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.     

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.     

Effects of aggregative behaviour on the bioenergetics of the freshwater predatory leech Nephelopsis obscura (Erpobdellidae)

1. Supplied with ad libitum prey, the effects of different group sizes (one, five, ten, twenty-five, fifty or 100) on the acquisition and allocation of energy were examined over the entire life cycle of the freshwater predatory leech Nephelopsis obscura , to evaluate the bioenergetic costs and/or benefits of aggregation.
2. In terms of growth, asymptotic biomass and ingestion, group sizes larger than one and less than ten are optimal. As group size increases from ten to 100, N. obscura has slower growth and lower weekly food ingestion, suggesting interference competition. Single leeches had lower food consumption than group sizes of less than 100 animals. With a lower asymptotic biomass, single leeches have lower fecundity and presumed lower fitness. Lipid deposition was unaffected by group size.
3. Size- and time-specific respiration rates declined with increasing group size. For group sizes between five and fifty, the same relative proportion of ingested energy was allocated to respiration. Above this threshold group size, leeches allocated a higher proportion of ingested energy to growth, i.e. had higher growth efficiency, as did leeches cultured individually.
4. In the largest group size, total time spent in activity was highest (reflecting the high degree of interference between conspecifics), but as a result of the lower hourly costs of respiration they allocated a lower proportion of ingested energy to total respiration.
5. Optimum group size of N. obscura in the laboratory is within the typical range of group sizes found on stony shores in the field.     

Effects of aggregative behaviour on the bioenergetics of the freshwater predatory leech Nephelopsis obscura (Erpobdellidae)

1. Supplied with ad libitum prey, the effects of different group sizes (one, five, ten, twenty-five, fifty or 100) on the acquisition and allocation of energy were examined over the entire life cycle of the freshwater predatory leech Nephelopsis obscura , to evaluate the bioenergetic costs and/or benefits of aggregation.
2. In terms of growth, asymptotic biomass and ingestion, group sizes larger than one and less than ten are optimal. As group size increases from ten to 100, N. obscura has slower growth and lower weekly food ingestion, suggesting interference competition. Single leeches had lower food consumption than group sizes of less than 100 animals. With a lower asymptotic biomass, single leeches have lower fecundity and presumed lower fitness. Lipid deposition was unaffected by group size.
3. Size- and time-specific respiration rates declined with increasing group size. For group sizes between five and fifty, the same relative proportion of ingested energy was allocated to respiration. Above this threshold group size, leeches allocated a higher proportion of ingested energy to growth, i.e. had higher growth efficiency, as did leeches cultured individually.
4. In the largest group size, total time spent in activity was highest (reflecting the high degree of interference between conspecifics), but as a result of the lower hourly costs of respiration they allocated a lower proportion of ingested energy to total respiration.
5. Optimum group size of N. obscura in the laboratory is within the typical range of group sizes found on stony shores in the field.     

The impact of vertebrate and invertebrate predators on a stream benthic community

I assessed the impact of both vertebrate and invertebrate predators on a lotic benthic community in a 1-month-long experiment, using enclosures containing cobble/gravel bottoms, with large-mesh netting that allowed invertebrates to drift freely. Brown trout (Salmo trutta) and leeches (Erpobdella octoculata) were used as predators and four treatments were tested: a predator-free control, leeches only, trout only, and leeches and trout together. A density of 26.7 leeches/m² (20 leeches/enclosure) and 1.3 trout/m² (one trout per enclosure) was stocked into the enclosures. The total biomass of invertebrate prey was significantly lower in the trout and trout plus leech treatments than in the leech and control treatments, which were due to strong negative effects of trout on Gammarus. On the individual prey taxon level, both trout and leeches affected the abundance of Asellus , Baetis and Ephemerella, whereas the abundance of Gammarus was only affected by trout, and the abundance of Orthocladiinae and Limnephilidae was only affected by leeches. In the treatment with trout and leeches together, the abundance of Ephemerella and Baetis was higher than when trout or leeches were alone, which was probably due to predator interactions. Leeches and trout had no effects on prey immigration but did affect per capita emigration rates. Both trout and leeches indirectly increased periphyton biomass in enclosures, probably due to their strong effects on grazers. Both trout and leeches were size-selective predators, with trout selecting large prey, and leeches selecting small prey. Size-selective predation by trout and leeches affected the size structure of five commonly consumed prey taxa. Trout produced prey populations of small sizes owing to consumption of large prey as well as increased emigration out of enclosures by these large prey. Leech predation produced prey assemblages of larger size owing to consumption and increased emigration of small prey. These results suggest that in lotic habits, predatory invertebrates can be as strong interactors as vertebrate predators. Received: 23 June 1997 / Accepted: 4 May 1998     

Contrasting mortality in young freshwater leeches and triclads

A guild of leeches and triclads coexist and are the most numerous invertebrate predators on the stony shores of productive British lakes. Populations of all species are food-limited. Mortality of recruited young is considerably higher in leech than in triclad populations, and this paper investigates reasons for this. In particular, the feeding success of young leeches and triclads in relation to prey species, prey size, prey condition (alive or crushed), spatial heterogeneity (with or without the presence of stones or gravel), and the presence or absence of other young or adults predators (leeches or triclads) of the same or different species are investigated in the laboratory. Feeding success by young leeches and triclads on crushed prey without the presence of stones was high, but declined dramatically in leeches but not triclads when stones were present. Young leeches and triclads were inept at capturing live prey, of a small or large size, with the exception of soft-bodied prey such as oligochaetes. Feeding success by young predators on live prey was not increased by the presence of other young predators of the same or different species. With only a few exceptions, the presence of adult leeches, and to a much lesser extent adult triclads, increased the feeding success, growth and survival of young leeches and triclads. It is concluded that the high mortality of young leeches, compared to triclads, in field populations is due to their inability to locate damaged food in an environment with spatial heterogeneity due to a poorly developed chemosensory system. High and low levels of juvenile morality are accompanied by high and low reproductive rates in leech and triclad populations, respectively. It is unusual for a food limited population to have a high level of recruitment, but it is speculated that the characteristically high reproductive output in parasitic leeches, from which predaceous leeches are derived or have affinities, has been retained to counterbalance high juvenile mortality rates.     

Are the lake-dwelling leeches,Glossiphonia complanata (L.) and Helobdella stagnalis (L.), opportunistic predators on molluscs and do they partition this food resource?

SUMMARY. 1. Predation on the mollusc genera Potamopyrgus, Bithynia, Valvata, Lymnaea, Physa, Planorbis and Pisidium by the leeches Glossiphonia complanata (L.) and Helobdella stagnalis (L.) was examined in five eutrophic lakes at monthly intervals over one year using a serological technique.
2. Feeding intensity varied seasonally, being lowest in winter and highest in summer. Small, medium and large leeches preyed to the same extent on the several mollusc genera; this was true for both leech species. Qualitatively, the diet of both glossiphoniids was similar throughout the year. Snail genera were consumed in proportion to their relative abundance in the field. Quantitatively, Glossiphonia preyed more heavily on snails than did Helobdella.
3. It is concluded that both leech species are opportunistic predators.     

Development of empirical feeding models for a benthic predator

Feeding on Chironomus riparius, Glyptotendipes paripes (Chironomidae). and Daphnia magna by the predatory freshwater leech, Nephelopsis obscura , was investigated in the laboratory and predictive models developed to estimate prey capture rate in the field. Experimental arena (container) size significantly affected predation rates when arena diameter was less than twice the total body length of the predator. Both chironomid and Daphnia magna capture rates were influenced by predator size, temperature and prey density.     

Study on foraging mechanism of leeches with different feeding habits based on chemoreception and foraging behavior

The leeches Whitmania pigra and Hirudo nipponia live in similar environments but have different feeding habits. At present, there are few studies of the foraging mechanism of leeches with different feeding habits. In this study, we first used maze tests to show that these two species of leeches could locate and distinguish their prey through chemosensory activity without mechanical stimulation. However, the two leech species have different foraging behaviors: Individuals of W. pigra move slowly and repeatedly adjust direction through probing and crawling to detect the location of prey (snails), whereas individuals of H. nipponia move quickly, and after determining the location of food (porcine blood), they quickly swim or crawl to the vicinity of their prey. Scanning electron microscopy (SEM) revealed that there are two types of sensory cilia and pore structures related to mucus secretion in the heads of both leeches. There are two differently sized types of chemoreceptors on the dorsal lip in W. pigra, which may have different functions during foraging, whereas in H. nipponia there is only one type of chemoreceptor, which is small. We detected the chemical components in the natural food of these two leech species by UHPLC–MS. There were 934 metabolites in the body fluid of snails and 751 metabolites in porcine serum; five metabolites unique to the body fluid of snails and to porcine serum were screened as candidate feeding attractants. Of these metabolites, betaine and arginine effectively attracted individuals of W. pigra and H. nipponia, respectively. In summary, leeches with different feeding habits use chemoreceptors to sense external chemical signals when foraging, and there are significant differences between species in foraging behavior, chemoreceptors, and attractants.     

Predation on leeches in a weedy pond

SUMMARY. 1. A range of sizes of Erpobdelta octoculata fL.), Glossiphonia complanata (L.) and Helobdella stagnalis (L.) were introduced to a small weeded pond harbouring invertebrate and amphibian predators. Control leeches were kept in protective cages. Subsequently, gut contents of potential predators were tested against three anti-leech sera, using the precipitin test. Five of fifteen species tested had fed on leeches; Agabus, Pyrrhosoma, Aeshna, Sympetrum and larval Trilurus.
2. The size distributions of introduced and surviving leeches were compared. Predation pressure had been greatest on smaller leeches and this may have accounted for the observed differential mortality between leech species.
3. It is concluded that predation may cause significant mortality in leech populations in weeded ponds, with severity determined by the types and abundance of predators present.     

Serine protease inhibitors of North American leeches

Serine protease inhibitors in extracts from three North American leeches, Nephelopsis obscura, Erpobdella punctata and Hemopis marmorata have been separated by anion exchange chromatography and the activity pattern against human granulocyte elastase and porcine chymotrypsin and trypsin determined. All three leech species contained a major peak with anti-trypsin activity, but Hemopis was unique in that the trypsin inhibitor was equally active against chymotrypsin. Nephelopsis was rich in anti-elastase activity of two types, one which was also active against chymotrypsin, and one which was a specific elastase inhibitor. Erpobdella contained inhibitors against elastase and chymotrypsin but with major activity against the latter.     

The Feeding Strategies of the Leech Erpobdella octoculata (L.): A Laboratory Study

The feeding behaviour of the freshwater leech Erpobdella octoculata was analysed by exposing potential invertebrate and vertebrate prey organisms (alive, wounded or dead) to leech attack in dishes, in the laboratory. The fact that E. octoculata is a macrophagous feeder that swallows living prey organisms whole (preferentially Chironomus larvae) is documented. However, it was repeatedly observed that adult leeches sucked the body fluids from wounded larvae. Likewise, cut pieces of earthworms, dead crustaceans and crushed water snails were attacked and the soft parts sucked in with the aid of the unarmed pharynx. Adult leeches sucked the body fluids from dead, decaying bodies of vertebrates (fish, newt larvae). Newly hatched young are blood suckers that rapidly attacked the wounded regions of Chironomus larvae and other invertebrates such as crushed water snails. It is concluded that the common leech E. octoculata is not only a predator, but also a fluid sucker and a scavenger. The ecological implications of this finding are discussed.     

Interactions between the leech Glossiphonia complanata and its gastropod prey

Summary Predator-prey interactions between the predatory leech, Glossiphonia complanata, and its gastropod prey were investigated in laboratory experiments, including behavioural observations with the aid of time-lapse video technique. Six gastropod species were investigated, viz. Lymnaea peregra, Planorbis planorbis, Physa fontinalis, Ancylus fluviatilis, Bithynia tentaculata, and Theodoxus fluviatilis. The species studied exhibited anti-predator defences, which had their maximum efficiency at different stages of encounter with G. complanata. The activity of B. tentaculata decreased with increasing leech activity, but was relatively higher when food was present than when not. Handling times were dependent on the time elapsed since the previous meal was captured (intercatch interval), which in turn was related to the size of the previous prey. Handling time was also related to the size of both predator and prey. The capture efficiency was high for small prey and the leeches spent more time in patches with higher yield. They were, however, unable to discriminate between patches of different prey density.     

Biological control of the exotic invasive snail Pomacea canaliculata with the indigenous medicinal leech Whitmania pigra

The apple snail Pomacea canaliculata has been an invasive species in China for decades and causes enormous losses to agriculture. The predation capability of the leech Whitmania pigra on P. canaliculata was studied for its economic benefit and potential application. In the present study, the leech W. pigra exhibited a strong predatory capacity in controlling P. canaliculata under both laboratory and field conditions, and it showed no bias towards consuming smaller snails during the experiments. More than 80% of the 80 snails (of which half had reached maturity) were preyed upon by 20 developing leeches (2–7?g) in miniature rice fields over a 15-day period, and the number of rice seedlings damaged by P. canaliculata was decreased in the presence of W. pigra. In a separate experiment, 15 developing snails were exposed to caged leeches and conspecific snails for four weeks. The food intake and growth of P. canaliculata were inhibited under the predation risk imposed by W. pigra, but the feeding rate, food conversion efficiency and survival of P. canaliculata were not conspicuously influenced.     

Competitive interactions between the lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis: an experimental investigation of the significance of a food refuge

The glossiphoniid leeches Helobdella stagnalis and Glossiphonia complanata co-exist on the stony shores of British lakes. Because both species have a similar life-style and are food limited, the question arises as to how coexistence persists. Laboratory experiments investigated if either leech has a competitive advantage on three foods, viz. oligochaete worms (Tubifex sp.), snails (Lymnaea peregra), and a worm-plus-snail mixture. A variety of densities with a range of ratios of the two leeches, and monospecific controls were used. The level of feeding ensured increasing food shortage with rising leech density. Experiments, conducted at 14° C, lasted 3 months. Regression values for growth against density in the controls indicated the occurrence of intraspecific competition in both leech species. Light mortality occurred at the highest densities. G. complanata gained significantly less weight in mixed leech cultures than in monospecific cultures at some of the highest densities when fed worms, but more weight when fed on snails. The opposite was true for H. stagnalis. When both prey types were provided, no differences at any density were observed for either leech. Differences in bodysize and feeding strategy between the leeches may be implicated in determining their feeding success on the prey types. Because the anti-predatory responses (e.g. shaking) exhibited by L. peregra are less when encountering an inactive than an active leech, the sit-and-wait strategy of G. complanata may aid snail capture. In contrast, the seek-out strategy of H. stagnalis, coupled with its relatively smaller size, may result in fewer successful captures. The active hunting strategy of H. stagnalis may be advantageous for the capture of oligochaetes which are relatively less mobile than snails. Offering both prey types simultaneously would have had an ameliorating influence on interactions between the two leeches. Findings provide support for the hypothesis that long-term co-existence between the two glossiphoniids in British lakes may depend, in part at least, on the occurrence of a snail food refuge for G. complanata.     

The effect of bladderwort (Utricularia) predation on microcrustacean prey

SUMMARY 1. The effects of the carnivorous plant Utricularia ( bladderwort) on its microcrustacean and macroinvertebrate prey were studied under seminatural and natural conditions. The results suggest that Utricularia is a strong interactor in littoral communities that influences its prey populations by direct predation and indirect facilitation.
2. In an 8-week enclosure experiment, effects on prey density were compared in three treatments with (1) U. vulgaris with intact trapbladders, (2) U. vulgaris without bladders and (3) no Utricularia present.
3. Utricularia predation caused a decrease in prey density over time, whereas presence of Utricularia without bladders increased prey density. In the controls without Utricularia , prey density was relatively constant over time.
4. Field samples were collected to quantify predation rates of three Utricularia species on two natural prey populations. Daily consumption rates on prey peaked from mid-July to mid-August for all Utricularia species, but were low in June and September. This pattern was explained mainly by a high number of trapbladders at this time, but also by a slight increase in the number of prey caught per bladder. Per capita prey mortality rates caused by Utricularia were substantial and ranged between 0.14 and 0.43 day⁻¹ for copepods, 0.1–0.27 day⁻¹ for ostracods and 0.04–0.2 day⁻¹ for chydorid cladocerans.
5. Predation and facilitation effects were observed for total prey and separately for epiphytic and benthic prey. Planktonic microcrustaceans showed no response to Utricularia presence.     

The life history,diet and migration of a lake-dwelling population of the leech Alboglossiphonia heteroclita (L.)

Alboglossiphonia heteroclita has an annual life cycle in Tabley Mere, England. Egg-carrying leeches occurred from early June to mid-July. Young were released from parents in August, and the old cohort died soon after. The mean weight of recruited young increased in early autumn, declined over winter due to low feeding activity, and increased again from early spring until the leeches reproduced.The disappearance of leeches from the littoral zone in winter was due to their migration into deeper waters.Six species of snails collected from shallow and deep waters did not harbour leeches inside their shells or mantle cavities at any time of the year. Laboratory experiments confirmed that the leech does not use snails as a refuge.A serological technique identified the gut contents of field-collected A. heteroclita. Leeches had fed most extensively on oligochaetes followed by snails and then chironomids, lightly on Asellus and caddisflies, and scarcely on amphiphods and cladocerans. In laboratory experiments, in which four prey taxa were offered simultaneously to leeches, the descending order of utilization was oligochaetes, chironomids, Asellus and snails.     

Non-lethal effects of predators on prey growth rates depend on prey density and nutrient additions

A number of studies show that predators can depress prey growth rates by inducing reductions in foraging activity, but the size of this non-lethal effect is quite variable. Here I investigate how prey density and resource productivity may alter the extent to which predators depress the growth rates of their prey. Theory predicts that when resources are overgrazed, an increase in predation risk will have little net effect on individual food intake because the decline in foraging effort will be offset by an increase in resource level. Thus, the non-lethal effects of predators on prey growth rates should depend upon prey density and resource productivity in a predictable manner, with the growth penalty imposed by predators being strongest when resources are undergrazed and weakest when resources are overgrazed. I tested this hypothesis by manipulating predation risk, prey density, and nutrient additions in a mesocosm experiment with the pulmonate snail Helisoma trivolvis . Refuge use by snails was 45% higher in the presence of caged crayfish than in their absence. Snail growth rates were reduced, on average, by 24% in the presence of caged crayfish. However, the magnitude of the growth penalty exacted by crayfish depended on snail density and nutrient additions. When snails were stocked at high density and nutrient additions were low, growth suppression was just 2.6%. At the other extreme, when snails were at low density and nutrient additions were high, growth suppression was 44.6%. Thus, the non-lethal effects of predators on prey growth depend on environmental context, illustrating an important link between individual traits and system-level properties.     

Influence of lake trophic status on the occurrence of microcystin-LR in the tissue of pulmonate snails

1. To assess the influence of lake trophic status on the occurrence of microcystin-LR (MCLR) in the tissue of resident pulmonate snails, we sampled seven lakes of varying primary productivity in Alberta, Canada. Parameters associated with productivity were measured every 2 weeks from mid-May through mid-September 1995. Phytoplankton and resident pulmonate snails were collected and analysed for MCLR concentration via high-performance liquid chromatography.
2. For all species of gastropod (i.e. Lymnaea stagnalis , Helisoma trivolvis and Physa gyrina ), the concentration of MCLR in the tissue was correlated ( P  ≤ 0.03) with toxin in the phytoplankton, but not with extracellular aqueous microcystin ( P > 0.28). The concentrations of toxin in the tissues of L. stagnalis and P. gyrina were also correlated with the relative abundance of Microcystis spp. ( P < 0.01).
3. Given that Microcystis spp. abundance and MCLR concentration within phytoplankton are correlated with indicators of productivity, we conclude that trophic status is important in influencing the occurrence and concentration of MCLR in pulmonate snails.     

Does body size difference in the leeches Glossiphonia complanata (L.) and Helobdella stagnalis (L.) contribute to co-existence?

The effect of predator and prey body size on the feeding success of the British lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis was examined in the laboratory, and any involvement of size difference between the leeches in allowing coexistence in the field assessed. G. complanata breeds in advance of H. stagnalis and maintains a body size advantage throughout their annual life-cycle. In experiments, conducted at 14 °C and a photoperiod of 16 hrs L: 8 hrs D, three size classes of leeches of each species were each exposed to each of three size classes of each of five prey species, viz. Tubifex sp., Chironomus sp., Asellus aquaticus, Lymnaea peregra and Potamopyrgus jenkinsi. For each prey species, three different types of experiments were performed: one leech exposed to four prey individuals; four leeches of the same species with sixteen prey; and two leeches of each species with sixteen prey. In the first experiment, all sizes of G. complanata were capable of feeding on all sizes of the prey types offered; the same was true for H. stagnalis with exceptions of feeding on large A. aquaticus and large L. peregra. For both species, but especially for G. complanata, there was a trend within each size class of leech for decreasing proportions of fed leeches with increasing prey size, and within each size class of prey for an increasing proportion of fed leeches with increasing leech size; however there were several exceptions to these trends. Both leeches fed extensively on Tubifex sp. but there were significant differences in the proportions feeding on other prey types; G. complanata fed more on A. aquaticus and the two snail species, and less on Chironomus, than H. stagnalis. The effect of increasing the number of leech individuals from one to four individuals, of the same or mixed species, had little effect on the proportion of leeches which had fed. It is concluded that large G. complanata will have access to large individuals of certain prey taxa denied H. stagnalis, which may lessen the intensity of interspecific competition.