Effects of macrophytes on feeding and life-history traits of the invasive apple snail Pomacea canaliculata

1. Biological invasions have become a serious threat to ecosystems worldwide. Various factors can contribute to the success of biological invasion. We examined how different macrophyte food affected feeding and life‐history traits of the invasive herbivorous snail Pomacea canaliculata, and whether differences in snail life‐history traits could explain its successful infestation of agricultural and non‐agricultural wetlands in Asia. 2. We tested five cultivated and five wild semi‐aquatic macrophytes. Snail daily feeding rate varied substantially with plant species, ranging from 1.3% to 22% of its body mass. Snails fed with four (Amaranthus gangeticus, Apium graveolens dulce, Ipomoea aquatica and Nasturtium officinale) of the five cultivated macrophyte species exhibited high survivorship, fast growth and high fecundity. Snails fed with Colocasia esculenta, however, grew poorly, did not reproduce and eventually died. 3. Of the five wild species (Eichhornia crassipes, Ludwigia adscendens, Murdannia nudiflora, Myriophyllum aquaticum and Polygonum hydropiper), M. nudiflora supported a high snail survival, but snails had slower growth and lower fecundity than those reared on the four palatable cultivated species. Snails fed with L. adscendens grew substantially slower than those fed with M. nudiflora, and produced only a small clutch of eggs. Snails fed with E. crassipes, M. aquaticum and P. hydropiper had very low survivorship, grew very little and did not reproduce. 4. We determined six plant properties and their correlation with the feeding, growth and reproduction of the apple snails. Cultivated macrophytes in general had a higher nutritional value and lower physical and chemical defences. Phenolic content was negatively correlated with snail feeding rate, while plant nitrogen and phosphorus contents were positively correlated with snail egg production and growth, respectively. 5. These results indicate that, due to their higher nutritional value and lower chemical and physical defences, cultivated macrophytes are in general desirable for the apple snail which may partly explain its successful invasion into wet agricultural areas in Asia. This snail may also selectively graze poorly defended wild macrophytes in non‐agricultural wetlands, leading to changes in floral diversity and wetland functioning. Management of this and other apple snails with similar life‐history traits should thus focus on the prevention of their further spread.     

Size-dependent effects of an invasive herbivorous snail (Pomacea canaliculata) on macrophytes and periphyton in Asian wetlands

1. The invasive golden apple snail (Pomacea canaliculata), native to South America, is a serious pest on rice seedlings in south‐east Asia and has also been shown to consume large amounts of macrophytes in natural wetlands, with large effects on ecosystem functioning. Earlier studies suggest that the snail undergoes an ontogenetic diet shift, feeding on algae and detritus as juveniles and shifting to aquatic macrophytes as adults. 2. Here, we study the effects of snail populations with a size‐structure typical of either populations at an invasive front or the size‐structure of established populations. In an enclosure experiment performed in a wetland in Laos, we compared treatments with small snails only (3 mm; invasive treatment) to treatments with small, medium sized (10 mm) and adult (>25 mm) snails (established treatment). The effects of snail grazing on three aquatic macrophyte species and periphytic algae were quantified. 3. We found that snails of all sizes had a strong negative effect on the biomass of all macrophyte species and periphytic algae. There was no evidence of an ontogenetic diet change, i.e. snails in both the invasive and established treatments affected macrophyte biomass. Foraging was size‐dependent in that small snails had higher relative foraging capacity (g plant consumed per g of snail) compared with medium and adult snails. Small snails, therefore, depressed growth of medium snails at increasing densities through exploitative competition for preferred resources, while adult snails did not grow at all in the presence of small snails. 4. Density dependence is common in freshwater invertebrates, including gastropod populations, but differences in size dependent foraging‐ and competitive‐ability have rarely been demonstrated in this group of organisms. Knowledge about intra‐specific differences in ecological performance may, however, both deepen our understanding of the processes that underlie population dynamics in invertebrates such as gastropods, and help develop control strategies for invasive golden apple snails.     

Regeneration of excised shell by the invasive apple snail Pomacea canaliculata

After excision of shell from Pomacea canaliculata, survival rates, repair process, haemocyte response, and calcium content were observed and quantified for three weeks. The following experimental treatments were used: black-colored individuals with large (BL-group) or small (BS-group) shell heights, yellow-colored individuals with large (YL-group) or small (YS-group) shell heights. The survival rates in BL-, YL-, BS-, and YS-groups after making partial excisions of snail shells were, respectively, 93.59, 94.87, 92.31, and 96.15%. Freshly regenerated shell could be seen at 1 day among the four groups after induction of shell regeneration. Regeneration shell filled the wound after 5–10 days. The area of regenerated shell in yellow-colored individuals was larger than that of black-colored individuals, but the thickness of regenerated shell was not significantly different. Multiple (four times) inductions of shell regeneration significantly enhanced the thickness of newly formed shells. Two types of circulating haemocytes (hyalinocytes and granulocytes) were identified under light microscopy based on Wright’s staining. Artificial induction of shell regeneration rendered a significant increase in the number of total circulating haemocytes which was followed by a decrease to pre-wounding levels. This peak value of total circulating haemocytes was 2.86, 2.43, 1.69, and 1.71-fold higher than pre-wounding levels in group BL, YL, BS, and YS, respectively. The number of total circulating haemocytes in yellow-colored individuals was significantly higher than in black-colored. Calcium concentrations in the mantles of snails are favorable for calcium nucleation. It is postulated that calcium content increased in the mantle increase at the start of the experiment and then returned to pre-wounding levels at the end of the experiment. This study shows that apple snails have effective shell regeneration abilities and that haemocytes and calcium transportation appear to play an important role in shell growth and regeneration.     

福寿螺的寄主植物及其对福寿螺体重的影响

为了明确福寿螺对寄主植物的选择性,进一步掌握其可能的危害及入侵暴发机制,对稻田水域及周边的24科43种植物进行了室外取食试验,分别在取食后3、5d对受试样品及成螺称重,比较其无选择条件下的取食偏好性及其对成螺增长率的影响。结果表明:福寿螺对受试的24科43种植物(样品)的根、茎、叶、果实以及块根(茎)均能取食,对水生(湿生)和陆生植物没有偏好性;在取食过程中,优先取食细嫩的植株和部分,硬老部分需经水浸泡软化后才能被取食;辣椒、苦瓜等果实的辣苦味对福寿螺无驱避作用;取食率与体重增长率呈显著正相关,取食越多生长越快;但体重与植物的总酚含量呈负相关。福寿螺的广食性、取食量、植物总酚含量、植物丰盛度等种群和生态系统特征是影响其快速扩散的重要原因,同时可以借助福寿螺对植物的不同利用类型防范其扩散和危害。     

The salinity tolerance of the invasive golden apple snail (Pomacea canaliculata)

We exposed snails of an invasive species of golden apple snail (Pomacea canaliculata) to five artificial sea water treatments at salinity levels of 0, 5, 10, 15 or 20 parts per thousand (ppt) to assess their salinity tolerance. We observed the behaviour, heart rate, total haemocyte counts, haemolymph ionic concentration and Na⁺/K⁺-ATPase activity in the mantle at 0, 12, 24, 48, 72 and 96 h post salinity exposures. The heart rate declined with increasing salinity, while Na⁺/K⁺-ATPase activity in the mantle presented a reverse trend, possibly to maintain normal osmolality. A trend of rising total haemocyte count was observed from 0 ppt and 5 ppt to 10 ppt salinities, while a sudden increase in the count was observed at 15 ppt and 20 ppt salinity groups. Furthermore, haemolymph Cl^?, Na⁺ and K⁺ concentrations increased directly with elevated salinity. An additional trial was performed to assess the growth performance of the snails under exposure to low salinities. During a 1 month trial, snails grew better at 5 ppt salinity treatment. Taken together, our results demonstrate that P. canaliculata can tolerate salt stress to some extent. The finding also obviously implies a possible invasive risk to estuaries.     

Changes in chemical components in the freshwater apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae), in relation to the development of its cold hardiness

The apple snail, Pomacea canaliculata, is an invasive freshwater snail. It increases its cold hardiness before winter. However, the physiological mechanism of cold hardiness in molluscs is poorly understood, especially in freshwater molluscs. In this study, we examined the changes in low molecular weight compounds, glycogen and lipids, in the body of P. canaliculata in association with the development of cold hardiness. When snails without cold hardiness were experimentally cold-acclimated, the amount of glycerol, glutamine, and carnosine increased, while glycogen and phenylalanine decreased. Overwintering cold-tolerant snails collected from a drained paddy field in November also showed increased glycerol in their bodies with decreasing glycogen concentration, compared to summer snails collected from a submerged field. Water content also decreased during the cold acclimation, although the water loss was minimal. These results indicate that the freshwater snail, P. canaliculata enhances cold hardiness by accumulation of some kinds of low molecular weight compounds in its body as some insects do. However, the actual function of each low molecular compound is still unknown.     

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

Hydrobiologia - 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...     

Allometric and trophic effects on shell morphology of Pomacea canaliculata (Caenogastropoda,Ampullariidae) from a geometric morphometrics viewpoint

Pomacea canaliculata, an invasive apple snail native to South America, is a serious pest of aquatic crops in several parts of the world. The origin of inter-population variation in shell shape is thought to be both genetic and environmental but the reaction norms to specific environmental factors are still poorly understood. Our aims were to analyze the existence of direct and indirect (allometric) effects of food availability (FA) on the shape of young adults of P. canaliculata. Full sibling hatchlings were reared under different levels of FA. Nine landmarks and 10 semi-landmarks were determined on photographs of mature shells and analyzed using geometric morphometrics. In both sexes significant allometry was found: a decrease in the spire height in both sexes, and an increase of the aperture size in males and of the last whorl in females. When this allometric component was removed a relationship between size-corrected shape and FA was found only in females, which were more globose and had a larger aperture when grown under high FA. This effect may be explained by the faster growth of the reproductive organs and the thinner shells of the best fed females.     

Dealing with a hyper-successful neighbor:effects of the invasive apple snail Pomacea canaliculata on exotic and native snails in South America

Pomacea canaliculata is a successful invader and also a competitor and predator of other snails and may play a key role in structuring freshwater snail communities both in its native and invaded range. In the present study we evaluated the contact and distant effects of P. canaliculata in its native range on exotic (Melanoides tuberculata and Physa acuta) and native snails (Heleobia parchappii, Biomphalaria peregrina, and Chilina parchappii). Habitat use was affected in P. acuta, H. parchappii, and B. peregrina by contact effects of P. canaliculata, whereas survival was only affected in P. acuta through combined con tact and dista nt effects. Fee undity was reduced in P. acuta and B. peregrina by combined con tact and distant effects;evidence of egg mass predation was also observed in both species. Melanoides tuberculata was not affected at all by P. canaliculata. The snail species with higher withdrawal resp on ses to con tacts with P. canaliculata were those that suffered less mortality by corporal contact, whereas snails with high crawling away responses suffered from higher mortality. The effects of P. canaliculata seem to be highly negative to small non operculate sn ails that lay gelati nous egg masses, whereas large operculate ovoviviparous snails are not affected in their survival and reproducti on. This apple snail may exert biotic resista nee agai nst P. acuta but could favor the establishme nt of M. tuberculata and other function ally similar species in new habitats in South America.     

A lentic dweller in lotic habitats: the behavior of the invasive South American apple snail Pomacea canaliculata in flowing water

The aim of this study was to test the hypothesis that positive rheotaxis and anti-detachment behaviors contribute to the persistence of Pomacea canaliculata in lotic environments. This invasive apple snail is commonly considered a lentic dweller. In a first series of trials in a laboratory flume, current velocity was gradually increased until snails’ detachment. Detachment velocity was highly variable, with some snails able to withstand strong currents during short periods. Sexually undifferentiated snails were the most resistant to detachment; most of the snails that resisted high velocities were facing flow before detachment. In a second series of trials, snails’ net displacement was estimated at three fixed velocities (0, 0.15, and 0.30 m s⁻¹). Current velocity did not influence mean net displacement, which was not different from zero. Marked snails were released in a stream and recaptured 24 h later estimating their net displacement. Most recovered snails dispersed a short distance from the release point and crawled through sites with very low current velocities. A small proportion of snails drifted downstream, indicating the existence of different dispersal mechanisms. Snails were able to resist current velocities that are among the highest recorded in streams in the Pampas region. P. canaliculata did not show a positive rheotactic response; in flowing water, snails crawl more often upstream, but at a slower pace than downstream. At the population level, a slow upstream spread seems possible in plain’s streams, probably being enough to compensate drift, but not to colonize headwaters. Irrigation systems are feasible pathways for the spread of this species in invaded regions.     

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

Hydrobiologia - Pomacea canaliculata, a freshwater snail native to tropical and temperate South America, has become an important invader and agricultural pest throughout tropical and subtropical...     

Effects of an invasive cattail species (Typha x glauca) on sediment nitrogen and microbial community composition in a freshwater wetland

Sediments from Cheboygan Marsh, a coastal freshwater wetland on Lake Huron that has been invaded by an emergent exotic plant, Typhaxglauca, were examined to assess the effects of invasion on wetland nutrient levels and sediment microbial communities. Comparison of invaded and uninvaded zones of the marsh indicated that the invaded zone showed significantly lower plant diversity, as well as significantly higher aboveground plant biomass and soil organic matter. The sediments in the invaded zone also showed dramatically higher concentrations of soluble nutrients, including greater than 10-fold higher soluble ammonium, nitrate, and phosphate, which suggests that Typhaxglauca invasion may be impacting the wetland's ability to remove nutrients. Terminal restriction fragment length polymorphism analyses revealed significant differences in the composition of total bacterial communities (based on 16S-rRNA genes) and denitrifier communities (based on nirS genes) between invaded and uninvaded zones. This shift in denitrifiers in the sediments may be ecologically significant due to the critical role that denitrifying bacteria play in removal of nitrogen by wetlands.     

Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance

Many invasive taxa are hybrids, but how hybridization boosts the invasive process remains poorly known. We address this question in the clonal freshwater snail Melanoides tuberculata from Martinique, using three parental and two hybrid lines. We combine an extensive field survey (1990-2003) and a quantitative genetic experiment to show that hybrid lines have outcompeted their parents in natural habitats, and that this increased invasiveness co-occurred with pronounced shifts in life-history traits, such as growth, fecundity and juvenile size. Given the little time between hybrid creation and sampling, and the moderate standing genetic variance for life-history traits in hybrids, we show that some of the observed trait changes between parents and hybrids were unlikely to arise only by continuous selection. We therefore suggest that a large part of hybrid advantage stems from immediate heterosis upon hybridization.     

Transformation of the offshore benthic community in Lake Michigan: recent shift from the native amphipod Diporeia spp. to the invasive mussel Dreissena rostriformis bugensis

1. The native amphipod Diporeia spp. was once the dominant benthic organism in Lake Michigan and served as an important pathway of energy flow from lower to upper trophic levels. Lake‐wide surveys were conducted in 1994/1995, 2000 and 2005, and abundances of Diporeia and the invasive bivalves Dreissena polymorpha (zebra mussel) and Dreissena rostriformis bugensis (quagga mussel) were assessed. In addition, more frequent surveys were conducted in the southern region of the lake between 1980 and 2007 to augment trend interpretation. 2. Between 1994/1995 and 2005, lake‐wide density of Diporeia declined from 5365 to 329 m⁻², and biomass (dry weight, DW) declined from 3.9 to 0.4 g DW m⁻². The percentage of all sites with no Diporeia increased over time: 1.1% in 1994/1995, 21.7% in 2000 and 66.9% in 2005. On the other hand, total dreissenid density increased from 173 to 8816 m⁻², and total biomass increased from 0.4 to 28.6 g DW m⁻². Over this 10‐year time period, D. r. bugensis displaced D. polymorpha as the dominant dreissenid, comprising 97.7% of the total population in 2005. In 2007, Diporeia was rarely found at depths shallower than 90 m and continued to decline at greater depths, whereas densities of D. r. bugensis continued to increase at depths greater than 50 m. 3. The decline in Diporeia occurred progressively from shallow to deep regions, and was temporally coincident with the expansion of D. polymorpha in nearshore waters followed by the expansion of D. r. bugensis in offshore waters. In addition, Diporeia density was negatively related to dreissenid density within and across depth intervals; the latter result indicated that dreissenids in shallow waters remotely influenced Diporeia in deep waters. 4. With the loss of Diporeia and increase in D. r. bugensis, the benthic community has become a major energy sink rather that a pathway to upper trophic levels. With this replacement of dominant taxa, we estimate that the relative benthic energy pool increased from 17 to 109 kcal m⁻² between 1994/1995 and 2005, and to 342 kcal m⁻² by 2007. We project that previously observed impacts on fish populations will continue and become more pronounced as the D. r. bugensis population continues to expand in deeper waters.     

Foraging behavior related to habitat characteristics in the invasive wasp Vespula germanica

When foraging on carrion resources, the wasp Vespula germanica usually makes repeated visits to the feeding site until depleting the resource. In the present study we analyzed how environmental cues affect wasps' behavior when re‐locating a protein food source. We studied this behavior in two different natural habitats: closed and open habitats. As closed habitats have more references to orient wasps to the feeding site than open habitats, we hypothesized that they would return to the foraging site more frequently in closed habitats than in open ones. We tested this hypothesis by studying wasp behavior in three different natural habitat conditions: (i) closed habitats, (ii) open habitats, and (iii) open habitats artificially modified by adding five sticks with flagging. Experiments consisted of training individual wasps to feed from a certain array, and at the testing phase we removed food and displaced the array by 60 cm. Therefore, we recorded wasps’choices when returning to the training area, by counting both the wasps’first approaches and the number of visits to the original feeding site and the displaced array. Wasps' behavior while re‐locating a protein food source was different if foraging at open or closed habitats. Wasps more frequently revisited a previous feeding location when foraging in closed habitats than when foraging in open ones. Furthermore, wasps more frequently visited the displaced array than the original feeding site in all three treatments. Nevertheless, when wasps were trained in closed habitats, they returned to the original feeding site more frequently than if trained in open ones. Interestingly, when five sticks with flagging were added in open habitats, wasps responded similarly as in closed habitats without these references. The results show that foraging behavior in V. germanica seems to be different in closed and open habitats, probably associated with the existence of references that guide foragers when re‐locating undepleted resources.     

Density-dependent growth and reproduction of the apple snail, Pomacea canaliculata: a density manipulation experiment in a paddy field

To examine density dependence in the survival, growth, and reproduction of Pomacea canaliculata, we conducted an experiment in which snail densities were manipulated in a paddy field. We released paint-marked snails of 15–20 mm shell height into 12 enclosures (pens) of 16 m² at one of five densities – 8, 16, 32, 64, or 128 snails per pen. The survival rate of released snails was 95% and was independent of snail density. The snail density had a significant effect on the growth and egg production of individual snails. This density dependence may have been caused by reduced food availability. The females at high density deposited fewer and smaller egg masses than those at low density, and consequently produced fewer eggs. The females at densities 8 and 16 deposited more than 3000 eggs per female, while the females at density 128 oviposited only 414 eggs. The total egg production per pen was, however, higher at higher snail density. The survival rates of juvenile snails were 21%–37% and were independent of adult density. The juvenile density was positively correlated with the total egg production per pen and hence was higher at higher adult density. However, the density of juveniles larger than 5 mm in shell height, i.e., juveniles that can survive an overwintering period, was not significantly different among density treatments. These results suggest that snail density after the overwintering period is independent of the density in the previous year. Thus, density dependence in growth and reproduction might regulate the population of P. canaliculata in paddies. Received: October 23, 1998 / Accepted: July 16, 1999     

Angiostrongylus cantonensis: experimental study on the susceptibility of apple snails, Pomacea canaliculata compared to Pila polita

Six groups (15 snails/group) of Pomacea canaliculata and Pila polita were infected orally with 0 (control), 200, 400, 800, 1600 and 3200 first-stage Angiostrongylus cantonensis larvae (L1). The respective mean+/-SD third stage larvae (L3) worm recovery 1-month post-infection (p.i.) for P. canaliculata was 0, 1.4+/-5.42 (0.7%), 0.13+/-0.35 (0.03%), 0.07+/-0.26 (0.009%), 0.07+/-0.26 (0.004%), 0, and for P. polita 0, 64.33+/-21.38 (32.25%), 115.36+/-36.82 (28.93%), 265.33+/-90.01 (33.27%), 471.33+/-92.98 (29.60%) and 849.00+/-243.23 (26.61%). The susceptibility of A. cantonensis in P. polita was dose-dependent (p<0.001). In the three groups (nine snails/group) of P. polita given 500 L1, we studied the distribution of L3 in the internal organs (i.e., foot, head+esophagus, kidney, albumin gland, mantle, intestine, digestive gland) and found the highest density after 1, 2 and 3 months p.i. in the mantle at 29.37%, 31.09% and 37.45%. The infection rate in P. canaliculata was too low to study distribution rates.     

Influence of water temperature on the activity of the freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) at its southernmost limit (Southern Pampas,Argentina)

1.

The effect of temperature on the activity of the freshwater snail Pomacea canaliculata was investigated through field surveys and laboratory trials.