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 1 | G. pallida 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 2 | G. pallida 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. 3 | G. pallida 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. 4 | G. pallida 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.