Philip C. Darby

Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

ABSTRACT Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.

THE EFFECTS OF WETLAND HABITAT STRUCTURE ON FLORIDA APPLE SNAIL DENSITY

Wetlands often support a variety of juxtaposed habitat patches (e.g., grass-, shrub- or tree-dominated) differentially suited to support the inhabiting fauna. The proportion of available habitat types has been affected by human activity and consequently has contributed to degrading habitat quality for some species. The Florida apple snail (Pomacea paludosa) has drawn attention as a critical prey item for wetlands wildlife and as an indicator of wetlands restoration success in peninsular Florida, USA. An apparent contradiction has evolved wherein this species appears intolerant of drying events, but these disturbances may be necessary to maintain suitable habitat structure for apple snails. We recently reported that assertions regarding intolerance to dry downs in this species were inaccurate. Here, we compared snail density in habitats with (wet prairie) and without (slough) emergent macrophytes, as well as evaluating the effects of structural attributes within the broad wet prairie habitat type. Snail densities were greater in prairies relative to sloughs (χ2= 12.90, df= 1, P=0.0003), often by a factor of two to three. Within wet prairie habitats, we found greater snail densities in Panicum hemitomon as compared to Eleocharis cellulosa (χ2=31.45, df=1, P=0.0001). Significantly fewer snails were found in dense E. cellulosa as compared to habitats with lower stem density (χ2= 10.73, df=l, P=0.011). Our results indicate that wet prairie habitat supports greater snail densities than Nymphaea- dominated slough. Our results have implications for wetlands water management in that continuous inundation has been shown to convert wet prairie to slough habitat, and we suggest this should be avoided in support of apple snails and their predators.

DRY DOWN IMPACTS ON APPLE SNAIL (POMACEA PALUDOSA) DEMOGRAPHY: IMPLICATIONS FOR WETLAND WATER MANAGEMENT

Florida apple snails (Pomacea paludosa Say) are prey for several wetland-dependent predators, most notably for the endangered Florida snail kite (Rostrhamus sociabilis Vieillot). Management concerns for kites have been raised regarding the impacts of wetland dry downs on snails, but little data exists to validate these concerns. We simulated drying events in experimental tanks, where we observed that snail survival patterns, regardless of hydrology, were driven by a post-reproductive die off. In contrast to earlier reports of little to no dry down tolerance, we found that 70% of pre-reproductive adult-sized snails survived a 12-week dry down. Smaller size classes of snails exhibited significantly lower survival rates (< 50% after eight weeks dry). Field surveys showed that 77% of egg production occurs in April–June. Our hydrologic analyses of six peninsular Florida wetlands showed that most dry downs overlapped a portion of the peak snail breeding season, and 70% of dry downs were ≤ 12 weeks in duration. Dry down timing can affect recruitment by truncating annual egg production and stranding juveniles. Dry down survival rates and seasonal patterns of egg cluster production helped define a range of hydrologic conditions that support robust apple snail populations, and illustrate why multiple characteristics of dry down events should be considered in developing target hydrologic regimes for wetland fauna.

Foraging Patch Selection by Snail Kites in Response to Vegetation Structure and Prey Abundance and Availability

Abstract The role of food abundance and vegetation structure in selection of foraging habitat by the Snail Kite (Rostrhamus sociabilis) was explored. Selection of available foraging patches of either dense or sparse habitat structure within two prairie habitat types used extensively by foraging kites, Eleocharis flats and Panicum flats were examined. Estimated Apple Snail (Pomacea paludosa) densities on our study site ranged from 0.33 to 1.58 per m2. Vegetation structure (sparse vs. dense) of the habitat type had a greater influence on where prey was captured than did site, the dominant emergent vegetation, or prey abundance. These results are consistent with previous suggestions that dense vegetation may obscure prey and limit or preclude use of densely vegetated habitats by foraging kites. This may be true, even when prey is in relatively high abundance, and may indicate the difference between prey abundance and availability. Most water management recommendations related to the Snail Kite call for prolonged inundation, based on an explicit assumption that this results in increased Apple Snail abundance. Even when directed at a single species such as the Snail Kite, water management may need to be considered in a more holistic framework that considers factors that influence the resulting vegetation communities, rather than just production of Apple Snails.

Florida apple snail (Pomacea paludosa Say) responses to lake habitat restoration activity

Water-level drawdown has long been recognized as an effective approach to enhance habitat conditions for aquatic fauna in lakes and impoundments. Although targeted species such as sport fish may benefit, increasingly there are concerns over non-target species. We assessed the impacts of a drawdown of Lake Kissimmee on Florida apple snails. Prior to the drawdown, we found apple snails at significantly higher densities in sites dominated by sandy substrates and emergent macrophytes; no snails were found in sites with deep layers of unconsolidated organic material and dominated by Nuphar luteum. Following the drawdown, some of the sites containing this unconsolidated organic material were also scraped with heavy equipment (e. g., bulldozers) to remove the organic layer. We monitored the response of 31 snails from one site, most of which were stranded in the dry littoral zone during the 1995-1996 drawdown. Mortality rates of stranded snails were high due to the dry conditions of the littoral zone, but also indirectly due to increased vulnerability to predation by several avian species. The survival data was corroborated by the 1996 and 1997 funnel trap data wherein our catch declined by 80% from 1995 (pre-drawdown) levels. The proportion of juveniles also declined significantly, indicating an impact on recruitment. Snail abundance did increase, albeit marginally, in some sites, indicating potential benefits of drawdown and organic substrate removal in some types of littoral zone habitats. However, the timing of drawdown events appears critical, as evident in poor recruitment and relatively low abundance following completion of lake restoration activity. In order to avoid substantial losses to non-target species such as apple snails, we suggest that natural resource managers give greater consideration to the potential negative impacts of deviating from the natural hydrologic regime in terms of timing, duration, and frequency.

The Effects of Prey Density on Capture Times and Foraging Success of Course-Hunting Adult Snail Kites

Abstract. Foraging-patch selection may be influenced by prey density, prey availability, and the energetic costs associated with searching for and capturing prey. Although prey density influences profitability, prey availability may be influenced by habitat and environmental characteristics. We made in situ observations of Snail Kites (Rostrhamus sociabilis) foraging on their exclusive prey, apple snails (Pomacea paludosa), in selected habitats and environmental conditions. We measured the time to capture a snail at 10 sites on Florida lakes (two sites sampled twice over different years for 12 data points total) and five sites in wetlands of the Everglades. Capture times had an inverse asymptotic relationship to snail density. As snail density increased from ∼0.1 to 0.2m-2, capture times declined from ∼600 to 200 sec; capture times leveled off to ∼75 sec between 0.4 and 1.4 snails m-2. Densities of emergent plant stems and water depths, which may influence capture times, were controlled for by site selection; analyses verified these factors had no effects. Snail Kites were significantly more likely to abandon a foraging bout if snail density was <0.2m-2. We interpret the results in the context of foraging for inconspicuous prey. Our data and other reports indicate ∼0.1–0.2 snails m-2 as an approximate threshold below which flight costs increase dramatically and fewer kites tend to forage. Our observations contribute to the limited information available on what constitutes prey density sufficient for the Snail Kite, and we discuss associated conservation implications for this endangered dietary specialist.

Gender-Based Differences in Florida Apple Snail (Pomacea paludosa) Movements

ABSTRACT Gastropod movements have been studied in the context of habitat selection, finding food and mates, and avoiding predation. Many of these studies were conducted in the laboratory, where constraints on spatial scale influence behavior. We conducted a field study of Florida apple snail (Pomacea paludosa) movements using telemetry. We hypothesized that Florida apple snail movements were driven by reproductive activity, and that gender differences would be evident. We documented male and female directions and distances traveled. We also conducted a trapping study that included conspecific bait to test if the presence of females attracted more males as measured by M:F ratios in traps. The greatest distances traveled were by males, and males were more likely to maintain a consistent bearing compared to females. Male distances peaked in what typically corresponds to peak breeding season. M:F ratios in traps were positively associated with reproductive activity in the study population as measured by egg cluster counts. Conspecific bait had no effect on the number of males or females captured. However, if a female crawled into the trap, we observed greater numbers of males compared to those with no trapped females. Males may have tracked females to increase mating encounters, following slime trails, as seen in other aquatic (including other Pomacea) snails. The capacity for mate finding has implications for reproductive success in the relatively low density populations often seen for Pomacea paludosa.

Quantifying edge effects on apple snails (Pomacea paludosa) and their eggs at the junction of two wetland habitat types

Plant community structure and the creation of ecotones from the juxtaposition of distinct habitats influence gastropod distribution, abundance and species diversity. However, the influence of edge effects associated with ecotones may be influenced by scale and sampling issues. In Florida’s Everglades, a common ecotone exists between dense sawgrass (Cladium jamaicense) and less-dense wet prairie habitats dominated by lower profile sedges and grasses. Previous studies indicate that Florida apple snails (Pomacea paludosa) concentrate their eggs along ecotones and that they appear to favour sawgrass for oviposition. However, snail densities along the ecotone have not been reported and total egg production at the landscape level has not been considered. Egg-cluster densities were greater along the sawgrass ecotone; however, total egg production in wet prairie (egg density multiplied by total area) was greater than in the sawgrass ecotone. Greater eggcluster density along the sawgrass ecotone may be a result of increased stem encounter rates by female snails. We found that snail densities were not significantly different between sawgrass ecotone and adjacent prairie habitats in the Everglades. The results of our study, combined with observations from previous reports, indicate that the importance of edge effects on apple snails depends on the spatial scale and the particular landscape being considered. Changes in plant community structure resulting from changes in hydrology caused by wetland restoration may impact recruitment of apple snails and, ultimately, those species that prey upon them.