Invasive Snail Research Articles

The cost of predator avoidance behaviors in an invasive freshwater snail

AbstractPredator avoidance behaviors are assumed to occur at a cost to the potential prey. The invasive New Zealand Mud Snail (Potamopyrgus antipodarum) exhibits several behaviors that appear to re...

Haplorchis pumilio (Trematoda: Heterophyidae) as a new fish-borne zoonotic agent transmitted by Melanoides tuberculata (Mollusca: Thiaridae) in Brazil: A morphological and molecular study

The fishborne zoonotic trematode Haplorchis pumilio (Looss, 1896) is here reported for the first time in Brazil based on morphological, experimental and molecular studies. Pleurolophocercous cercariae emerged from the invasive snail Melanoides tuberculata collected in the municipality of Ceará-Mirim, state of Rio Grande do Norte, Northeast region of Brazil, in November 2018, were used for experimental infection of guppies, Poecilia reticulata. Metacercariae were extracted from the caudal musculature of these fishes and were used to infect mice. Adult parasites recovered in the small intestine of the mice were morphologically identified as H. pumilio. Molecular sequences were obtained for the Brazilian and Peruvian isolates of H. pumilio, and were compared with data available in GenBank. Analyses of fragments of the nuclear genes 28S (1219bp) and ITS-2 (290 bp) revealed 98.48-100% similarity between the South American and Asian isolates of H. pumilio. Moreover, new sequences of the mitochondrial gene cox-1 obtained for the Brazilian (797bp) and Peruvian (646pb) isolates were 100% similar to a Mexican isolate of this species and 97.54% similar to an isolate from Thailand. This finding reveals the potential for occurrence of human haplorchiasis in Brazil, especially because of the increasing popularity of raw fish dishes in the country.

Disappearing apple snails (Caenogastropoda: Ampullariidae) of Thailand: a comprehensive update of their taxonomic status and distribution

ABSTRACT Ampullariidae include the largest of all freshwater snails and are of ecological, evolutionary and anthropogenic importance in Southeast Asia (SEA). Native ampullariids belonging to the genus Pila face various threats but are understudied, with their species taxonomy being confused and data on their distributions being scarce. We provide a comprehensive update on the nomenclature, status and distribution of Pila species in Thailand, based on DNA barcoding and geometric morphometric analysis of recently collected material. We confirm that at least five Pila species are extant in Thailand: Pila virescens, P. celebensis, P. turbinis, P. gracilis and P. pesmei. Pila celebensis, which has distinctive egg masses among all the known Southeast Asian Pila, appears to be sister to a clade comprising other SEA and some African Pila. Our results suggest that Pila may have dispersed into SEA on at least two separate occasions. Two singletons collected from northern and eastern Thailand may constitute separate species, but this requires further study. Intraspecific diversity of the mitochondrial cytochrome c oxidase subunit I gene was relatively high for P. celebensis, P. gracilis and P. pesmei (maximum uncorrected p-distances varied from 7% to 9%), and may include cryptic species. Conversely, P. virescens showed low intraspecific p-distances (c. 0%) among clades collected from different localities. This strongly suggests that introductions by humans may be the major cause of this pattern, and our own observations—we found that this species is being cultured and is commonly sold in markets for human consumption—are consistent with this. Pila turbinis was the rarest species, with live snails being collected from only two localities. Throughout Thailand, invasive confamilial Pomacea species appear to be replacing native Pila species, particularly in the Chao Phraya basin. While Thai Pila exhibit surprisingly high genetic diversity, with cryptic species likely being present, widespread invasive snails pose a major threat to their survival and urgent conservation action is needed.

A Comparative Transcriptomics Approach to Analyzing the Differences in Cold Resistance in Pomacea canaliculata between Guangdong and Hunan

Pomacea canaliculata, known as an invasive freshwater snail, is also called a golden apple snail; its survival and expansion are greatly affected by temperature. In this study, high-throughput sequencing (RNA-seq) was used to perform comparative transcriptome analysis on the muscular tissue (G_M) of snails in Guangdong and Hunan. Differential gene screening was performed with FDR <0.05 and |log2FoldChange| >1 as the threshold, and a total of 1,368 differential genes were obtained (671 genes showed upregulation in snails from Guangdong, and 697 genes displayed upregulation in snails from Hunan). Fifteen genes were identified as candidate genes for the cold hardiness of Pomacea canaliculata. Among them, three genes were involved in energy metabolism (glycogen synthase, 1; DGK, 1; G6PD, 1); seven genes were involved in homeostasis regulation (HSP70, 2; BIP, 1; GPX, 1; GSTO 1, G6PD, 1; caspase-9, 1); two genes were involved in amino acid metabolism (glutamine synthetase, 1; PDK, 1); and four genes were involved in membrane metabolism (inositol-3-phosphate synthase, 1; Na+/K+-ATPase, 1; calcium-binding protein, 2). This study presents the molecular mechanisms for the cold hardiness of Pomacea canaliculata, which could provide a scientific basis for the forecast and prevention of harm from Pomacea canaliculata.

Life history variation in space and time: environmental and seasonal responses of a parthenogenetic invasive freshwater snail in northern Germany

The processes that lead to a successful invasion are complex. Here, we investigated life history characteristics potentially explaining the invasion success of Potamopyrgus antipodarum, a small parthenogenetic and ovoviviparous freshwater snail that was recently added to the top “hundred worst” alien species in Europe. We monitored monthly, over the course of 1 year, shell size, number of brooded embryos, and the presence of castrating parasites at three Northeast German sites: a lake (the Kiessee), a stream (Hohen Sprenz), and a small spring brook (Rügen) (N = 1165). We found that (1) despite sharing the same clonal lineage, drastic differences in space and time for size and fecundity were observed, and these differences were linked to specific environmental variables (water temperature, salinity, and current); (2) P. antipodarum reproduces all year around, except at one of our sites, the spring Rügen, where the reproduction was seasonal; (3) none of our dissected specimens was infected by parasites. Together with ovoviviparity and the ability to reproduce parthenogenetically while being released from parasite pressure, the ability to adapt readily to a wide range of habitat conditions is likely paramount for the invasive success of P. antipodarum.

Effects of salinity on survival, growth and reproduction of the invasive aquatic snail Pomacea canaliculata (Gastropoda: Ampullariidae)

Pomacea canaliculata, a freshwater snail native to tropical and temperate South America, has become an important invader and agricultural pest throughout tropical and subtropical regions around the world. Colonization of various aquatic habitats by P. canaliculata in coastal regions of South China and its establishment potential in estuaries have raised great concern, yet little is known about the biological response of the snail and its tolerance under saline environments. We first examined the salinity tolerance of P. canaliculata using a total of 30 experimental juvenile snails exposed to eight salinity levels (from 0 to 14 psu in 2 psu steps). Daily survival of the snails was measured for each salinity treatment over 30 days. Based on salinity exposure test, influence of salinity on snail reproduction was investigated for a period of 30 days using 30 adult snails exposed to four salinity treatments (0, 2, 4 and 6 psu). Each salinity test replicated three times. Pomacea canaliculata could tolerate salinity levels ranging from 0 to 6 psu in which probability of survival was greater than 72% during a 30 days exposure. Lethal time leading to 50% mortality (LT50) of the snail declined from 71 days at 0 psu to 27 days at 6 psu. Pomacea canaliculata could ingest and reproduce normally at salinities ranging from 0 to 4 psu. Average mass daily gain, specific growth rate, and the hatching of egg clutches decreased significantly with elevated salinities. Results show a general threshold response of P. canaliculata to salinity. This freshwater snail falls into “2nd degree” euryhaline limnobionts tolerating salinities of 3–8‰.

The potential risk of Schistosoma mansoni transmission by the invasive freshwater snail Biomphalaria straminea in South China.

Schistosomes infect more than 200 million people worldwide, and globally, over 700 million people are at risk of infection. The snail Biomphalaria straminea, as one of the intermediate hosts of Schistosoma mansoni, consecutively invaded Hong Kong in 1973, raising great concern in China. In this study, a malacological survey was conducted over a period of four years, and investigations were performed on the mechanism of susceptibility of B. straminea to S. mansoni. B. straminea was investigated in China from 2014 to 2018. Out of 185 investigated sites, 61 were positive for stages of black B. straminea (BBS), which shows pigmented spots. Twenty of the 61 sites were positive for red B. straminea (RBS), which is partially albino and red colored. Phylogenetic analyses based on cox1 and 18S rRNA sequences demonstrated that both phenotypes were clustered with Brazilian strains. No S. mansoni infections were detected in field-collected snail. However, in laboratory experiments, 4.17% of RBS were susceptible to a Puerto Rican strain of S. mansoni, while BBS was not susceptible. The highest susceptibility rate (70.83%) was observed in the F2 generation of RBS in lab. The density of RBS has increased from south to north and from west to east in Guangdong since 2014. Five tyrosinase tyrosine metabolism genes were upregulated in BBS. Transcriptome comparisons of RBS and BBS showed that ficolin, C1q, MASP-like, and membrane attack complex (MAC)/perforin models of the complement system were significantly upregulated in BBS. Our study demonstrated that B. straminea is widely distributed in Hong Kong and Guangdong Province, which is expanding northwards very rapidly as a consequence of its adaptation to local environments. Our results suggest that B. straminea from South China is susceptible to S. mansoni, implying the high potential for S. mansoni transmission and increased S. mansoni infection risk in China.

New record of the invasive snail Melanoides tuberculata (Gastropoda, Thiaridae) - Ceará State, Brazil.

Melanoides tuberculata is a freshwater gastropod native to Africa and Asia, and currently presents distributed worldwide. The first record of Melanoides tuberculata in South America occurred in Brazil, in the city of Santos, state of São Paulo, in 1967. Therefore, the objective of the present study is to report the occurrence of Melanoides tuberculata for Banana Lagoon and to characterize the current population situation. The gastropods were collected through direct visualization of shells, morphometric measurements of Melanoides tuberculata shells were determined using a digital caliper. After identifying the gastropod and its first distribution in the area, a preliminary descriptive analysis of the population was carried out. The gastropods were classified by grouping the individuals into four classes according to the shell width (mm). This is the first record of the occurrence of Melanoides tuberculata, in Banana Lagoon, Caucaia municipality, Ceará state, Northeast Brazil, being the largest specimen cited in the literature (33.77 mm) and 92.65% of the gastropods present in sizes above the first reproduction stages.

Detecting aquatic invasive species in bait and pond stores with targeted environmental (e)DNA high-throughput sequencing metabarcode assays: Angler, retailer, and manager implications

Bait and pond stores comprise potential, yet poorly understood, vectors for aquatic invasive species (AIS). We tested for AIS and illegal native species in 51 bait and 21 pond stores from the central Great Lakes (Lake Erie, Ohio and Lake St. Clair, Michigan) and the adjacent Wabash River (Indiana) using environmental DNA (eDNA) metabarcode assays of water samples and morphological identifications. Retailers were questioned about supply chains, and anglers surveyed about baitfish use and disposal. Assays revealed unadvertised species eDNA in 100% of bait stores, with 61% containing illegal native non-bait (totaling 13 species) and 88% having AIS (11 species). Illegal native non-bait species included juvenile walleye, yellow perch, and white sucker eDNA. AIS eDNA included Eurasian ruffe in seven stores (all states), silver carp in five (including a Lake Erie store in two separate years), and bighead carp in two Lake Erie stores that also had silver carp. Among pond stores, two in Lake St. Clair had bighead carp eDNA, one also contained silver carp, and a Wabash River location showed European ide. Unadvertised invasive snails were discerned in 55% of pond stores. Four contained zebra mussel eDNA and two had invasive bryozoans. Illegal native species and AIS were widespread, but showed little relationship to the retailers' variable and extensive supply chains. Live baitfish releases were reported by 50% of Lake Erie anglers and 35% in Lake St. Clair. Consumer behavior and AIS prevalence in the bait and pond trades thus pose serious risks for introductions and spread.

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.

Using golden apple snail to mitigate its invasion and improve soil quality: a biocontrol approach.

The invasive and widespread golden apple snail (GAS, Pomacea canaliculata) is a harmful crop pest in many parts of Asia. The heavy use of molluscicides to control GAScould result in soil and water pollution as well as in loss of biodiversity. A sustainable and pollution-free control method is urgently needed to counteract this invasion. In this study, we proposed using dried and powdered GAS residue to neutralize and fertilize soils. We compared the effects of adding GAS residue (i.e., ground GAS shell and meat residue) to the effects of adding lime upon soil properties and microbes in a greenhouse pot experiment. Each pot was incubated for 120days, and soil pH, nutrients, microbial species, and enzyme activity were assessed. Results showed that addition of GAS residue significantly improved soil pH, contents oftotal organic carbon (TOC), total nitrogen (TN), total phosphorus (TP), and available nitrogen but decreased soil available phosphorus (AP) content due to phosphorus sorption induced by soil organic matter (OM) and high pH. The GAS residue added to soil released nutrients and alleviated soil acidity, as well as provided more resources to soil microbes to increase their bioactivity, although lime addition was better at mitigating soil acidity. We found that with added GAS residue of 25gkg-1, the soil nitrate nitrogen (NO3-N) content increased by 10 times; microbial biomass increased by 43%; and enzyme activity of β-1,4-glucosidase, β-1,4-N-acetylglucosaminidase, and β-D-cellobiosidase also were enhanced, compared to the control. Our findings suggest that GAS residue functions well as a fertilizer and soil amendment to aid the remediation of barren and acidic soils, making it a valuable and useful option in the control of the invasive GAS.

Mortality of the invasive white garden snail Theba pisana exposed to three US isolates of Phasmarhabditis spp (P. hermaphrodita, P. californica, and P. papillosa).

Theba pisana is a serious snail pest in many parts of the world and affects diverse crops including grain, vegetables, grapevines, and ornamental plants and shrubs. Due to its gregarious nature, ability to reproduce rapidly, and the difficulty of controlling it by conventional methods, it has the potential to become a significant pest where introduced. Mitigating this pest is an important challenge that must be addressed. Phasmarhabditis hermaphrodita, is a gastropod-killing nematode that is commercially available only in Europe (Nemaslug ®) and Sub-Saharan Africa (Slugtech ® SP). The use of effective gastropod-killing nematodes in the genus Phasmarhabditis (P. hermaphrodita, P. californica and P. papillosa) in California may provide one strategy for alleviating the potential damage and further spread of these snails, which are currently limited to San Diego and Los Angeles counties. Laboratory assays demonstrated for the first time that US isolates of P. hermaphrodita, P. californica and P. papillosa at 150 DJs/cm2 caused significant mortality and are equally lethal to T. pisana. Molluscicidal efficacy of these nematodes are comparable with those of iron phosphate, at the recommended high dose of 4.88 kg/m2. Additional trials are needed to determine their effects at lower dose and whether they are dependent on the size or age of the snails.

Fresh Cucumber as an Attractant for the Invasive Snail Xerolenta obvia

Attraction of the invasive snail Xerolenta obvia (Menke, 1828) to chopped cucumber and to a previously identified attractant based on a steam distillate of dry cat food was assessed with an established field population in Montana. Snails were significantly more attracted to the chopped cucumber than bottled water (control), using both traps and direct observations of attractants deployed in Petri dishes. The chopped cucumber also attracted significantly more snails to traps than the cat food distillate. These results suggest that chopped cucumber could constitute a cheap and simple lure for this and other invasive mollusk species. In addition, odors of chopped cucumber may support development of a new artificial lure, through analysis and reconstruction of the odor with synthetic compounds.

Multiple factors contribute to the spatially variable and dramatic decline of an invasive snail in an estuary where it was long-established and phenomenally abundant

Boom-bust dynamics of invasive species have long intrigued scientists and managers alike, but quantification of such dynamics, let alone their causes, is rare. We documented the decline of a previously prolific invasive mudsnail, Batillaria attramentaria, at Elkhorn Slough estuary in central California, USA. The mudsnail was the most abundant epibenthic invertebrate in the estuary, maintaining very high densities for many decades before declining heterogeneously throughout the estuary over the past decade, decreasing in density by three orders of magnitude at some sites. We used field and laboratory experiments to test several possible mechanisms for its demise. We show that the crab Pachygrapsus crassipes can prey heavily on Batillaria. We detected high dissolution rates of Batillaria shells, and we measured greater predation rates on tethered snails with dissolved versus intact shells. Warm water temperatures and high water levels coincided with the period of most dramatic Batillaria declines (2013–2015). Localized water impoundments appear to buffer environmental drivers of the decline because Batillaria remained abundant at sites with artificial tidal restriction, while the population crashed at one site after full tidal exchange was restored. We also investigated trematode parasite prevalence and molluscicide applications to the surrounding watershed as possible causes of mudsnail declines, but they had little explanatory power. Our findings illustrate the potential for population crashes even for long-established introduced species at pest levels of abundance, and demonstrate that such declines can exhibit spatial heterogeneity. Both of these results highlight the value of investigating population dynamics of invaders across multiple temporal and spatial scales.

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.

Morphological and molecular identification of the invasive freshwater snail Physa acuta (Gastropoda: Physidae) into Llanquihue Lake, Chilean Patagonia.

The sewage snail Physa acuta, native to North America, is an effective invasive species around the world. In Chile, it was first reported in 2014 in the north central area of the country. So far, the species has not been recorded in southern Chile. Sampling performed in 2015 in three localities from Llanquihue Lake, Chilean Patagonia, only provided native freshwater snails. However, new collections performed in February 2018 in the same three sites were successful for physid specimens suggesting a biological invasion entailing a large southward range expansion of these snails. Here we performed morphological, microstructural and phylogenetic analyses to investigate whether the new samples belong to Physa acuta. The shell morphology, male copulatory complex and radula microstructure of the new material agree with those of the sewage snail. The molecular phylogenetic analyses using the cytochrome c oxidase subunit 1 (COI) gene confirmed morphological identification. We suggest to take prompt measures to prevent the expansion of Physa acuta in Llanquihue Lake or nearby aquatic ecosystems.

The invasive New Zealand mud snail Potamopyrgus antipodarum (J.E. Gray, 1843) in central Pennsylvania

The invasive New Zealand mud snail Potamopyrgus antipodarum (J.E. Gray, 1843) in central Pennsylvania

Experimental evidence that the invasive snail Potamopyrgus antipodarum (Gray, 1843) survives passage through the digestive tract of common riverine fish

Experimental evidence that the invasive snail Potamopyrgus antipodarum (Gray, 1843) survives passage through the digestive tract of common riverine fish

Control of eosinopilic meningitis caused by Angiostrongylus cantonensis in China.

Rat lungworm Angiostrongylus cantonensis is the major infective agent of human eosinophilic meningitis (EM) in the world. The parasite was first noted in China in 1933. However, the public health importance was not realized until several EM outbreaks occurred recent years. Such disease is considered as emerging infectious disease in the People's Republic of China (P.R. China) since the major source of infection is invasive snail species, particularly Pomacea spp. National Institute of Parasitic Diseases (NIPD) initiated a systematic implementation research on this disease since 2003. Our researchers in NIPD developed the lung-microscopy for detecting A. cantonensis larvae in Pomacea snails and further accomplished the atlas of larval morphology by this method. We studied the determinants in infection, which helped the field collection of snails and improved the infection procedure in laboratory. Our researches promoted the promulgation of diagnosis criteria of angiostrongyliasis cantonensis by the Ministry of Health. We explored the molecular diversity of rat lungworm and its major snail host for development of source-tracing technique. The transmission modelling could provide the vulnerable area for surveillance. All the studies supported the surveillance system of EM caused by A. cantonensis in P.R. China. Such implementation research will provide a case study for control of emerging infectious diseases.

Trematode prevalence and an invasive freshwater snail: fewer infections and parasites likely contribute to the success of an invasive snail

The enemy release hypothesis postulates that non-native species establish and become abundant because coevolved enemies from the native range are missing or greatly reduced in the introduced range. We assessed whether the invasive New Zealand mud snail, Potamopyrgus antipodarum, is released from castrating trematode parasites by comparing prevalence and diversity of trematode parasites in P. antipodarum and co-occurring native snails in the western United States. Consistent with the enemy release hypothesis (1) P. antipodarum was not infected by trematodes at 80% of the sites and, relative to native snails, had low prevalence (4–5%) at the remaining sites, (2) across all sites, mean prevalence of trematodes was nine times lower in P. antipodarum than in co-occurring native snails and, (3) P. antipodarum were infected by half or fewer of the trematode taxa that infected co-occurring native snails. Taken together, our results suggest that fewer trematode infections and fewer trematode taxa in P. antipodarum could contribute to the success of this invasive snail. However, despite the large geographic scale of our survey (32 rivers sampled) and the large number of sites that we visited (n = 82), few sites had either enough snails or trematode parasites in native snails to be informative. Thus, our conclusions are based on a small number of sites (n = 10).