E. nuttallii is a perennial submerged aquatic plant native to North America. It was introduced as an aquarium plant into Europe, reported for the first time in Belgium in 1939 (...
E. nuttallii is a perennial submerged aquatic plant native to North America. It was introduced as an aquarium plant into Europe, reported for the first time in Belgium in 1939 (Simpson, 1984; Cook and Urmi-König, 1985), and in Japan, circa 1960 (Ikushima and Kabaya, 1965), where it is commonly considered a weed (GCW, 2007). Several traits of the species are typical of successful invaders: rapid growth, vegetative reproduction through fragments and easily dispersed by waterfowl and currents (Cook and Urmi-König, 1985; Nichols and Shaw, 1986; Cook, 1987).
The spread of E. nuttallii has resulted in displacement of E. canadensis (itself an invasive alien from N. America) from many localities where the latter had previously become well established in Europe (Simpson, 1990; Thiébaut et al., 1997; Barrat-Segretain, 2001; Larson, 2007). E. nuttallii is itself being replaced by Lagarosiphon major. Where it establishes it can form exceptionally dense monocultures, excluding native species through competition, and it can cause major problems by blocking pipes; strongly invaded waters may become less attractive and safe for recreation. Flooding may be caused by heavy infestations choking drainage systems and sluices.
It is not known as a weed species in its native range, and in the US states of Kentucky and Tennessee it is listed a threatened species (USDA-NRCS, 2009). It is included in the list of invasive alien plants in EPPO region (EPPO, 2009).
Historically there has been much confusion in the classification of the species of the genus Elodea (Family Hydrocharitaceae). However, Cook and Urmi-König (1985), in the latest revision of the genus, recognize five species of Elodea, all of them from the New World: E. potamogeton (Bert) Espinosa, and E. callitrichoides (Rich.) Caspary are endemic to South America, while E.bifoliata St. John, E. canadensis and E. nuttallii grow in North America. Elodea nuttallii (Planch.) H. St. John, which is accepted by Tutin et al. (1980), was first named as Anacharis nuttallii Planchon in 1848 and later was replaced in the genus Elodea by St John in 1920. The taxon can be cited as H St. John or St John (IPNI, 2009). The epithet nuttallii, is after Thomas Nuttall (1786-1859), one of the first naturalists to explore the American West in the early nineteenth century.
E. nuttalli is a submerged-root aquatic plant, dioecious with floating flowers and rooting at nodes. The stems long and slender, often freely branched. Leaves pale green more or less equally spaced along the stem middle and upper leaves typically in whorls of 3 or occasionally 4, linear to narrowly lanceolate often recurved with folded margins; 6-13 mm long, 0.7-1.5 mm wide, acute at tip. Lower leaves in pairs and reduced in size, ovate-lanceolate. Stem slender, round in cross section, often freely branched, 30-100 cm long. Root white, unbranched, from nodes along the stem and not always present. The flower is small no more than 8 mm across; waxy white flowers occur at the ends of long, thread-like stalks and have 3 petals and usually 3 sepals. Male and female flowers occur on separate plants, but male flowers are rarely produced. Male flower spathes borne in middle axils, sessile, ovoid, about 2 mm long, spathe in 2 parts but the lobes twisted together so appears pointed; male flowers solitary and sessile in the spathe, breaking free and floating to the surface, where the flower opens, allowing pollen to drift on water's surface - hence the common name of free-flowering waterweed. Sepals ovate, about 2 mm long, sometimes reddish; petals lacking or to 0.5 mm long, ovate-lanceolate; stamens 9, pedicels briefly remaining attached following anthesis; inner 3 filaments connate proximally, forming column; anthers 1-1.4 mm; pollen in tetrads. Female flower spathes borne in upper axils, narrowly cylindric but slightly broadened at the base and the tip, 9-25 mm long; extended to the surface by a threadlike hypanthium up to 9 cm long; sepals green, tiny obovate, ca. 1 mm long; petals white, obovate, longer than the sepals; stigmas slender, slightly exceeding the sepals. Fruit narrowly ovoid to fusiform capsule, 5-7 mm long; containing several seeds. Ripens underwater. Seeds fusiform, 3.5-4.6 mm long, base with long hairs (Larson, 1993; FNA, 2009).
E. nuttallii is native to temperate North America common throughout most of the USA and south Canada and has a similar distribution to E. canadensis (eFloras, 2009; USDA-ARS, 2009; USDA-NRCS, 2009). In its non-native distribution, it is found in central and western Europe and Japan (Cook and Urmi-König, 1985).
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
E. nuttallii was reported in Belgium in 1939 (with a definite identification in 1955) (Simpson, 1984); and in Britain in 1966, and spreading rapidly from 1970 onwards from the southeast and scattering throughout Wales, Scotland (Preston and Croft, 1997) and Ireland (1984). It was also reported in the Netherlands in 1941 and in Germany in 1961, where it has since spread across the country. There are also reports of finds in Denmark (1974) (DAISIE, 2009), in Switzerland, where it was reported in the 1980s, and is spreading along the Rodan (Rhone) river (CPS-SKEW, 2008). It was first found in Sweden in 1991, in Lake Mälaren (Anderberg, 1992) and, together with E. canadensis and Nymphoides peltata, it is one of the three most troublesome species in Sweden (Josefsson and Andersson, 2001). Thereafter, its spread was noted in 1998 in the Danube delta in Romania, covering the majority of the delta (Sârbu et al., 2006); and from there to Slovakia in 2001 (Otahelová and Valachovic, 2002) and Hungary (Mesterházy et al., 2009) and then spreading into Western Europe (Wittenberg, 2005; Branquart, 2007). It is not unlikely that additional finds have been made, but that they have been mistaken for Canadian waterweed. In Asia, it was reported for the first time in 1960 in Japan (Lake Biwa) (Ikushima and Caballa, 1965). Since then, it has expanded very rapidly, and is regarded as one of the most troublesome aquatic weeds together with Egeria densa (Kunii and Maeda, 1982; Oki, 1994; Nagasaka et al., 2002). It was also introduced into China around the 1980s (Xu et al., 2007).
E. nuttallii has been unintentionally introduced outside its natural range via the trade in live aquarium plants, and has spread by escaping from garden ponds and during the disposal of garden waste near waterways. As this species is sold commercially as an aquarium or garden plant, there is a high risk of unintentional introduction. Different studies have established that E. nuttallii is probably in an expansion phase in Europe and is likely to spread to new areas (Simpson, 1984; Thiébaut et al., 1997; Barrat-Segretain, 2001; Larson, 2007), and it should be regarded as having a high risk of being invasive and must be strongly recommended as a priority target for eradication or control in new sites (Thiébaut et al., 1997; Barrat-Segretain, 2001). E. nuttallii is included in the black list in Belgium (Branquart, 2007) and Switzerland (CPS-SKEW, 2008) because of its high environmental risk, so further introductions, at least in these regions, are unlikely.
E. nuttallii has been found growing in a wide range of water bodies, in general in quiet water such as shorelines of lakes, reservoirs and ponds, along rivers and streams, and also in wetlands, canals and ditches (Hickman, 1993). In England, it has been recorded in lowland habitats only (Preston and Croft, 1997).
E. nuttallii is either a diploid or triploid, with aneuploid populations (Cook and Urmi-König, 1985). Populations of E. nuttallii may exhibit a high level of genetic polymorphism (Vanderpoorten et al., 2000). The number of basic chromosomes varies from 8 to 12, and the number of chromosomes of the populations varies according to country (2n = 32, 42, 44 in the USA, 2n = 48 in England, 2n = 48 in Britain, 2n = 44, 2n = 56 in France and Switzerland) (Thiebaut, 2008; FNA, 2009).
Reproductive Biology
E. nuttallii is dioecious; sexual reproduction occurs on the water surface, when the female flowers, like those of E. canadensis, are borne on long hypanthia and float on the water surface. The male flower, however, is released by abscission of the pedicel when still in bud. The bud contains a gas bubble and floats to the surface, where it opens to release the pollen (Bowmer et al., 1995; Preston and Croft, 1997). Fruiting specimens are very rare in North America (Lawrence 1976) and very few fully mature fruits were recorded in Canada (Catling and Wojtas, 1986). Although E. nuttallii reproduces both sexually and asexually by vegetative clonal propagation in its native range, in Europe the majority of plants are female, with the exception of a male colony known in Germany (Preston and Croft, 1997). In Japan all plants are male (Kunii 1984), so vegetative reproduction seems to be the dominant method of propagation - essentially by fragmentation and division of the stems and the production of winter buds from stem tips (Preston and Croft, 1997). It has been observed that, when introduced to a new habitat, the establishment of Elodea buds is rapid, since the propagules sink into the sediment and grow rapidly (Barrat-Segretain et al., 2002).
Physiology and Phenology
Phenological and seasonal patterns observed by Kunii (1984) in a pond in Japan, where abundance is high, show that shoot elongation starts in spring when the temperature of the bottom reaches 10°C; elongation ceases when the shoot reaches the surface water, and then a dense canopy is formed, with 40 to 65% of shoot biomass being found in the top 30 cm of water. The maximum biomass (712 g dry wt/ m2) is obtained in late July; in Europe, 300 g dry wt/ m2 has been reported (Pot and ter Heerdt, 2009). Flowers appear in California from July to August (Hickman, 1993). The anchoring roots die at the end of September and then a large floating mat is formed that drifts up to the lake shore (Kadono, 2004). It sinks in December, when the water temperature drops below 10°C, and it can survive over winter, forming a dense mat of vegetation just above the lake bottom (Oki, 1994), with slight growth during winter if the temperatures are higher than 4°C (Kunii, 1981).
The European populations grow more vigorously and taller than their conspecifics in the native range possibly because of different selection pressures (Thiébaut and De Nino, 2009). Introduced E. nuttallii exposed to environmental stresses show great phenotypic plasticity variations with increasing water nutrient enrichment and increases in leaf area with decreases in internode length, while the shorter broad-leaved phenotype typically occurs in shallow streams, whereas the longer spacer narrow-leaved phenotype occurs in lakes. Larger leaf width and higher number of lateral shoots - when nutrients are not limiting - may enhance plant performance (Simpson, 1988; Vanderpoorten et al., 2000; Di Nino et al., 2007).
The plants absorb phosphorus via both roots and shoots. The phosphorus uptake via shoots may significantly exceed the phosphorus uptake via roots (Angelstein and Schubert, 2008). E. nuttallii is able to utilize bicarbonate by active transport as carbon dioxide supply becomes limiting, and its physiological plasticity can be compared with that shown by E. canadensis (Jones et al., 1993). E. nuttallii can be regarded as a low-light adapted plant, under photorespiratory conditions (Angelstein and Schubert, 2009). All Elodea species tend to take up metals from the sediment and release them into the water. E. nuttallii is very tolerant of copper in particular and shows a high capacity to accumulate contaminants such as alkylphenols (Zhang et al., 2008).
Associations
E. nuttallii, native to North America, is closely related to E. canadensis and grows in shallow water among Potamogeton, Callitriche, and Ceratophyllum on soft bottoms (Josefsson and Andersson, 2001). It is often found in its invasive range in species-poor macrophyte communities in managed rivers, canals and gravel pits, where characteristic associates include Myriophylllum spicatum, Potamogeton pectinatus, Potamogeton pusillus and filamentous algae (Preston and Croft, 1997). It is often found in species-poor macrophyte communities subject to boat traffic and in eutrophic drainage ditches.
It can occur to depths of 3 m (Simpson, 1990) and 5 m (Ikusima, 1984) where it develops into dense pure stands, but it is most frequently found in shallow water. Optimum pH has been found to be between 7 and 9 (Jones et al., 1993). It is tolerant of disturbance, oil pollution and is typically found in calcareous water, from fresh to slightly brackish coastal water (St John, 1965) up to 14 ppt salinity, and in fine sediment soil, where it is particularly successful. It is found at altitudes from 0 to 275 m, and in its eastern area of distribution in the USA between 1372-2742 m (Missouri Botanic Garden, 2009). All regions in which it is present are characterized by a temperate climate.
E. nuttallii is relatively unpalatable (Elger et al., 2004) due its high synthesis of phenolic compounds (allelopathic effect) (Newman, 1991; Lemoine et al., 2009) and because it contains allelochemicals that are active against competing algae and cyanobacteria (Erhard and Gross, 2006; Wu et al., 2009). The chemical defence in E. nuttallii is a powerful trait to protect the plants against herbivores and might further strengthen the invasiveness of this species (Erhard et al., 2007).
When the plant is non-anchored; it can easily drift as a result of wind and water currents and can be dispersed by becoming attached to machinery, footwear, fishing equipment, dredgers or by human-assisted dispersal, as was the case in Japan, where fragments of the plant were transported together with the fry of Plecoglossus altivelis from Lake Biwa to the rivers of various regions in Japan (Ikusima, 1980).
Vector Transmission (Biotic)
It is likely to be spread by birds and animals.
Accidental Introduction
It is not reported to be introduced accidentally.
Intentional Introduction
Introduction into another country has almost certainly been via the trade in live aquarium plants, legal or otherwise (Bowmer et al., 1995); thereafter, it has spread by escaping from garden ponds and through the disposal of garden waste near waterways (Preston and Croft, 1997).
E. nuttallii as well as E. canadensis have the potential to develop into dense submerged beds, which prevent the use of water for recreational and professional purposes (Larson, 2003), navigation and port infrastructure (CPS-SKEW, 2008). The plant can also clog and impede drainage waterways.
E. nuttallii populations are rarely troublesome in natural habitats in North America, but plants can become dominant in altered or created aquatic systems, especially when bicarbonate, reduced iron, and phosphorus are plentiful (Thiébaut and De Nino, 2009). E. nuttallii tends to dominate native macrophyte communities, which may lead to their local extinction. This species may also have a significant impact on protected sites.
Impact on Biodiversity
It often forms dense, monospecific stands and displaces other aquatic plants from many localities (Simpson, 1984, 1990; Barrat-Segretain, 2005). E. nuttallii and E. canadensis have shading effects during phases of rapid growth and mass occurrence. The plants compete with and displace indigenous vegetation, thus reducing biodiversity (Josefsson and Andersson, 2001).
Dense populations of plants reduce water movement, cut off light, produce anoxic conditions and trap sediments in the system. Plant decomposition at the end of the growing season typically induces a secondary eutrophication leading to the accumulation of end products toxic to many plants. In Japan, it has been reported that the biomass of native plants declined drastically after the invasion of E. nuttallii, which also has a competitive advantage over the native aquatic plants and competes with Ranunculus nipponicus and other species adapted to spring-fed water, threatening the unique ecosystems of Japan (Kadono, 2004). E. nuttallii is also known to replace other invasive species as the dominant species in an impacted ecosystem; it has replaced E. canadensis at many sites due to increased eutrophication, and is in turn being replaced by Lagarosiphon major. Impacts have also been recorded on invertebrate communities.
It is a submerged plant, and just like E. canadensis it forms large and dense stands that interfere with boating, fishing and adversely affect recreation activities.
E. nuttallii is used in cool water aquariums and it has a little economic importance in its native range.
Environmental Services
Elodea species are often a preferred food for waterfowl or crayfish (Lodge, 1991; van Donk and Otte, 1996), and can also be used as shelter for small fishes and aquatic invertebrates.
In its native range, it may be confused with Brazilian elodea (Egeria densa), which has a similar appearance, but has longer leaves in whorls of 4 to 6; also with Hydrilla (Hydrilla verticillata), which has tubers and spiny leaf edges, and with coontail (Ceratophyllum sp.), which has forked, needle-like leaves, both of which are easily confused with each other. Flower structure and leaf width are the most reliable distinguishing characteristics, but due to infrequent and ephemeral flowering, together with the minute size of the flowers, leaf morphology is often the trait used to differentiate Elodea species in North America (Catling and Wojtas, 1986; Lawrence, 1976). Unfortunately there is overlap in the characteristics and there is little agreement among authors on the nature of these characteristics. According to Catling and Wojtas (1986), leaf width partially separates male plants of E. canadensis and E. nuttallii but not female plants.
Distinction between E. canadensis and E. nuttallii is possible from inflorescences: E. nuttallii has sessile male flowers, which are released at anthesis, and female flowers with a shorter floral tube (up to 9 cm).
In Europe, Elodea species can be distinguished from all other aquatic and plants except Egeria densa and Hydrilla verticillata by their whorls of undivided leaves, which lack a sheathing base but have a single central vein and small marginal teeth. E. densa can be distinguished from Elodea by its generally much larger size, the presence of small teeth along the central vein on the leaves and by the nature of the teeth on the leaf margins. Lagarosiphon major has very strongly recurved leaves and these are in spirals whereas those of Elodea are in whorl (Lansdown, 2008).
Determination of sterile Elodea species has also been an area of controversy in Europe. The leaves are either linear or linear-lanceolate and the shape of the leaf apex is narrowly acute to acuminate in E. nuttallii’s European populations (Thiébaut and De Nino, 2009); and the determination keys should emphasize the difficulties of distinguishing plants with long plane leaves vegetatively (Vanderpoorten et al., 2000).
EPPO (2009) strongly recommends that countries in the EPPO region, endangered by this species, take measures to prevent its introduction and spread, or manage unwanted populations (for example with publicity, restrictions on sale and planting, and controls).
Control
Physical/mechanical control
Cutting is best carried out before July, and a second cut will be required later in the season. However, cutting very early in the season, from mid-February onwards, using trailing knives, or chains, will limit the early season growth, and if regular treatments are made in this way during the summer, at 6-8 week intervals, then maximum biomass should not be reached. This also limits the amount of floating material produced late in the season. During this process it is essential to prevent the spread of plant fragments by creating filters downstream before any mechanical treatment is carried out. All plants removed must be carefully disposed of to prevent dissemination of fragments (Newman, 2009). Di Nino et al. (2005) have reported that harvesting causes a drastic reduction of biomass of E. nuttallii and that two harvests causes almost total disappearance.
Another mechanical option is creating shade, which can be achieved by planting trees on the south side of water bodies or by using a floating sheet of opaque material. Care must be taken when using the latter to prevent sudden deoxygenation (Newman, 2009).
Biological control
The use of herbivorous Chinese grass carp is appropriate as a control method for this plant. Common carp, and other bottom-feeding fish, which create turbid water, can also be effective in preventing regrowth of the plant after mechanical removal or chemical control (Newman, 2009).
Chemical control
E. nuttallii is susceptible to terbutryn and dichlobenil applied in spring before the plant is fully grown (Newman, 2009); it has also shown high phytotoxicity to butachlor, quinclorac, bensulfuron-methyl and atrazine, which inhibited the growth rate and decreased the photosynthetic pigment content (Pan et al., 2009).
The best option is a combination of mechanical and chemical control, removing as much of the plant as possible by mechanical means after the end of June and before the end of August and for early season control using herbicides before the end of April (Newman, 2009).
Manuel A. Duenas, Universidad de Cordoba, Dept. de Botanica, Ecologia y Fisiología Vegetal. Edificio C-4, Celestino Mutis, Campus de Rabanales, 4071-Cordoba, Spain
