The reaction time of leech and triclad species to crushed prey and the significance of this for their coexistence in British lakes

1. Three species of leeches, Erpobdella octoculata, Glossiphonia complanata and Helobdella stagnalis, and four species of triclads, Polycelis nigra, P. tennis, Dugesia polychroa and Dendrocoelum lacteum, commonly coexist on stony shores in productive British lakes. All species are food limited and there is much overlap in their diet. For both leech and triclad communities, coexistence of species is through the occurrence of food refuges. Leeches are more successful than triclads at capturing live prey, whereas both groups feed on damaged prey, comprising incapacitated, live or dead animals that are leaking body fluids. If triclads are better than leeches at exploiting damaged prey, this could be a mechanism for their coexistence. 2. Laboratory experiments investigated the comparative speeds at which leeches and triclads responded to crushed prey. Young and adult predators were offered a crushed specimen of the oligochaete Tubifex tubifex, the snail Lymnaea peregra, the crustacean Asellus aquaticus or the chironomid Chironomus sp., and their reaction times recorded. These four prey groups constitute the main diet of the predators in the field. Only D. polychroa and D. lacteum showed a significantly different reaction time between young and adults to crushed prey, and the reason for this is unclear. All predators, except H. stagnalis and D. polychroa, showed a difference in reaction time to the four types of prey, presumably a consequence of differences in both the ‘quality’ and ‘concentration’ of the different prey fluids, and there were some differences between predators in their speed of reaction to the same prey type. The following sequence, from fastest to slowest, in general reaction time to prey was obtained: E. octoculata, D. polychroa, P. tenuis, D. lacteum, P. nigra, H. stagnalis and G. complanata. 3. The location of the damaged food by the predators can be explained partly in terms of their foraging behaviour, with E. octoculata, D, polychroa and P. tenuis exhibiting a more seek-out strategy than other species which have a more sit-and-wait behaviour, and partly on the level of sophistication of their chemosensory system used to detect leaked prey fluids. This system is highly developed in triclad species but poorly developed in leeches. 4. In a second type of experiment in which prey, L. peregra, A. aquaticus or Chironomus sp., were offered at different time intervals after crushing to H, stagnalis and P. tenuis, few predators fed on food crushed for 24 h or longer, although a few leeches fed on Chironomus crushed for up to 72 h. 5. It is concluded that coexistence of leech and triclad species on stony shores in lakes is assisted by partitioning of food on a damaged or live basis.     

The food of Planaria torva (Müller) (Turbellaria-Tricladida), a laboratory and field study

The food of Planaria torva was examined in the laboratory by exposing a range of potential prey to the triclad and observing prey mortality. Under these conditions P. torva fed mainly upon tubificid oligochaetes and gastropods. The former activity was regarded as untypical of the field situation and due to limitations of the laboratory habitat. The food of P. torva was determined in the field by taking monthly samples from October 1967 to May 1969 of a population living in Linlithgow Loch, West Lothian, Scotland. A serological technique was used to examine the gut contents of the field triclads. For reasons explained in the text, the prey organisms tested for serologically were gastropods, oligochaetes (Tubificidae), Asellus and chironomid larvae. Planaria torva fed most extensively on Gastropoda, Asellus was the second main food while Tubificidae and Chironomidae were taken only seasonally and in small numbers. The limited extent of feeding on tubificids supports the laboratory data. Small P. torva gave proportionately fewer positive reactions to the prey antisera than large individuals. This was explained by the fact that small individuals occurred most frequently in the warmer months and took smaller meals; both of these features shorten the detection period of food in the gut and therefore give fewer reactions. The diet of small and large P. torva was similar in the field and showed considerable overlap with that of Dugesia polychroa. The food of Polycelis tenuis, Dendrocoelum lacteum and Dugesia polychroa in Linlithgow Loch was described on an annual basis and the results confirmed earlier observations.     

The consequence of a food refuge collapse on a guild of lake-dwelling triclads and leeches

The diets ofPolycelis nigra, P. tenuis, Dugesia polychroa, Dendrocoelum lacteum, Glossiphonia complanata, Helobdella stagnalis andErpobdella octoculata in an English lake were examined, using a serological technique, and compared between 1981–82 and 1989–90. Leech, triclad and prey abundances were also recorded. Between the two studies, snail numbers crashed whereas the abundances ofAsellus andGammarus increased.Dugesia andGlossiphonia numbers decreased substantially, whilstPolycelis tenuis andHelobdella abundances increased. In the second study, the snail component in the diet was greatly reduced resulting in a broader food niche, particularly forDugesia andGlossiphonia, and greater food overlap between the predators with the exception ofDendrocoelum andErpobdella which do not eat molluscs. It is postulated that the reduced size of the snail refuge, and consequent increase in severity of interspecific competition with other predators, particularlyPolycelis andHelobdella, led to the observed decrease in abundances ofDugesia andGlossiphonia. The decline in the last two genera, perhaps coupled with increased crustacean abundance, could have contributed to the numerical increase of the competitively superiorPolycelis tenuis andHelobdella.     

Allopatric and sympatric populations of Polycelis nigra in competition with P. tenuis (Turbellaria; Tricladida)

Two allopatric populations of Polycelis nigra (MuUller), one from lowland productive Llyn Maelog on Anglesey and the other from upland unproductive Llyn Dinas in Snowdonia, were each subjected to competition in the laboratory from the same Polycelis tenuis Ijima population from productive Llyn Llygeirian, also on Anglesey, where it coexists with P. nigra. The triclads were fed weekly on crushed Asellus (Isopoda) and their biomasses calculated monthly over five months. Results suggest that sympatric P. nigra are more successful competitors against P. tenuis than allopatric P. nigra. The data also suggest that the inferior competitive ability of allopatric P. nigra may be a consequence of both exploitative and interference competition. Coexistence of P. nigra with P. tenuis appears to increase P. nigra's tolerance to environmental stress; the current experiments and observations during several decades of research have indicated poorer survival and growth in allopatric than sympatric populations.     

Predation on snails by three species of triclad and its bearing on the distribution of Planaria torva in Britain

Dugesia polychroa, D. lugubris and Planaria torva preyed upon snails of differing morphologies and while the Dugesia spp. fed approximately in proportion to snail abundance, PL torva was more selective on Potamopyrgus jenkinsi. The incidence of feeding on four snail taxa by the Dugesia spp. was significantly correlated and differed strikingly from that of PI. torva where feeding was related to its annual life cycle. Large peaks of feeding coincided in the Dugesia spp. for the four snail types; this was attributed to snail vulnerability being increased by environmental disturbance. Comparison of feeding by Dugesia spp. in the presence and absence of PI. torva indicated that severe competition was occurring for food with PI. torva having a food refuge in P. jenkinsi. The distribution of PI. torva in Britain is largely confined to productive habitats in the Glasgow-Edinburgh and East Anglia regions. It is concluded that historical rather than ecological events have played the major part in its distribution to date. The strong association of PL torva with port areas and the canal system suggests that it is a recent introduction via the timber trade with Fennoscania.     

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.     

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.     

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.     

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.     

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.     

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.     

A field and laboratory study of the parasites of the triclad Phagocata vitta (Duges)

SUMMARY. 1. Over 13 months, fifty Phagocata vitta were collected from a smalt tributary of the Afon Anafon (Wales) and the occurrence of the ciliate Tetrahymena pyriformis and an unnamed nematode studied.
2. During the study, prevalence ranged from 5% to 22% and mean intensity from two to twenty-nine ciliates per infected triclad, whilst relative density never exceeded three per triclad. There was a trend for these values to be highest in summer and lowest in winter, but a significant positive correlation with field temperature was only found for mean intensity. The mean values of mean intensity and relative density were not significantly correlated with triclad size.
3. For the nematode, prevalence varied from 2% to 6% and relative density from 0.02 to 0.08 individuals per triclad, whilst mean intensity remained about one per infected triclad. No significant correlations between seasonal fluctuations of any of these values and field temperature were obtained.
4. In laboratory experiments lasting 5 weeks, triclads which had been initially fed tubificid worms infected with T. pyriformis and kept in uninfected water had much higher prevalence and mean intensity values than triclads fed uninfected tubiticids and kept in infected water. The main source of infection by the ciliate in the field seems likely to be through the ingestion of infected food. In infected triclads cultured at either 5, 10, 15 or 20°C, prevalence, mean intensity and relative density values increased with rising temperatures, whilst mortality was negligible at the two lowest temperatures and substantial at the two highest. Laboratory findings are related to field events.
5. It is concluded that the ciliate and nematode parasites may not cause significant mortality in the fieid population of P. vitta .     

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.     

An experimental study of the role of gradient and substratum in the distribution of two stream-dwelling triclads, Crenobia alpina (Dana) and Polycelis felina (Dalyell) in North Wales

A laboratory stream is described which has simulated steep- and shallow-gradient bottoms whose gradients can be varied. It was found that Polycelis felina, the principal triclad of shallow-gradient streams had a much reduced ability to colonize the simulated steep-gradient bottoms when compared to Crenobia alpina, which is the principal triclad of the steep-gradient bottoms in the field. P. felina is unable to move in the steep-gradient bottoms to any great extent, while C. alpina showed considerable ability to do this. When a reduction in flow was made this did not increase the proportion of P. felina to be found in the steep-gradient regions. The triclads were also tested for possible acclimatory responses and it was found that their responses were more fundamentally based. On the basis of the above evidence it is suggested that the absence of P. felina from the steep-gradient regions of streams in North Wales is due to a behavioural inability to tolerate the current regimes present in the steep-gradient bottoms.     

Triclads (Turbellaria: Tricladida) as predators of lake-dwelling stonefly and mayfly nymphs

It has been demonstrated by using a serological technique that Polycelis nigra (Müller) and P. tennis (Tjima) feed on mayfly and stonefly nymphs in unproductive lakes. Such feeding is less in productive lakes where these insects form a smaller proportion of the invertebrate fauna of the stony littoral zone. These nymphs form a significantly larger part of the diet of P. nigra than of P. tenuis; both triclad species feed more on stoneflies than mayflies.     

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.     

The realized food niches of three species of stream-dwelling triclads (Turbellaria)

SUMMARY. 1. The diet of Phagocata vitta, Crenobia alpina and Polycelis felina in a Welsh stream was examined, using a serologicat technique, at monthly intervals over 18 months.
2. For each triclad species, dietary composition changed little with time or increasing body size, and overall feeding intensity was greatest in summer and least in winter.
3. Alt species fed most heavily on oligochaetes, chironomids and Gammarus. Phagocata vitta fed lightly on Plecoptera, Trichoptera and Ephemeroptera whilst the other two triclad species fed substantially on the first two of these prey categories.
4. Food niche breadth indices indicated a wide diet for all species with some specialization in some months. Electivity indices showed positive electivity for oligochaetes and chironomids by all species and for Plecoptera by C. alpina and P. felina .
5. Diets overlapped and none had a food refuge: therefore the potential for interspecific competition for food exists.     

Seasonal variability in the palatability of freshwater macrophytes: a case study

The pond snail Lymnaea stagnalis (L.) was used for a laboratory assessment of seasonal variation in palatability of three freshwater macrophytes: Potamogeton lucens, Elodea canadensis and E. nuttallii. For each species, 2–5 populations were investigated in spring and in summer. Preliminary results showed that the feeding rate of similarly-aged snails bred under standard conditions was stable over time. In contrast, snail feeding rate on the three macrophyte species decreased from spring to summer, which was therefore interpreted as a decrease in plant palatability. This decrease was probably due to tissue maturation, as suggested by the concomitant increase in the dry matter content of leaves of the three species. The high palatability of the species studied during the spring may prove detrimental in cases of strong herbivore pressure, and could have consequences for macrophyte distribution among aquatic habitats.     

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.