B. Blossey, M. Schwarzländer, P. Häfliger, R. Casagrande and L. Tewksbury in Driesche, F.V.; Blossey, B.; Hoodle, M.; Lyon, S.; Reardon, R. Biological Control of Invasive Plants in the Eastern United States. United States Department of Agriculture Forest Service. Forest Health Technology Enterprise Team. Morgantown, West Virginia. FHTET-2002-04. August 2002. 413 p.
Pest Status of Weed
Common reed (Fig. 1), Phragmites australis (Cav.) Trin. ex Steudel, is a widely distributed clonal grass species, ranging all over Europe, Asia, Africa, America, and Australia (Holm et al., 1977). Extensive reed beds are protected in Europe (Tscharntke, 1992) because of their important ecological functions. In contrast, the rapid expansion of P. australis in North America, particularly along the Atlantic coast (Chambers et al., 1999), is considered a threat to biodiversity in natural areas (Marks et al., 1994). Peat core analysis (Orson, 1999) shows that P. australis was an uncommon component of marshes in New England several thousand years ago. Recent genetic evidence (Saltonstall, 2002) has now confirmed that a more aggressive genotype has been introduced to North America (Metzler and Rosza, 1987; Tucker, 1990; Mikkola and Lafontaine, 1994; Besitka, 1996, Orson, 1999), probably in the late 1800s along the Atlantic coast (Saltonstall, 2002). The distribution of the native genotypes is not well known but they appear more common in the western part of the continent (Saltonstall, 2002). At present, invasive P. australis occurs throughout the whole of the United States, except Alaska and Hawaii; however, problems caused by non-indigenous P. australis are most severe along the Atlantic coast.
Nature of Damage
Economic damage. Phragmites australis is largely a weed of natural areas and direct economic damage has not been assessed or reported.
Ecological damage. Phragmites australis invasion alters the structure and function of diverse marsh ecosystems by changing nutrient cycles and hydrological regimes (Benoit and Askins, 1999; Meyerson et al., 2000). Dense Phragmites stands in North America decrease native biodiversity and quality of wetland habitat, particularly for migrating waders and waterfowl species (Thompson and Shay, 1989; Jamison, 1994; Marks et al., 1994; Chambers, 1997; Meyerson et al., 2000). A survey of Connecticut marshes showed that rare and threatened bird species in the area were associated with native, short-grass habitats and were excluded by Phragmites invasion (Benoit and Askins, 1999).
Extent of losses. Lack of long-term data makes quantification of direct losses difficult. At sites where Phragmites eradication programs have been instigated, such as Primehook National Wildlife Refuge in Delaware, waterfowl abundance has significantly increased following control procedures (G. O’Shea, pers. comm.). Recovery of bird communities after chemical control of P. australis suggests a significant habitat loss due to encroachment by common reed.
Presently, non-indigenous, invasive P. australis is most abundant along the Atlantic coast and in freshwater and brackish tidal wetlands of the northeastern United States, and as far south as North Carolina. It occurs in all eastern states and populations are expanding, particularly in the Midwest.
Background Information On The Pest Plant
Phragmites australis is a perennial monocot in the family Poaceae, tribe Arundineae (Clayton, 1967). The genus Phragmites includes four species, with P. australis being distributed worldwide; Phragmites japonicus Steudel being found in Japan, China, and eastern areas of Russia; Phragmites karka (Retz.) Trin. found in tropical Africa, Southeast Asia, and northern Australia; and Phragmites mauritianus Kunth in tropical Africa and the islands of the Indian Ocean (Darlington and Wylie, 1955; Clayton, 1967; Tucker, 1990; Besitka, 1996). The status of the eleven recently discovered native haplotypes (Saltonstall, 2002) needs further evaluation. All species show high phenotypic plasticity making species identification difficult (Clayton, 1967).
Phragmites australis is a clonal grass species with woody hollow culms that can grow up to 6 m in height (Haslam, 1972). Karyotypic studies in North America have identified different ploidy levels with populations of 3x, 4x, and 6x plants, but with 4x being the dominant chromosome number in modern day populations (Besitka, 1996). Leaves are lanceolate, often 20 to 40 cm long and 1 to 4 cm wide. Flowers develop by mid-summer and are arranged in tawny spikelets with many tufts of silky hair.
P. australis is wind pollinated but self-incompatible (Tucker, 1990). Seed set is highly variable and occurs through fall and winter and may be important in colonization of new areas. Germination occurs in spring on exposed moist soils. Vegetative spread by below-ground rhizomes can result in dense clones with up to 200 stems/m2 (Haslam, 1972).
Analysis of Related Native Plants in the Eastern United States
Phragmites australis is a member of the Poaceae with more than 100 genera represented in the northeastern United States alone (Gleason and Cronquist, 1991). The closest related species to P. australis is Arundo donax L., an invasive introduced species. The most important genera to consider for their wildlife value include species of Typha, Spartina, Carex, Scirpus, Eleocharis, Juncus, Arundinaria, and Calamagrostis.
History of Biological Control Efforts in the Eastern United States
Research in North America and Europe began in 1998 with literature and field surveys for potential control agents (Tewksbury et al., 2002)
Area of Origin of Weed
The current distribution of P. australis includes Europe, Asia, Africa, America, and Australia (Holm et al., 1977), however, the origin of the species is unclear. The rapid spread of Phragmites in recent years in North America has led wetland ecologists to believe that the species may be introduced. However, Phragmites rhizomes were found in North American peat cores dated 3,000 years old (Orson, 1999). Several different hypotheses have been proposed to explain the recent population explosion in North America, including the introduction of more aggressive European genotypes about 100 years ago (Besitka, 1996; Orson, 1999). The absence of specialized North American herbivores of P. australis in North America and the lack of wildlife use are indications for the introduced status of the species (Tewksbury et al., 2002). Saltonstall (2002) has compared historic and present day populations of P. australis from North America and other continents using advanced genetic techniques. Her results show that present day populations in North America consist of a mixture of eleven non-invasive native North American haplotypes and one distinctive introduced invasive (most likely European) haplotype (Saltonstall, 2002). The status of an additional haplotype (either native or introduced) growing along the Gulf of Mexico is still unresolved (Saltonstall, 2002).
Areas Surveyed for Natural Enemies
In 1997, literature surveys and limited field surveys in the northeastern Unites States began. Work in Europe started in 1998 with additional literature surveys and the estblishment of field sites in Hungary, Austria, Germany, and Switzerland (Schwarzländer and Häfliger, 1999).
Natural Enemies Found
Literature and field surveys (in the northeastern United States and eastern Canada) reveal that currently 26 herbivores are known to attack P. australis in North America (Tewksbury et al., 2002). Many of these species were accidentally introduced during the last decades; only five are potentially native (Tewksbury et al., 2002). Only the Yuma skipper, Ochlodes yuma (Edwards) (a species distributed throughout the western United States); a dolichopodid fly in the genus Thrypticus; and a gall midge, Calamomyia phragmites (Felt), are considered native and monophagous on P. australis (Gagné, 1989; Tewksbury et al., 2002). The native broad-winged skipper, Poanes viator (Edwards), has recently included P. australis in its diet (Gochfeld and Burger, 1997) and the skipper is now common in Rhode Island (Tewksbury et al., 2002). The dolichopodid fly and the gall midge C. phragmites are widespread in North America but appear to be restricted to native North American haplotypes of P. australis (Blossey, unpub. data). The European moth Apamea unanimis (Hübner) was first collected in North America in 1991 near Ottawa, Canada (Mikkola and Lafontaine, 1994). Larvae feed on leaves of P. australis and species of Phalaris and Glyceria. A second European species, Apamea ophiogramma (Esper), was first reported in 1989 from British Columbia, Canada (Troubridge et al., 1992), but it has now been found in New York, Vermont, Quebec, and New Brunswick (Mikkola and Lafontaine, 1994). Additional species such as several shoot flies in the genus Lipara, Dolichopodidae; a rhizome feeding noctuid moth Rhizedra lutosa (Hübner); the gall midge Lasioptera hungarica Möhn; the aphid Hyalopterus pruni (Geoffr.); and the wasp Tetramesa phragmitis (Erdös), Eurytomidae – all appear widespread. The mite Steneotarsonemus phragmitidis (Schlechtendal) was recently discovered in the Finger Lakes Region of New York and the rice-grain gall midge Giraudiella inclusa (Frauenfeld) in Massachusetts, Connecticut, New Jersey, and New York (Blossey and Eichiner, unpub.). In Europe, at least 140 herbivore species have been reported feeding on P. australis, some causing significant damage (Schwarzländer and Häfliger, 1999; Tewksbury et al., 2002). About 50% of these species are considered Phragmites specialists (Schwarzländer and Häfliger, 1999) and almost 40% of the species are monophagous. Lepidoptera (45 species) and Diptera (55) are the most important orders. More than 70% of all these herbivores attack leaves and stems of P. australis, and only five of the monophagous species feed in rhizomes (Tewksbury et al., 2002). Of the 151 herbivore species known from outside North America, already 21 (13.9%) have been accidentally introduced (Tewksbury et al., 2002).
Host Range Tests and Results
Rhizedra lutosa larvae were exposed to a number of ornamental grasses (Balme, 2000). The larvae did not feed on any of the species tested, and no host specificity screening has been conducted for any other herbivores of P. australis.
No deliberate releases have been made, but at least 21 species feeding on common reed have been accidentally introduced to North America (Tewksbury et al., 2002).
Biology and Ecology of Key Natural Enemies
The following is a summary of life history and ecology on potential natural enemies associated with P. australis in North America and Europe. Species included in this list were selected according to their abundance and potential impact on plant performance. Species marked by an asterix have already invaded North America.
Lipara rufitarsis* Loew, L. similis* Schiner,
L. pullitarsis* Doskocil and Chvala,
L. lucens* Meigen (Diptera: Chloropidae)
The genus Lipara Meigen is restricted to the Palaearctic region, and all nine presently recognized species use P. australis as their sole host plant (Beschovski, 1984). The European species L. lucens, L. rufitarsis, L. similis, and L. pullitarsis cause more or less distinct apical shoot galls, in which the mature larvae overwinter (Chvala et al., 1974). A single larva develops per shoot (De Bruyn, 1994). All four species are widely distributed through Europe with variable but usually low (5 to 10%) attack rates (Schwarzländer and Häfliger, 1999).
Sabrosky (1958) records 1931 as the first North American record of L. lucens, based on material from Connecticut. The same author reports intercepting L. similis in New York in a shipment from the Netherlands where dry Phragmites stems were used as packaging materials (Sabrosky, 1958). Use of Phragmites as packaging material may be a major mode of introduction for many other insects that overwinter in dry stems of this species. Recent regional surveys in the northeast United States (Tewksbury et al., 2002; Blossey and Eichiner, unpub.) reveal a widespread distribution and high abundance of L. rufitarsis, L. similis (Fig. 2), and L. pullitarsis. However, L. lucens has not been found after the initial record in 1931 and may not be established in North America. Taxonomic identification of adult flies is difficult and the species recorded in 1931 may have been misidentified and may have been L. rufitarsis. Attempts to locate the original specimens have been unsuccessful (Muth, pers. comm.). Attack rates in the northeastern United States, particularly of L. similis, can approach 80% (Balme, 2000; Blossey and Eichiner, unpub.). The different Lipara species can be best distinguished using criteria of gall morphology and larval overwintering habit. Attack by L. lucens causes stunting of 10 to 13 internodes and larvae penetrate the growing point to feed in a gall chamber. Attack by L. rufitarsis causes stunting of only five to six internodes with larvae also penetrating the growing point. Attack by L. pullitarsis causes stunting of apical internodes and gall formation similar to L. rufitarsis, but larvae overwinter above the growing point. Attack by L. similis causes only slight alterations of shoot diameters. Similar to L. pullitarsis, L. similis larvae feed and overwinter above the growing point of attacked shoots. Attack by all Lipara species can easily be identified by dried up apical leaves and the lack of inflorescences on infested shoots. Pupation of larvae occurs in early spring and flies emerge in May.
Lasioptera hungarica Möhn (Diptera: Cecidomyiidae)*
Lasioptera hungarica is a univoltine gall midge with P. australis as the only recorded host plant (Skuhrava and Skuhravy, 1981). The species appears to be more common in eastern and southern Europe (Schwarzländer and Häfliger, 1999). Shoots infested by L. hungarica show no obvious signs of damage; however, they often break in strong winds at the site of attack, suggesting a weakening of stem tissues. Larvae overwinter in the stem, and 30 to 300 yellow-orange larvae often can be found in a single internode. The species is easily identified by its association with a black fungal mycelium (genus Sporothrix) (Skuhrava and Skuhravy, 1981) that fills the internode (Fig. 3). Oviposition by females also infects the stem with fungal spores, providing food for the developing larvae. Lasioptera hungarica was recognized in North America in 1999 (Tewksbury et al., 2002) but the species is widespread throughout the northeastern United States (Blossey and Eichiner, unpub.).
Chaetococcus phragmitis Marchal (Homoptera: Pseudococcidae)*
The legless reed mealybug, Chaetococcus phragmitis (Fig. 4), has recently been found in Delaware, Maryland, New Jersey, southern New York (Kosztarab, 1996; Krause, 1996), Virginia and Connecticut (Blossey and Eichiner, unpub.), and Rhode Island (Tewksbury et al., 2002). Native to central Europe, Armenia, Azerbaijan, and the Mediterranean region (Ben-Dov, 1994), this mealybug is only known to feed on Phragmites and Arundo species (Kosztarab, 1996). In North America, C. phragmitis is regionally very common (Krause, 1996). The mealybugs feed and overwinter under leaf sheaths.
Rhizedra lutosa (Hübner) (Lepidoptera: Noctuidae)*
The rhizome feeding noctuid moth Rhizedra lutosa (Fig. 5) was first reported in 1988 from New Jersey (McCabe and Schweitzer, 1991). It was subsequently found in the Catskills in New York in 1991 (Mikkola and Lafontaine, 1994) and by 1999 was widespread in Rhode Island, Connecticut, Massachusetts, New York, and as far west as Ohio (Tewksbury et al., 2002). This moth overwinters as eggs deposited on Phragmites leaves. Larvae hatch in spring, enter newly growing Phragmites shoots, and feed in the rhizome. Attack by larvae results in shoot death, visible as dying yellow shoots in the middle of the growing season. Larvae complete development by July or August and pupate in the soil; adults fly in the fall. Attack rates appear low (Balme, 2000) and further work is needed to assess the potential of this species as a biological control agent.
Archanara geminipuncta (Haworth) (Lepidoptera: Noctuidae)
This shoot-boring moth has been extensively researched in Europe because of the damage it does to reed beds. Larvae mine the shoots in spring and early summer; adults fly in the summer and eggs overwinter. Mined portions of shoots and the growing point wilt after attack. A single larva needs several shoots to complete development, and attack rates of more than 50% of stems are common. Attack by this shoot-boring moth can reduce shoot height by 50 to 60% and result in significant reed dieback.
Phragmataecia castaneae (Hübner) (Lepidoptera: Cossidae)
This large moth needs two years to complete its development, which occurs at the base of the shoot and in the rhizomes. Moths fly in summer and females lay 200 to 400 eggs. Larvae may move from shoot to shoot as they look for new food during their development. Larvae can be found in both dry reed stands and those that are permanently flooded.
Chilo phragmitella (Hübner) (Lepidoptera: Pyralidae)
Like P. castaneae, this species mines shoots and roots of Phragmites. Larvae are active in the summer; older larvae mine deeper parts of the rhizome and are difficult to detect. Infested shoots remain small and wilt.
Schoenobius gigantella (Denis and Schiffermüller) (Lepidoptera: Pyralidae)
Larvae of this moth mine shoots of flooded Phragmites below the water level, causing considerable damage. Attacked shoots wilt and break apart. Little is known about the life history of the species, but it is assumed that larvae need two years to complete development. Adults fly in the summer.
Platycephala planifrons (Fabricius) (Diptera: Chloropidae)
Platycephala planifrons (Fig. 6) attacks Phragmites shoots early in the year leading to severe stunting of attacked stems by killing the growing point. Platycephala planifrons was one of the most damaging species found during surveys in Europe. Attack can cause biomass reductions of >50%. Females fly in the summer and are long lived. Eggs are laid in late summer. Larvae hatch in late summer, feed for a limited period, and overwinter.
Evaluation of Project Outcomes
Establishment and Spread of Agents
No deliberate introductions of biological control agents have been made. The diversity of accidentally introduced Phragmites herbivores is highest closest to New York City (Blossey and Eichiner, unpub.). This suggests that a major area for the introduction of arthropods is the harbor. Various introduced species associated with Phragmites appear to be spreading from New York City along highways, rivers, and the coastline.
Suppression of Target Weed
No work on evaluating the effects of these European herbivores on Phragmites has yet been done in North America. However, the recent discovery of several such species in the northeast provides an opportunity to measure the influence of these organisms on Phragmites performance.
Recommendations for Future Work
Genetic analysis (Saltonstall, 2002) has confirmed the presence of native North American genotypes of P. australis. Promising biological control agents have been identified in Europe and their impact and host specificity need to be determined experimentally. Native North American genotypes of P. australis do exist, therefore it will be extremely important to assess whether the potential control agents show any peferences among different genotypes. The fact that some native North American herbivores appear restricted to native P. australis genotypes and that some accidentally introduced European insect herbivores do not attack native North American genotypes (Blossey, unpub. data) is some indication that genotype-specific biological control may be possible. However, detailed investigations as to preference and performance of potential biological control agents on native North American and introduced European genotypes have to be conducted.
A large number of European herbivorous insects that are specific to P. australis have become accidentally established in North America. Some of these insects species are widespread and abundant in the northeastern United States. However, we do not know their full distribution, habitat requirements, or potential control value. In particular, gall flies in the genus Lipara and the rhizome-feeding moth R. lutosa are widespread, although only the Lipara species reach high abundances. These observations should form the basis for a more intensive analysis of the ecology and impact of these species and their potential to control the spread or reduce existing invasive populations of P. australis. It needs to be determined why R. lutosa does not build up to higher population levels and whether the attack by the gall flies or R. lutosa can stop the spread of Phragmites or weaken existing stands. Before any of these species may be used as biological control agents, their host specificity or impact on native P. australis must be determined. We plan to establish a web-based system to collect information from land managers about the distribution of the various reed insects already present and spreading within the United States. The web site will feature pictures and drawings of the accidentally introduced insects and their feeding damage. For most of these organisms, their gross appearance or damage is distinctive, allowing non-entomologists to participate in data collection. This system will allow the production of distribution maps, and potentially will be able to track the spread of these organisms across the continent.
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