Invasive Apple Snail Research Articles

Invasive Apple Snail Diets in Native vs. Non-Native Habitats Defined by SIAR (Stable Isotope Analysis in R)

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.

Phenotypic plasticity of the invasive apple snail, Pomacea canaliculata, in China: a morphological differentiation analysis

ABSTRACT Pomacea canaliculata is listed among the world’s 100 worst invasive species, for threatening rice production and wetland biodiversity. We compared morphological and genetic characteristics of the 14 P. canaliculata geographic populations in mainland China to explore morphological differentiation in relation to geographical isolation and climate effects. The results showed that the average shell height, standing height and body width of P. canaliculata samples were 29.39, 18.52 and 19.91 mm. Morphological characteristics were significantly different among the P. canaliculata geographic populations. The changes in morphological characteristics fitted a linear model. Geometric measurement showed a significant difference in centroid size among the 14 populations. Canonical variates analysis revealed three distinct clusters and that four geographic populations were independent in shell shape variation. Mahalanobis distances showed significant relationships among all populations except Pingtang vs. Zhangzhou. The cumulative contribution of PC1, PC2 and PC3 in principal component analysis reached 80%. The overall identification accuracy was 97%. However, only 3.9% of pairwise Coefficient of Difference values exceeded 1.28. The difference in morphological traits did not conform to the isolation-by-distance model. The P. canaliculata phenotype was closely related to local climatic factors. In summary, the adaptation of Chinese P. canaliculata populations is ongoing.

Pomacea canaliculata (invasive apple snail)

Pomacea canaliculata (invasive apple snail)

Stopping Winter Flooding of Rice Fields to Control Invasive Snails Has no Effect on Waterbird Abundance at the Landscape Scale

The invasive apple snail (Pomacea maculata) appeared in 2010 in the Ebro Delta Natural Park, an important area for rice production and waterbird conservation in the eastern Mediterranean. To control crop damage, farmers stopped flooding their rice fields in winter, an agri-environmental scheme (AES) applied for more than 20 years in some European and American regions to favor flora and fauna from wetlands, including wintering waterbirds. Thus, apple snail control is controversial because of its potential side effects on international waterbird conservation efforts. Despite the fact that 10 years have passed since the first flooding limitations, and the alarms raised by the managers of the Natural Park, the side effects of apple snail management on waterbird conservation have not been evaluated. Here we fill this gap by analyzing a 35-year time series to assess whether abundance trends of 27 waterbird species, from five functional groups, decreased in the Ebro Delta after stopping winter flooding. We considered the effects of confounding local factors by also assessing trend changes in l’Albufera, a similar nearby not invaded wetland where flooding has not been interrupted. In addition, as a control of the positive effect of winter flooding, we also assessed whether abundance trends increased in both wetlands after applying this AES winter flooding. Our results showed complex and decoupled trend changes across species and geographical areas, without statistical evidences, in general or for any particular functional group, on the positive effect of winter flooding in both wetlands neither on the negative effect of its cessation in Ebro Delta. These results suggest the safety of this apple snail control in terms of waterbird abundance at a landscape scale. In addition, these results question, at least in two important wintering areas in Europe, the attractor role associated with the flooding agri-environmental scheme applied for decades.

Palatability of mangrove leaves to invasive apple snails: the relation between feeding electivity and multiple plant characteristics

Palatability of mangrove leaves to invasive apple snails: the relation between feeding electivity and multiple plant characteristics

Regional Expansion and Chemical Control for Invasive Apple Snails (Pomacea Maculata) in Louisiana Rice and Crawfish Production Systems

Regional Expansion and Chemical Control for Invasive Apple Snails (Pomacea Maculata) in Louisiana Rice and Crawfish Production Systems

Comparative proteomics suggests the mode of action of a novel molluscicide against the invasive apple snail Pomacea canaliculata, intermediate host of Angiostrongylus cantonensis

Angiostrongylus cantonensis is a zoonotic parasitic nematode that is the most common cause of human eosinophilic meningitis. The invasive apple snail Pomacea canaliculata is an important intermediate host of A. cantonensis and contributes to its spread. P. canaliculata control will help prevent its invasion and transmission of A. cantonensis. The new molluscicide PBQ (1-(4-chlorophenyl)-3-(pyridin-3-yl)urea) exhibits great potency against P. canaliculata and has low toxicity against mammals and non-target aquatic organisms. We studied the mode of action of PBQ using TMT-based comparative quantitative proteomics analysis between PBQ-treated and control P. canaliculata snails. A total of 3151 proteins were identified, and 245 of these proteins were significantly differentially expressed with 135 downregulated and 110 upregulated. GO and KEGG enrichment analyses identified GO terms and KEGG pathways involved in de novo purine biosynthesis, ribosome components and translation process were significantly enriched and downregulated. The results indicated that PBQ treatment had substantial effects on the synthesis of genetic material, translation process, and protein synthesis of P. canaliculata and were likely the main cause of snail mortality.

Control of invasive apple snails and their use as pollutant ecotoxic indicators: a review

Control of invasive apple snails and their use as pollutant ecotoxic indicators: a review

Costs to Ecuador's rice sector during the first decade of an apple snail invasion and policy recommendations for regions at risk

Invasive Alien Species (IAS) can become a tremendous burden to national economies; however, few studies have quantified the economic impacts of IAS, particularly for developing nations. The golden apple snail, Pomacea canaliculata (Lamarck), was introduced into Ecuador in 2005. By 2012, the snail had affected 94% of Ecuador's rice-growing areas. We used government surveys of rice production and snail distributions, as well as yearly production costs and rice prices, to estimate snail-associated losses to rice productivity and profitability between 2005 and 2015 – the first decade of P. canaliculata in Ecuador. Based on the intensity of the invasion and changing management practices, we estimate that the golden apple snail caused accumulated losses of 35.65 K tons of rice grain (worth US$23.10 M) with further productivity losses (lost inputs and labour) of US$9.61 M (total = US$32.71 M), until 2015. Based on survey information, we estimate that 90% of affected fields were treated with pesticides during the 5 years following initial establishment of the snail on individual rice farms. Pesticides potentially saved up to $10 M in damage during peak snail densities in 2012. By 2015, prophylactic molluscicide treatments were costing the nation US$15.24 M annually (including application costs: accumulated 10-year cost = $123.46 M, assuming 90% coverage). Increasing pesticide and labour costs, but relatively stable farm-gate rice prices, suggest that the continued chemical control of golden apple snail in Ecuador is economically unsustainable. We discuss possible alternatives to prophylactic molluscicide applications that can increase the economic and environmental sustainability of rice production in the face of high densities of apple snails during post-introduction outbreaks. We suggest that nations at high risk from invasive apple snails (e.g., Bangladesh, India, Colombia and Peru) could avoid substantial losses by pre-emptively researching and adopting mechanized crop establishment practices that not only reduce labour costs, but also prevent potential damage from apple snails to rice.

Comparison of Invasive Apple Snail (Pomacea canaliculata) Behaviors in Different Water Temperature Gradients

Pomacea canaliculata (known as invasive apple snail) is a freshwater snail native to South America that was introduced into many countries (including Asia and North America) as a food source or for organic farming systems. However, it has invaded freshwater ecosystems and become a serious agricultural pest in paddy fields. Water temperature is an important factor determining behavior and successful establishment in new areas. We examined the behavioral responses of P. canaliculata with water temperature changes from 25 °C to 30 °C, 20 °C, and 15 °C by quantifying changes in nine behaviors. At the acclimated temperature (25 °C), the mobility of P. canaliculata was low during the day, but high at night. Clinging behavior increased as the water temperature decreased from 25 °C to 20 °C or 15 °C. Conversely, ventilation and food consumption increased when the water temperature increased from 25 °C to 30 °C. A self-organizing map (an unsupervised artificial neural network) was used to classify the behavioral patterns into seven clusters at different water temperatures. These results suggest that the activity levels or certain behaviors of P. canaliculata vary with the water temperature conditions. Understanding the thermal biology of P. canaliculata may be crucial for managing this invasive snail.

The effects of different water temperatures on survival and growth rate of juvenile invasive apple snail, Pomacea canaliculata (Lamarck, 1822) under controlled environment

Invasive apple snail, Pomacea canaliculata is one of the major mollusc pests affecting rice production in Malaysia. This pest not only gives fatal effects to rice but also decreases the water quality in the ecosystem due to the use of pesticides to control it. With the unpredictable changes on global climatic in Malaysia, it is important to have knowledge on the effect of water temperature on growth and survival rate of P. canaliculata in water bodies, in order to avoid loss in paddy field and its adverse effects on aquatic ecosystems. Water temperature is one of the most important environmental factors influencing the survival, growth rate, reproduction and behaviour of freshwater snails. The aim of this study is to evaluate the growth and survival rate of juvenile P. canaliculata at different temperature regimes. Growth and survival of juvenile P. canaliculata were evaluated at different constant water temperatures (15, 20, 25, 30 and 35°C). Our findings show, at 30° C the growth rate of P. canaliculata is higher compared with the other temperatures, however had low survival rate. Meanwhile, at room temperature (21 - 24°C), a higher survival rate (100%) was recorded. The results showed that different water temperatures affect the growth and survival rate of P. canaliculata and it is an important indicator for predicting and understanding the changes of water temperature when controlling this pest.

Taxonomic shortcuts lead to long delays in species discovery, delineation, and identification

Invasive species threaten biodiversity, ecosystem functions, and human health around the world. Accurate and reliable species delineation and identification are prerequisites for any effort to control the introduction of new species and the spread of those already introduced. The advent of DNA assisted taxonomic tools has fueled the development of diverse and innovative approaches often touted as simple, inexpensive, and universally applicable for addressing impediments to rapid identification of non-native species. Ampullariidae (apple snails) are a family of freshwater snails with at least five species that have been introduced outside their native range and a prime example of how taxonomic uncertainty may hamper our understanding of invasion biology. Matsukura et al. (Appl Entomol Zool 43(4):535–540, 2008) and Cooke et al. (Conserv Genet Resour 4(3):591–593, 2012) developed species-specific PCR primers as rapid, simple, and inexpensive approaches to distinguishing among and identifying the most notorious and widespread invasive apple snails, Pomacea canaliculata and Pomacea maculata, and a third species in the aquarium trade, Pomacea diffusa. Neither approach was evaluated within the context of the overall genetic diversity of the target species, or with consideration for the species diversity within the family. To evaluate both shortcut approaches, the primers were tested for their utility in delineating and identifying the target species and other closely related taxa, including 24 apple snails representing 21 species. The results indicate that the primers are of limited taxonomic utility, and fail to consistently identify the target taxa, or congenerics. More importantly, use of these primers without additional data leads to misidentifications, potentially endangering native biodiversity and allowing novel introduced species to go undetected.

An Invader’s Peculiar Trophic Behavior: Diel Fluctuations and Environmental Drivers

AbstractThe trophic ecology of the invasive apple snail Pomacea canaliculata was intensely investigated because of the impacts of its grazing on aquatic vegetation, including crops. However, this freshwater snail also gathers food from the water surface by using a pedal funnel, a distinctive trophic behavior called pedal surface collecting. We investigated the diel fluctuations of this trophic behavior through four whole-day field observations in a stream. We recorded the lowest pedal funnel frequencies during light hours and the highest after sunset, a pattern similar to that of general activity. We evaluated through laboratory experiments the influence of water temperature and velocity, photoperiod, and a possible endogenous rhythm on this behavior. Pedal funnels are formed within the whole temperature range in which this snail is active. The highest pedal funnel formation rates were recorded at 30 °C, but the food captured was the same regardless of temperature. Pedal funnels were not observed at water velocities above 0.12 m·s-1, but below this limit the rate and time spent in funnels remained constant with velocity. Despite the time of day, pedal funnels were scarce under constant artificial light, ruling out an endogenous rhythm. Both in the laboratory and in the stream, the highest levels of pedal funnels were observed during dark periods, probably as a strategy to avoid detection by visual predators. Pedal surface collecting on floating matter could represent an additional impact of invasive apple snails on freshwater ecosystems, but it could also be used for the specific delivery of molluscicides against them.

Exceeding its own limits: range expansion in Argentina of the globally invasive apple snail Pomacea canaliculata

Pomacea canaliculata is a freshwater snail native to southern South America. The aims of this work are to update its distribution in Argentina and to analyze through niche models whether the environmental conditions from its original distribution can anticipate its recently expanded range. Almost all records of P. canaliculata before 1958 (original records) belong to del Plata or connected basins. A quarter of the new present records are located in basins not connected to del Plata, indicating a recent expansion of the distribution range of P. canaliculata in Argentina. Recently colonized areas are mostly environmentally suitable according to the projection of the original distribution model, thus natural barriers were probably the main limits to its distribution in the past. According to the model, many regions outside its original range, including several not yet colonized, are suitable for the establishment of P. canaliculata. Consequently, it is likely that this species will continue establishing new populations in Argentina, especially if fishermen and aquarists continue to move snails to new locations. Our study revealed that an extensive but overlooked invasion is in process in its native range, where the impacts on diversity and ecosystems functioning may differ from those already described elsewhere.

Both quiescent and proliferating cells circulate in the blood of the invasive apple snail Pomacea canaliculata

Gastropod hematopoiesis occurs at specialized tissues in some species, but the evidence also suggests that hemocyte generation is maybe widespread in the connective tissues or the blood system in others. In Ampullariidae (Caenogastropoda), both the kidney and the lung contain putative hematopoietic cells, which react to immune challenges. In the current study, we wanted to explore if hematopoiesis occurs in the blood of Pomacea canaliculata. Thus, we obtained circulating hemocytes from donor animals and tested their ability to proliferate in the blood of conspecific recipients. We tracked cell proliferation by labeling the donors' hemocytes with the fluorescent cell proliferation marker carboxyfluorescein diacetate succinimidyl ester (CFSE). Transferred CFSE-labeled hemocytes survived and proliferated into the recipients’ circulation for at least 17 days. We also determined the cell cycle status of circulating hemocytes by using the propidium iodide (PI) and acridine orange (AO) staining methods. Flow cytometry analyses showed that most PI-stained hemocytes were in the G1 phase (~96%), while a lower proportion of cells were through the G2/S-M transition (~4%). When we instead used AO-staining, we further distinguished a subpopulation of cells (~5%) of low size, complexity-granularity, and RNA content. We regarded this subpopulation as quiescent cells. In separate experimental sets, we complemented these findings by assessing in circulating hemocytes two evolutionary conserved features of quiescent, undifferentiated cells. First, we used JC-1 staining to determine the mitochondrial membrane potential (Ψm) of circulating hemocytes, which is expected to be low in quiescent cells. Most hemocytes (~87%) showed high aggregation of JC-1, which indicates a high Ψm. Besides that, a small hemocyte subpopulation (~11%) showed low aggregation of the dye, thus indicating a low Ψm. It is known that the transition from a quiescent to a proliferating state associates with an increase of the Ψm. The specificity of these changes was here controlled by membrane depolarization with the Ψm disruptor CCCP. Second, we stained hemocytes with Hoechst33342 dye to determine the efflux activity of ABC transporters, which participate in the multixenobiotic resistance system characteristic of undifferentiated cells. Most hemocytes (>99%) showed a low dye-efflux activity, but a small proportion of cells (0.06–0.12%) showed a high dye-efflux activity, which was significantly inhibited by 100 and 500 μM verapamil, and thus is indicative of an undifferentiated subpopulation of circulating hemocytes. Taken together, our results suggest that, among circulating hemocytes, there are cells with the ability to proliferate or to stay in a quiescent state and behave as progenitor cells later, either in the circulation or the hematopoietic tissues/organs.

The efficiency of universal mitochondrial DNA barcodes for species discrimination of Pomacea canaliculata and Pomacea maculata.

Invasive apple snails, Pomacea canaliculata and P. maculata, have a widespread distribution globally and are regarded as devastating pests of agricultural wetlands. The two species are morphologically similar, which hinders species identification via morphological approaches and species-specific management efforts. Advances in molecular genetics may contribute effective diagnostic tools to potentially resolve morphological ambiguity. DNA barcoding has revolutionized the field of taxonomy by providing an alternative, simple approach for species discrimination, where short sections of DNA, the cytochrome c oxidase subunit I (COI) gene in particular, are used as ‘barcodes’ to delineate species boundaries. In our study, we aimed to assess the effectiveness of two mitochondrial markers, the COI and 16S ribosomal deoxyribonucleic acid (16S rDNA) markers for DNA barcoding of P. canaliculata and P. maculata. The COI and 16S rDNA sequences of 40 Pomacea specimens collected from six localities in Peninsular Malaysia were analyzed to assess their barcoding performance using phylogenetic methods and distance-based assessments. The results confirmed both markers were suitable for barcoding P. canaliculata and P. maculata. The phylogenies of the COI and 16S rDNA markers demonstrated species-specific monophyly and were largely congruent with the exception of one individual. The COI marker exhibited a larger barcoding gap (6.06–6.58%) than the 16S rDNA marker (1.54%); however, the magnitude of barcoding gap generated within the barcoding region of the 16S rDNA marker (12-fold) was bigger than the COI counterpart (approximately 9-fold). Both markers were generally successful in identifying P. canaliculata and P. maculata in the similarity-based DNA identifications. The COI + 16S rDNA concatenated dataset successfully recovered monophylies of P. canaliculata and P. maculata but concatenation did not improve individual datasets in distance-based analyses. Overall, although both markers were successful for the identification of apple snails, the COI molecular marker is a better barcoding marker and could be utilized in various population genetic studies of P. canaliculata and P. maculata.

The invasive apple snail Pomacea canaliculata in Indonesia: a case study in Lake Rawa Pening, Central Java

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.

Antagonistic effects of a native apple snail on other snails and macroinvertebrates in Southern Pampas waterbodies: A mesocosm approach

Macroinvertebrates represent an important component of communities and trophic webs of freshwater ecosystems. Pomacea canaliculata (family Ampullariidae), an invasive apple snail native to the Pampas ecoregion, acts as a voracious grazer and plays a structuring role on submerged macrophytes that serve as food, habitat or foraging ground for many macroinvertebrates. Laboratory studies show that P. canaliculata can also act as a competitor or predator of other macroinvertebrates. Using a mesocosm approach, we sought to investigate if this species of apple snail affects other freshwater snails (Chilina parchappii, Heleobia parchappii, Biomphalaria peregrina and Melanoides tuberculata) as well as other macroinvertebrates and if consumption of submerged macrophytes and detritus mediates these effects. After twelve weeks we estimated in mesocosms with and without apple snails the abundance of snails and macroinvertebrates through samples taken separately from sediment and from macrophytes. We also estimated the coverage and biomass of macrophytes and the detritus biomass. Significantly lower abundance occurred in mesocosms with apple snails for all snail species and representative macroinvertebrates (i.e., Hirudinea, Ephemeroptera, Chironomidae and Odonata). Mesocosms with apple snails also resulted in lower total abundance of macroinvertebrates. We speculate that the negative effects of P. canaliculata on most other snails and macroinvertebrates living on macrophytes relates to their grazing on detritus and macrophytes. In contrast, the density of snails and macroinvertebrates in the samples from sediments were not affected by P. canaliculata. One snail species and Ephemeroptera were negatively affected by mechanisms not related to the reduction in macrophyte biomass and detritus. A decrease in the microhabitats provided by macrophytes probably mediated the negative effects on Odonata nymphs. The reduction in the abundances of snails and macroinvertebrates caused by P. canaliculata may have cascading effects on higher trophic levels in waterbodies from Southern Pampas but also in invaded regions.

Limpkin, Aramus guarauna (L., 1766) (Gruiformes, Aramidae), extralimital breeding in Louisiana is associated with availability of the invasive Giant Apple Snail, Pomacea maculata Perry, 1810 (Caenogastropoda, Ampullariidae)

We document the first breeding record of Limpkin, Aramus guarauna (Linnaeus, 1766) (Gruiformes, Aramidae), for Louisiana, describe an additional unpublished breeding record from Georgia, as well as a possible record from Alabama, and associate these patterns with the concurrent establishment of the invasive Giant Apple Snail, Pomacea maculata Perry, 1810 (Caenogastropoda, Ampullariidae). We predict that an invasive prey species may facilitate range expansion by native predator species, which has ramifications for conservation and management.

Sex Differences in Cold Hardiness and Desiccation Tolerance of Invasive Apple Snails in South China

Sex differences in stress responses may be a key factor that determines population structure. Sex ratios of Pomacea canaliculata populations usually average 1:1 at birth, but are often female-biased for adults. Low temperatures and drought are the main abiotic stresses affecting reproductive dispersal and population development. Therefore, we investigated whether Pomacea sp. (mainly P. canaliculata but might include P. maculata) exhibited sex differences in cold hardiness and desiccation tolerance. The results show that more females survived than males during cold-drought stress and overwintering. Following cold-drought stress, 58% of females and 40% of males survived at 3°C drought conditions for 6 days. With the development of cold-drought hardiness, increased amounts of bound water, glycerol and lipids were found in Pomacea sp. along with decreased free water levels. These physiological parameters exhibited sex differences in the snails, except for lipids, and the changes all showed tendencies favoring the survival of females under cold-drought stress. These results suggest that female Pomacea sp. may be more viable than males under cold and dry conditions.