How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species

1. How species reach and persist in isolated habitats remains an open question in many cases, especially for rapidly spreading invasive species. This is particularly true for temporary freshwater ponds, which can be remote and may dry out annually, but may still harbour high biodiversity. Persistence in such habitats depends on recurrent colonisation or species survival capacity, and ponds therefore provide an ideal system to investigate dispersal and connectivity. 2. Here, we test the hypothesis that the wide distributions and invasive potential of aquatic snails is due to their ability to exploit several dispersal vectors in different landscapes. We explored the population structure of Physa acuta (recent synonyms: Haitia acuta, Physella acuta, Pulmonata: Gastropoda), an invasive aquatic snail originating from North America, but established in temporary ponds in Doñana National Park, southern Spain. In this area, snails face land barriers when attempting to colonise other suitable habitat. 3. Genetic analyses using six microsatellite loci from 271 snails in 21 sites indicated that (i) geographically and hydrologically isolated snail populations in the park were genetically similar to a large snail population in rice fields more than 15 km away; (ii) these isolated ponds showed an isolation‐by‐distance pattern. This pattern broke down, however, for those ponds visited frequently by large mammals such as cattle, deer and wild boar; (iii) snail populations were panmictic in flooded and hydrologically connected rice fields. 4. These results support the notion that aquatic snails disperse readily by direct water connections in the flooded rice fields, can be carried by waterbirds flying between the rice fields and the park and may disperse between ponds within the park by attaching to large mammals. 5. The potential for aquatic snails such as Physa acuta to exploit several dispersal vectors may contribute to their wide distribution on various continents and their success as invasive species. We suggest that the interaction between different dispersal vectors, their relation to specific habitats and consequences at different geographic scales should be considered both when attempting to control invasive freshwater species and when protecting endangered species.     

Field observations of the alarm response to crushed conspecifics in the freshwater snail Pomacea canaliculata: effects of habitat,vegetation, and body size

The freshwater snail Pomacea canaliculata shows alarm responses to chemical cues released from injured conspecifics, but its behavioural responses in the field are unknown. We investigated effects of habitat (canals or paddy fields), vegetation, and body size on alarm responses in the field. Snails responded to crushed conspecifics within 4 min by burying themselves, but the proportions of self-buried snails were generally lower (0–28% depending on experiments) than those reported in the laboratory. Snails not only showed the alarm response, but also frequently fed on crushed conspecifics. There were no influences of habitat or body size on the proportions of individuals showing the alarm response. Nevertheless, in paddy fields with high-density vegetation a higher proportion of snails showed the alarm response than in paddy fields with low-density vegetation.     

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.     

Complex interactions among fish, snails and macrophytes: implications for biological control of an invasive snail

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

鄱阳湖沿岸带螺类的物种组成及其生境

2011年5月和6月在鄱阳湖沿岸带的62个样点采集了淡水螺类样本并调查了生境类型,分析了淡水螺类的物种组成及其生境分布特征。结果表明:共采集到淡水螺类19种,分属田螺科（8种）、觿螺科（8种）、椎实螺科（2种）和黑螺科（1种）。与前人的研究相比,本次调查的螺类物种数有较大的下降,但田螺科和觿螺科的物种仍是整个螺类群落的主要组成部分。淤泥生境的螺类物种组成与其他生境的差异较大,淤泥生境的螺类物种丰富度显著高于沙土、砂石和水草3种生境（P0.05）,表明螺类对生境具有一定的栖息偏好性。最后详细讨论了淡水螺类种数变化、物种组成及其生境分布的影响因素。       

An experimental investigation of interactions in snail-macrophyte-epiphyte systems

Summary An experimental investigation under field conditions of enclosures containing freshwater pulmonate snails, the macrophyteCeratophyllum demersum and epiphytes, produced evidence of beneficial interactions.Ceratophyllum growth, measured in terms of stem length, numbers of leaf-nodes and growing tips and leaf survival was significantly enhanced in the presence of snails. This effect was attributed to the increased availability of plant nutrients of snail origin, such as phosphates and ammonia, as well as to the snails' action as “cleaning symbionts” in reducing the density of bacterial and algal epiphyton potentially deleterious to macrophytes. Principal component analysis revealed both seasonal and treatment effects of snail grazing on algal epiphyton. Small adnate algal species (e.g.Cocconeis placentula) survived grazing and benefited from the removal of larger, competitor, species. Snail densities increased in all treatments, despite high (86%) juvenile mortality. It is concluded that freshwater pulmonate snails are strong interactors in lentic habitats, enhancing the growth ofCeratophyllum and producing characterisic epiphyte communities. This benefits not only the snails, but also the plants and epiphytes that are associated with them. Thus the interactions between these component parts of the community can be considered as mutualistic.     

A preliminary investigation into the use of the invasive golden apple snail,Pomacea canaliculata (Lamarck, 1822), as a water purifier and food source in the breeding ponds of the oriental weatherloach Misgurnus anguillicaudatus (Cantor, 1842)

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

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.     

The maintenance of shore-level size gradients in an intertidal snail (Littorina sitkana)

Summary The size of many intertidal animals varies with tidal height. These size gradients could be produced by growth or survival varying with tidal height, or by animals moving to a preferred tidal level. The body size of the snail, Littorina sitkana, increases steadily with tidal height in rocky high intertidal habitats of British Columbia. To determine how size gradients were maintained in L. sitkana, I quantified how growth, survival, and snail movement varied with tidal height. I studied populations of L. sitkana found on sheltered pebble beach and exposed basaltic shelf habitats. Mark-recapture studies and experimental transplants showed that growth could not have produced the size gradients because snail growth rates in both habitats were as fast or faster at low tidal levels (where the snails were the smallest) than at high tidal levels. However, survival rates were lowest at low tidal levels. On pebble beaches, this was due to size selective predation on large snails by the pile perch, Rhacochilus vacca. On basaltic shelves, heavy wave action at low tidal levels may have caused the poor survival rates. Transplanted snails moved homeward on pebble beaches, but not on basaltic shelves. Reduced survival rates at low tidal levels cause size gradients in both habitats, and snail movement helps to maintain size gradients on pebble beaches.     

Predation and the distribution and abundance of a pulmonate pond snail

Summary The abundances of a freshwater pulmonate snail, Lymnaea elodes were studied in a temporary pond and a permanent, more productive pond in northeastern Indiana, USA. When snails from both populations were reared in each of the ponds in containers excluding predators, snails grew to be 1.3 to 2 times as large in the more productive pond, and laid 9 times as many eggs. However, field sampling data showed adults to be more abundant in the temporary pond. The only obvious difference between the two ponds was the presence of the molluscivorous central mudminnow (Umbra limi) in the permanent pond. These fish fed upon L. elodes when eggs and juvenile snails were abundant. In an experiment in the temporary pond, addition of mudminnows lowered egg and juvenile snail survival in pens where snail abundances had been increased. We suggest that vertebrate predators like the mudminnow can be significant sources of mortality for thin shelled species like L. elodes, possibly excluding them from habitats like lakes and rivers.Address for offprint requests     

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.     

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.     

Freshwater population of Ulva flexuosa (Ulvaceae,Chlorophyta) as a food source for great pond snail: Lymnaea stagnalis (Mollusca,Lymnaeidae)

Cosmopolitan species of the genus Ulva (Ulvaceae; Chlorophyta) that populate the littoral zone of marine habitats constitute a staple diet for a variety of organisms, particularly snails, shellfish, polychaetes, and birds. Occurrence of Ulva species (e.g., U. flexuosa and U . prolifera) has also been observed in freshwater inland ecosystems that have no contact with saline water. However, the influence of the development of macroalgal mats of Ulva on indigenous organisms in limnic ecosystems has not been established. This study investigates the trophic relationships between Ulva flexuosa and one species of snail from freshwater habitats in central Europe. During the summer, the great pond snail (Lymnaea stagnalis) consumed Ulva as a source of nutrition even when other algae and plants were available. Lymnaea stagnalis consumed an average of 100 mg of Ulva thalli per day. This level of biomass exceeded the consumption of an alternative food source, the shoots of Elodea canadensis. Ulva thalli are more actively consumed by great pond snails than Elodea shoots, and this is expressed in terms of the differences of biomass consumption. It was also observed that the interior of the monostromatic tubular thalli of Ulva flexuosa serves as a protective shelter for juvenile great pond snails.     

Leech predation on juvenile freshwater snails: effects of size,species and substrate

Summary The leechGlossiphonia complanata does not appear to have substantial impact on snail populations, but this may be due to most studies focusing on adult snails rather than juvenile snails. In this study I investigated how predation rates ofG. complanata feeding on newly-hatched and juvenile snails was affected by snail species, snail size, snail density and substrate, in a laboratory experiment. Number of snails eaten increased with increasing density resulting in a type II functional response curve. Predation rates were higher when leeches were feeding onLymnaea emarginata than onPhysa gyrina, whereas there was no significant difference in predation rates when they were feeding onL. emarginata andHelisoma anceps. Sandy substrates and greater snail size resulted in decreased predation rates. Sand reduced movement speed ofG. complanata, which probably reduced encounter rates. Thus, there was a comparatively large effect of leech predation on newly-hatched snails, due to a high probability of encounter and high predation rates, but spatial and temporal refuges probably reduce the importance of leech predation as a structuring force in freshwater snail assemblages.     

Genetic variation in sexual and clonal lineages of a freshwater snail

Sexual reproduction within natural populations of most plants and animals continues to remain an enigma in evolutionary biology. That the enigma persists is not for lack of testable hypotheses but rather because of the lack of suitable study systems in which sexual and asexual females coexist. Here we review our studies on one such organism, the freshwater snail Potamopyrgus antipodarum (Gray). We also present new data that bear on hypotheses for the maintenance of sex and its relationship to clonal diversity. We have found that sexual populations of the snail are composed of diploid females and males, while clonal populations are composed of a high diversity of triploid apomictic females. Sexual and asexual individuals coexist in stable frequencies in many ‘mixed’ populations; genetic data indicate that clones from these mixed populations originated from the local population of sexual individuals without interspecific hybridization. Field data show that clonal and sexual snails have completely overlapping life histories, but individual clonal genotypes are less variable than individuals from the sympatric sexual population. Field data also show segregation of clones among depth‐specific habitat zones within a lake, but clonal diversity remains high even within habitats. A new laboratory experiment revealed extensive clonal variation in reproductive rate, a result which suggests that clonal diversity would be low in nature without some form of frequency‐dependent selection. New results from a long‐term field study of a natural, asexual population reveal that clonal diversity remained nearly constant over a 10‐year period. Nonetheless, clonal turnover occurs, and it occurs in a manner that is consistent with parasite‐mediated, frequency‐dependent selection. Reciprocal cross‐infection experiments have further shown that parasites are more infective to sympatric host snails than to allopatric snails, and that they are also more infective to common clones than rare clones within asexual host populations. Hence we suggest that sexual reproduction in these snails may be maintained, at least in part, by locally adapted parasites. Parasite‐mediated selection possibly also contributes to the maintenance of local clonal diversity within habitats, while clonal selection may be responsible for the distribution of clones among habitats. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 79 , 165–181.     

Refuge function of marine algae complicates selection in an intertidal snail

Species with restricted gene flow often show trait-shifts from one type of environment to another. In those rock-dwelling marine gastropods that lack larval dispersal, size generally decreases in wave-exposed habitats reducing risk of dislodgement, while increases in less exposed habitats to resist crab-crushing. In Littorina fabalis, however, snails of moderately exposed shores are generally much larger (11–14 mm) than snails of sheltered shores (5–8 mm). Observations from the White Sea (where crabs are not present) indicate that in the absence of crabs snails are small (6–7 mm) in both habitats. We assumed that the optimal size for L. fabalis in the absence of crabs is less than 8 mm, and thus that increased size in moderately exposed habitats in areas with crabs might be a response to crab predation. In a crab-rich area (Sweden) we showed that crab predation is an important mortality factor for this snail species in both sheltered and moderately exposed habitats. In sheltered habitats, snails were relatively more protected from crab-predation when dwelling on their habitual substrate, fucoid algae, than if experimentally tethered to rocks below the algae. This showed that algae function as snail refuges. Snail dislodgement increased, however, with wave exposure but tethering snails in moderately exposed habitats showed that large snails survived equally well on rocks under the algae as in the canopy of the algae. Thus in sheltered habitats a small snail size is favored, probably due to life-history reasons, while increased risk of being dislodged from the algae refuges promotes a large size in moderately exposed habitats. This study shows an example of selection of a trait depends on complex interactions of different factors (life-history optimization, crab predation, wave induced dislodgement and algal refuges).     

Phenotypic plasticity in reproductive traits: importance in the life history of Helix aspersa (Mollusca: Helicidae) in a recently colonized habitat

Reproductive traits of the land snail Helix aspersa Mtiller were investigated under artificial conditions from two samples, one collected from a population exposed to unpredictable human pressures in its natural environment, i.e. a recently created polders area with intensive agriculture, and the other from a snail farm in which animals were reared under constant conditions denned as 'optimal' for growth and reproduction. Results were compared with data collected from natural populations of the same region (Brittany) and from habitats spanning the environmental heterogeneity of the range of the species. A large part of the variation among populations could be explained by different phenotypic covariances between shell size, clutch size and egg size, but not by the number of clutches per snail. Thus, the higher egg production of snails from the polders was related to (i) a strong correlation between clutch size and shell size, shell size being in the upper limit of the overall range for the region concerned; (ii) an uncommonly low egg weight in comparison with the 'norm' of Helix aspersa , this trait seeming to be involved in a trade-off with clutch size. Second clutches were smaller than the first ones, but their eggs were significantly heavier. This difference may be linked to a size-dependent mortality of juveniles during winter which arises in all populations in which hibernation occurs as an adaptation to low temperatures. In addition to the selective regime usually involved for populations of helicid snails from Western Europe, several unpredictable mortality factors occurred in the polders area: herbicide and pesticide treatments (lethal for young snails), human predation (lethal for adults) and burning (letiial for all snails). Life-history patterns of Helix aspersa are discussed in relation to its ability to successfully colonize a large range of habitats modified by humans, to such an extent that it can become a pest.     

Biological control of Salvinia by the snail Pila globosa Swainson

The recent spread of Salvinia molesta , a free floating weed in tropical and sub-tropical regions has attracted attention the world over. In India, many states face serious problems on account of Salvinia infestation. Several methods of controlling the weed have been tried, but with limited success. Biological control by snails, especially Pila globosa , a common tropical snail found in Kerala and other parts of India is suggested. It was found to feed voraciously on Salvinia , but not on paddy which forms a major crop in Kerala and other parts of India. The snail has efficient adaptations for a tropical environment in aquatic, semi-aquatic and even terrestrial habitats and its flesh is edible. Further studies on the performance of the snails in the field are, however, required.     

Chemical cues modify species interactions: the ecological consequences of predator avoidance by freshwater snails

Chemical signals released by predators or injured prey often induce shifts in the traits of prey species, which may in turn affect species interactions. Here we investigate the role that chemical cues play in mediating species interactions in the littoral food web of lakes. Previous studies have shown that predators induce shifts in the morphology, life history, and behavior of the freshwater snail Physella, but the ecological consequences of developing these inducible defenses are not well documented. We observed habitat use of the freshwater snail Physella gyrina along a depth gradient in a natural lake, and found they increased their use of covered habitats with increasing depth. We hypothesized that this habitat shift was due to changes in the level and type of predation risk, and that the habitat shift would affect periphyton standing crops. These hypotheses were tested in a mesocosm experiment in which we manipulated the presence of molluscivorous fish and crayfish. Predators were confined to cages and snail density was identical in all treatments, so any effects of predators were mediated through trait shifts induced by chemical cues. In the presence of fish, Physella moved under cover, but in the presence of crayfish, Physella avoided cover and moved to the water surface. These non‐lethal effects of predators on snail habitat use influenced the interaction between snails and their periphyton resources. In the presence of fish, periphyton standing crop in covered habitats was reduced to just 8% of periphyton in the absence of fish. Crayfish had no significant effect on periphyton in covered habitats, but they reduced periphyton in near‐surface habitats to 39% of the standing crop in the absence of crayfish. The combined effects of fish and crayfish were generally intermediate to their individual effects. We conclude that because chemical cues often have strong effects on individual traits and trophic interactions are sensitive to trait values, chemical cues may play an important role in shaping the structure and dynamics of food webs.     

Fleeing towards death – leech‐induced behavioural defences increase freshwater snail susceptibility to predatory fish

Prey species are often exposed to multiple predators, which presents several difficulties to prey species. This is especially true when the response to one predator influences the prey’s susceptibility to other predators. Predator‐induced defences have evolved in a wide range of prey species, and experiments involving predators with different hunting strategies allow researchers to evaluate how prey respond to multiple threats. Freshwater snails are known to respond to a variety of predators with both morphological and behavioural defences. Here we studied how freshwater snails Radix balthica responded behaviourally to fish and leech predators, both separately and together. Our aim was to explore whether conflicting predator‐induced responses existed and, if so, what effect they had on snail survival when both predatory fish and leeches were present. We found that although R. balthica increased refuge use when exposed to predatory fish, they decreased refuge use when exposed to predatory leeches. When both predators were present, snails showed a stronger response towards leech than fish and responded by leaving the refuge. This response made the snails more susceptible to fish predation, which increased snail mortality when exposed to both fish and leech compared to fish only. We show that predators that have a relatively low predation rate can substantially increase mortality rates by indirect effects. By forcing snails out of refuges such as rock and macrophyte habitats, leeches can indirectly increase predation from molluscivorous fish and may thus affect snail densities.