1. Introduction

1.2. Asian Clams Dispersal in Massachusetts, USA

Previous studies reported that the Asian clam was first sighted in Massachusetts in the Charles River in 2001. This is fitting as the state’s likely origin of infestation as the Charles River is a central figure in the Eastern Massachusetts landscape and is a hotspot for boating year-round [14]. However, newly discovered historical data reveal that Asian clams were first detected in Massachusetts farther South in Long, Pond at Lakeville as early as 1999 [15]. Long Pond is frequently used for recreational boating, fishing, and swimming, all of which are common vehicles for aquatic invasive species introduction and contamination. Before 2017, Asian clams were found in 36 waterbodies, mostly in the south and southeast of the state with an abundance of up to 6,124 clams/m² recorded in an infested unnamed tributary in Forest Park, Springfield, Massachusetts [16]. Since their introduction in 1999, Asian clams have been found in 45 waterbodies, including 8 rivers and 37 ponds and lakes in Massachusetts [14]. In the past 5 years, Asian clams have expanded into waterbodies farther northwest within Massachusetts (Figure. 1), where minimum water temperatures are usually lower. This northern expansion of range is consistent with other research as the species’ presence has recently been detected in other New England states, such as Lake Bomoseen in the State of Vermont [14,17] and in the lower Merrimack River and in several ponds in the State of New Hampshire [14,18,19].

Figure 1. Distribution map depicting Corbicula fluminea in Massachusetts. Sightings were grouped by first reported sight years and color coded to demonstrate the northwestern expansion of their range over 24 years (See supplementary material Table S1 for site descriptions).

Figure 1. Distribution map depicting Corbicula fluminea in Massachusetts. Sightings were grouped by first reported sight years and color coded to demonstrate the northwestern expansion of their range over 24 years (See supplementary material Table S1 for site descriptions).

1.4. Management Strategies

While prevention of aquatic invasive species infestations is the ideal management strategy, an integrated approach is necessary to best treat waterways once Asian clams have been detected to prevent further spread. Wong [14] lists that this integrated strategy should contain 4 steps:

• Identify the primary means of spread.
  • The most vulnerable waterbodies must also be identified to allocate resources in the most cost-effective manner.

2.

Create a plan to stop or slow the spread.

• Public awareness plays a large role in limiting dispersal so developing educational content and signage should be a priority. There also must be an investment in infrastructure to prevent spread, such as installing washing stations at susceptible waterbodies.

3.

Analyze the ecological and economic impact of infestations on new water bodies.

4.

Create an emergency response plan to proactively limit the species’ invasiveness.

The emergency response plan will contain components of all 4 steps outlined above, but it will focus primarily on the active treatment. These methods can be both reactive, once a population of Asian clams has been detected, and proactive, targeting Asian clams in the larval stage before they have been established. Proactive treatments tend to be more effective, versatile, and cost-effective than reactive measures. However, due to limited resources, they are often not employed until after infestations have been detected [14,26]. Treatments options include physical, biological, genetic, and chemical options, as depicted in Table 1. While each treatment type can be employed individually, there is potential to combine techniques to enhance their efficacy.

Table 1. Evaluation characteristics of each option available for treating Asian clams.

Table 1. Evaluation characteristics of each option available for treating Asian clams.

1.6. Treatment Selection

Chemical treatments have the largest range of options available that allows for site specific Asian clam control plans. A variety of factors must be considered when determining which chemical treatment to use to achieve the goals of the project. A summary of the most crucial factors to consider when choosing a chemical treatment are listed below in Table 2. However, special attention is needed to determine whether a water system is considered open or closed. Closed systems include water intake pipes, wastewater treatment facilities, and electric powerplants cooling systems [16]. Treatment is aimed at eradicating existing or preventing biofouling clams from accumulating on these commercial structures. Due to their great potential economic impact, many treatments have been specifically designed to be used in in these industrial settings [26]. Non-target species are of minimal concern in this setting so more aggressive control strategies can be employed. In these closed systems, usually oxidative chemicals such as chlorine or bromide are used to eradicate the invasive bivalves quickly and effectively. However, chlorine and bromide produce carcinogenic byproducts and halogens that are toxic to non-target species [35,36]. To prevent environmental contamination, chemical treatments used to prevent or treat biofouling clams in closed systems are not suitable chemical treatments for open water systems [27].

It is more difficult to stop the spread of Asian clams in open water systems, where treatment methods are more restricted due to their potential to negatively impact water quality, including drinking water contamination, and non-target species [14]. Additional consideration and extensive testing protocols must be employed to ensure that the chemical treatment used to eradicate invasive Asian clams does not have deleterious environmental consequences. For the purposes of this review, only treatments that have been used or have the potential to be used in open water systems have been included in the analysis. One of the most common active ingredients used in molluscicides for Asian clam chemical treatment is copper-based compounds. The copper-based treatments induce mortality in Asian clams through binding to receptors on the bivalves’ gills, thus inhibiting gas exchange across the cellular membrane [14,37].

Table 2. Variables to consider when selecting a control strategy for Asian clams.

Table 2. Variables to consider when selecting a control strategy for Asian clams.

2. Methods

2.1. Systematic Review

A variety of Asian clam control methods have been developed for practitioners that include physical, biological, and chemical control. This review will focus primarily on chemical control as this strategy requires natural resource managers to use the least resources while achieving the greatest impact. A systemic review was conducted on Google Scholar using the key words “Asian clam Chemical Treatment” to identify peer-reviewed articles, state and federal regulatory documents, and chemical product safety data sheets through March 2024. In addition to these documents, the Invasive Mussel Collaborative website was used to identify primary, peer-reviewed sources. The sources were then categorized by subject matter, determined by whether reported studies were conducted on Asian clams in the field, Asian clam toxicity studies in a laboratory setting, or if the study focused on the treatment of other species of invasive bivalves of which the treatment could potentially be applied to Asian clams in future studies. The following results are categorized as such.

Figure 2. Workflow of systematic review categorization process.

Figure 2. Workflow of systematic review categorization process.

3. Results

3.2. Toxicity Studies

Apart from existing chemical applications, there are numerous toxicity studies on Asian clams and some of these treatments may have potential to be applied as new methods in the future. These molluscicides and their concentrations under various dissolved oxygen concentrations are listed in Table 3 and the original studies are described below.

Table 3. Toxicity of common active ingredients in molluscicides on Asian clams..

Table 3. Toxicity of common active ingredients in molluscicides on Asian clams..

3.2.1. Asian Clam Sensitivity in Laboratory Testing

Wild-caught adult Asian clams were acclimated to municipal water maintained at 20 ± 2 °C with a 16hr^L and 8hr^D photoperiod cycle with continuous aeration. Mortality tests were then conducted under a geometric range of concentrations for each of the six chemicals. Each treatment was conducted under both normoxic conditions (>7mg/L dissolved oxygen) and under hypoxic conditions where nitrogen gas was infused into the water to decrease the dissolved oxygen content to less than 2 mg/L. While Asian clams display great physiological plasticity and are able to acclimate to various environmental conditions, they are largely intolerant to low oxygen levels. The results of this study demonstrate that the hypoxic conditions increased the susceptibility of clams to the chemical treatment by up to 400% relative to the same treatments performed under normoxic conditions [4]. The concentrations for the minimum effective concentration as well as the most effective concentrations of each chemical treatment under both hypoxic and normoxic conditions are summarized in Table 3.

The results of this study have important implications for managing invasive Asian clam populations. This toxicity study provides target concentrations for a variety of chemical treatments options. However, it also highlights how natural resource managers can combine treatment options to optimize results. Combining physical and chemical management of invasive species could increase the effects of chemical treatment while decreasing the concentration of chemicals used, thereby minimizing the deleterious effects on non-target species and the surrounding environment. Use of curtain barriers reduces dissolved oxygen content and increases Asian clam oxidative stress as well as boosts the efficacy of chemical treatments. Similarly, the use of benthic barriers over treatment areas could help to induce hypoxic conditions to increase treatment efficacy and clam mortality [30].

3.3. Chemical Treatments on Other Bivalves

Numerous molluscicides have already been developed to induce mortality in other invasive bivalves, such as zebra, quagga, and golden mussels. There is potential to expand the targeted species to include Asian clams following laboratory toxicity and field testing. As such, Table 4 represents an inexhaustive list of chemical treatments currently used to treat other invasive bivalves that should be the subject of further study for use in Asian clam chemical treatment studies.

Table 4. Chemical Treatments of other Invasive Bivalves with potential applications for Asian clam management.

Table 4. Chemical Treatments of other Invasive Bivalves with potential applications for Asian clam management.

3.3.1. Potassium Chloride and Formalin

In a study by Layhee et al. [48], a laboratory toxicity study was performed to determine if the molluscicide of 750 mg/L KCl and 25 mg/L Formalin (37% formaldehyde) used to treat zebra mussel veligers in hatcheries had similar success in Asian clams. Using this process, commonly referred to as the Edward’s protocol [38], the study determined that there was 100% mortality of Asian clam veligers after 3- and 5-hour exposure times [48]. While further testing is needed to determine how this treatment effects different life stages as well as its potential for use in open-water systems, this initial study is promising that chemical treatments used in management of other invasive bivalves can successfully be used to treat Asian clams.

3.3.2. Zequanox®

Another potential treatment for Asian clams is a biopesticide under the brand name Zequanox® that contains Pseudomonas fluorescens strain CL145A cells in a spent fermentation media. This bacterium naturally occurs in soil and water and is ingested by filter feeders, subsequently destroying their digestive lining and selectively killing dreissenid mussels [36,55]. While current studies discuss the effectiveness of Zequanox® to control zebra and quagga mussels, evidence suggests it could be applied to treat Asian clams as well. Bolam et al. [39] investigated the feeding rates and prey selection of Asian clams and determined that they prefer diatoms in warmer months but switch their diet to preferentially feed on flagellates in the fall [39]. The bacterium Pseudomonas fluorescens in Zequanox® is a flagellate bacterium, and thus this product has potential to be an effective treatment for invasive Asian clams specifically during the fall months. Further testing is required to determine if Asian clams will preferentially filter out Zequanox® bacterium to ingest, what life stages it will treat, and what concentrations are required for the population density and feeding rates of a detected population during different seasons.

3.3.3. Combination of Zequanox®, EarthTec QZ®, potash (KCl)

Treatments can be combined to facilitate a rapid response to early detection of invasive bivalves. Such was the case in Christmas Lake, Minnesota when in 2014, a localized population of zebra mussels was detected near the public boat landing. A combination of Zequanox®, EarthTec QZ®, and potash were used in successional treatments, with Zequanox® used first in September 2014, only 23 days after initial infestation detection. This instance also represents the first time Zequanox® had been employed as a treatment for Zebra mussels in the field. In October and November of the same year, a series of EarthTec QZ® treatments were used in the initial detection area and in the area immediately surrounding it, although no curtain barrier was installed until the second treatment. Finally, in December 2014 and in April and ay of the following year, potash was used to maintain a concentration of 73.5 and 110 ppm K⁺ within the treatment area for 10 days. Although these treatments resulted in no detected surviving Zebra mussels, individuals were found a year later in untreated parts of the lake. While this study represents an immediate response with early success, it also highlights the need for post-treatment monitoring and the limitations of treatments in only a portion of a water body [30]. The use of chemical treatment combinations and the lessons learned from this field study should be applied to treatments of all invasive bivalves, including Asian clams as field studies continue to increase in frequency.

3.3.4. Microencapsulation

Microencapsulation represents a promising technology that could be applied to a variety of active ingredients already approved and used in molluscicides to treat invasive bivalves [35]. Microencapsulation technology encases the control agent in an edible coating to bypass a bivalve’s shell-closing response. Instead of sensing a harsh chemical such as chlorine and closing its shell for 2-3 weeks at a time, the encapsulated active ingredient is ingested quickly during filter feeding and thus is taken up more rapidly than harsh chemicals [32]. As the active ingredient is selectively absorbed by the target species, microencapsulation requires lower concentrations of active ingredients while increasing its toxicity. This allows for more effective treatment while also reducing the residual environmental contamination [35].

BioBullets® are a manufactured lipid walled microparticle that encases various control agents. In a report by Tang and Aldridge [40], two new formulations of BioBullets® with the smallest particle size most similar to filter feeder’s prey were tested on Rangia cuneata or Wedge clams. The SB 1000 model had a particle size of 9.5 ± 0.5µm with a smooth surface and the SB 2000 model had a particle size of 24.6 ± 1.3µm with a crystallized surface. Asian clams have a prey particle size preference of <20-25µm, so both models are likely to be ingested by Asian clams. Despite their small size, SB 2000 had an extended-release rate over 20 hours. A single dose of 2-6mg/L of the active ingredients resulted in 90% mortality within 30 days [40]. While the study does not specify what the active ingredients are in the tested BioBullets®, it does refer to SB 1000 as having a cationic polymer that acts as a surfactant, which is most likely poly-diallyldimethyl ammonium chloride (polyDADMAC) used in previously reported studies [4] while the SB 2000 BioBullets® used an anionic salt, most likely KCl. While both active ingredients are toxic to bivalves, Calazans et al. [35] reported that encapsulated polyDADMAC was 9.3 times more toxic than encapsulated KCl in golden mussels [35]. As the prey particle size is within the preferred range and the various models with differing surface texture could be used according to their seasonal diet preferences, BioBullets® have great potential for use as Asian clam chemical treatments [40].

3.3.5. Essential Oils

There is rising interest in essential oils and their constituents as a safer alternative to pesticides used to treat aquatic gastropods. To determine the immersion lethal toxicity value of various essential oils, researchers immersed adults and egg clusters of freshwater Pomacea canaliculata snails in essential oils for 24 hours followed by a recovery period in dechlorinated tap water. After a 12-hour exposure, 100% mortality was achieved at 156.25µg/ml . However, this review also showed that essential oil constituents were more deadly to aquatic gastropods when ingested through baiting as opposed to diffuse essential oils released into the water column. Specifically, feeding on baits that contained sublethal concentrations of eugenol, a compound found in cinnamon, clove, and bay leaves, the 24- hour lethal concentration of 50% of the sample size (24 h-LC50) ranged between 2.55 and 10.73µg/ml, with the highest toxicity occurring in conjunction with elevated temperatures. Eugenol also reduced fecundity, hatchability, and survival of young Lymnaea acuminata [33]. Although Asian clams are different from gastropods, there is potential to combine essential oil baiting techniques with microencapsulation technology to enable invasive bivalves to filter out and consume the toxic essential oils constituents and maximize their efficacy.

Although the mechanism of toxic action remains unknown, it has been proposed that the various constituents of essential oils interfere with metabolic, physiological, and behavioral functions [33]. Further research is needed to identify the mode of action to determine the most effective formulation and delivery system to reach the target species. Site-specific toxicity testing is also needed to determine the impacts of essential oils on non-target species.

4. Future Directions

5. Conclusions

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