Early-stage invasive apple snails exhibit elevated ROS levels and enhanced oxidative stress defenses compared to non-invasive species

Since 2009 the apple snail Pomacea maculata has become a new invader of Oryza sativa (rice) fields and wetlands in Europe, only invading the Ebro Delta (north‐eastern Spain) thus far. It is considered a highly invasive and damaging species, resulting in large economic losses worldwide. Despite the severe impact of the invasive apple snail on both cultivated and natural wetlands, it has become an abundant potential resource for native avian predators. In this study, stable isotope analysis was used to assess the consumption of the apple snail by the glossy ibis Plegadis falcinellus in the Ebro Delta. The results indicate the importance of the apple snail in the diet of this native bird. In particular, isotopic results indicated that apple snails and freshwater coleopterans were the main prey in the diet of glossy ibis chicks, accounting for 26–40% of their diet. Thus, this native bird species could potentially help in the biological control of this invasive snail, but is not expected to eradicate it. Although the spread of this pest in rice fields and wetlands is not desirable, we predict that the apple snail will follow a path similar to other invasive species, such as the red swamp crayfish Procambarus clarkii, in establishing itself as part of the wetland food web.

BackgroundGut microbiota play a critical role in nutrition absorption and environmental adaptation and can affect the biological characteristics of host animals. The invasive golden apple snail (Pomacea canaliculata) and native Chinese mud snail (Cipangopaludina chinensis) are two sympatric freshwater snails with similar ecological niche in southern China. However, gut microbiota comparison of interspecies remains unclear. Comparing the difference of gut microbiota between the invasive snail P. canaliculata and native snail C. chinensis could provide new insight into the invasion mechanism of P.canaliculata at the microbial level.MethodsGut samples from 20 golden apple snails and 20 Chinese mud snails from wild freshwater habitats were collected and isolated. The 16S rRNA gene V3–V4 region of the gut microbiota was analyzed using high throughput Illumina sequencing.ResultsThe gut microbiota dominantly composed of Proteobacteria, Bacteroidetes, Firmicutes and Epsilonbacteraeota at phylum level in golden apple snail. Only Proteobacteria was the dominant phylum in Chinese mud snail. Alpha diversity analysis (Shannon and Simpson indices) showed there were no significant differences in gut microbial diversity, but relative abundances of the two groups differed significantly (P < 0.05). Beta diversity analysis (Bray Curtis and weighted UniFrac distance) showed marked differences in the gut microbiota structure (P < 0.05). Unique or high abundance microbial taxa were more abundant in the invasive snail compared to the native form. Functional prediction analysis indicated that the relative abundances of functions differed significantly regarding cofactor prosthetic group electron carrier and vitamin biosynthesis, amino acid biosynthesis, and nucleoside and nucleotide biosynthesis (P < 0.05). These results suggest an enhanced potential to adapt to new habitats in the invasive snail.

Exotic invaders routinely move faster than scientific publication processes. Lacking aerial dispersal stages, snails generally match descriptions of slow colonizers. However, reminiscent of the pace with which zebra mussels gained notoriety, a growing sense of urgency has emerged from management communities regarding established populations of exotic, invasive island apple snails (Pomacea insularum). Recently separated by mitochondrial markers as a related, yet distinct, species, P. insularum sits poised to follow along the invasive trajectory of its better known relative, the golden apple snail (P. canaliculata). Literature studies examining mechanisms that promote invasiveness suggest family history of invasion serves as a sufficient enough warning sign. Furthermore, a paucity of natural history information exists on this larger (max wet weight 166-g), more fecund (2000 eggs as average clutch size) aquatic plant consumer. Without insights into basic life history, actions within management agencies often stall. In just the past five years, multiple introductions gave rise to established reproductive populations across the entire Gulf Coast, from Texas to Florida and even northward to South Carolina. Using a combination of empirical results from multiple experiments and recently compiled insights from researchers studying invasive apple snails (encapsulated as a blog: http://snailbusters.wordpress.com/), we explore three questions. First, what patterns in life history emerge for P. insularum? Second, what natural history aspects appear missing? And third, how can dissemination of new findings shape future studies? Synthesis of experiments and observations from Texas provide compelling (i.e. statistically significant) evidence that P. insularum preferentially chooses to deposit clutches on emergent plants. Snails favor plants with strong circular stems, particularly wild taro (Colocasia esculenta). Unfortunately, easy to measure clutch characteristics (e.g. length, width, depth, volume) fail to predict hatching success. Female P. insularum snails tend to oviposit clutches substantially higher on plant stems than smaller female P. canaliculata. Permanent inundation of newly laid clutches completely prevents hatching, although the impact of water stress on clutch hatching efficiency varies with stress intensity and frequency. Complimentary research also notes differences depending in clutch developmental stage. Among managers and researchers, agreement clearly exists that the egg stage represents our best chance at slowing down the invasion. Relatively few studies focus on interactions (i.e. competition, predation) with native organisms. In conclusion, because clear time-pressure exists to protect native biodiversity, rise in popularity of non-traditional formats (i.e. blogs) to speed research along and increase networking has started in the case of invasive apple snails.

Background/Question/Methods Exotic invaders routinely move faster than scientific publication processes. Lacking aerial dispersal stages, snails generally match descriptions of slow colonizers. However, reminiscent of the pace with which zebra mussels gained notoriety, a growing sense of urgency has emerged from management communities regarding established populations of exotic, invasive island apple snails (Pomacea insularum). Recently separated by mitochondrial markers as a related, yet distinct, species, P. insularum sits poised to follow along the invasive trajectory of its better known relative, the golden apple snail (P. canaliculata). Literature studies examining mechanisms that promote invasiveness suggest family history of invasion serves as a sufficient enough warning sign. Furthermore, a paucity of natural history information exists on this larger (max wet weight 166-g), more fecund (2000 eggs as average clutch size) aquatic plant consumer. Without insights into basic life history, actions within management agencies often stall. In just the past five years, multiple introductions gave rise to established reproductive populations across the entire Gulf Coast, from Texas to Florida and even northward to South Carolina. Using a combination of empirical results from multiple experiments and recently compiled insights from researchers studying invasive apple snails (encapsulated as a blog: http://snailbusters.wordpress.com/), we explore three questions. First, what patterns in life history emerge for P. insularum? Second, what natural history aspects appear missing? And third, how can dissemination of new findings shape future studies? Results/Conclusions Synthesis of experiments and observations from Texas provide compelling (i.e. statistically significant) evidence that P. insularum preferentially chooses to deposit clutches on emergent plants. Snails favor plants with strong circular stems, particularly wild taro (Colocasia esculenta). Unfortunately, easy to measure clutch characteristics (e.g. length, width, depth, volume) fail to predict hatching success. Female P. insularum snails tend to oviposit clutches substantially higher on plant stems than smaller female P. canaliculata. Permanent inundation of newly laid clutches completely prevents hatching, although the impact of water stress on clutch hatching efficiency varies with stress intensity and frequency. Complimentary research also notes differences depending in clutch developmental stage. Among managers and researchers, agreement clearly exists that the egg stage represents our best chance at slowing down the invasion. Relatively few studies focus on interactions (i.e. competition, predation) with native organisms. In conclusion, because clear time-pressure exists to protect native biodiversity, rise in popularity of non-traditional formats (i.e. blogs) to speed research along and increase networking has started in the case of invasive apple snails.

Invasive snails alter multiple ecosystem functions in subtropical wetlands

Invasive apple snails with their core microbes are underestimated hotspots for disseminating antibiotic resistance genes and virulence factors in aquatic habitats.

The occurrence of the invasive apple snail Pomacea canaliculata in Indonesia was first reported in 1984. The species was introduced as an ornamental aquarium pet. Since then, people have begun to culture the snail in ponds usually adjacent to rice fields. When it was realized that the species multiplied rapidly and was a serious pest, this invasive apple snail had already spread widely. There are many cultural methods of controlling and preventing its distribution, but none are effective in keeping them at non-damaging levels. We mapped the distribution of P. canaliculata in Indonesia from the MZB’s collections as well as literature references and found that the snail invaded almost all large islands, such as Sumatra, Java, Kalimantan, Sulawesi, Maluku, and West Papua. We also studied the impact of P. canaliculata on the native apple snails P. ampullacea, P. scutata, and P. virescens in Lake Rawa Pening (a popular tourism destination) as a case study. The results showed that two species of Pila already disappeared from Lake Rawa Pening. Only P. scutata occurs still in the region and was found alive usually in shallow water and rice fields surrounding the lake. To resolve the problem we recommend that cleaning the lake periodically from the invasive aquatic weed Eichhornia crassipes (known to locals as “eceng gondok”) by a private company and harvesting the weeds for the local small craft industry by the local fishermen could be an alternative measure to reduce the population of the P. canaliculata, as well as collecting P. canaliculata for local food or for feeding ducks. Rearranging the number of fish-pens “karamba” and their location in the lake could be seen as an alternative way also for reducing the population of P. canaliculata, since the snails lay their egg masses on the bamboo stakes of “karamba.” Such rearrangement could make the landscape more attractive for tourism.

ABSTRACTThis study investigated the feasibility of using an invasive snail, Pomacea canaliculata, as a food source and water purifier for the commercial breeding of the loach Misgurnus anguillicaudatus. The predatory potential of M. anguillicaudatus (3.5–5.5 g) against hatchling snails was evaluated in aquaria and simulated paddy fields. Some hatchling snails left the water to avoid being preyed upon by the loaches, and approximately 10 hatchlings died per day in the presence of five loaches in aquaria, whereas a weaker snail control effect was observed in the simulated paddy fields. The growth of rice seedlings (Oryza sativa) was not reduced by the presence of hatchling snails alone, but the shoot biomass of seedlings coexisting with snails was promoted after introducing the loaches. Additionally, the presence of P. canaliculata adults improved the aquatic environment in the short term for loach breeding by decreasing the turbidity of the water. Importantly, M. anguillicaudatus (12–18 g) mortality decreased and its weight increased in the presence of adult snails.

The golden apple snail (Pomacea canaliculata), a native of freshwater wetlands of South America, has invaded many Asian countries and grazed heavily in agricultural and wild areas. Common carp (Cyprinus carpio) has been proposed as a biological control agent against this snail, but little is known about its impact on non-target aquatic plants and animals. In a 8-week enclosure experiment, we quantified the impact of common carp on three species of aquatic macrophytes and nine species of snails, including the apple snail, in a shallow pond. The results showed that the apple snail or carp alone significantly reduced the plant biomass, although the apple snail had a stronger overall herbivorous effect than the carp. The carp completely removed juvenile apple snails, but had only a weak predatory effect on larger apple snails and no effect on the adults’ oviposition frequency. Furthermore, the carp significantly reduced the populations of most species of other snails that occurred naturally in the pond. Our results thus indicate that common carp can be an effective biological control agent against the invasive apple snail, but caution should be taken about its potential to reduce wetland floral and faunal diversity.

Few studies have tested for the potential of invasive species, particularly pests, to contribute to ecosystem services. The apple snail Pomacea canaliculata is invasive in many countries around the globe. They are best known as pests of rice and great efforts are made by farmers to control the snails. However, apple snails might also act as decomposers of organic litter, and it was hypothesised that they might enhance the decomposition of rice straw. To test the ability of apple snails to feed on rice straw, choice and no choice feeding experiments were conducted offering rice straw to P. canaliculata for 2 weeks. As mature rice plants are not consumed by apple snails, the straw was incubated in water for 5 days and in water with a mixture of microorganisms for 25, 50 and 75 days prior to the feeding experiments. Rice straw of all treatments was consumed by snails without preference (11.6% more weight loss on average compared to controls in which snails had no access). In another experiment, snails were fed on rice straw for 6 weeks; body mass of snails was measured weekly. In treatments where access to straw was not restricted, all snails survived and body mass remained constant, whereas if access was restricted, snails lost body mass slightly. It was concluded that rice straw served as an alternative food for apple snails. Invasive apple snails spared in times when rice plants are not vulnerable could accelerate nutrient release from rice straw providing a benefit for farmers.

The high-risk invasive apple snail Pomacea canaliculata has greatly threatened the agriculture, ecosystem integrity and public health. In order to provide scientific evidence for effective prevention and control of P. canaliculata, a most suitable ecological niche model was selected to predict the potential suitable distribution areas of P. canaliculata in China. Based on 377 reported occurrence points and 19 bioclimatic variables, four ecological niche models, MaxEnt, GARP, BIOCLIM, and DOMAIN, the potential geographic suitable distribution areas were predicted for the invasive snail. Then, the results of different models were analyzed and compared with two statistical criteria, the area under the Receiver Operating Characteristic curve (AUC) and Kappa value. The results showed that all of the four ecological niche models could simulate the snail's distributions very well. More specifically, the MaxEnt model outperformed the others in all aspects of predicting the snail's potential distribution (AUC=0.955±0.004, Kappa=0.845±0.017), followed by GARP and DOMAIN. Although BIOCLIM offered the lowest prediction accuracy, its AUC was 0.898±0.017 and its Kappa value was 0.771±0.025. Based on the MaxEnt model, the prediction results showed that the potential suitable distribution areas of P. canaliculata were mainly located in the south of 30° N in China, but there was some regions spreading over the north of 30° N. The potential areas accounted for 13.2% of the national land in area. Notably, Guangdong, Guangxi, Hunan, Chongqing, Zhejiang and the coastal areas of Fujian were potentially high-risk areas. In conclusion, this study would be an important reference for the prevention and control of the invasive apple snail P. canaliculata and it also would be an example of predicting the potential distribution of aquatic alien species on large scale.

Genome-wide identification and characterization of the HSP gene superfamily in apple snails (Gastropoda: Ampullariidae) and expression analysis under temperature stress

Invasive apple snails adversely impact the ecological function of non-native habitats, resulting in eutrophication as well as reduced biodiversity, which diminishes ecosystem goods and services, thereby [negatively] impacting human well-being. The onus here is to define the diet of an invasive apple snail (Pomacea canaliculata) in native (Maldonado, Uruguay) versus non-native habitats (Hangzhou, China, and Oahu, HI, USA). Diets for apple snails, in five sites, within both native and non-native habitats were defined via SIAR (Stable Isotope Analysis in R) with δ13C and δ15N stable isotope data collected therein. SIAR models indicate P. canaliculata shift diet from generalist (where myriad plant species comprise relatively small proportions of overall diet) to a specialist diet (where plants species constitute much larger proportions of said diet). What may be more telling is that in (anthropogenically disturbed) portions of the native habitat, and progressively more so in non-native habitats, invasive apple snail diets are increasingly composed of aquatic plants. The inherent and pronounced dietary differences amongst pristine and anthropogenically disturbed native habitats, as well as non-native habitats, provide a mechanism that may elucidate the variable ecological impacts of invasive apple snails within native and non-native habitats.

Impact of invasive apple snails on the functioning and services of natural and managed wetlands

Apple snails, in the genus Pomacea, have gained considerable notoriety for their impact on invaded habitats. Louisiana is currently under invasion by Pomacea maculata, which represents a potential threat to the state's valuable plants and cash crops. Insight into the physiology of the invasive snail may assist in developing control measures and enhance our understanding of the processes of adaptation and coevolution that accompany introductions. This paper addresses the capacity, extent, and means by which aquatic apple snails in Louisiana tolerate aerial exposure, as well as the factors that contribute to desiccation tolerance in P. maculata. Invasive P. maculata in Louisiana survived about 10 months of aestivation before 50% mortality was incurred, during which body mass was reduced by only about 30%; mortality and loss of body mass were positively correlated during aestivation. Size affects the loss of body mass in snails under 20 grams. Relative humidity interfered with the induction of aestivation, but it did not significantly affect the loss of body mass. Invasive apple snails in Louisiana also demonstrated the inclination and ability to sustain travel for at least three hours over dry land, at a rate of two meters per hour. The results of this study show that P. maculata is well adapted for survival in the absence of water. The ability to sustain travel over land and to endure long periods of aerial exposure suggests that the dry-down of infested bodies of water would not significantly impact populations of P. maculata in Louisiana.