EPPO Datasheet: Amaranthus tuberculatus
Authority: (Moquin-Tandon) Sauer
Taxonomic position: Plantae: Magnoliophyta: Angiospermae: Basal core eudicots: Caryophyllales: Amaranthaceae: Amaranthoideae
Other scientific names: Acnida altissima (Riddell) Standley, Acnida tuberculata Moquin-Tandon, Amaranthus altissima Riddell, Amaranthus rudis Sauer
Common names in English: rough-fruit amaranth, rough-fruited water-hemp, tall waterhemp (US)
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EPPO Categorization: A2 list
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EPPO Code: AMATU
GEOGRAPHICAL DISTRIBUTION 2021-01-27
History of introduction and spread
Amaranthus tuberculatus is native to North America (Central and Eastern Central United States), where the species is recorded as being weedy in the United States and Canada (Costea et al., 2005; USDA‐NRCS, 2019). There is some uncertainty to the status of the species in the Canadian provinces of Ontario and Quebec. The species ‘… has gone from virtual obscurity to being the most commonly encountered and troublesome weed’ in agriculture, in particular in the Midwestern United States over the last 30 years (Sarangi & Jhala, 2018; Sarangi et al., 2019). In North America, A. tuberculatus occurs mostly at latitudes between 45° and 30° North (USDA‐NRCS, 2019).
A. tuberculatus was introduced into the EPPO region presumably in the middle of the 20th century. However, the species might have already been introduced before (e.g. in Switzerland). The early records were of small and transient populations scattered across the EPPO region (e.g. Austria and the United Kingdom). The first naturalized populations presumably occurred from the middle of 1970s onwards in Italy. Established populations occur in Italy, Israel and most probably in Spain (Sánchez Gullón & Verloove, 2013).
DistributionEPPO Region: Belgium, Bosnia and Herzegovina, Croatia, Czech Republic, Finland, Germany, Israel, Italy (mainland), Jordan, Netherlands, Romania, Russia, Spain (mainland), Ukraine
Asia: Israel, Jordan
North America: Canada (British Columbia, Ontario, Prince Edward Island, Québec), United States of America (Alabama, Arkansas, California, Colorado, Connecticut, Delaware, Georgia, Idaho, Illinois, Indiana, Iowa, Kansas, Kentucky, Louisiana, Maine, Maryland, Massachusetts, Michigan, Minnesota, Mississippi, Missouri, Nebraska, Nevada, New Hampshire, New Mexico, New York, North Carolina, North Dakota, Ohio, Oklahoma, Pennsylvania, South Carolina, South Dakota, Tennessee, Texas, Vermont, Washington, West Virginia, Wisconsin)
Misidentification of Amaranthus species can occur throughout its range due to the morphological variation within species and hybridization between species (Wetzel et al., 1999). There are several identification keys that can be used to distinguish between Amaranthus species (e.g. Pratt & Clark, 2001; Horak et al., 2019). Some of the key characteristics include flower morphology (needing magnification due to their small size), leaf shape, presence or absence of hair on the stem, seed head shape and seedling shape (Pratt & Clark, 2001). Iamonico (2015) provides short descriptions of Amaranthus species that can been found in the EPPO region.
The following description is primarily based on Costea et al. (2005) and Mosyakin & Robertson (2003): A. tuberculatus is an annual herbaceous dioecious species, with a taproot, and it reproduces only by seeds. Stems of mature plants are erect, sometimes ascending, up to (5–) 20–200 (–300) cm in height, glabrous or with sparse hairs. Leaves are long petioled, ovate, rhombic‐oblong to lanceolate‐oblong (2–10 cm long, 1–3 cm wide), while the upper leaves are reduced and narrow. Male and female flowers occur on separate plants (dioecious) and the terminal inflorescences are 10–20 cm long, usually unbranched or with numerous panicled branches. Fruits are about 1.5 mm long, transversal (circumscissile) dehiscent at the middle, rugose, often reddish. Seeds are elliptic to obovate, dark reddish brown to dark brown, and 0.7–1 mm in diameter.
BIOLOGY AND ECOLOGY 2021-01-27
A. tuberculatus is a small‐seeded, summer annual species. In its native range, A. tuberculatus is a late‐emerging weed species. In Southern Ontario (Canada), it typically initiates emergence from the beginning of June to August. In Iowa (United States), emergence begins in mid‐May to late May and continues through early August. Flowering depends on the photoperiod.
A. tuberculatus is a prolific seed producer (Costea et al., 2005; Heneghan & Johnson, 2017). When allowed to develop for a full growing season, A. tuberculatus has demonstrated the ability to produce up to 1 million seeds per plant (Steckel et al., 2003). There is no specific information regarding natural seed dispersal of A. tuberculatus (Costea et al., 2005). The species can produce a large amount of seeds which are light in weight, though they have no special adaptions for wind‐dispersal. Seeds are assumed to fall near the mother plant. However, natural local dispersal is most likely accomplished by water, as with other Amaranthus spp., as both seeds and fruits can float easily (Costea et al., 2005). Seeds may be dispersed by raindrops and streamlets produced on the soil by rain.
Seeds persist for approximately 4–5 years in the soil in normal conditions (Steckel, 2007). However, seeds buried at 20 cm soil depth retained 3% viability after 17 years (Nebraska/United States, Burnside et al., 1996). The seed bank of A. tuberculatus in crop fields may contain tens of thousands of seeds per m2 as shown by Buhler et al. (2001), comprising up to 90% of the total seed bank (Iowa/United States). A. tuberculatus has a rapid growth rate at an average of 0.135 cm of growth per growing degree day (Steckel, 2007).
In its native range, A. tuberculatus was initially described as growing in wet areas such as margins of rivers, ponds, marshes, lakes and creeks (Sauer, 1955). Nowadays, it is found in any disturbed habitats lacking permanent vegetation, in particular in summer crop fields, along roadsides and railroads up to 1000 m above sea level (Sauer, 1955; Mosyakin & Robertson, 2003; Costea et al., 2005).
Within the EPPO region, A. tuberculatus is present in a number of different environments, including floodplains and banks of major rivers such as the Po, Rhine, Maas and Waal (Verloove, 2019), ruderal habitats (e.g. railway tracks, port areas; Sánchez Gullón & Verloove, 2013; Junghans, 2016) and to a lesser extent crop fields (Banfi & Galasso, 2010; Masin & Scortegagna, 2012; Pellizzari et al., 2015; Iamonico, 2015). Some data is available on A. tuberculatus showing that it is able to invade natural riverside vegetation in Italy (Iamonico, 2015).
A. tuberculatus occurs over a wide climatic range. In North America, it occurs preferably at latitudes between 45° and 30° North (USDA‐NRCS, 2019). Costea et al. (2005) summarizes the ecological preferences of this species as follows: ‘thermophyte, hygrophyte to mesophyte, heliophyte and nitrophilous’. It can tolerate a broad range of soil types and textures but prefers those that are well‐drained and rich in nutrients (Costea et al., 2005). A. tuberculatus also grows well on poorly drained soils (CABI, 2020). Plants can survive temporary flooding but have no salinity or frost tolerance (Costea et al., 2005).
The species can survive and reproduce even under a high degree and duration of water stress (low water conditions). Grantz et al. (2019) showed that A. tuberculatus (Californian biotype) was highly tolerant to ozone and deficit irrigation (33% of field capacity) under greenhouse conditions. This competitive advantage allows the species to occur in areas that are prone to drought, such as recently discovered in Southern and Central California (Calflora, 2019), and facilitates its weedy behaviour there.
The species requires warm temperatures for germination and growth. Steckel et al. (2002) observed the highest germination rates under a temperature range between 25 and 35°C under controlled conditions (seeds collected from Illinois, United States). Above 20°C, the species had higher germination rates with an alternating temperature regimen (temperature varied by 40% of each constant temperature in a sinusoidal fashion during a 14‐day period) than with a constant regimen (constant temperature during a 14‐day period). Seeds failed to germinate significantly when exposed to temperatures less than 20°C. The minimum temperature for germination was 10°C for populations from Iowa (United States) and over 15/10°C for populations from Kansas (United States) (Guo & Al‐Khatib, 2003; Leon & Owen, 2003).
Growth of A. tuberculatus is influenced by both temperature and light. For example, biomass accumulation, height and root volume were higher at 25/20°C and 35/30°C than at 15/10°C according to a greenhouse trial by Guo & Al‐Khatib (2003). Steckel et al. (2003) demonstrated that in full sunlight a A. tuberculatus plants produced 720 g of biomass and under 40% and 68% shading plants produced only 550 and 370 g, respectively (under field conditions, Illinois, United States).
Within the EPPO region, there are no host‐specific natural enemies of A. tuberculatus. Generalist natural enemies will potentially attack the plant, but these are unlikely to inflict enough damage at the population level to influence establishment.
Uses and benefits
There are no known uses or benefits of A. tuberculatus for the EPPO region.
PATHWAYS FOR MOVEMENT 2021-01-27
A. tuberculatus has presumably been introduced into the EPPO region as a grain contaminant. Records from ruderal sites in port areas and along (nearby) riverbanks indicate its introduction via imported goods (grain, animal feed mixture). A. tuberculatus has been intercepted in bird feed in the USA (Oseland et al., 2020). In Israel and Romania, it is assumed that the species was introduced by fish food from North America (Greuter & Raus, 1986) and with soybean waste and cereals (Costea, 1996).
In Belgium, A. tuberculatus is usually found under grain conveyors, near grain mills, on unloading quays or along road verges. The weed is also observed growing from soybean waste (http://alienplantsbelgium.be/content/amaranthus‐tuberculatus). In Canada, different Amaranthus spp. were intercepted in grain of maize, soybean, cereals, pulses, canola, sunflower and millet from the United States between 2007 and 2015 (Wilson et al., 2016). Shimono & Komuna (2008) showed a contamination of spring wheat destined for milling for human food trade imported from Canada to Japan with A. retroflexus.
Although A. tuberculatus has not been intercepted as a contaminant of seed, this remains a potential pathway of seed from crops which are invaded by the weed in North America. Both the Canadian Food Inspection Agency (2018) and the USDA (2019) highlight the movement of A. palmeri seed as a contaminant of seed. A. palmeri has also been identified from certified soybean in seed lots and seed bags in Louisiana (J. Ferrell, pers. comm., 2020). Uncertified commercial seeds from Australia, the United States and Europe (e.g. novel forage seeds) have been demonstrated to harbour seed contaminants, including several Amaranthaceae species (Cossu et al., 2019).
There are no reports of the presence of A. tuberculatus in seed mixtures and native seeds from North America; however, this has been reported for other Amaranthus species (including A. palmeri) and A. tuberculatus can potentially enter the EPPO region via this pathway.
Seed of A. tuberculatus may become a contaminant of machinery and equipment. However, there is probably very little movement of used machinery from the countries where the pest occurs into the EPPO region and if there is, it is probable that such equipment would undergo phytosanitary procedures such as decontamination (e.g. in the EU, Regulation (EU) 2019/2072).
Effects on plants
A. tuberculatus is a competitive annual weed in maize, soybean and cotton in the United States Corn Belt and Canada (Schryver et al., 2017; Sarangi et al., 2019), though competitiveness varies with density and time of emergence relative to the crop (Bensch et al., 2003).
Steckel & Sprague (2004) reported that season‐long interference of A. tuberculatus at 270 plants/m2 can reduce maize yield by 74% (Illinois/United States). Jones et al. (1998) reported that A tuberculatus emerging with soybean caused yield losses of 5% and 18% at densities of 7.9 and 31.5 plants/m2, respectively. A study from Hager et al. (2002) reported that A. tuberculatus allowed to compete with soybean up to 10 weeks after soybean unifoliate expansion at a density up to 362 plants/m2 reduced soybean yield by 43% (Illinois/United States).
In Canada, interference of A. tuberculatus resulted in soybean yield losses of up to 73% in weedy versus weed‐free controls (Vyn et al., 2007). A study by Cordes et al. (2004) reported a maize yield loss of 36% occurred, with A. tuberculatus density ranging from 369 to 445 plants/m2 full‐season interference (Missouri/United States).
Bensch et al. (2003) described the effect of the density of A. tuberculatus on soybean yield loss using a rectangular hyperbola model (Kansas/United States). Soybean yield loss varied depending on year and location from 27% to 63%. Maximum soybean yield loss occurred at eight plants/m of row length and was 56% for A. tuberculatus as determined by the model. Even the competitive impact of late emerging individuals can result in a 10% reduction in soybean yield (Bensch et al., 2003).
An important problem is also the evolution of herbicide‐resistant A. tuberculatus biotypes (Sarangi et al., 2019). Resistant biotypes have been confirmed in populations of the species to seven different herbicide mechanisms of action: ALS‐inhibiting herbicides (e.g. imazethapyr), auxins (e.g. 2,4‐D), EPSPS (e.g. glyphosate), HPPD inhibitors (e.g. mesotrione), protoporphyrinogen oxidase (PPO, e.g. acifluorfen), photosystem II (PSII, e.g. atrazine) and VLCFA (e.g. metolachlor) (Oliveira et al., 2018, HEAP, 2019; Sarangi et al., 2019). Many populations of A. tuberculatus contain more than one of these resistances and thus severely limit the options for effective herbicide control. According to Sarangi et al. (2019), the dioecious nature of A. tuberculatus promotes the spread of herbicide‐resistant traits through pollen‐mediated gene flow. Furthermore, an individual A. tuberculatus female plant can produce over a million seeds (Hartzler et al., 2004). Thus, herbicide resistance may evolve and spread faster in A. tuberculatus than in monoecious weedy Amaranthus spp. The species is classified among the worst herbicide‐resistant weeds (HEAP, 2019).
The potential economic impact of A. tuberculatus in the EPPO region for farmers could be significant if the species spreads and establishes in further areas and therefore effective weed control is essential in A. tuberculatus‐infested fields.
Environmental and social impact
There is potential for impacts on biodiversity in meso‐hygroscopic environments (riverbanks, wet grasslands). There is no evidence that A. tuberculatus invades natural areas with high conservation value in the EPPO region.
A. tuberculatus can hybridize with other Amaranthus species, thus adversely affecting the gene pools of other species. Hybridization is also a route by which herbicide resistance can be moved between different Amaranthus spp. (Costea et al., 2005). However, native European Amaranthus species are monoecious (Steckel, 2007) and are not expected to hybridize in field conditions with A. tuberculatus when present in limited numbers.
Amaranthus spp. are prolific pollen producers and should be considered as ‘hay fever plants’ in areas where they are abundant (Oh, 2018). If significant A. tuberculatus populations become established in the PRA area, the substantial pollen production may contribute to allergic rhinitis caused by its pollen. However, allergy impacts specific to A. tuberculatus have not been recorded in the EPPO region to date and such an impact is not foreseen to be as important as for other invasive alien plants (e.g. Ambrosia species).
In general, A. tuberculatus can be managed in crops in the same way as other weeds by herbicide use, mechanical control and integrated pest management. However, A. tuberculatus has a prolonged emergence pattern throughout the crop growing season and thus evades weed control attempts. The species will most likely show the same behaviour in the EPPO region. Seedlings will likely establish after initial post‐emergence herbicide applications and mechanical weed control tactics, therefore requiring additional weed management actions throughout the crop’s life span and this could raise control costs. The introduction of herbicide‐resistant genotypes of A. tuberculatus appears high and such an introduction may indeed severely limit the options for effective herbicide control and would result in an increase in control costs due to the adoption of specific herbicide programs (e.g. Meyer et al., 2015).
Without the implementation of integrated control against this species – effective chemical weed control, rotation including winter crops and appropriate tillage – the negative effects of A. tuberculatus will probably increase. Effective chemical control options (e.g. post‐emergence herbicides in soyabean in the EU) may be limited within the EPPO region due to the decrease of the number of herbicides available in the context of legislation, and due to the species being resistant to a number of active ingredients.
A proactive and integrated weed management strategy will be required to effectively manage A. tuberculatus in agricultural systems. Heavy tillage, as opposed to light soil disturbance, at the beginning of the season will prepare a proper seedbed for crop planting and eliminate all weeds that have emerged up to this point. Following planting, interrow cultivation can assist to eliminate small seedlings from establishment. In general, significant soil disturbance from heavy tillage discourages small‐seeded dicots such as A. tuberculatus.
It should be noted that in natural environments, management practices should be tailored to the habitat invaded.
REGULATORY STATUS 2021-02-02
In the United States, Wisconsin law prohibits the sale of agricultural seed containing A. tuberculatus seed (USDA, 2019a; https://www.ams.usda.gov/rules‐regulations/fsa). In Canada, A. tuberculatus is listed as a Primary Noxious Weed Seed under the Weed Seeds Order of the Seeds Act (http://www.gazette.gc.ca/rp‐pr/p2/2016/2016‐05‐18/html/sor‐dors93‐eng.html). In Argentina, A. tuberculatus is included on the A1 (absent) List at 2019 (EPPO, 2020a). In Australia, A. tuberculatus (listed as A. rudis) is listed as a quarantine pest. The genus Amaranthus is regulated in China.
EPPO (2020b) recommends phytosanitary measures for grains and seeds for relevant crops. Grains of Glycine max, Phaseolus vulgaris, Sorghum bicolor and Zea mays should be produced in a pest‐free area, or found free from A. tuberculatus after inspection for and testing of Amaranthus seeds, or should have been devitalized according to an appropriate method. Measures for grains should apply to all commodities that contain the species specified, i.e. irrespective of whether they are intended for animal feed (including bird seeds), human consumption or processing.
Seeds of Beta vulgaris, Glycine max, Gossypium hirsutum, Medicago sativa, Phaseolus vulgaris, Sorghum bicolor and Zea mays should be produced in a pest‐free area or found to be free from A. tuberculatus after inspection for and testing of Amaranthus seeds.
Seed mixtures and native seeds should have been produced in a pest‐free area found to be free from A. tuberculatus after inspection for and testing of Amaranthus seeds.
New associated crops should be added if A. tuberculatus is shown to develop in these crops and if their seeds or grains may present a risk of contamination with A. tuberculatus seeds.
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This datasheet was produced following an expert working group that risk analysed A. tuberculatus for the EPPO region in February 2020. The composition of the expert working group was G. Brundu (University of Sassari, Department of Agriculture, IT), D. Chapman (Stirling University, UK), J. Ferrell (University of Florida, US), S. Follak (AGES, AT), G. Fried (ANSES, FR), B. Hartzler (Iowa State University, US), U. Starfinger (Julius Kühn Institut, DE), C. Picard (EPPO) and R. Tanner (EPPO).
How to cite this datasheet?
Datasheet history 2021-01-27
This datasheet was first published in the EPPO Bulletin in 2020 and is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity' and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.
EPPO (2020) Amaranthus tuberculatus (Moq) J.D. Sauer. Data sheets on pests recommended for regulation. EPPO Bulletin 50(3), 543-548. https://doi.org/10.1111/epp.12716