Southeastern Naturalist 607 J.L. Bernatis and G.L. Warren 22001144 SOUTHEASTERN NATURALIST 1V3o(3l.) :1630,7 N–6o1. 83 Effectiveness of a Hand Removal Program for Management of Nonindigenous Apple Snails in an Urban Pond Jennifer L. Bernatis1,* and Gary L. Warren1 Abstract - Introduced applesnails (Ampullariidae: Pomacea) have been responsible for crop and habitat damage in freshwater systems around the world. Two Pomacea species known to damage aquatic vegetation, P. maculata (Island Apple Snail) and P. canaliculata (Channeled Apple Snail), have been introduced into Florida. This investigation was conducted to evaluate efficacy of a hand-removal program for the management of nonindigenous Pomacea in a small (1.62 ha), relatively isolated urban pond. We removed snails and egg masses from the pond by hand at pre-determined time intervals during May 2008–June 2011. We made a total of 107 collections; 21,343 snails and 20,244 egg masses were removed during the study period with >90% of both removed during the first year (20,961 and 18,934, respectively). Snail densities were reduced in the wadeable near-shore habitat from 1–3/m2 to <0.001/m2. The total cost of the project (salary, supplies, travel) was $10,475. At the time of the final collection in year 3, we observed no snails and removed only two egg masses. Four followup assessments September 2011–May 2012 indicated that the hand-removal program was successful and snails had been nearly eradicated from the site. Occasional connections with a population occupying an adjacent drainage ditch could result in a future re-colonization of the pond. Compared with chemical methods, control was achieved with lower monetary cost and less ecological risk. Further evaluations of this method will be necessary to apply it or use it in larger connected ecosystems. Introduction In the last decade, apple snails (Ampullariidae: Pomacea) have received much attention because of their ability to damage crops and vegetated habitats in freshwater systems (Carlsson et al. 2004, Joshi 2001, Yusa and Wada 1999). Pomacea are native to the New World, but only one species, P. paludosa (Say) (Florida Apple Snail), is native to North America. Other Pomacea species are native to South and Central America and have been introduced into North America and Asia (Hayes et al. 2009, Rawlings et al. 2007). In the US, nonindigenous apple snails are established in at least 10 states (Fig. 1; Byers et al. 2013, Rawlings et al. 2007). Florida has more Pomacea species than any other state. These include the native Florida Apple Snail and at least four nonindigenous species: P. canaliculata (Lamarck) (Channeled Apple Snail), P. maculata (Perry) (Island Apple Snail), P. diffusa (Blume) (Spike-topped Apple Snail), and an unknown Pomacea species previously described as P. haustrum (Reeve) (Titan Apple Snail) (Hayes et al. 2009, 2012; Rawlings et al. 2007). As of 2013, Florida had nonindigenous Pomacea populations in at least 29 watersheds and in 38 of the state’s 67 counties (Fig. 2; J.L. Bernatis, unpubl. data). The majority of the locations were inhabited by Island Apple Snail, but two locations were inhabited 1Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Gainesville, FL. Corresponding author - Jennifer.Bernatis@myfwc.com. Manuscript Editor: Nathan Dorn Southeastern Naturalist J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 608 by Channeled Applesnail, which appeared on the IUCN’s 100 of the World’s Worst Invasive Alien Species List (Lowe et al. 2000). Apple snails belonging to the Channeled Apple Snail group (e.g., Giant Applesnail) have been documented as threats to wetland agriculture, especially in the rice paddies of Japan and Southeast Asia and, to a lesser degree, to Colocasia esculenta (L.) Schott (Taro) production in Hawaii (Joshi et al. 2001, Nakamura 2006, Yusa and Wada 1999). The potential for wetland agricultural crop impacts in Florida is low and has yet to be documented. However, the overall potential for adverse impacts in natural aquatic systems may be high. In very large systems with nonindigenous Pomacea populations, such as Lake Okeechobee (189,000 ha), or moderate-sized systems, such as Lake Brantley (117 ha; Seminole County), the impacts are unknown because there is no evidence to date that conclusively demonstrates a cause-and-effect relationship between the presence of nonindigenous applesnails and the loss of vegetation. However, the impacts on aquatic vegetation in small urban ponds (<10 ha) have been qualitatively documented by community residents and government agencies (J.L. Bernatis, unpubl. data). Apple snails are capable of near complete removal of aquatic macrophytes (J.L. Bernatis, pers. observ.). Urban ponds are often community focal points, and hundreds of thousands of dollars have been spent on their restoration. The presence of nonindigenous Pomacea may negate restoration efforts through the rapid consumption of purposely planted aquatic vegetation, resulting in economic loss and ecosystem alteration (J.L. Bernatis, pers. observ.; Carlsson et al. 2004). Various methods (e.g., chemical, biocontrol, mechanical, integrated) have been used in attempts to control the spread and impacts of nonindigenous apple snails, Figure 1. Distribution of established Pomacea spp. populations. Florida (dark grey) has 4 species of nonindigenous Pomacea (P. maculata [Island Apple Snail], P. canaliculata [Channeled Apple Snail], P. diffusa [Spike-topped Apple Snail], and Pomacea sp.) one native species (P. paludosa [Florida Appple Snail]), and one other nonindigenous Ampullariidae (Marisa cornuarietis (L.) [Giant Rams-horn]). Species present in the other states (light grey) vary, see text for distribution references. Southeastern Naturalist 609 J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 each with varying degrees of success and most with a focus on crop protection (Calumpang et al. 1995, Estebenet and Cazzaniga 1990, Halwart et al. 1998, Litsinger and Estano 1993, Wada 2004, Yusa et al. 2006). The St. Johns River Water Management District attempted chemical eradication of nonindigenous apple snails using copper sulfate (CuSO4) in a small portion (14.57 ha) of Newnans Lake (2700 ha, Alachua County, FL). At the conclusion of the treatments, live snails and egg masses remained, and the snail population subsequently spread throughout the lake (J.L. Bernatis, pers. observ.). Several chemical treatments have been tested and are moderately effective, but impacts upon non-target organisms, residual toxins, and economic considerations have led most authors to conclude that other methods such as hand removal, manipulation of water level, and addition of natural predators are preferable (de la Cruz et al. 2000, Litsinger and Estano 1993, Sin 2003). Many aquatic ecosystems in Florida are dominated by native submerged and emergent aquatic vegetation and are at risk to damage by any organism that forages Figure 2. Locations of nonindigenous Pomacea populations throughout Florida as of 2013; diamond = P. canaliculata (Channeled Apple Snail), triangle = P. diffusa (Spiketopped Apple Snail), circle = P. maculata (Island Apple Snail), and × = unidentified Pomacea sp. These are point locations (FWC) and do not exhaustively represent the distribution of the snails in canal and river systems or around the periphery of lakes. Locations just above the state line are in Florida/Georgia shared waters. Southeastern Naturalist J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 610 voraciously on macrophytes. Protecting these systems requires the selection of an adequate control program, which is a difficult task because each aquatic ecosystem is unique; regardless, the overall goal of minimizing economic cost and ecological impacts while maximizing control of the snails is the same. In this paper, we report the results of a 3-year hand-removal program of Channeled Apple Snails and egg masses in an isolated urban retention pond. Maximal effectiveness would be achieved through complete eradication. We considered our control efforts to be successful when the total numbers of snails and egg masses collected or destroyed during a sampling event were ≤1% of the corresponding numbers in the initial collection (i.e., ≥100-fold decrease). Methods We chose a retention pond in a residential neighborhood of southeast Jacksonville, FL, as a site to evaluate the use of hand removal for control of nonindigenous applesnails (Fig. 3). The pond had a surface area of ~1.62 ha and a circumference of 850 m. The perimeter of the pond had a submerged shelf extending approximately 3.5 m from the shore; maximum depth of the shelf was 1.7 m. Beyond the shelf, the pond reached a maximum depth of 8.2 m. The area to the north and west of the pond was ephemeral swamp and Pinus (pine) forest that drained into Julington Creek (approximately 2.5 km from the pond) and ultimately to the St. Johns River (approximately 12.5 km from the pond). The area to the east and south of the pond was primarily residential and commercial development. We conducted 5 pilot surveys of this Channeled Apple Snail population during 2006–2008. We waded on the shelf and counted all the snails we observed and estimated density from the total number of snails and the approximate area of the shelf. During this period, snail density on the shelf ranged from 1–3 snails/m2. Vegetation in the pond included Hydrilla verticillata (L.f.) Royle (Water-thyme), Hydrocotyle sp. (marsh-pennywort), Ceratophyllum demersum L. (Common Hornwort), and Sagittaria sp. (arrowhead). No other apple snail species (i.e., Florida Applesnail) were present, and the only other gastropods were Planorbella duryi (Weatherby) (Seminole Rams-horn), Planorbella scalaris (Jay) (Mesa Rams-horn), and Physella cubensis (Pheiffer) (Carib Physa). In May 2008, we initiated a 3-y study to evaluate the efficacy of hand removal as a method for controlling nonindigenous apple snails in a small pond. One day per week a Florida Fish and Wildlife Conservation Commission (FWC) field technician waded the perimeter of the pond along the shelf and hand-removed all observed Channeled Apple Snails (e.g., egg masses, and hatchlings through adults) within reach. Based on the actual wadeable area of the lake, we collected snails from ~0.276 ha of surface area. The number of snails and eggs decreased dramatically as the project progressed and, in December 2008, we reduced collection frequency to once every two weeks in year 2 and then to once every 3 weeks in year 3. We killed collected snails by freezing at -12 °C for at least 2 weeks and then we buried them; egg masses were scraped from the substrate and crushed at the pond. The monetary costs of the removal included supplies (i.e., bags for snails and eggs), technician Southeastern Naturalist 611 J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 salary (i.e., time spent traveling to/from site and collecting), and gas (calculated as a mileage rate). In April of 2010, two scuba divers (Karst Environmental Services Inc., High Springs, FL) conducted a benthic transect survey of the retention pond with the purpose of determining the presence and depth distribution of Channeled Apple Figure 3. Representation of primary study site in Duval County, FL. The pond has an 850- m perimeter and is approximately 1.62 ha in total area. The maximum depth is 8.2 m. The numbered lines indicate the transects of the dive survey. The drainage-creek study area is indicated by the shaded area. Dashed lines are drain culverts connecting areas with snail populations. The No Access Areas are fenced off electric company substation facilities. Channeled Apple Snails were present in the pond of the smaller fenced off area and connected to the ditch via a cement culvert. Southeastern Naturalist J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 612 Snails in the pond. Divers surveyed 8 transects across the pond perpendicular to the long side and evenly dividing the pond (Fig. 3). Visibility was sufficient for the divers to survey 3–3.5 m on both sides of the transect line, for a 6–7-m-wide sweep of each line per diver. The average depth of transects 1–6 was 6.4 m, and the average depth of transects 7 and 8 was 4.6 m and 3.0 m, respectively. Overall, the divers searched approximately one-third of the total bottom-surface area. In July 2009, Channeled Apple Snail was found in an ephemeral drainage ditch located adjacent to the primary study pond (Fig. 3). The ditch was connected to the pond by culverts and was considered a source for pond re-colonization by Channeled Apple Snails. Subsequently, snails and egg masses were removed from the ditch on the same schedule as the main pond, but were not quantified. After the discovery of the ditch population, all ponds within a 3-km radius of the primary study pond were surveyed quarterly for snails and egg masses. Because of this discovery and our goal to completely remove snails from this location, we conducted 4 post-study surveys during June 2011–May 2012 to determine whether snails were repopulating the pond. We used the study protocols (e.g., wading the shelf) to conduct these surveys. Results During the 3-y study, we made a total of 107 collections. Total time spent collecting snails and egg masses was 245 person-hours. The total numbers of snails and egg masses removed from the pond were 21,343 and 20,244, respectively, with >90% of both groups removed in the first year (Fig. 4). The overall cost of the project was $10,475, and covered 29.5 ha ($354.44/ha or just under $100 per field-visit). On the first collection day in 2008, 4 people collected 2948 snails and 1737 egg masses. Throughout the first year (29 May 2008–26 May 2009), 49 collections were made and 20,961 snails (Fig. 4A) and 18,934 egg masses (Fig. 4B) were removed. Three collection dates were missed due to inclement weather (e.g., tropical storms). The average time spent per collection in year 1 was 3.28 person hours. During year 2 (3 June 2009–11 May 2010), the number of snails and eggs collected was markedly decreased from year 1. The number of snails removed, n = 327, decreased by 98.5% from year 1 (Fig. 4A). Likewise, the number of egg masses removed, n = 1249, was a 93.5% decrease from year one (Fig. 4B). On the first collection day, the number of snails and egg masses removed, n = 30 and n = 48, respectively, was 99% and 97.3%,respectively, less than year 1. During this collection year, all 38 scheduled collections were made, with an average collection time of 1.68 person hours. During year 3 (27 May 2010–1 June 2011), we removed a total of 55 snails (Fig. 4A) and 61 egg masses (Fig. 4B); both were less than 1% of the first-year totals. On the day of the final collection, no snails were observed, and two egg masses were removed. We visited the site on 20 dates during the final year, and the average time per collection was 1.0 person hour. Southeastern Naturalist 613 J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 Results of the dive survey conducted in April of year 2 indicated that snails were either absent from the pond or present in such low numbers that they were not detectable. During the dive survey, applesnail shell material was retrieved at all depths on all transects, but divers retrieved no live snails. Three follow-up visits confirmed the success (e.g., no live snails) of the handremoval method. On the first of these visits, in early September 2011, only one old and damaged egg mass was observed on a drain culvert, and no snails were found. Figure 4. The total number of Channeled AppleSnails (A) and egg masses (B) collected each month from an urban pond in Florida. Main graph represents entire 3-year removal period, and the insets re-scale years 2 and 3. * indicates that no collections were made in that month. The number of collections varied from 1–4 per month (see details in Methods). Southeastern Naturalist J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 614 No egg masses or snails were observed in November 2011 or February 2012. However, in May 2012, after a tropical storm, 2 snails and 6 small egg masses (less than 20 eggs) were observed in the main pond, and numerous snails were observed in the adjacent ditch. Based on results from the last 5 collections, the snail density of the nearshore habitat was less than 0.001/m2. As of June 2012, no other ponds or creeks within a 3-km radius of the main pond and drainage ditch contained Channeled Apple Snail. Discussion Nonindigenous Pomacea are abundant in many of Florida’s aquatic ecosystems and are spreading throughout the southeastern US (Byers et al. 2013). The goal of this study was to evaluate the effectiveness of hand removal to manage Channeled Apple Snail in a small urban pond. The results of this removal study provide a framework for considering control options in other infested systems. Because nonindigenous Pomacea establish in a variety of large and small systems, the system-specific effects, logistics, and available financial resources should be considered when tailoring a control plan. The results of this study demonstrate that regular removal of snails and eggs eventually controlled (e.g., negligible Channeled Apple Snail presence) the Channeled Apple Snail population. The greatest impact was made in year 1, but continued removal helped ensure that snails initially missed during collection efforts were eventually removed from the system. The post-study follow-up surveys further demonstrated that we achieved Channeled Apple Snail control in the focal pond and that our efforts resulted in complete local eradication. Any reproductive-aged female apple snail that has mated is a potential re-colonization threat because females store sperm for months and produce at least one egg mass per week (J.L. Bernatis, unpubl. data; Estebenet and Cazzaniga 1992). Therefore, the reappearance of a few snails in the primary study pond one year after the conclusion of the study was noteworthy. There are a number of explanations for their presence. First, the drainage ditch behind the pond continued to harbor snails for the duration of the study, and the rains of May 2012, which exceeded 40 cm, reconnected the ditch and the pond through a culvert. Unfortunately, we were not able to remove snails from those habitats. Second, it is beleived that the apple snails were originally introduced to the pond by human residents to control vegetation; therefore, it is possible that a second introduction may have occurred. Finally, it is possible we missed an egg mass or snails on the last visit in 2011. Unfortunately, egg masses and snails had also been observed in connected storm-sewer drains that were out of collection reach (e.g., underground). Because the snails did not reappear until after the May 2012 rains, we suspect that they re-invaded from the ditch. This observation reinforces the need to consider adjacent locations when conducting removals. Determining the best method of control is system-dependent, and in some situations control programs may not be necessary. It is clear from studies in Asia that small wetland and pond ecosystems can dramatically change following invasions of Pomacea (Carlsson et al. 2004, Fang et al. 2009), but whether Pomacea Southeastern Naturalist 615 J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 will attain similar population sizes and ecological effects in large lake and river systems is not clear. Researchers are just beginning to study the distribution and density of nonindigenous apple snails, but one recent study suggests that aquatic predators (fish and/or crayfish) might limit Channeled Apple Snail density in some sections of an urban river in Japan (Yamanishi et al. 2012). It is important to identify efficient predator species (Carlsson et al. 2009), but invaded locations with existing infestations, like the urban pond in this study, clearly do not support efficient predators. Ecologically, in contrast to chemical methods, the impacts of hand removal were negligible (J.L. Bernatis, pers. observ.). Some studies using chemical applications have succeeded in reducing snail densities to levels that were considered low enough to minimize damage, but success has come with high mortality of non-target organisms (Calumpang et al. 1995, de la Cruz et al. 2000, Maini and Morallo-Rejesus 1993). Chemical treatment to control apple snails has proven most effective when the chemical directly contacts snails (de la Cruz and Joshi 2001). In many lake and river systems, water visibility and flow prevent direct contact application. Also, Pomacea spp. have strong chemosensory abilities coupled with survival mechanisms that may allow them to outlast the toxin (Aizaki and Yusa 2009); molluscicides generally have a half-life of several days, but nonindigneous adult Pomacea can survive more than a year without feeding or emerging from their shell (J.L. Bernatis, unpubl. data). In contrast, hand removal guarantees removal of individual snails from the system, prevents general contamination of the water, and has no known negative impacts on non-target organisms such as insects, fish, or plants (Newman and Clements 2008) . Submersion of egg clutches may reduce nonindigenous apple snail populations. Horn et al. (2008) and Pizani et al. (2005) suggested that submersion of egg clutches causes mortality of developing snails. Submersion can result from intentional or natural water-level rises or from herbicide treatment of emergent aquatic plants. Chemically treated plant stems usually decay and bend into the water within 2–3 weeks after treatment, thus submersing any attached egg clutches. Nonindigenous apple snail eggs hatch 7–14 d after being laid, whereas native Florida Apple Snail eggs require at least 18 d to hatch; therefore, the potential for impacting recruitment increases as the time of submersion increases (J.L. Bernatis, pers. observ.; Hanning 1979; Naylor 1996). Furthermore, the effects of direct contact with herbicides and surfactants have not been extensively studied, but there is evidence that some chemicals (e.g., morpholine) reduce hatch rates (Wu et al. 2005). Cost is a consideration in management strategies. In this study, exclusive of the dive survey, the cost of manual removal was $354.44/ha, making it 35% less than the cost of the 3 copper sulfate applications carried out on Newnans Lake ($540.34/ha, exclusive of travel, salaries, and support equipment; J.L. Bernatis, pers. observ.). Although the cost of this program was relatively low, any cost may be too great for some municipalities or homeowners’ associations, and so hand removal could be implemented with even less cost through organized volunteer events. Southeastern Naturalist J.L. Bernatis and G.L. Warren 2014 Vol. 13, No. 3 616 This study was designed to evaluate a 3-y hand-removal program in an urban pond. A substantial impact was made by the end of the first year, and although we cannot be sure all snails were removed, we concluded that control of the population was maintained for the last year and a half of the study. The removal program was successful, in part, because we were able to access to the entire pond shoreline. Removal programs in systems with limited access to emergent vegetation (e.g., egg-laying substrate) or large portions of the shoreline may not experience the same level of success. Furthermore, success in systems that are permanently connected to other snail habitats will likely be inhibited. Assuming adequate access and personnel, the actual size of the system may not be a factor, but control may take longer to achieve in larger systems, and their treatment may require adjusted protocols. Increasing the frequency of collections during peak reproductive periods (i.e., summer months) may increase success, particularly in systems that harbor snails in deeper water. Increased collection frequency may lead to a more rapid removal of the snails and egg masses deposited by snails not visible on the weekly visit. Although the hand-removal method is not appropriate for all systems, in small, controlled water bodies the method effectively removed most snails. The handremoval method allows for constant monitoring, is adaptable based on the number of egg masses and snails present, and the results are quantifiable. Additional benefits could be gained from a weekly removal program, such as observations on the general health of the system (e.g., algal blooms, changes in vegetation). Regardless, management of invasive apple snails must be tailored to each system to avoid fiscal inefficiency and unnecessary ecological impacts. Acknowledgments The authors would like to thank Dr. Timothy Collins at Florida International University for genetic confirmation of the snail population at the study site. 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