniles could survive sub-zero temperatures by supercooling, though unhatched nematodes in cysts survived more extreme temperatures, even in the presence of water (Perry and Wharton 1985). Hatched juveniles could survive brief periods down to -5 to -6°C until freezing was initiated, which subsequently results in 100% mortality. More than 50% of eggs within cysts, however, were still alive after brief exposure to -20°C (Perry and Wharton 1985). Globodera pallida is considered to be adapted to lower hatching and juvenile development temperatures than G. rostochiensis (Moens, Perry, and Jones 2018; Ebrahimi et al. 2014), so the cold tolerance estimates for G. rostochiensis are assumed reasonable for G. pallida.

USDA Zone 4b covers roughly 40% of Minnesota. Though the information available is uncertain, based on laboratory experiments of G. rostochiensis, it is likely that G. pallida can establish in colder USDA Hardiness Zones than those in which it currently occurs. The indigenous region of both species is the high Andean region of Peru were prolonged frost can occur (Perry and Wharton 1985). Globodera pallida overwinters as unhatched juveniles within a cyst (Mackesy, Molet, and Sullivan 2016), which would occur underground, attached to the host root or detached in the surrounding soil. This can significantly buffer the surrounding temperature depending on depth, though the tolerance to prolonged sub-zero temperature is unknown for either species. For example, minimum 10-cm soil temperatures during five recent winters in Minnesota were typically around -6°C (Morey et al. 2012). Therefore, >40% of Minnesota is estimated as suitable based on climate.

It is noted that G. pallida, like G. rostochiensis, usually have an obligate diapause during their first season of development, but a facultative diapause occurs in the second season onwards. Diapause is terminated in late spring for these species (Moens, Perry, and Jones 2018). How this may impact their distribution and climate tolerance is unknown.

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Presence of Hosts: LOW

RANKING High >10% of Minnesota with suitable hosts (or habitat for weeds) Medium >1 to 10% of Minnesota with suitable hosts (or habitat for weeds) Low >0 to 1% of Minnesota with suitable hosts (or habitat for weeds) Negligible 0% of Minnesota with suitable hosts (or habitat for weeds)

Globodera pallida is an obligate parasite of solanaceous plants (Christoforou et al. 2014). The known host range includes mainly Solanum spp., but other genera within Solanaceae are also suitable (e.g., Lycopersicon, Datura, Hyoscyamus) (CABI 2019; Ferris 2019; Sullivan et al. 2007; Boydston et al. 2010). The major host of G. pallida is the potato (Solanum tuberosum), with S. lycopersicum (tomato), S. melongena (eggplant/aubergine), and S. dulcamara considered minor hosts (Mackesy, Molet, and Sullivan 2016). Some reproduction of G. pallida was observed on tobacco in a laboratory setting (Skantar et al. 2007).

Potato production in Minnesota was about 46,000 acres in 2017 (Lofthus 2018). This amounts to <1 % of state land. In 2017, 577 acres of tomato were harvested either as open fresh market or processing, or under protection (quickstats.nass.usda.gov). Combined, these crops are <1 % of state land. Though wild weedy hosts may also be present in the state, their contribution is assumed not significant to the total area at risk.

Hybridization/Host Shift: HIGH

RANKING High Species reported to hybridize or has undergone a documented host shift Medium Species in the same genus have been reported to hybridize/shift hosts Low Hybridization/Host shifts have not been reported for this genus or species

Hybridization between G. rostochiensis and G. pallida is said to naturally occur (Mackesy, Molet, and Sullivan 2014). It is noted that a few pathotypes have been identified in G. pallida, which are identified based on their inability to develop on specific potato cultivars (Mackesy, Molet, and Sullivan 2016; EPPO 2019), and that the species was previously synonymized with G. rostochiensis as a pathotype (Moens, Perry, and Jones 2018).

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SPREAD

Existence of Pathways: MEDIUM

Globodera pallida does not currently occur in Minnesota. The state is among the top potato producers in the U.S. (Mackesy, Molet, and Sullivan 2016), making spread within the state highly likely were the species to arrive.

Pathways for spread of G. pallida within Minnesota are similar as those of arrival into the state. Human-mediate movement of soil from an area infected with G. pallida is considered the primary pathway of spread into new areas, such as soil adhere to farming equipment, seed potatoes, tare dirt, animals, and humans (Mackesy, Molet, and Sullivan 2016; USDA-APHIS 2015). Cysts can also be present in soil adhering to other plant materials and in water run-off (Moens, Perry, and Jones 2018). It is believed that G. pallida (and G. rostochiensis) were first introduced into Europe from potatoes originating from the nematodes native range in South America. Subsequent introductions to North America appear to have occurred from infested potato seed pieces coming from Europe (Mackesy, Molet, and Sullivan 2016).

Dispersal Capacity-Reproductive Potential: MEDIUM

RANKING High Annual reproductive potential (r) of pest is >500 descendants per year Medium Annual reproductive potential (r) of pest is 100 to 500 descendants per year Low Annual reproductive potential (r) of pest is <100 descendants per year

Globodera pallida reproduces sexually and typically has one generation a year (Moens, Perry, and Jones 2018; Ferris 2019), though more than one can occur depending on the crop cycle (Mackesy, Molet, and Sullivan 2016). Between 200-600 eggs develop within the body of a G. pallida female; once the female dies, her body forms a cyst that remains attached to roots or detaches into the soil (Mackesy, Molet, and Sullivan 2016).

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At 25°C, the viability of G. pallida eggs in a lab study was over 97% (Christoforou et al. 2014). Another source states hatch to be up to 80% in the presence of host root diffusates (Ferris 2019). Using 80% viability, 160-480 descendants could be produced each year.

Extent of Invasion: HIGH

RANKING Very High >60 countries likely to have established populations of the pest High 30-60 countries likely to have established populations of the pest Moderate 15-29 countries likely to have established populations of the pest Moderately Low 7-14 countries likely to have established populations of the pest Low 1-7 countries likely to have established populations of the pest

Globodera pallida is not currently documented in Minnesota (see Proximity to Minnesota). If G. pallida were to arrive as a single point in Minnesota within the next year, here estimated as Hennepin Co. (a centralized county with high relative potato production in USDA Zone 4b), the following considerations were made to estimate an invasion extent:

As a presumed Zone 4b species, 56 total counties are climatically suitable within Minnesota (see Suitability of Minnesota Climate).

Based on host availability (see Presence of Hosts), in 2017, ~46 counties throughout Minnesota showed reportable acreage of potatoes (quickstats.nass.usda.gov). Of those, about 15 were in areas colder than Zone 4b (USDA-ARS 2012), leaving 31 counties.

Assuming a 50km/year spread via innate dispersal, (half of the estimated maximum; see Innate Dispersal) which may be an underestimate given the most likely route of spread is unintentional human-mediated movement, a 500km radius from the Hennepin Co. would include all 31 counties with suitable hosts and climate.

Existence of Vectors: NONE

RANKING High Vectored by birds or long distance insect migrants Medium Vectored by insects or bats Low Vectored by other mammals None No evidence of any vectors

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There is no evidence that G. pallida is vectored by any of the above. CABI (2019) stated that cysts can survive passage through the gut of animals to infest new areas. However, this could not be further substantiated.

IMPACT

Problem Elsewhere: HIGH

RANKING High Noted as a problem within its native range and areas where it has invaded Medium Noted as a problem only in areas where it has invaded Low Not reported as a problem elsewhere

Globodera pallida is considered native to the central Andes of Peru and Boliva (Picard, Sempere, and Plantard 2007; Moens, Perry, and Jones 2018; CABI 2019). It is considered a major pest of potatoes in South America, including the Andean region (Picard, Sempere, and Plantard 2007).

Globally, G. pallida and G. rostochiensis are considered the most important nematode threats to potato production (Mimee, Dauphinais, and Bélair 2015). Globodera pallida is present in some 55 countries, and on the quarantine list of some 80 countries (Moens, Perry, and Jones 2018; CABI 2019; Mackesy, Molet, and Sullivan 2016).

Impact to Yields and Marketability: HIGH

RANKING High >$5 million Medium $5 million to 0.5 million Low <$0.5 million

The economic impact of G. pallida by itself is difficult to measure because this species can co-occur in mixed populations with G. rostochiensis.

Unmanaged infestations of G. pallida have been listed to cause yield losses between 20-70% in potatoes (USDA-APHIS 2016; Mackesy, Molet, and Sullivan 2016). Other estimates state potato yields can be reduced up to 80%, though this may be in circumstances of co-infection with G. pallida and G. rostochiensis (Zasada and Dandurand 2018; Mackesy, Molet, and Sullivan 2016; USDA-APHIS 2015). In Europe, G. pallida and G. rostochiensis are responsible for potato tuber losses of up to 9% (Moens, Perry, and Jones 2018; Mackesy, Molet, and Sullivan 2016), and an average loss of 50-60% in Norway (CABI 2019).

Globodera pallida appears to be more responsive to potato root diffusates than G. rostochiensis, and consequently, G. pallida reproduces more and predominates where both species are present (Ferris 2019). This is exacerbated due to

8 | G. pallida commercially-available potato cultivars being more susceptible to G. pallida than G. rostochiensis (CABI 2019; Ferris 2019); in some regions, G. pallida appears to be replacing G. rostochiensis (Trudgill et al. 2003).

The value of potato production in Minnesota was $172,855,000 in 2017 (Lofthus 2018). If just 20% yield reduction (i.e., lowest of the estimates) were to occur in Minnesota potatoes, a total of $34.6 million could be lost.

Costs of Quarantine or Other Mitigation (annual): HIGH

RANKING High >$5 million Medium $5 million to 0.5 million Low <$0.5 million

The discovery of G. pallida in Idaho caused Japan, Korea, Canada, and Mexico to ban fresh potato imports from Idaho, though not all of the bans persisted (Ferris 2019). Should G. pallida be found in MN, similar quarantines would likely result (MDA 2019), thus halting statewide potato movement.

The value of potato production in Minnesota was $172,855,000 in 2017 (Lofthus 2018). Less than 3% of this production would need to be lost to quarantine to surpass $5 million. Moreover, an estimated $11 million has been allocated to eradicate and control G. pallida in Idaho (CABI 2019).

Impacts to Recreation or Real Estate (annual): NONE

RANKING High >$5 million Medium $5 million to 0.5 million Low <$0.5 million None $0

There are no documented negative impacts to recreation or real estate due to the presence of G. pallida. However, the long lifespan of egg-containing cysts in the soil (Zasada and Dandurand 2018; Christoforou et al. 2014) could affect sales of farm land.

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Consequences to Native Species (Score): 2

References are only needed for the “worst case” situation.

RANKING Could reasonably be expected to affect federally listed Threatened and 5 Endangered Species Could directly, negatively impact pollinator 4 Causes local loss of native species 4 Lowers density of native species (empirical support) 3 Infection to native fauna or flora 2 Consumes native fauna or flora 2 Production of toxic substances including allelochemicals 2 Lowers density of native species (presumed due to dense thicket or vining) 2 Host for recognized pathogens/parasites of native species 1 None of the above apply 0

Some native Solanum spp. occur in Minnesota, including S. rostratum (Chayka and Dziuk 2017), which is a listed host of G. pallida and G. rostochiensis (Sullivan et al. 2007).

Consequences to Ecosystem Services (Score): 0

RANKING Modification of soil, sediments, nutrient cycling Alteration of genetic resources Alteration of biological control Changes in pollination services Alteration of erosion regimes Affects hydrology or water quality (includes effects of management) Creates a fire hazard Interferes with carbon sequestration

No documented effects of G. pallida on ecosystem services were found.

Facilitate Other Invasions: MEDIUM

Invasion by the organism could lead to invasions of other species.

RANKING High The invasive species has facilitated invasions elsewhere The invasive species is a plant or animal that could reasonably be expected Medium to be a host or vector of another invasive species The species has not been reported to facilitate invasion elsewhere and is Low not likely to directly aid in the invasion of other species

There is no evidence that G. pallida facilitates the invasion of another species. Globodera pallida has been found in co-infection with the fungal pathogens

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Verticillium dahliae and Rhizoctonia solani, which can lead to earlier plant death. When eggs hatch from the cysts, ruptures in the root may provide easier entry into the plant for soil borne pathogens (Back, Haydock, and Jenkinson 2002; Mackesy, Molet, and Sullivan 2016). However, the nativity of these fungal pathogens is not clear.

REFERENCES

Back, M. A., P. P. J. Haydock, and P. Jenkinson. 2002. “Disease Complexes Involving Plant Parasitic Nematodes and Soilborne Pathogens.” Plant Pathology 51 (6): 683–97. https://doi.org/10.1046/j.1365-3059.2002.00785.x. Boydston, R. A., H. Mojtahedi, C. Bates, R. Zemetra, and C. R. Brown. 2010. “Weed Hosts of Globodera Pallida from Idaho.” Plant Disease 94 (7): 918–918. https://doi.org/10.1094/PDIS-94-7-0918B. CABI, CAB International. 2019. “Globodera Pallida (White Potato Cyst Nematode).” Invasive Species Compendium. 2019. https://www.cabi.org/isc/datasheet/27033. CERIS, Center for Environmental and Research Information Systems. 2019. “Survey Status of Pale Cyst Nematode - Globodera Pallida (2018).” Purdue University. http://pest.ceris.purdue.edu/map.php?code=NEFBBBC#. Chayka, K., and P.M. Dziuk. 2017. “Minnesota Wildflowers.” 2017. https://www.minnesotawildflowers.info/. Christoforou, M., I. S. Pantelides, L. Kanetis, N. Ioannou, and D. Tsaltas. 2014. “Rapid Detection and Quantification of Viable Potato Cyst Nematodes Using QPCR in Combination with Propidium Monoazide.” Plant Pathology 63 (5): 1185–92. https://doi.org/10.1111/ppa.12193. Ebrahimi, Negin, Nicole Viaene, Kürt Demeulemeester, and Maurice Moens. 2014. “Observations on the Life Cycle of Potato Cyst Nematodes, Globodera Rostochiensis and G. Pallida, on Early Potato Cultivars.” Nematology 16 (8): 937– 52. https://doi.org/10.1163/15685411-00002821. EPPO, EPPO Global Database. 2019. “Globodera Rostochiensis and Globodera Pallida.” Data Sheets on Quarantine Pests. 2019. https://gd.eppo.int/taxon/HETDRO/documents. Ferris, H. 2019. “Globodera Pallida.” Nemaplex - Globodera. 2019. http://nemaplex.ucdavis.edu/Taxadata/G053s1.aspx. Hafez, S. L., P. Sundararaj, Z. A. Handoo, A. M. Skantar, L. K. Carta, and D. J. Chitwood. 2007. “First Report of the Pale Cyst Nematode, Globodera Pallida , in the United States.” Plant Disease 91 (3): 325–325. https://doi.org/10.1094/PDIS-91-3-0325B. Lofthus, D. 2018. “Minnesota Ag News – Potatoes.” St. Paul, MN: USDA National Agricultural Statistics Service. https://www.nass.usda.gov/Statistics_by_State/Minnesota//Publications/Crop s_Press_Releases/2018/MN-Potatoes-09-18.pdf. Mackesy, D., T. Molet, and M. Sullivan. 2014. “CPHST Pest Datasheet for Globodera Rostochiensis” 5: 1–19. ———. 2016. “CPHST Pest Datasheet for Globodera Pallida.” USDA-APHIS-PPQ- CPHST. http://download.ceris.purdue.edu/file/3313. MDA, Minnesota Department of Agriculture. 2019. “Potato Cyst Nematode.” Insect Pests & Dieseases. 2019. https://www.mda.state.mn.us/plants-insects/potato-

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cyst-nematode. Mimee, Benjamin, Nathalie Dauphinais, and Guy Bélair. 2015. “Life Cycle of the Golden Cyst Nematode, Globodera Rostochiensis, in Quebec, Canada.” Journal of Nematology 47 (4): 290–95. Moens, Maurice, Roland N Perry, and John T Jones. 2018. “Cyst Nematodes - Life Cycle and Economic Importance.” In Cyst Nematodes, edited by R.N. Perry, M. Moens, and J.T. Jones, 1–18. Wallingford, UK: CAB International. Morey, Amy C., William D. Hutchison, Robert C. Venette, and Eric C. Burkness. 2012. “Cold Hardiness of Helicoverpa Zea (Lepidoptera: Noctuidae) Pupae.” Environmental Entomology 41 (1): 172–79. https://doi.org/10.1603/EN11026. NRC, Natural Resources Canada. 2014. “Extreme Minimum Temperature Zones.” Minister of Natural Resources Canada. http://planthardiness.gc.ca/images/PHZ_2014_USDA_Map_30M.pdf. Perry, R.N., and D.A. Wharton. 1985. “Cold Tolerance of Hatched and Unhatched Second Stage Juveniles of the Potato Cyst-Nematode Globodera Rostochiensis.” International Journal for Parasitology 15 (4): 441–45. https://doi.org/10.1016/0020-7519(85)90031-1. Picard, Damien, Thierry Sempere, and Olivier Plantard. 2007. “A Northward Colonisation of the Andes by the Potato Cyst Nematode during Geological Times Suggests Multiple Host-Shifts from Wild to Cultivated Potatoes.” Molecular Phylogenetics and Evolution 42 (2): 308–16. https://doi.org/10.1016/j.ympev.2006.06.018. Skantar, A. M., Z. A. Handoo, L. K. Carta, and D. J. Chitwood. 2007. “Morphological and Molecular Identification of Globodera Pallida Associated with Potato in Idaho.” Journal of Nematology 39 (2): 133–44. http://www.ncbi.nlm.nih.gov/pubmed/19259482. Stone, A.R., P.R. Thompson, and B.E. Hopper. 1977. “Globodera Pallida Present in Newfoundland.” Plant Disease Reporter 61 (7): 590–91. https://babel.hathitrust.org/cgi/pt?id=chi.23661245&view=1up&seq=74. Sullivan, M., R.N. Inserra, J. Franco, and N. Greco. 2007. “Potato Cyst Nematodes: Plant Host Status and Their Regulatory Impact.” Nematropica 37 (2): 193–202. Trudgill, D. L., M. J. Elliott, K. Evans, and M. S. Phillips. 2003. “The White Potato Cyst Nematode (Globodera Pallida) - A Critical Analysis of the Threat in Britain.” Annals of Applied Biology 143 (1): 73–80. https://doi.org/10.1111/j.1744- 7348.2003.tb00271.x. USDA-APHIS, United States Department of Agriculture Animal and Plant Health Inspection Service. 2015. “Pest Alert: Potato Cyst Nematode.” USDA-APHIS-PPQ. https://doi.org/10.1111/ppa.12065/abstract. ———. 2016. “Pale Cyst Nematode; Update of Quarantined Areas.” Federal Register. Vol. 81. https://www.aphis.usda.gov/plant_health/plant_pest_info/potato/downloads/ pcndocs/frnotices/2016-0047.pdf. USDA-ARS, United States Department of Agriculture - Agricultural Research Service. 2012. “USDA Plant Hardiness Zone Map.” 2012. https://planthardiness.ars.usda.gov/PHZMWeb/. Zasada, Inga, and Louise-Marie Dandurand. 2018. “PCN by the Numbers.” Globodera Alliance Newsletter, December 2018. https://www.globodera.org/sites/default/files/newsletters/Issue 7 Globodera Alliance Newsletter Dec 2018_0.pdf.

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