Lethal and non-lethal effects of multiple indigenous predators on the invasive golden apple snail (Pomacea canaliculata)

1. We investigated the individual and combined effects of two predators (the climbing perch, Anabas testudineus, and the wetland crab, Esanthelphusa nimoafi) indigenous to wetlands in Laos, on the behaviour and survival of the invasive South American golden apple snail (Pomacea canaliculata). The snail is considered a pest, consuming large amounts of rice and other aquatic vegetation in the region. 2. Snail avoidance reactions to released predator chemical cues were investigated in aquaria while the effects of predators on a mixed snail population were studied in field enclosures that contained native aquatic plants (Salvinia cucullata, Ludwigia adscendens and Ipomoea aquatica). 3. In the aquaria experiment, neonate (2–3 mm) and medium‐sized snails (8–10 mm) responded to fish chemical cues by going to the surface, whereas adult snails (35–40 mm) went to the bottom. In contrast, no size class of snails reacted to chemical cues released by crabs. 4. In the field experiment, fish reduced the abundance of neonate snails, and crabs reduced the abundance of all size classes. The effect of the combined predators could not be predicted from the mortality rate observed in single predator treatments. The survival of neonate and medium‐sized snails was greater and of adults less than expected. The presence of predators did not affect egg production. Snails consumed significant amounts of plants despite the presence of predators. 5. Our findings suggest that some indigenous Asian predators have lethal and sublethal effects on P. canaliculata that depend on snail size and predator type. When in the presence of several predators the response of snails to one predator may either increase or decrease the vulnerability of snails to the others.     

Size-selective predation by all-male prawns: implications for sustainable biocontrol of snail invasions

All-male populations of the freshwater prawn Macrobrachium rosenbergii were recently produced by a novel temporal RNA interference (RNAi)-based biotechnology for aquaculture purposes. This biotechnology opens the way to the wide use of all-male prawn populations as sustainable biocontrol agents against invading populations of freshwater snails, for which there is currently no environmentally friendly solution. Among the most damaging of the invasive freshwater snail species are the apple snails (Pomacea spp.), which inflict major damage on natural ecosystems and rice fields. The proposed use of all-male prawn populations as environmentally friendly biocontrol agents against invasive freshwater snails has several advantages: efficient predation by the prawns over a wide range of freshwater snails, the ready availability of the prawns, and the monosex non-reproductive nature of the biocontrol agents. Since the aquatic predators are strongly size selective, we quantified the predation rate as a function of body size of both predator and prey (M. rosenbergii and P. caniculata). Medium-sized and large prawns (~10–30 g) efficiently preyed small and medium-sized snails (up to 15 mm), while small prawns (up to 4 g) immediately and completely eradicated snail hatchlings. Medium-sized prawns (~22 g) exterminated a significant fraction of snail biomass within 24 h (up to 58% of their body mass) after being introduced into a tank of snails. A typical ‘climbing-to-the surface’ anti-predator behavior of the snails was recorded. The potential of all-male prawns as efficient biocontrol agents over hatchling and adult apple snails as part of an integrated pest management program is discussed. Our experiments set the stage for evaluating the ecological and economic implications of this generic solution for a wide variety of habitats.     

不同壳色福寿螺形态性状与体质量的关系

【背景】福寿螺因其食性杂、抗逆性和繁殖力强以及自然天敌少等不断扩散,侵害农作物,被列为我国首批外来入侵物种。国内外学者一直致力于研究对其的防治与监控。自然界中福寿螺存在2种壳色——黄色和黑色,壳色受遗传因素和环境因素的双重影响。广东省福寿螺多以黑色为主,福寿螺倾向于与不同壳色的螺交配。壳色在一定程度上影响其交配的选择性,但2种壳色的福寿螺繁殖力指标差异不显著。而关于这2种壳色的螺在形态学上的差异鲜有报道。【方法】利用生物统计软件和分析方法进行相关性分析、通径分析及多元回归分析,计算相关系数、通径系数和决定系数,研究2种壳色福寿螺形态性状与体质量的关系。【结果】2种壳色福寿螺的体质量、层高的变异系数较大,且黄色比黑色变异系数大。对黄色福寿螺体质量影响较大的依次为壳高、口宽;对黑色福寿螺体质量影响较大的依次为口宽、层高。【结论与意义】2种壳色福寿螺在形态性状方面差异显著,可以将壳色作为特征标记,为福寿螺的监测与灾害评估提供参考。     

Life history traits determine the differential vulnerability of native and invasive apple snails (<Emphasis Type="Italic">Pomacea</Emphasis> spp.) to a shared juvenile-stage predator

The vulnerability of gastropods to their predators varies with life history traits such as morphology, body size, behavior, and growth rates as well as predator size. A recent study suggested that the invasive apple snail, Pomacea maculata, was considerably more vulnerable to crayfish predators than the native Florida apple snail, P. paludosa. The difference was hypothesized to be caused by the relatively small hatchling size of P. maculata. To test this hypothesis, we conducted a series of feeding assays designed to quantify maximum feeding rates and selective foraging of crayfish on apple snails. The rate at which crayfish killed individual P. maculata (i.e., kill rates) decreased with snail size, and kill rates on both species increased with crayfish size. Kill rates on juvenile P. maculata were higher than kill rates on size-matched hatchling P. paludosa, and crayfish fed selectively on P. maculata when offered mixed groups of size-matched snails. Further analyses revealed that hatchling P. paludosa possess shells 1.8× heavier than size-matched P. maculata suggesting differences in vulnerability to crayfish were consistent with interspecific differences in shell defenses. Differences in hatchling size and defensive traits in combination make crayfish kill rates on hatchling P. maculata approximately 15.4× faster than on hatchling P. paludosa, but the relative contribution of hatchling size to differences in apple snail vulnerability was >3× greater than the contribution of defensive traits.     

Gene regulation of shell banding in a land snail from Israel

The Israeli land snail, Xeropicta vestalis, offers a particularly clear example of gene regulation in relation to natural selection, in that within each population the appropriate phenotype is generated only at the correct part of the animals life cycle, and a contrasting phenotype develops when the forces of natural selection change. In the mountains of Jerusalem, where the winter is cold, the shells are dark. Westwards, towards the coastal plain where the winter is warmer, the shells gradually become paler. As dark shells absorb more radiation than pale ones, this clinal variation in morph frequencies can be explained in thermal terms. (Banded shells are also more cryptic than non-banded shells, so that in the mountains visual selection by predators may be an additional force which favours dark shells.) Xeropicta vestalis is an annual, semelparous species: the snails hatch in winter, become mature within one year, reproduce, and then die. In the coastal plain the snails are active throughout most of the year, and they have a long period in which to grow to reach adult size. In the mountains and hills, on the other hand, the snails are active for only a very short period. They spend most of their lives as small snails, in a state of aestivation. Xeropicta vestalis must be dark in mountains because when it finally awakens, it must very rapidly and hastily reach reproduction size. A dark shell, by speeding up temperature-dependent processes in this critical stage, assists the snail to mature rapidly. Shell darkness varies with age: in the mountains and hills the shells are moderately dark when they hatch, but become darker whilst growing in early winter. In the coastal plain also, the snails are moderately dark when they hatch; but here they become paler, whilst growing in winter and spring. In both cases, each snail is darker in the colder months and paler in the hot ones. A strategy of gene regulation of shell colour is thus favoured when the subsequent forces of the environment are very contrasting in their direction, very severe—yet also very predictable.     

Trade-offs between force and fit: extreme morphologies associated with feeding behavior in carabid beetles

We explored how functional trade-offs in resource handling strategies are associated with the divergent morphology of predators. The malacophagous carabid Damaster blaptoides shows two extreme morphologies in the forebody; there is an elongate small-headed type and a stout large-headed type. A feeding experiment showed that the small-headed type obtained a high feeding performance on snails with a thick shell and a large aperture by penetrating the shell with its head. In contrast, the large-headed type showed a high feeding performance on snails that had a thin shell and a small aperture, and they ate these prey by crushing the shell. The large-headed, strong-jawed beetles are efficient at shell crushing but are ineffective at shell entry; the large mandibles and musculature that allow for shell crushing make the beetle's head too wide to penetrate shell apertures. On the other hand, small-headed, weak-jawed beetles crush poorly but can reach into shells for direct predation on snail bodies. These findings are hypothesized to be functional trade-offs between force and fit due to morphological constraints. This trade-off would be a primary mechanism affecting both resource handling ability in animals and phenotypic diversity in predators and prey.     

Crayfish predation on the common pond snail (Lymnaea stagnalis): the effect of habitat complexity and snail size on foraging efficiency

Optimal foraging theory was used to explain selective foraging by the introduced signal crayfish (Pacifastacus leniusculus) on the thin-shelled common pond snail (Lymnaea stagnalis). Crayfish predation efficiency was studied in relation to habitat complexity and snail size. In a pool experiment (area 1.3 m²) single adult crayfish were allowed to feed on four size classes of snails for one week. A pair-wise preference trial (aquarium experiment) tested if adult crayfish selectively predated on particular size classes of snail and if prey value (expressed as snail dry mass per handling time) could explain the size range of snails chosen. Crayfish preferred the smallest size classes of snails in both pool and aquaria experiments. In the pool experiment crayfish had a strong effect on snail survival. Habitat complexity did not affect overall snail survival, but resulted in reduced predation pressure on the smallest size classes of snails. Handling time and shell-thickness increased exponentially with increasing snail size, and the two smallest size classes had the highest prey values. The results suggest that crayfish can structure the abundance and size distribution of thin-shelled snails, through size-selective predation and reduction of macrophytes. The mechanisms behind the choice of snails may be based on prey value and reduced exposure time to predators and conspecifics. Crayfish effects on snail size distribution may be less pronounced in complex habitats such as macrophyte beds. This revised version was published online in July 2006 with corrections to the Cover Date.     

Changes in the selection differential exerted on a marine snail during the ontogeny of a predatory shore crab

Empirical estimates of selection gradients caused by predators are common, yet no one has quantified how these estimates vary with predator ontogeny. We used logistic regression to investigate how selection on gastropod shell thickness changed with predator size. Only small and medium purple shore crabs (Hemigrapsus nudus) exerted a linear selection gradient for increased shell‐thickness within a single population of the intertidal snail (Littorina subrotundata). The shape of the fitness function for shell thickness was confirmed to be linear for small and medium crabs but was humped for large male crabs, suggesting no directional selection. A second experiment using two prey species to amplify shell thickness differences established that the selection differential on adult snails decreased linearly as crab size increased. We observed differences in size distribution and sex ratios among three natural shore crab populations that may cause spatial and temporal variation in predator‐mediated selection on local snail populations.     

Biology and conservation of the rare New Zealand land snail Paryphanta busbyi watti (Mollusca, Pulmonata)

Abstract. The biology of Paryphanta busbyi watti , an endangered carnivorous land snail, was studied mostly by following large juvenile and adult snails with harmonic radar. The snails are nocturnally active and most (79%) hide during the day under leaf litter or in dense vegetation. Fecal analysis showed that the diet is primarily earthworms, but some cannibalism of smaller snails occurs. Empty shells appear to be an additional source of dietary calcium. Mating occurred most frequently between April and July. Mating snails stayed together for 4–7 days, and each pair reversed their positions at least twice. Four snails were first found mating 151–1240 d after they acquired adult shells, and 7 snails were observed mating a second time after 66–298 d. We found 8 nests and observed 6 snails ovipositing; 5 snails laid eggs in holes they dug and one laid eggs in a crevice between rocks. In 2 instances, oviposition was recorded 52 and 140 d after mating. Snails were estimated to lay on average ∼17.5 eggs per year in 3–5 clutches. Most oviposition was observed in August/September, but some occurred between November and February. Of the snails that died, pigs killed 13.6% and humans inadvertently killed another 13.6%. Other snails died from unknown causes mostly during the drier and warmer months, from November to April. This large land snail survives in the presence of introduced predators, but some life history traits could predispose it to a rapid decline in numbers if new predators arrive.     

Experimental Test of Preferences for an Invasive Prey by an Endangered Predator: Implications for Conservation

Identifying impacts of exotic species on native populations is central to ecology and conservation. Although the effects of exotic predators on native prey have received much attention, the role of exotic prey on native predators is poorly understood. Determining if native predators actively prefer invasive prey over native prey has implications for interpreting invasion impacts, identifying the presence of evolutionary traps, and predator persistence. One of the world’s most invasive species, Pomacea maculata, has recently established in portions of the endangered Everglade snail kite’s (Rostrhamus sociabilis plumbeus) geographic range. Although these exotic snails could provide additional prey resources, they are typically much larger than the native snail, which can lead to lower foraging success and the potential for diminished energetic benefits in comparison to native snails. Nonetheless, snail kites frequently forage on exotic snails. We used choice experiments to evaluate snail kite foraging preference in relation to exotic species and snail size. We found that snail kites do not show a preference for native or exotic snails. Rather, snail kites generally showed a preference for medium-sized snails, the sizes reflective of large native snails. These results suggest that while snail kites frequently forage on exotic snails in the wild, this behavior is likely driven simply by the abundance of exotic snails rather than snail kites preferring exotics. This lack of preference offers insights to hypotheses regarding effects of exotic species, guidance regarding habitat and invasive species management, and illustrates how native-exotic relationships can be misleading in the absence of experimental tests of such interactions.     

Biological control of invasive apple snails by two species of carp: Effects on non-target species matter

Molluscivorous fish, especially carp, have been adopted as bio-control agents of the invasive apple snail Pomacea canaliculata, but previous studies have focused on their effectiveness, with little attention paid to their undesirable effects on non-target plants and animals. We conducted an 8-week mesocosm study to compare the effectiveness of two indigenous fish, common carp (Cyprinus carpio) and black carp (Mylopharyngodon piceus), in removing P. canaliculata, and their potential side effects on macrophytes and non-target mollusks in a freshwater wetland. Three species of macrophytes and a community of mollusks in the wetland sediment were enclosed in 1 × 1 × 1 m enclosures either with apple snails (AS), with apple snails and common carp (AS + CC), with apple snails and black carp (AS + BC), or without apple snails and fish. Both species of carp were effective predators of P. canaliculata, removing most of the individuals in the enclosures except a few that were too big to fit into their mouth. By reducing apple snail population, black carp reduced grazing of apple snail on macrophytes. In contrast, although common carp controlled apple snail population, it did not reduce overall loss in plant biomass as the fish might also fed on macrophytes. Both species of carp preyed on non-target mollusks. Application of bio-control agents in invasive species management needs to consider their effects on both the pest and non-target plants and animals. Adoption of common and/or black carp to control apple snail populations thus depends on the weight given to their effectiveness and subtle different effects on non-target organisms by wetland management authority.     

Predation as the primary selective force in recurrent evolution of gigantism in Poecilozonites land snails in Quaternary Bermuda

During the last half million years, pulses of gigantism in the anagenetic lineage of land snails of the subgenus Poecilozonites on Bermuda were correlated with glacial periods when lower sea level resulted in an island nearly an order of magnitude larger than at present. During those periods, the island was colonized by large vertebrate predators that created selection pressure for large size and rapid growth in the snails. Extreme reduction in land area from rising seas, along with changes in ecological conditions at the onset of interglacial episodes, marked extinction events for large predators, after which snails reverted to much smaller size. The giant snails were identical in morphology during the last two glacials when the predators included a large flightless rail Rallus recessus (marine isotope stages (MIS) 4-2) and a crane Grus latipes and a duck Anas pachysceles (MIS 6). In a preceding glacial period (MIS 10), when the fauna also included the tortoise Hesperotestudo bermudae, the snails were not only large, but the shells were much thicker, presumably to prevent crushing by tortoises. Evolution of Poecilozonites provides an outstanding example of dramatic morphological change in response to environmental pressures in the absence of cladogenesis.     

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.     

Predatory Potential of Freshwater Animals on an Invasive Agricultural Pest, the Apple Snail Pomacea canaliculata (Gastropoda: Ampullariidae), in Southern Japan

The apple snail Pomacea canaliculata is an invasive species and a serious pest of rice in many Asian countries. We studied predatory activities of various animals living in Japanese freshwater habitats, by keeping each individual of a potential predator species with 36 snails of various sizes for three days in the aquarium. Forty-six species were tested, and 26 in eight classes fed on small snails. A species of leech, crabs, the common carp, turtles, the mallard duck and the Norway rat attacked even adult snails of 20–30 mm in shell height. These findings will be helpful in identifying effective predators for biological control of the pest snail. In addition, most of the animals attacking snails are reported to be common in rivers or ponds, but few live in modernized paddy fields having little connections with natural water systems. This may be a reason why this snail maintains large populations in paddy fields but not in other freshwater habitats.     

Mechanisms and consequences of shell fouling in the kelp snail,Norrisia norrisi (Sowerby) (Trochidae): Indirect effects of octopus drilling

The kelp snail, Norrisia norrisi (Sowerby), dwells on the large kelps Macrocystis pyrifera (L.) and Eisenia arborea Areschoug, and is rare on benthic substrata. Approximately 4% of the snail population is dislodged from plants each day. Per capita mortality of snails on the benthos is an order of magnitude greater than individuals on kelp. Even though snails displaced to the bottom actively seek a plant to climb, we found that between 20–40% of marked snails released on the bottom were killed over a 24-day period. While most N. norrisi are free of epibionts on their shells, ≈30% of the population are encrusted by the barnacle Megabalanus californicus (Pilsbry). The majority of barnacle fouling was the result of failure by Octopusbimaculatus (Verrill) to kill Norrisia norrisi; barnacle cyprids settled in octopus drill holes in the shells of live kelp snails. N. norrisi encrusted by barnacles were less effective in exploiting kelp compared with unfouled snails. Moderately to heavily fouled snails were dislodged from kelp twice as frequently and remained on the benthos much longer than snails without epibionts. Laboratory tests revealed that escape velocities of N. norrisi from asteroid predators were much reduced by shell fouling, and that snails carrying barnacles were most likely to be captured and consumed. Hence octopus increase mortality of kelp snails in two ways. First, octopus can kill N. norrisi encountered on the bottom. Second, kelp snails drilled by octopus, but not killed outright, will become fouled by barnacles. This results in a subsequent risk of mortality from all benthic predators that is at least 8-fold greater than for unfouled kelp snails.     

The effect of calcium and pH on Florida apple snail, Pomacea paludosa (Gastropoda: Ampullariidae), shell growth and crush weight

Pomacea (Ampullariidae) snails, commonly referred to as apple snails, serve as prey for many freshwater-dependent predators, and some species are highly invasive. Identifying limits to apple snail distribution and abundance are pertinent to understanding their ecology. Calcium (Ca²⁺) availability and pH generally influences freshwater snail populations, yet scant data exist for Pomacea snails. We measured 6-week change in shell length (ΔSL) in P. paludosa in two laboratory experiments with varying Ca²⁺ and pH levels. ΔSL was significantly higher in ≥28 mg Ca²⁺/l compared with treatments ≤14 mg/l. Snails from populations living in low Ca²⁺/pH waters did not appear genetically predisposed at growing faster in these conditions. Smallest ΔSL was in snails treated with 3.6 mg Ca²⁺/l and pH < 6.5 water; these snails had signs of shell erosion. Shell crush weights (CWs) were lowest for snails grown in the lowest Ca²⁺/pH treatment. Smaller shells and lower CWs have implications for predation vulnerability and reproductive success. Our results are consistent with reports associating relatively low snail densities with relatively low Ca²⁺/pH waters, and they are consistent with the geographic distribution of P. paludosa as related to the underlying water chemistry as influenced by geology.     

Some evidence for different ecological pressures that constrain male and female body size

The dwarf morph of the Lake Tanganyika cichlid Telmatochromis temporalis uses empty snail shells as shelters and breeding sites in shell beds, in which many empty shells exist. Here, we assessed selection forces regulating body size in this fish. Field observations showed that large males tended to have a greater number of females in their territories, suggesting that sexual selection favours large males. Nonetheless, a transplant experiment suggested that male body size was limited by the ability to hide in empty shells from large piscivorous fish. In females, the number of ovarian eggs increased with body size, suggesting that fecundity selection favours large females. However, females are smaller than males. Females spawned eggs close to the apices inside the shells. The small space there would decrease the risk of egg predation by egg predators, and small body size of females may be a result of adaptation to spawn eggs in the small, safe spaces. This study provides support for the idea that male and female body sizes have been limited by different ecological pressures (predation on adult fish in males, predation on eggs in females), which has not been reported previously in any animal.     

Native and non-native fish predators differ in their consumptive and non-consumptive impacts on a native freshwater snail

Aquatic Ecology - Florida apple snails, Pomacea paludosa, serve as the nearly exclusive prey for the endangered Florida snail kite, Rostrhamus sociabilis, and many other predators in Florida...     

Predation on freshwater snails in Miocene Lake Steinheim: a trigger for intralacustrine evolution?

Shells of the freshwater gastropods Gyraulus trochiformis (Planorbidae or ramshorn snails) and Bania pseudoglobula (formerly Pseudamnicola, Hydrobiidae) from Miocene Steinheim Basin in SW Germany contain small holes with a mean diameter of 0.8 mm. Analyses of comparable holes are so far unknown from fossil or extant assemblages of freshwater shells. This analysis of the perforated shells suggests that the holes were not formed by post‐depositional or pure taphonomic processes. Instead, they were most likely produced by predators. This analysis widens the means for identification of predation on freshwater snail shells that can be used in other palaeolimnological studies. The co‐occurrence of fish teeth and perforated shells in the studied samples as well as the perforation features suggest that the predator was either barbel or tench fish. The correlation between shell sizes and hole diameters suggests a size relationship between predator and prey that may generally be related to gape‐limited fish predators. The co‐occurrence of perforated shells in these lake sediments with a dominance of large and armoured shells suggest that these larger shells with protuberances and knobs could not be crushed by the gape‐limited fish predators. This analysis is the basis for a hypothesis that the endemic evolution of Gyraulus in Lake Steinheim, with some varied forms of shell thickness and morphology, was triggered by a predator–prey relationship based on adaptations to avoid shell‐breaking predators.