Food partitioning by lake-dwelling triclads and glossiphoniid leeches: field and laboratory experiments

The triclads Polycelis tenuis and Dugesia polychroa and the glossiphoniid leeches Glossiphonia complanata and Helobdella stagnalis are abundant on the stony shores of productive British lakes. All species are food limited and there is considerable overlap in the diets of these triclads and leeches. This paper investigates interactions between the two groups using field and laboratory experiments to try to identify the mechanism of their co-existence. Triclad and leech numbers were manipulated inside experimental enclosures, mathced by controls, erected on the stony shore of an eutrophic English lake. Increasing the numbers of P. tenuis and D. polychroa prior to the reproductive season in spring resulted in a significant decrease in the numbers and body size of G. complanata and H. stagnalis compared with control populations in the summer months, and vice versa. However, increases and decreases were temporary with a readjustment of numbers and body size to control levels in the autumn after reproduction had ceased. It is suggested that increasing the numbers of either group elevated the severity of both intra- and interspecific competition for food. The condition of prey may, in part, determine the strength of competition, and this was examined in laboratory experiments in which different densities and ratios of P. tenuis and H. stagnalis were offered either live of recently crushed Asellus aquaticus. In monospecific controls, growth rates of P. tenuis were greater when fed on crushed than live Asellus, but there was no significant difference in the growth of H. stagnalis fed either live or crushed prey. In mixed cultures of predators, P. tenuis and H. stagnalis were the superior competitors when fed on crushed and live Asellus, respectively. However, when competitive pressure was low, at low densities of predators, the presence of H. stagnalis in mixed cultures fed on live prey was beneficial to the growth of P. tenuis. These results are explained in terms of the greater ability of triclads to detect damaged prey, leaking body fluids, due to their sophisticated chemosensory system, and the ability of leeches to capture live prey due to the presence of suckers. It is concluded that co-existence of the two groups in British lakes is assisted by the partitioning of food on a live or damaged basis.     

A comparative study of the food niches of lake-dwelling triclads and leeches

The food niches of four species of triclads and three species of non-parasitic leeches living in the littoral zone of British lakes of different trophic status were investigated, over one year, using a serological technique. Antisera against ten potential prey groups were employed. The basic data were adjusted to compensate for differences in predator size and seasonal changes in field temperatures. Data on two of the leech species have been presented elsewhere, but comparisons of the diet of all seven predator species are made in this paper. Much overlap in diet between the various predator species occurs, but, with one exception, each of the genera has a major food resource. The Polycelis spp. feed extensively on oligochaetes, Dugesia polychroa on molluscs, Dendrocoelum lacteum on Asellus, Erpobdella octoculata on chironomids and Glossiphonia complanata on molluscs. Helobdella stagnalis is a generalist feeder. Problems of coexistence of the leech species, and of the leech and triclad species are discussed.     

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.     

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.     

Continuing dispersal of freshwater triclads (Platyhelminthes; Turbellaria) in Britain with particular reference to lakes

1. A survey of lakes in Anglesey and Snowdonia, Wales, in the summer of 1997 recorded changes in the triclad fauna which had occurred since earlier studies in the 1950s and in 1973. Two native species, Polycelis tenuis and Dugesia polychroa, and two immigrants, Planaria torva and especially Dugesia tigrina, have increased their range. The triclad fauna has remained unchanged with time in eleven out of sixteen lakes in Snowdonia, in contrast to only one out of fourteen lakes on Anglesey. This supports the hypothesis produced in the 1950s, that the triclad fauna of the ion-poor, unproductive lakes in Snowdonia would change little with time, being maintained by ecological interactions, whereas the ion-rich, productive lakes on Anglesey, from which native Dugesia spp. and Dendrocoelum lacteum are historically absent, would increase in triclad diversity. 2. An examination of national records for the distribution of D. tigrina and Pl. torva indicated their continuing dispersal in both still and running waters in mainland Britain, with the former species having the greater frequency of occurrence. 3. The reasons for this may be that D. tigrina is (a) more easily dispersed, (b) a more opportunistic, catholic feeder, (c) a more vigorous competitor, (d) able to reproduce asexually and (e) able to prey to some extent on other triclad species, as shown in the laboratory but not yet confirmed in the field. The absence of D. tigrina and Pl. torva from unproductive lakes may be explained in terms of low temperature and feeding mode, and a low standing crop of gastropods, respectively. 4. Seven surveys (1961–1997) of the triclad fauna (six species) of Colemere, England, revealed that D. tigrina was confined to one small area of the littoral zone until the mid-1980s, after which it spread fairly rapidly to occupy the entire shore by 1997. Its expansion has been to the detriment of all the native species, particularly P. tenuis, except Dd. lacteum. The possible extinction of Pl. torva may be linked to a numerical reduction in snails, particularly Potamopyrgus jenkinsi. 5. Dugesia tigrina has an adverse effect on the native triclad fauna in lakes, particularly when only a few species are present. This has been explained in terms of the availability of a wider variety of food. The presence of a larger number of triclad species denies the immigrant food items, particularly crustaceans and snails, the food refuges of Dd. lacteum and Dugesia spp., respectively. However, the long-term study of Colemere has shown that more diverse triclad faunas may also be vulnerable to this immigrant. The effect of Pl. torva on native triclads remains uncertain.     

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.     

A Quantitative Study of the Comparative Distribution of Non-parasitic Leeches and Triclads in the Stony Littoral of British Lakes

For each of the three species of leeches and four species of triclads inhabiting the stony littoral of 100 British lakes of diverse trophic status, numbers, biomass and mean weight were correlated against a wide range of physical, chemical and other variables. Very few significant correlations were found between the various biological variables and the non-chemical variables. Significant, positive correlations were obtained for all leech and triclad variables against all of the chemicals, with the exception of Erpobdella octoculata numbers, Helobdella stagnalis mean weight and all of the Polycelis nigra variables which did not correlate with any. Relationships between biological variables and calcium content are given special consideration. Over the range of lakes investigated, total triclad numbers exceeded leech numbers but the reverse was usually true for total biomass. Correlations between the various leech and triclad variables are examined.     

Competition and coexistance between Glossiphonia complanata and Helobdella stagnalis (Glossiphoniidae: Hirudinoidea)

Summary The prey utilization of Glossiphonia complanata and Helobdella stagnalis from Bruce Lake, Alberta, Canada was examined quantitatively using serological techniques. While considerable prey range overlap occurred between the species, niche overlap was low during the winter, peaked in March and declined through the summer. Temporal differences in feeding and intraspecific weight class differences in prey utilization were found in both species but more distinctly in G. complanata. It is suggested that co-existance of G. complanata and H. stagnalis is based on adjustments of weight class food resource partitioning on a temporal basis.     

Chromosome bands in freshwater triclads

Four species of Triclads belonging to three families, Dugesia polychroa and Dugesia mediterranea (Dugesiidae), Planaria torva (Planariidae) and Dendrocoelum lacteum (Dendrocoelidae) were studied for chromosome banding: C-banding for all the species, ASG banding for Dugesia polychroa and G-banding for Dugesia polychroa and Dugesia mediterranea. C-banding results for Dugesia lugubris-polychroa group suggest a high level of heterochromatin evolution in the group. Small bands strictly limited to the centromeric region were seen in Dugusia lugubris and this pattern is similar to the patterns of some species belonging to other families, notably Planaria torva and Dendrocoelum lacteum. This could be considered a primitive character. In contrast numerous heterochromatin bands which are useful to characterize the different karyotypes were seen in Dugesia polychroa and Dugesia mediterranea. Our data suggest that heterochromatin is important in freshwater triclad speciation.     

Effects of Ration and Temperature on Reproduction of a Semelparous and an Iteroparous Triclad

Summary

This paper compares aspects of the reproduction of a semelparous triclad, Dendrocoelum lacteum, with those of an iteroparous triclad, Dugesia polychroa. Cocoon output was less sensitive to ration and possibly temperature for the former as compared with the latter species. Cocoons of D. lacteum were on average bigger and contained more hatchlings than those of D. polychroa. The sizes of hatchlings did not differ between species, but for D. lacteum only, the hatchlings emerging from late cocoons were significantly larger, and less numerous, than those emerging from earlier cocoons. Possible reasons for these differences are considered.     

Reproductive ecology of Dendrocoelum lacteum (Turbellaria) in a rapid stream in southern Sweden and comparisons with a lake population

Rapid streams in southern Sweden are often inhabited by the triclad Dendrocoelum lacteum. Outside Fennoscandia, this species is mainly restricted to lentic habitats. The normal food refuge for D. lacteum, the isopod Asellus aquaticus, is seldom found in the stream habitats, and probably the prey here is the amphipod Gammarus pulex. With respect to spatial and trophic niche components, it seems that D. lacteum has taken the place of Crenobia alpina in southern Sweden.Two parameters of reproduction, namely production of cocoons and of hatchlings, both peaked approximately one month later in a stream than in an adjacent lake. This difference was attributed to a low temperature regime in the stream. Number of hatchlings per cocoon and cocoon sterility were higher in the stream than in the lake. Similar cocoon and hatchling output per adult was found in the two habitats, indicating a similar reproductive effort for the two triclad populations. I suggest that D. lacteum, by virtue of its choice of microhabitat, viz., under stones, is not so vulnerable to the more severe stream environment.     

The feeding biology of the triclad Phagocata vitta (Dugès): A laboratory study

A series of laboratory experiments investigated the diet and feeding behaviour of Phagocata vitta (Dugès). Its fundamental food niche comprises oligochaetes and chironomid larvae, in order of importance. Other arthropod groups, when wounded, are also eaten.Increasing prey density resulted in the ingestion rate increasing in a type 2 functional response curve, sensu Holling. Group feeding by triclads did not widen the food niche but did result in small triclads being more successful in obtaining a meal.When a range of size classes of prey were offered to various size classes of triclad, small triclads were found to take mainly small prey, whilst other sizes would take prey sizes in proportion to their presence in the mixture.Mucous traps do not appear to have an important role in the feeding biology of the triclad.     

Observations on some predators of stream-dwelling triclads

A serological technique was used to demonstrate that one species of trichopteran and three species of plecopteran nymphs were feeding on stream-dwelling triclads. Observations on streams in Caernarvonshire, North Wales, suggested that, in general, these predators were not typical members of the fauna at springheads, where triclads were frequently abundant. In contrast, further downstream the presence of predators was considered to be one of a number of factors which contributed to lower population densities of triclads. However, two small stony streams were encountered where the plecopteran predator Dinocras cephalotes occurred in close proximity to stream-dwelling triclads from the springhead downwards. In one, both predators and prey were found at all stations but highest triclad numbers were recorded where predators were few. In the second stream the population density of the predator was higher, and here, triclads were very scarce on the undersides of stones and were almost entirely confined o t patches of moss. It appears that the predators may be both limiting the micro-distribution of the triclad and also perhaps feeding selectively on larger individuals since mature triclads were rare, except at the springhead.     

The food niches of the invasive Dugesia tigrina (Girard) and indigenous Polycelis tennis Ijima and P. nigra (Müller) (Turbellaria; Tricladida) in a Welsh lake

The invasion of Llyn Coron in North Wales by the American immigrant Dugesia tigrina resulted in the almost entire displacement of the native Polycelis tenuis and P. nigra populations. Because competition for food is the most important factor controlling and regulating populations of British lake-dwelling triclads, the diets of the invasive and native triclads in the lake were examined in an attempt to explain the successful invasion.A serological technique, the precipitin test, identified the gut contents of field-collected triclads. Niche breadth, electivity and niche overlap indices were used in analysis of the data. A broad food niche was recorded for all the triclad species. Oligochaetes predominated in the diet of D. tigrina followed by Asellus and chironomids, in almost equal proportions, snails and caddisflies, with mayflies scarcely eaten. Both Polycelis species fed heavily on oligochaetes followed by Asellus. P. tenuis ate slightly higher proportions of chironomids and caddisflies than snails and mayflies, whilst P. nigra consumed similar proportions of these four prey taxa. Gammarus, scarce in Llyn Coron, and cladocerans were not eaten by the Polycelis species and by only a few D. tigrina.To-date there has been no apparent shift in the diet of the Polycelis species as a consequence of the invasion by D. tigrina. In the absence of any evidence for the partitioning of food on the basis of prey size or condition, the considerable overlap in the diets of D. tigrina and the Polycelis species suggests the potential for severe inter-specific competition for food. The superior exploitation by D. tigrina of the available food resource requires explanation.     

Predators and planariid competitors of the triclad Phagocata vitta (Dugés)

When Phagocata vitta, Crenobia alpina and Polycelis felina were exposed separately to each of seventeen potential invertebrate predators in the laboratory, only two stonefly species, Dinocras cephalotes and Perlodes microcephala, fed on the three triclad species, whilst the trichopteran Rhyacophila dorsalis ate the last two triclads. On exposing pairs of triclad species to D. cephalotes, significantly more P. felina than Ph. vitta were consumed, whereas similar numbers were eaten in each of the other two triclad combinations. Cannibalism and interspecific predation by triclad species were not observed. It is concluded that predation is unlikely to have a major influence in determining the observed distribution and abundance of triclad species in a Welsh study stream which harbours low numbers of effective predators.The de Wit model of competition was used to examine the competitive relationships between Ph. vitta, and C. alpina and P. felina, using chironomids or tubificid worms as food. In mixed cultures of Ph. vitta and P. felina fed on tubificids a stable equilibrium existed within the range of relative densities used in the experiments, whereas Ph. vitta was competitively superior to C. alpina in cultures fed on each of the food types, and to P. felina fed on chironomids. However, in theory, an equilibrium could occur when 10 or 6–7 times as many Ph. vitta as P. felina and C. alpina respectively are in the culture, when intraspecific rather than interspecific competition would become more important. Where the three triclad species coexist in the Welsh study stream, they are in similar numbers. This could imply that food is not limiting, with no consequent interspecific competition, or that the laboratory experiments were too simplistic to allow any interpretation of the field situation.     

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.     

The feeding biology of the immigrant triclad Phagocata woodworthi in Loch Ness, Scotland

Laboratory feeding experiments and a serological examination of the gut contents of field-collected triclads indicated that Phagocata woodworthi Hyman feeds heavily on oligochaetes. Its realized food niche also includes Asellus , caddisflies, molluscs, chironomids, stoneflies and mayflies. It is concluded that Ph. woodworthi is a considerable threat to the British triclad fauna, because of the considerable overlap in diet with native species, its fast reaction time to damaged prey, and its polypharyngeal state.     

The leeches of Rutland Water

Seven species of leeches have been recorded in Rutland Water between September 1977 and October 1979 by monthly samples taken by Ekman grab.The preliminary analysis of leeches from the four study sites of the reservoir (46 grab samples) showed that Helobdella stagnalis was the most abundant species with Erpobdella octoculata and Glossiphonia complanata (cf. Bullock et al. 1982). The life cycle of H. stagnalis was elucidated from these samples by dividing the animals into weight classes (2 mg live weight) and revealed that this species has two breeding seasons. The overwintering population reproduces in June. The juveniles grow rapidly and produce the next generation in August and September. This life cycle is similar to that reported in Europe and Canada.The population density ranged from 32 m^–2 to 90 m^–2, being generally higher during Summer and Autumn after breeding, but low in Winter and Spring. The population biomass increased from June until October each year because of high growth and then declined through the Winter. There are marked variations in density and biomass between the two years of the study period, which probably reflects the dramatic change in benthic abundance and distribution found in many new impoundments.In order to calculate the energy budget, the respiration rate of H. stagnalis has been studied by using a Gilson respirometer operated at three temperatures 5 °C, 10 °C and 15 °C, and the respiration rate of individual H. stagnalis increased logarithmically with weight. The relationship between O₂ consumption and dry weight was examined using linear regression (log/log) for the three temperatures. There are significant differences between the three regressions with slopes of 0.54, 0.69, and 0.73 at 5 °C, 10 °C and 15 °C respectively. The repiratory coefficient (Q₁₀) for the range 5 °C to 15 °C was almost constant for all class weights.The food of the leech was determined qualitatively by exposing potential prey organisms to it, using all the common zoobenthos of Rutland Water. H. stagnalis fed extensively on oligochaetes (Tubificidea). Food consumption was estimated at the three different test temperatures for different weight classes. Similar studies have been undertaken on E. octoculata and G. complanata.     

Factors affecting the occurrence of Dendrocoelum lacteum (Turbellaria) in Swedish lakes

By discriminant analysis on data from 115 lakes in South Sweden it was shown that the distribution and abundance of the triclad Dendrocoelum lacteum was predominantly governed by the density of the isopod Asellus aquaticus, its main food. The occurrence of the latter was mainly correlated with the nutrient richness of the lakes, most probably via presence of appropriate detritus, chiefly allochtonous material. As opposed to British oligotrophic lakes, most Swedish nutrient-poor lakes are surrounded by deciduous vegetation, which indirectly promotes the existence of A. aquaticus and consequently D. lacteum. Presence of mat-forming plants generally seemed to depress triclad density, whereas smaller stones promoted their occurrence, at least in nutrient-rich lakes.     

Activity of selected hydrolytic enzymes from leeches (Clitellata: Hirudinida) with different feeding strategies

Hydrolase activities of extracts from different parts of the bodies of parasitic (Theromyzon tessulatum, Piscicola geometra) and predatory (Erpobdella octoculata, Glossiphonia complanata) leeches were examined. The highest activity was detected in the extracts from sections containing the intestine. Hydrolase activities in the crop and intestine of parasitic leeches were higher than in predatory leeches. The high activity of most of hydrolases in those segments may indicate the intensity of digestion and absorption processes in leeches. A lack of trypsin activity and low chymotrypsin activity are likely to result from the presence of inhibitors of these enzymes. The high activity of the majority of the analyzed hydrolases in extracts derived from the head segment of predatory leeches enables, through digestion of tissues, their easy access to physiological fluids of a host. In turn, in extracts from the head segment of predatory leeches, only four hydrolases were shown to be active. Lipase activity was not found in any of the samples, while α-galactosidase activity was found only in extracts from the head segment of T. tessulatum and P. geometra. Trypsin activity was detected in the extract from the intestine contents of H. sanguisuga and in the extract from the head segment of P. geometra. The results demonstrate the presence of majority of hydrolases occurring in other animals in the alimentary tract of leeches. The study also shows that the crop of leeches is not only a food reservoir, but also the site where digestion and absorption processes take place.