Integrating Invasive Weed Biological Control in Aquatic Ecosystem Restoration Projects

Abstract

A primary goal of many aquatic ecosystem restoration (AER) projects is to alter and improve plant communities by increasing relative abundance of native species while reducing invasive species abundance, establishment, and spread. Biological control or the use of host-specific pathogens, predators, or herbivores from the native range of a target invader, has been used for invasive plant control, but underutilized as part of integrated pest management (IPM) in government-sponsored AER programs. Weed biological control should be vetted and integrated where possible in all project phases—planning, design, implementation, and maintenance. Using a publicly-funded AER framework—U.S. Army Corps of Engineers or USACE—we define and describe biological control, how it can be seamlessly incorporated at various project stages, a list of common invasive plants that have approved biological controls, and regulatory issues surrounding implementation. Our aim is to illustrate to project managers, planners, environmental personnel, and economists how regulatory agency-approved biological control agents can be a valuable component of AER projects to assist in meeting vegetation community restoration trajectory goals.

1. Introduction

With wide-ranging anthropogenic impacts across various aquatic habitats, aquatic ecosystem restoration (AER) has become an essential feature of natural resource management with the aim to restore areas affected by pollution, biological invasions, or habitat degradation and fragmentation [1, 2, 3]. AER objectives often focus on regaining ecosystem function, biodiversity, and productivity—clean water and air, wildlife habitat, carbon sequestration, pest management, and soil fertility [4, 5]. As such, invasive plants, and their management, are a major focus of many AER projects, and their negative habitat impacts are compounded by other disturbances, such as climate change [6]. Even with early detection and response, plant invasions can be challenging to stop and reverse, and may pose significant economic, health, and environmental harm [7, 8]. Thus, invasive species management efforts in the context of AER projects are often multi-faceted and require an iterative, adaptive management approach to meet project goals.

Meeting the goals of AER projects usually requires vegetation community establishment, manipulation, and/or management [9]. Objectives commonly seek to restore degraded native vegetation communities or, in some cases, assist in the development of a vegetation community where none existed before. Due to the pervasive occurrence of non-native invasive vegetation prone to establish in disturbed ecosystems, most AER projects must couple native plant establishment with invasive plant management. If problematic species are present, removal or other forms of control—manual, mechanical, chemical, biological, cultural, and integrated—are necessary to reduce competition and promote the establishment of native species [10, 11, 12, 13]. When untreated, invasive plants often outcompete native species for limited resources, including space, water, nutrients, and light, reducing restoration outcomes [14, 15]. Installing a diverse assemblage of native plantings increases community resistance to current and future invasions [16, 17]. Therefore, AER practitioners aim to prioritize and manage invasive plants, and then establish a desirable composition of native plants to counter such negative impacts and enhance other ecosystem attributes.

Of the available invasive species control tools, classical biological control (biocontrol)—the use of host-specific pathogens/predators/herbivores from the invasive species host range—is a management tool largely overlooked in project planning, implementation, and long-term maintenance [18]. This is despite the potential of biocontrol to reduce long-term costs, sustain invasive species suppression, and promote native species [18, 19]. In contrast to other invasive species management techniques, biocontrol does not induce major soil disturbance, which leads to unintentional harm to native species or susceptibility to secondary invasions [20]. Biocontrol programs are subject to strict regulations for selecting and releasing host-specific agents and mitigating the risk of adverse effects on non-target plant species [21]. Biocontrol is the only invasive species management tool that provides the ability to target individual species for management or control. Biocontrol can also provide long-term, sustained invasive plant management once agents are established at field sites [19, 22]. Therefore, in many cases, it may be favorable to implement biocontrol in coordination with other treatment methods to safely reduce invasive plant dominance in a targeted way. The lack of proper project inclusion and vetting may be because of the tool’s long-term nature, regulatory issues, or the lack of awareness by natural resource managers of availability and/or applicability [23].

In this paper, we (1) define and describe the general concept and practice of biocontrol, including theory and development of the technology, (2) frame the potential for incorporation into multiple phases of AER projects using a government-sponsored program case example (U.S. Army Corps of Engineers or USACE), (3) provide an example list of common weeds that impact such projects, whether they have approved biological control agents available, and (4) discuss permitting and regulatory issues surrounding the use of biological control in the U.S. Our goal is that the technology will ultimately see more practical considerations in AER planning efforts as well as utility as a management and transfer tool for sponsors and partnerships at project implementation, and monitoring and maintenance phases. Although we focus on USACE projects, themes throughout can be applied to AER projects worldwide, where a goal is to manage the plant community towards a more-native and less invasive dominated trajectory. Importantly, we only support the potential inclusion of biocontrol agents in AER projects that have already been subjected to rigorous testing and government/regulatory agency approvals in their respective locals as discussed herein.

2. USACE AER background

The USACE is one of the largest environmental engineering agencies in the world. It is responsible for operating more than 600 dams, 12,000 miles of commercial inland navigation channels, 24% of the U.S. hydropower capacity, dredging over 200 million cubic yards of material annually, maintaining over 900 inland and coastal harbors, providing over 325 million acre-feet water storage capacity, supporting military installations, and developing technologies through research to protect and enhance the environment [24]. The USACE’s Environmental Mission is merged into these responsibilities, focusing on AER of degraded ecosystems, construction of sustainable facilities, regulation of waterways, management of natural resources, and clean-up of contaminated sites from past military activities. As such, USACE is authorized by U.S. Congress to conduct AER under numerous funded programs. In general, AER project activities are framed in the following phases: planning, development, implementation, and maintenance. In USACE AER projects, this corresponds with feasibility, design, construction, monitoring, and adaptive management (MAM)/operations and maintenance (O&M) (Figure 1).

Figure 1.

General USACE AER project phase process with specific components of each phase; HEP = habitat evaluation procedure, MAMP = monitoring and adaptive management plan, MAM = monitoring and adaptive management, O&M = operations and maintenance.

3. Biological control

Classical biological control (CBC; ‘biocontrol’) of invasive plants is the intentional introduction of a host-specific organism to achieve meaningful suppression of the invader and to mitigate environmental and/or economic impacts stemming from the invasion [25, 26, 27]. Approved or permitted CBC agents are required to be host-specific (TAG-BCAW Manual 2020) with minimal direct impacts on non-target plant species. These requirements make them potentially valuable tools for applying targeted environmental pressures against invasive species while reducing their negative competitive effects on beneficial species. Common wetland weed targets of CBC in the U.S. include purple loosestrife, alligator weed, giant cane and giant salvinia, among others, all of which are problematic in mitigation and restoration projects (Table A1). Although achieving suppression may not occur rapidly as with other management tools (i.e., herbicides, mechanical harvesting/cutting), the slow progressive actions of CBC agents serve to promote recruitment of beneficial species on more realistic ecological timescales. As the effectiveness of CBC increases, limited resources become available for beneficial species, further suppressing invaders through a positive feedback loop [52]. Once invasive species are under control, regardless of the management tool(s) used, CBC and beneficial plant revegetation may provide for long-term, vegetation community stability.

CBC is predicated on the concept that co-evolved specialist natural enemies rely completely on their host for nutrition and whose populations would not persist without the host. CBC of weeds has been implemented globally since at least the late nineteenth century, with moderate to good success rates and low non-target impacts [53, 54]. Biological control is thought to be successful, in part, due to both ecological and evolutionary processes during the introduction and establishment phases of plant invasion. When plants are introduced from their native range into a new area in which natural enemies are absent, plant fitness and competitive strength often increase because there is a novel absence of regulation by herbivory or disease. This promotes rapid population growth and the formation of monocultures [55]. Limited biotic pressures in the introduced range may also lead to evolutionary changes in plant populations in which chemical or physical defenses against herbivory are lost over time in favor of rapid growth and reproduction [56]. Regardless, when biological control agents are introduced plant fitness is expected to decline.

CBC development typically proceeds through the “biocontrol pipeline” (Figure 2), which consists of discrete but sometimes overlapping phases: overseas exploration, quarantine and host-range studies, release and establishment, evaluation of efficacy, dissemination, and transfer of the technology to stakeholders (often the public). Typical biocontrol agent development costs and timelines vary, depending on the location of the native range and available infrastructure (i.e., roads, airports, etc.) needed for travel, whether the overseas exploration phase can be combined with searches for agents of other species, whether multiple agents are simultaneously collected and developed, and whether potential agents are already known from previous surveys or are in use elsewhere (e.g., [57, 58]).

Figure 2.

General process to develop biological control agents. Stars signify stages in development that require regulatory actions.

It is important local resource managers and stakeholders are involved in choosing appropriate metrics to determine target weed suppression and ultimately the success of the CBC program [59]. Because expectations of biocontrol success vary widely, it is essential to set realistic goals for management along with realistic timelines that fit within the overall restoration time horizon. Although CBC is a long-term prospect compared to other technologies that may deliver near-immediate, but often short-term results, CBC provides ongoing, sustained value when agent populations persist beyond the life of the release program [22]. The success of biological control can be categorized for monitoring and analysis as biological, ecological, economic, and social, but should be determined with the objectives of restoration projects in mind.

The process of testing and approval of CBC agents has received considerable scrutiny over the past 50 years because of rare but documented unintended consequences [53, 60, 61]. However, the process of modern CBC development is designed to promote safety and reduce non-target attack outcomes (e.g., TAG BCAW Manual 2020). In addition to being good practice, regulatory bodies require rigorous testing of potential agents to ensure they are safe for environmental release.

In the U.S., biocontrol agent importation and interstate movement are regulated by the United States Department of Agriculture Animal and Plant Health Inspection Service (USDA APHIS). Release within a state is regulated by the USDA APHIS in consultation with state governments. Specific authority for regulating importation and release of CBC agents is provided in numerous Acts and Executive Orders (TAG-BCAW Manual). Specifically, APHIS PPQ 526 Permits for Importation are required to import CBC agents into the U.S. from abroad, typically into a quarantine facility. APHIS PPQ 526 Permits for Removal from Containment are subsequently required for field releases and PPQ 526 Permits for Interstate Movement are required to transport agents between states, for instance with the purposes of making releases. However, some agents do not require APHIS permitting in the U.S. [62].

4. Incorporating biocontrol into USACE projects

Because the restoration environment can be complex—heterogenous habitats, fluctuating water levels, adjacent unmanaged lands—and invasive species responses to management can vary in those environments [63, 64], targeted management of invasive species can be challenging [65, 66, 67]. Frequently, widely used traditional tools used as stand-alone processes, fall short of managing invaders in the long term without repeated, costly treatments [11, 12]. The integration of multiple approaches, including herbicide application, physical removal/harvesting, enhancing native plant competition, and biocontrol, may provide the best chance for long-term sustainable outcomes [68, 69]. Most of these technologies are commonly considered and incorporated into all USACE AER project phases—feasibility, design, construction and MAM/O&M. However, biocontrol has been historically overlooked, despite the potential to add long-term invasive plant control benefits.

Biocontrol has been shown to substantially contribute to declines in invasive species when applied in a proper and timely manner [54]. Although natural recruitment of native species after implementation of biocontrol is the desired outcome, in practice, active—or requiring human intervention—revegetation programs may be necessary to provide a diverse community and resist reinfestation [70, 71, 72, 73]. Thus, the inclusion of biocontrol into an active revegetation program, which occurs during AER or habitat mitigation projects, may provide increased control relative to either biocontrol or revegetation separately, and simultaneously promote the native plant community by reducing target plant vigor.

Because of the magnitude of financial investment annually by USACE, other Federal agencies, and internationally in invasive species management, it is critical to identify the best technologies for long-term, sustaining control, while allocating resources wisely. Incorporating biocontrol during planning, design, implementation, and maintenance provides several key benefits, including (1) species-selective control that leverages co-evolved relationships between the invasive species and natural enemies (e.g., herbivorous insects or pathogens), (2) long-term suppression after project turnover with natural resource and economic benefits, (3) ability to target adjacent or complex habitats, where typical construction/herbicide activities physically cannot occur or are very expensive (e.g., slopes, islands, outside of project area) or legally cannot occur (e.g., cultural resources considerations), and (4) cost-reduction—follow-up management activities (monitoring of agent establishment and effectiveness) are reduced once the program is implemented and biocontrol agents are established.

Integrating biocontrol into the AER process is met with several barriers: (1) lack of guidance documents to inform regional invasive plant management decisions, overall, (2) biological control efficacy may be program or site-specific, so specialized frameworks are needed to support prioritization of management approaches and decision making, (3) biocontrol tools are not available for all important weeds and agent source and accessibility is unknown for most invasive species managers, and (4) for new, emerging weeds, protocols for implementing biocontrol and associated control efficacy are unknown, but important for resource managers to make decisions about control prioritization and spending. Below, we suggest specific moments throughout the AER project process to introduce biocontrol considerations and potential implementation strategies.

4.1 Planning/feasibility

In USACE AER projects, feasibility studies are conducted to assess problems related to water resources, develop sets of alternative solutions to correct them, model and compare solution outcomes, and recommend the best solution for the problem that meets both project-specific economic and environmental needs. The potential incorporation of biocontrol as a vetted tool for invasive plant management in an AER project should begin during this initial planning phase. Here, early, and consistent biocontrol subject-matter expert engagement in project planning should occur to provide expertise. This will help inform plan formulation (i.e., features, risks, cost estimation, and justifications of selected recommended plans), monitoring and adaptive management plans (MAMP), data requirements, and appropriate environmental and economic modeling (Figure 3).

Figure 3.

Typical AER project phases and applicable implementation moments during the process to implement biological control of invasive weeds (adapted from seeding AER considerations, [74, 75]). Veg = vegetation management, BC = biocontrol, MAMP = monitoring and adaptive management plans, ID IAS = identify invasive alien species, O&M = operations and maintenance, AM = adaptive management.

Problem invasive species at restoration sites should be identified and biocontrol management options or regulatory agency-approved agents and potential costs to undertake those management options should be identified and analyzed. Literature reviews and natural resource manager engagements should be undertaken to estimate efficacy and costs of management options. When species-specific information is not available, inferences can be based on similar species-habitat examples. For example, there are several floating aquatic weeds with biocontrol agents available and, while cost estimates are not available for all these floating species, a close approximation could be made using available data [76, 77]. Although a comparison can then be made between estimated costs of biocontrol and various other management options, their combined use may be most advantageous. In this way, various control methods feasibility-usage and impacts should be considered for both complex and sensitive habitats and locations, such as areas with cultural resources implications. This will assist in delineating between biocontrol and other management tools, their accessibility and costs, and timelines for reaching management objectives. In turn, this will function to assist in the determination and justification of a recommended restoration plan—including economic considerations—as well as eventual project O&M costs.

Potential hurdles for implementing a biocontrol program within a project are regulations, safety, and appropriate material source of control agents. Once applicable invasive species are identified within the project footprint and regulatory agency-approved agents identified, a project-specific regulatory and permitting plan should commence for that agent, including local resource agency coordination and any interstate movements necessary. This may be accomplished, in part, in coordination with the supplier of the control agent, who often has permits in place to ship agents across state lines for releases. For example, personnel at the USACE Jacksonville District distribute Agasicles hygrophila Selman & Vogt—a biocontrol agent of alligatorweed—annually to Federal and state requestors [24]. The USACE has APHIS PPQ526 permits for distribution of A. hygrophila from FL, U.S. to several states and can amend the permit if additional states require releases. Depending on the scale of the invader problem and whether agent releases are expected to occur over several years, local mass-rearing operations can be instituted with volunteer or local agency help [77].

4.2 Development/design

The development or design—pre-construction, engineering, and design (PED in USACE)—involves the development of plans, specifications, and actions that will meet project goals. In the design phase, all designs and protocols for acquiring, culturing, releasing, and monitoring approved biocontrol agents’ releases should begin (Figure 3). Here, public resource agencies as well as private contractors with viable biocontrol programs should be engaged for potential project incorporations. Once approved agents are chosen, and permits are acquired (if necessary), culture and rearing should begin. This can be accomplished by the internal project delivery team (PDT) or another public or private entity with a viable program and applicable permits. The primary goal is to ensure biocontrol source material/agents are obtained properly and culturing commences for project implementation releases in subsequent phases. Plant-culturing and agent-rearing protocols may be species-specific and should be handled at an individual level (Table A1). During culturing and rearing, small-scale experiments can be done to inform agent release densities. Some of this information may already be reported in the literature or unpublished but available from the scientists who provide the agents.

Next, biocontrol release sites at the project site should be identified and assessed. Biocontrol will be an integrated tool for invasive species management, in addition to other chemical, physical, and cultural control methods. It is important to delineate the project footprint and invasive species coverages to identify the appropriate or most cost-effective and environmentally beneficial areas to apply the technology. This would generally include adjacent, complex, sensitive, inaccessible to machinery, or native-dominated areas where other control tools are likely to be non-selective or ineffective. The team should keep the overarching goal of vegetation management focused AER projects—shifting species dominance from invasive to native—as paramount. Multiple sites of varying physical and biological parameters should be selected.

Biocontrol agent release and monitoring protocols should be developed in coordination with resource agencies and the PDT. For releases, the first question is related to successful establishment: ‘what balance of agent abundance (total number of agents) and number (spatial extent) of releases is required for establishment [78, 79]?’ This plan can be developed through literature and subject-matter experts. Protecting the initial releases during their sensitive establishment phase is another important consideration. Ensuring adequate source plant material is available and protecting agents from predators with caging, which also promotes mating and prevents agents from premature dispersal from the release location, will assist in agent establishment. Protective devices are subsequently removed, and agents can disperse freely.

Because approved agent releases will likely occur alongside active native plantings, a subset of release sites can include in situ plant competition experiments to quantify control and inform monitoring and adaptive management procedures for the current and subsequent projects. Experimental units may include (a) no invasive-no agent-no plantings, (b) no invasive-no agent-plantings, (c) invasive-agent-no plantings, (d) invasive-no agent-plantings, and (e) invasive-agent-plantings. In terms of monitoring efficacy, protocols should include appropriate plant variables to determine agent efficacy. This will likely vary by species, growth form, and type of impact in the environment, but may include flower and fruit production, recruitment, areal coverage, damage, and agent abundance.

4.3 Implementation/construction

Project implementation or construction is the active installation of restoration features including physical improvements, invasive species management, and native plant establishment efforts. Regarding invasive species management via approved biocontrol agents, three primary actions are undertaken during this phase: (1) continued rearing and culturing, (2) agent releases for impact on invasive species, and (3) monitoring agent efficacy (Figure 3). Using release methods developed in coordination with resource agencies during design and informed by experiments, continued releases are made into selected sites. During this phase of the project, and pending confirmed establishment of agents at release sites, efforts should be geared towards maximizing and measuring agent impact on the target species. Releases may continue largely unchanged from the design phase or be modified to increase agent abundance and impact. Site characteristics should be documented over time, during subsequent releases of agents is often convenient. For each assessment, plant condition (flowering/fruit production on release and non-release plants) and agent condition (population size and dispersal) should be documented. Agents can be counted in the field or collected, preserved, and returned to the laboratory for counting and as reference specimens. Vegetation community structure, or dominance changes in invasive and native species abundance/diversity, within release sites, should be documented as relevant to project objectives.

4.4 Monitoring and adaptive management/operations and maintenance

In USACE AER projects, MAM and O&M are separate phases but overlap to some extent depending on the project. In MAM, costs are still shared between USACE and a non-Federal sponsor; projects are turned over fully to the non-Federal sponsor at the start of O&M. During MAM (generally lasting 3–5 years, with a max of 10), USACE may do all the monitoring, partner with agencies/organizations, or contract this out to private. Adaptive management here is either done by the non-Federal sponsor as part of their O&M or as part of a design change to the original project via a new contract. Long-term project O&M is then accomplished by local, non-Federal cost-share sponsors.

One of the benefits of biocontrol is its potential self-sustaining nature which provides long-term site management benefits. During MAM and prior to O&M, site owners, natural resource managers, and other stakeholders should be trained on collecting, relocating, and monitoring agents with continued assessments and releases as needed. This will assist in the long-term vegetation community trajectory goals after project turnover, which will support project function and habitat requirements. In addition, lessons learned during rearing, releases, and monitoring should be considered and discussed for current and subsequent project-process improvement.

5. Conclusion

In this paper, we are only advocating for the potential AER project vetting and inclusion of biological control agents that have already been subjected to rigorous testing and government/regulatory agency approvals. Although biocontrol has potential to be a valuable tool when used alone or in combination with other weed management approaches, it may not be suitable in all situations. There may not be approved agents available for a target species. The timeline of control once agents are introduced may not be acceptable. For example, biocontrol typically takes months to years to achieve meaningful suppression at a location, but project objectives may require immediate action. In those cases, it may be more appropriate to use herbicides or mechanical removal or target species from priority areas, then follow up with biocontrol or other actions for longer-term control. There are several biocontrol programs in which the introduced agents and their host do not fully overlap geographically in the introduced region, for example, because of differences in climate envelopes of the species [80]. In cases where the climate is not suitable for the persistence of agents from year to year, agents must be continually reintroduced to achieve control, which may negate the cost-savings aspect of biocontrol in certain cases.

We do suggest that in many cases when invasive plant management is a component of an AER project, approved biocontrol agents should be considered for inclusion in an IPM plan. Biocontrol has historically been treated as a stand-alone tool and should be considered for its role in complementing other management actions. It can be cost-effective, self-sustaining, and functions in long-term site management which contributes to reducing the imbalance in abundance of invasive and native plant species. In this way, use of biocontrol can assist in invasive species management while potentially overcoming budgetary, environmental, and sensitive cultural resource limitations. Although biocontrol should be included, when applicable, in all phases of a project, it begins in planning. It is in planning where invasive species to be managed are identified and prioritized, alternatives to control are analyzed, cost analyses are completed, and monitoring and adaptive management plans are developed. The potential for biocontrol agents to be utilized during the project should be identified at this point along with potential cost-savings and environmental benefits. This vetting is generally lacking in project planning and its inclusion has myriad potential economic and environmental benefits over the life of a project.

Acknowledgments

This work was funded by the USACE Ecosystem Management and Restoration Research Program (EMRRP) and the Aquatic Plant Control Research Program (APCRP). Thanks to Dr. Nathan Beane, Tara Whitsel, Micheal Greer, and Dr. Brook Herman for their previous USACE internal reviews and comments on the manuscript.

See Table A1.

Weed species	Common name	Region affected	Types of impacts	Biocontrol agent	Regulatory agency	Comments	Reference
Acer platanoides	Norway maple	NE, NW	Produces a large quantity of seeds that can germinate rapidly and crowd out native species. Also creats a dense canopy shading out neighbors.	Pathogen: Chondrostereum purpureum (silver leaf)	USDA USFS		[28, 29]
Ailanthus altissima	Tree of heaven	Entire US excluding N-MW	Prolific seed producer, grows rapidly, and can overrun native vegetation. Once established, can quickly take over a site and form an impenetrable thicket. Produces toxins that prevent establishment of other plant species. Root system is aggressive enough to cause damage to sewers and foundations.	Pathogen: Verticillium dahliae (Verticillium wilt), Fusarium oxysporum (Agent green); Predator: Eucryptorrhynchus brandti (snout weevil)	USDA USFS		https://www.texasinvasives.org/plant_database/detail.php?symbol=AIAL
Albizia julibrissin	Mimosa (Albizia)	SE, SW	Can grow in a variety of soils, produce large seed crops, and resprout when damaged. It is a strong competitor and dense stands severely reduce the sunlight and nutrients available for other plants.	None currently, but potential agents known from the native range include: Pathogen: Fusarium oxysporum (fusarium wilt); Predator: Bruchidae spp. (bruchid beetle), and Acizzia jamatonica (albizia psyllid)			[30]
Alternanthera philoxeroides	Alligatorweed	SE	Terrestrial form grows into a dense mat with a massive underground rhizomatous root system. Has potential to completely disrupt aquatic environments by blanketing the surface, impeding light penetration and gaseous exchange. Also promotes sedimentation and flooding.	Predator: Amynothrips andersoni (alligator weed thrip), Agasicles hygrophila (alligator weed flea beetle), Arcola malloi/ Macrorrhinia endonephele (alligator weed stem borer)	USDA		https://www.cabi.org/isc/datasheet/4403; [31]
Arundo donax	Giant cane	SW, SE	Chokes riversides and stream channels, crowds out native plants, interferes with flood control, increases fire potential, and reduces habitat for wildlife, including the Least Bell’s vireo, a federally endangered bird.	Predator: Tetramesa romana (Arundo wasp), Rhizaspidiotus donacis (rhizome-stem feeding beetle), Lasioptera donacis (gall midge)	USDA ARS USDHS CBP		[29, 30, 32]; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Butomus umbellatus	Flowering rush	N, NE	Can displace native riparian vegetation, form dense stands, and spreads locally by rhizomes and root pieces that break off and form new plants.	None currently, but potential agents include: Predator: Bagous nodulosus (flowering rush weevil), B. validus (weevil), Phytoliriomyza ornate (agromyzid fly); Pathogen: Doassansia niesslii (white smut)	WSDA WDOE WSDNR USDD ACE MNWTF MDNRC USDA USFS USDA USFS FHTET Kalispel Tribe BC MFLNRORD CABI		[33]; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf; https://platform.cabi.org/projects/project/56422
Cabomba caroliniana	Carolina fanwort	E, SE, W	Can form extremely dense stands which can clog drainage systems and interfere with recreational activities. The rhizomes are fragile and easily broken, facilitating vegetative spread and transport.	None currently, but potential agents include: Predator: C. idella (Triploid grass carp)			[33]
Colocasia esculenta	Elephant ears/Taro	SE	Fast-growing weed with the potential to displace native vegetation by growing dense thickets.	None currently, but potential agents known from the native range include: Predator: Papuana woodlarkiana (taro papuana beetle), P. biroi (taro beetel), P. huebneri (taro beetle), Papuana trinodosa (taro beetle), Heliothrips indicus (groundnut thrip); Pathogen: Phytophthora colocasiae (taro leaf blight), Taro large bacilliform virus (TLBV) which is transmitted by the plant hopper Tarophagus Proserpina (taro planthopper), Taro small bacilliform virus (TSBV) which is transmitted by the mealybug Planococcus citri (citrus mealybug)			[34]; https://www.cabi.org/isc/datasheet/17221; https://www.invasive.org/browse/subinfo.cfm?sub=5369
Cynodon dactylon	Bermuda grass	Entire US excluding N-MW	Plant residues and actively growing plant parts may pose a direct threat to the growth of neighboring plants.	None currently, but potential agents include: Pathogen: Erysiphe graminis (Powdery/barley/corn mildew)			[35]; https://www.cabi.org/isc/datasheet/22075
Eichhornia azurea	Anchored water hyacinth	SE	Has the potential to form thick mats over the water surface, shading out native vegetation and altering water chemistry.	None currently, but potential agents known from the native range include: Pathogen: Cercospora piaropi, Alternaria eichhornia, Myrothecium roridum (leaf spots); Predator: Neochetina bruchi (hevroned waterhyacinth weevil) N. eichhorniae (mottled water hyacinth weevil), Niphograpta albiguttalis (waterhyacinth moth) Xubia infusellus, Orthogalumna terebrantis (water hyacinth mite), Eccritotarsus catarinensis (sap sucking mirid), Cornops aquaticum (grasshopper),; Megamelus scutellaris (planthopper)			https://www.cabi.org/isc/datasheet/108967
Elodea canadensis	Canadian waterweed	E, AK	Grows rapidly in favorable conditions and can choke shallow ponds, canals, and the margins of some slow-flowing rivers.	None currently, but potential agents include: Predator: Ctenopharyngodon idella (triploid grass carp); Pathogen: Fusarium spp. (Panama disease)			[33]
Hydrilla verticillata	Hydrilla; (Monoecious & Dioecious)	SE, SW, NW	Forms dense masses, which may completely fill the volume of waterbodies. Alters the physical and chemical characteristics of lakes: affecting stratification of the water column, decreasing oxygen levels, and impeding the movement of irrigation and drainage water. Dense stands also alter water quality by increasing pH and water temperature.	Predator: Hydrellia pakistanae (asian hydrilla leaf-mining fly), H. balciunasi (australian hydrilla leaf-mining fly), Bagous affinis (hydrilla tuber weevil), B. hydrillae (hydrilla stem weevil), Cricotopus lebetis (hydrilla tip mining midge), Parapoynx diminutalis (hydrilla leafcutter moth)	USDA ARS UF-IFAS USDD ACE		[29, 33]; https://www.cabi.org/isc/datasheet/28170
Lespedeza cuneata	Sericea/Chinese lespedeza	SE	Extremely aggressive invader of open areas and outcompetes native vegetation. Once established, is very difficult to remove due to the seed bank, which may remain viable for decades. High tannin makes it unpalatable to wildlife.	None currently, but potential agents known from the native range include: At least ten fungi and 65 arthropods			[30, 36]; https://www.invasive.org/weedcd/pdfs/asianv1/lespedeza.pdf
Ligustrum sp.	Privet	SE, MW	Forms dense thickets, can shade out and exclude native understory species, perhaps even reducing tree recruitment.	Predator: Leptoypha hospita (lace bug)	USDA USFS		[29, 37]; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Lygodium japonicum	Japanese climbing fern	SE	Can form dense mats that smother understory vegetation, shrubs and trees. Persists and colonizes by rhizomes and spreads rapidly by wind-dispersed spores.	None currently, but potential agents include: Predator: Neomusotima conspurcatlis (defoliating moth), Neostrombocerus spp. (Lygodium-specific saw fly), Manobia spp. (flea beetles)			[33]; https://www.cabi.org/isc/datasheet/31783
Lythrum salicaria	Purple Loosestrife	NE, MW, NW	Can quickly form dense stands that completely dominate the area excluding native vegetation. This plant can spread very rapidly due to its prolific seed production; each plant can produce up to 2.5 million seeds per year. It can also hybridize with native loosestrife species, potentially depleting the native species gene pool.	Predator: Hylobius transversovittatus (weevil), Galerucella calmariensis (black-margined loosestrife beetle), G. pusilla (black-margined leafstrife leaf beetle), Nanophyes marmoratus (loosestrife seed weevil)	USDA		[29, 38]
Melaleuca quinquenervia	Melaleuca	SE	Forms impenetrable thickets, reduces biodiversity, displaces native vegetation and reduces habitat value. Also accelerates loss of groundwater due to increased evapotranspiration.	Predator: Oxyops vitosa (melaleuca leaf weevil), Boreioglycaspis melaleuca (Melaleuca psyllid), Lophodiplosis trifida (melaleuca gall midge); Pathogen: Puccinia psidii (guava rust); Combo: Fergusobia quinquenervia (nematode) in combination with Fergusonina turneri (gall fly)	USDA FWC SFWMD		[29, 33]; https://www.cabi.org/isc/datasheet/34348; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Melia azedarach	Chinaberry	SE	Has the potential to grow in dense thickets, restricting the growth of native vegetation. Leaf litter may alter soil chemistry, with increased pH and mineralizable nitrogen.	None currently, but potential agents known from the native range include: Predator: Leptocneria reducta (white cedar moth)			https://www.cabi.org/isc/datasheet/33144; [39]
Microstegium vimineum	Japanese stilt grass	NE, SE	Very shade tolerant and can completely displace native vegetation. Individual plants may produce 100 to 1,000 seeds. Seed remains viable in the soil for five or more years and germinates readily.	None currently, but potential agents known from the native range include: Thirteen species of fungi and eight arthropod species	USDA USFS FHAAST		[40]; https://www.cabi.org/isc/datasheet/115603; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Myriophyllum spicatum	Eurasian watermilfoil	NE, SE, MW, NW	Interferes with flow of irrigation water, transport, hydro-electric power production, fisheries, recreation, and increases risk of flood and associated hazards to human life.	Predator: Phytobius leucogaster (weevil), Triaenodes tarda (long horned caddisfly), Euhrychiopsis lecontei (weevil), Acentria ephemerella (watermilfoil moth or water veneer)	LCWC UM-LCCMR USDA ARS		https://www.cabi.org/isc/datasheet/34941; [29, 41]
Nitellopsis obtusa	Starry stonewort	NE	Can outcompete other vegetation and forms monotypic stands that can reduce fish spawning habitat.	None			https://dnr.wisconsin.gov/topic/Invasives/fact/StarryStonewort.html
Oxycaryum cubense	Cuban bulrush	SE	Forms large monotypic floating mats on the surface of standing water. This may send out runners over other emergent plant species and crowd them or exclude them.	None currently, but potential agents include: Predator: Agasicles hygrophila (Alligatorweed flea beetle), C. idella (Triploid grass carp)			[33]
Panicum repens	Torpedo grass	SE	Can form dense pure swards that replace native species.	None currently, but potential agents from native range include: Predator: S. panici (Indian tarsonemid mite); Pathogen: Drechslera gigantea (eyespot disease), Exserohilum longirostratum, E. rostratum (leaf spots, crown/root rot)			[33]; https://ipm.ifas.ufl.edu/pdfs/Torpedo-grass.pdf
Pennisetum/; Cenchrus ciliare	Buffelgrass	SW	Dead biomass of C. ciliaris tends to accumulate across years in the absence of fire, leading to increased fire risk in unburned stands over time.	None currently, but potential agents known from the native range include: Predator: Aeneolamia albofasciata (spittle bug), Mampava rhodoneura (bufflegrass seed moth); Pathogen: Magnaporthe oryzae (blast fungus)			https://www.cabi.org/isc/datasheet/14502
Phalaris arundinacea	Reed canarygrass	Entire US	Can exclude all other vegetation and is extremely difficult to eradicate once established. Can be harmful to grazers.	None currently, but potential agents from native range include: Predator: Sitodiplosis phalaridis (phalaris gall); Pathogen: Septoria bromi var. phalaricola (septoria disease)			[33]; https://www.cabi.org/isc/datasheet/55423#tonaturalEnemies
Phragmites australis	Common reed	MW, SE	Thickets displace native wetlands plants, alter hydrology and block sunlight to the aquatic community.	None currently, but potential agents from native range include: Predator: Archanara geminipuncta (twin-spotted wainscot moth), Cecidomyiidae spp. (gall midges), Shoot flies, C. idella (triploid grass carp)	USDD ACE USDI FWS BC MFLNRORD NY DOT		https://www.cabi.org/isc/datasheet/40514; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Pistia sp.	Waterlettuce	SE, NE	Forms extensive mats that can block navigational channels, impede water flow in irrigation and flood control canals, and disrupt submersed animal and plant communities.	Predator: Neohydronomus affinis (waterlettuce weevil), Spodoptera pectinicornis (waterlettuce moth)	USDA		[29, 42]
Pontederia crassipes	Water hyacinth	SE	Grows rapidly and can very quickly form expansive mats of floating plants, completely covering even large lakes. This complete coverage of the surface of the water blocks sunlight and depletes the oxygen available to the rest of the aquatic community.	Pathogen: Cercospora piaropi (fungus), Acremonium zonatum (fungus); Predator: Neochetina bruchi (hevroned waterhyacinth weevil), N. eichhorniae (mottled water hyacinth weevil), Niphograpta albiguttalis (waterhyacinth moth)	USDA ARS USDD ACE		https://nas.er.usgs.gov/queries/greatlakes/FactSheet.aspx?SpeciesID=11&Potential=Y&Type=2; https://www.invasive.org/browse/subinfo.cfm?sub=4677; [29]; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Salvinia minima	Common salvinia	SE	Dense mats shade out native aquatic species, reduce dissolved oxygen levels in the water, and clog waterways.	Predator: Cyrtobagous salviniae (salvinia weevil)	USDA		https://www.cabi.org/isc/datasheet/107785; [29]
Salvinia molesta	Giant salvinia	SE, SW	Forms chains of leaves that run together to form thick mats on the surface of the water. These mats restrict oxygen and light availability causing death of the primary producers and disrupting the aquatic food chain.	Predator: Cyrtobagous salviniae (salvinia weevil)	LSU FUEDEI INIA USDA ARS		https://www.cabi.org/isc/datasheet/48447; [43]
Schinus terebinthifolius	Brazilian peppertree	FL, TX, CA, HI, PR, and Virgin Islands	Ability to form dense thickets and rapidly invades disturbed sites, displacing native vegetation. Possible allelopathy.	Predator: Episimus unguiculus (moth) Hawaii-permitted only, Lithraeus atronotatus (invertebrate), Megastigmus transvaalensis (Brazilian peppertree seed chalcid), Crasimorpha infuscate (moth), Pseudophilothrips ichini (Brazillian peppertree thrips),; Calophya latiforceps (yellow Brazilian peppertree leaf-galler	UF-IFAS USDA, ARS FDACS DPI SFWMD FIPR		https://www.cabi.org/isc/datasheet/49031; [29, 44, 45]; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Sorghum halepense	Johnsongrass	SE, MW	Spreads aggressively and can form dense colonies which displace native vegetation and restrict tree seedling establishment. Invades and disrupts feed crops. Can cause poisoning of cattle under some circumstances due to its cyanic content during periods of vigorous growth, drought or following frost.	None currently, but potential agents known from the native range include: Predator: Hispellinus moestus/callicanthus (leaf miner); Pathogen: Pseudomonas syringae (bacterial leaf spot), Sphacelotheca holci (loose smut)			https://www.cabi.org/isc/datasheet/50624; [35]
Tamarix spp.	Salt cedar	SE	Can crowd out native riparian species, diminish early successional habitat, and reduce water tables and interferes with hydrologic process.	Predator: Diorhabda elongata (mediterranean tamarix beetle), Diorhabda carinata/carinulata (northern tamarix beetle), Diorhabda sublineata (leaf beetle), Coniatus splendidulus (splendid tamarix weevil)	USDA	There has been a moratorium on interstate releases of Diorhabda because of endangered willow flycatcher habitat	[29, 46]
Trapa natans/T. bispinosa var. iinumaii.	Water chestnut	NE	Forms dense mats of floating vegetation; impacts navigation, recreation, and aquatic habitat.	None currently, but potential agents include: Predator: Galerucella birmanica (Leaf beetle), C. idella (Sterile grass carp),	NY DEC		https://www.cabi.org/isc/datasheet/55040; http://nyis.info/invasive_species/water-chestnut/; https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=263; https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=2974 [47, 48, 49, 50]
Triadica sebifera	Chinese tallow	SE, CA	Can displace native vegetation as well as alter soil conditions due to the high amount of tannins present in the leaf litter. Fallen tallow leaves contain toxins that create unfavorable soil conditions for native plant species.	None currently, but potential agents known from the native range include: Predator: Bikasha collaris (root feeding beetle)	FFWCC USDA ARS USDA USFS FHP BCIP		[51]; https://www.cabi.org/isc/datasheet/48351; https://bugwoodcloud.org/ibiocontrol/publications/Weed_Classical_Bio_Ctrl_Directory_Contacts-2-13-28.pdf
Urochloa maxima/; Megathyrsus maximus	Guinea grass	SW, SE	Regenerates rapidly from underground rhizomes. Suppresses or displaces local plants. Its resistance to drought also means it builds up a dangerous mass of plant material so when fires occur, the blaze is fiercer and native plants which have not built up fire-tolerance are wiped out. As guinea Grass can survive fires, it can dominate the ground after a fire.	None currently, but potential agents include: Pathogen: Drechslera gigantean (eyespot disease), Exserohilum rostratum (leaf/crown/root rot), E. longirostratum, combination of all 3 is most effective	USDA ARS	E. rostratum and E. longirostratum are also possible human pathogens – exercise caution	[33]; https://www.cabi.org/isc/datasheet/38666

Table A1.

Common weed species in USACE ecosystem restoration or habitat mitigation projects and their biological control agents, if any.

Acronyms: UF-IFAS = University of Florida Institute of Food and Agricultural Sciences; USDA ARS = United States Department of Agriculture Agricultural Research Service; FDACS DPI = Florida Department of Agriculture and Consumer Services Division of Plant Industry; SFWMD = South Florida Water Management District; FIPR = Florida Industrial and Phosphate Research Institute; USDD ACE = United States Department of Defense Army Corps of Engineers; LCWC = Les Cheneaux Watershed Council; UM-LCCMR = University of Minnesota Legislative-Citizen Commission on Minnesota Resources; LSU = Louisiana State University; FUEDEI = Fundacion Para El Estudio De Especies Invasivas (Foundation for the Study of Invasive Species); INIA = Institute of Agricultural Research; FFWCC/FWC = Florida Fish and Wildlife Conservation Commission; USFS = United States Forest Service; FHP = Forest Health Protection; BCIP = Biological Control of Invasive, Native and Non-Native Plants; USDHS CBP = Unites States Department of Homeland Security Customs and Border Patrol; WSDA = Washington State Department of Agriculture; WDOE = Washington State Department of Ecology; WSDNR = Wisconsin Department of Natural Resources; MNWTF = Montana Noxious Weed Trust Fund; MDNRC = Montana Department of Natural Resources and Conservation; FHTET = Forest Health Technology Enterprise Team; BC MFLNRORD = British Colombia Ministry of Forests, Lands and Natural Resource Operations Region and District; CABI = Center for Agriculture and Bioscience International; FHAAST = Forest Health Assessment and Applied Sciences Team; USDI FWS = United States Department of the Interior Fish and Wildlife Service; NY DOT = New York Department of Transportation; NY DEC = New York Department of Environmental Conservation.

Author contribution

ANS, led effort, lead on Incorporating section, co-wrote Introduction, USACE Background, Conclusion; NEH, lead on Biological Control, co-wrote Incorporating; DA, LLD, KH, JK, JN, literature, co-wrote Introduction, USACE Background; GOD, DA, lead on USACE Background.