Host-constrained epidemiology of the fish tapeworm Ligula intestinalis (L.)

Investigations into the biology of the roach, Rutilus rutilus (L.), and Ligula intestinalis (L.) populations at Slapton Ley, Devon were carried out between October 1982 and December 1984, and additional data collected from the lake since 1977 have been re-analysed. The Ligula population exhibited some unusual features: a limited specificity, a persistently low abundance and a scarcity of multiple infections. The population dynamics of the roach were also unusual in that the individual growth rate was one of the fastest in Britain, the survival was very poor and the year classes tended to alternate in strength. Whether the unusual epidemiology of Ligula could be explained by the unusual population dynamics of the roach is investigated. The transmission period of Ligula to the roach was limited to their first few months of life, probably due to a limited period of feeding on copepods by the fry. This narrow transmission window was almost certainly the major factor that has prevented the abundance of Ligula plerocercoids attaining high levels in the fry or of increasing in subsequent years, and has resulted in their abundance being determined entirely by transmission events to the fry. The limited transmission period has also caused the life-cycles of the roach and Ligula populations to become synchronized. At other localities, the abundance of Ligula is typically high, and can have a significant effect on the mortality of the host population, but, with the low abundance at Slapton, Ligula-induced roach mortality was insignificant. The rapid growth of the roach fry was the most likely explanation for the limited period of feeding on copepods, and the large size, short life-span and low abundance of the roach probably also constrained the build-up of the Ligula population in the lake. The random frequency distribution and scarcity of multiple infections was not considered unusual in view of the very low plerocercoid abundance. The very low abundance of Ligula, the separation of the spawning of roach and rudd in time and space, and the scarcity of rudd may account for the absence of infection in this species. It was concluded that the Ligula population in Slapton Ley was being constrained by the atypical population dynamics of the roach, and not vice versa as theory predicts.     

The cause of extreme year class variation in a population of roach, Rutilus rutilus L., from a eutrophic lake in southern England

Investigations into the biology of the roach population at Slapton Ley, Devon, U.K. were carried out between October 1982 and December 1984 and data collected from the lake since 1977 have been re-analysed to assist interpretation. The roach population has been characterized in recent years by extreme year class variation and a tendency for year classes to alternate in strength. The survival of the roach was very poor, and the spawning population therefore consisted largely of 2-and some 3-year-old fish. Consequently, the size of the spawning stock was small and dependent on the strengths of the year classes that it contained. Recruitment to many year classes was probably limited by the size of the spawning stock. The occurrence of a poor year class in the population would therefore set up an autonomous cycle of poor recruitment to alternate year classes in a manner similar to many tropical marine fisheries. Observation of other British roach populations showed that a short life-span may be associated with conditions that promote very rapid growth rates. The growth rate of individual roach at Slapton was found to be one of the fastest in Britain, and this was apparently due to the very high productivity of Slapton Ley together with the persistence of the roach population at very low densities.     

Studies on Ligula intestinalis (L.) effects on a roach population in a gravel pit

The effects of the plerocercoids of Ligula intestinalis were studied on a population of roach, Rutilus rutilus in a gravel pit. The incidence of the cestode fell from 92% in 0+ roach in April to 25 % in January of the succeeding year. The fall in the number of parasitized fish was due to predation, mainly by pike, Esox lucius. Observations indicated most of the parasitized fish failed to become sexually mature although the actual growth rate of the fish was not markedly reduced. The plerocercoids of L. intestinalis grew more rapidly during the summer. The author recommends roach of less than 9 months of age should not be introduced into confined water such as a gravel pit, since after this period they appear to be much less likely to be parasitized.     

The occurrence and natural alleviation of stunting in a population of roach, Rutilus rutilus (L.)

Two sudden and pronounced changes in the growth rate of roach, Rutilus rutilus (L.), in Slapton Ley, Devon, have been observed between 1972 and 1976. At first the growth rate declined to the point at which the population became stunted, then subsequently it improved again. These changes were correlated with population density; the numbers of roach were increasing during the late 1960's/early 1970's, and this increase was substantially reinforced by very strong year classes in 1972, and, to a lesser extent, in 1973. The increase in population density resulting from the strong 1972 year class was apparently adequate to accelerate the onset of the stunting observed. The improvement in growth rate in 1976 followed immediately after extensive mortalities amongst the roach during 1975, caused by an epidemic of the parasite Ligula intestinal is (L.). Some improvement in the growth of O group roach had been evident during 1975, but this was not observed in the population. Ford-Walford plots showed a decline in the value of L after the onset of stunting in 1972.
Differences in the reproductive biology of the fish were found following the alleviation of stunting; the gonads of both sexes achieved a greater relative weight, and correspondingly the fecundity of the females was higher, although this latter effect became progressively less marked with increasing size. It was not apparent amongst the largest individuals. There was also some evidence of a decline in the proportion of fish maturing at minimum size. The changes in the reproductive biology were associated with the improvement in conditions for individual fish following the decline in population density.     

The biology of pike, Esox lucius L., in a southern eutrophic lake

The biology of pike, Esox lucius L., in a southern productive lowland lake is described. Scales and opercular bones were difficult to read and interpret, and growth estimated had perforce to be based on scale readings. Growth of Slapton pike is average and intermediate between recorded extremes. Both male and female pike reached maximum condition in February, just prior to spawning. The population of pike of over 450 mm fork length in the lake was estimated at 870·6 ± 389·3 in 1975, and 950·4 ± 143.3 in 1976/77. This leads to the conclusion that the pike population has one of the highest biomasses per surface area of water ever recorded. Number of pike per unit area of surface was also high, despite the fact that a significant proportion of the population (fish under 450 mm) could not be adequately sampled. Mean instantaneous mortality rate was 0·53, and mean instantaneous survival rate was 0·59. The roach provided the main item of diet of the pike, with perch taken less readily. Immature pike ate a significant proportion of invertebrates, but roach was again a common feature of the diet of even small fish. Two spawning migrations were identified; at other times of the year, pike were non territorial. The majority of pike spawned in March. Fecundity of a sample of females was assessed. Overall sex ratio was 1:1.     

Food web manipulation in a small,eutrophic Lake Wirbel,Poland: effect of stocking with juvenile pike on planktivorous fish

In a four year experiment (1988–1991) carried out in a shallow, eutrophic lake, an increase in young-of-the-year pike (Esox lucius) density was used to control planktivorous fish assemblages consisting mainly of small-sized cyprinids: roach (Rutilus rutilus), Leucaspius delineatus, and white bream (Blicca bjoerkna). Stocking with pike fry of ca 30 mm in three successive springs resulted in large-scale mortality among prey of vulnerable sizes. Rotenone treatment at the end of the fourth year showed that roach and white bream populations contained few 0+ to 2+ fish, but very high numbers of 3+ to 6+ fish. By this time, short-lived, slow-growing L. delineatus, with no size refuge from predators, had been driven almost to extinction.     

The role of phosphorus release by roach [Rutilus rutilus (L.)] in the water quality changes of a biomanipulated lake

SUMMARY 1. Following fish removal, the water quality in biomanipulated lakes often improves concomitant with decreased phosphorus (P) levels. Because the decrease in P concentrations derives most probably either directly or indirectly from fish, which are the main target of biomanipulation, this study examined the P release of 0+, 1+ and 2+ roach [Rutilus rutilus (L.)] and changes in the P release during summer in a shallow eutrophic lake in Finland. 2. The P release was separated into P derived from benthic and littoral food items and into recycled P derived from feeding on zooplankton, to estimate the contribution of net P additions to the water column by the fish to the increase in P concentrations of the lake water (75–110 mg P m^?3) in summer 1991–96. 3. Individual P release of roach by both egestion and excretion was estimated with a bioenergetics model. The size of the roach population was estimated with a depletion method and the proportions of different age groups from catch samples, using a programme separating mixtures of normal distributions. The sensitivity of the release estimates to variation in the growth data was estimated with the jackknife technique. 4. The biomass‐specific P release by 0+ roach (0.36–0.54 mg P g^?1 day^?1) was higher than that by older roach (0.07–0.16 mg P g^?1 day^?1) throughout the summer. The P release by the whole roach population deriving from benthic and littoral food items (0.7–2.7 mg m^?3 during July to August, representing a net addition to the water column) was 5–19 times lower in 1991–96 than the recycled P release deriving from zooplankton (8.9–25.7 mg m^?3), and too low to explain the increase in the P concentration of the lake water during the summer. Because the biomass‐specific P release and roach diet composition vary with fish age, it is important to consider the age structure of fish populations to obtain correct estimates of P release and net additions to the water column. 5. The removal of roach by fishing diminished the roach stock greatly, but the fish‐mediated P release to the water column changed little. This effect was because of the high compensation capacity of the roach population, leading to high recruitment of young fish with higher biomass‐specific P release rates. 6. External loading is very low during summer months and therefore it cannot explain the increase in the P concentration of water during that time. Internal loading from the sediment might be as high as 10.2 mg P m^?2 day^?1, i.e. 50 times higher than the maximum net P addition by the total roach population.     

An investigation into the growth of 0-group roach, (Rutilus rutilus L.) with special reference to temperature

The growth of 0-group roach in a chalk-fed river is traced over six seasons and the growth compared to that in a nearby gravel pit. The growth rate, the daily weight increase and the condition of the fish are all highest during the summer, falling to a minimum over the winter period and rising again in the spring. Considerable yearly variation in the growth of roach in the river was observed and correlated with water temperatures above 14° C. It is suggested that water temperature, acting through the food supply, is the dominant factor governing growth. The hot summer of 1976 appears to have resulted in excellent growth of roach in both habitats.     

Changes in roach (Rutilus rutilus L.) population structure induced on draining a large reservoir

The influence of draining a large reservoir (Pareloup, South of France) on the population structure and the growth of roach is studied in this work. This reservoir, with an area of 13 km², drained in June 1993, was refilled 2 months later. Fish were sampled monthly before draining (1981) and after refilling (1997) by nylon monofilament gill nets used at the same catching effort for both periods. This permitted a comparison to be made between the density of roach and length distribution before and after refilling. Changes in growth were determined by scalimetry. The observed difference in population structure and growth underlined that the differences are mainly due to a greater growth rate after refilling during the first 2 years of roach life. These growth changes are explained by the decrease in roach density and the increase in 1993 of the biomass of Zooplankton, which constitute the main feeding resource for 0⁺ and 1⁺ roach. The study led us to propose hypotheses on the ecological significance of growth changes induced by refilling, which can be considered as a rejuvenation of the aquatic ecosystem.     

Modelling roach (Rutilus rutilus) microhabitat using linear and nonlinear techniques

• 1 Multiple linear regression (MLR), generalised additive models (GAM) and artificial neural networks (ANN), were used to define young of the year (0+) roach (Rutilus rutilus) microhabitat and to predict its abundance.
• 2 0+ Roach and nine environmental variables were sampled using point abundance sampling by electrofishing in the littoral area of Lake Pareloup (France) during summer 1997. Eight of these variables were used to set up the models after log₁₀ (x+ 1) transformation of the dependent variable (0+ roach density). Model training and testing were performed on independent subsets of the whole data matrix containing 306 records.
• 3 The predictive quality of the models was estimated using the determination coefficient between observed and estimated values of roach densities. The best models were provided by ANN, with a correlation coefficient (r) of 0.83 in the training procedure and 0.62 in the testing procedure. GAM and MLR gave lower prediction in the training set (r = 0.53 for GAM and r = 0.32 for MLR) and in the testing set (r = 0.48 for GAM and r = 0.43 for MLR). In the same way, samples without fish were reliably predicted by ANN whereas GAM and MLR predicted absence unreliably.
• 4 ANN sensitivity analysis of the eight environmental variables in the models revealed that 0+ roach distribution was mainly influenced by five variables: depth, distance from the bank, local slope of the bottom and percentage of mud and flooded vegetation cover. The nonlinear influence of these variables on 0+ roach distribution was clearly shown using nonparametric lowess smoothing procedures.
• 5 Non‐linear modelling methods, such as GAM and ANN, were able to define 0+ fish microhabitat precisely and to provide insight into 0+ roach distribution and abundance in the littoral zone of a large reservoir. The results showed that in lakes, 0+ roach microhabitat is influenced by a complex combination of several environmental variables acting mainly in a nonlinear way.

     

Studies on Ligula intestinalis Some aspects of the pathology in the second intermediate host

A 3 year survey of a lake, in which 120 roach, Rutilus rutilus , were examined revealed the presence of the plerocercoids of Ligula intestinalis in more than 90 % of the fish. The average number of parasites per fish was 4.2 although fish exceeding 32 g were not ligulosed. Gudgeon, Gobio gobio , of all sizes were affected. Implants of the plerocercoids into small roach, gudgeon and goldfish, Carassius auratus , were successful but not in the case of Perca fluviatilis, Esox lucius and Leuciscus cephalus. The pathological effects of the plerocercoids on roach and gudgeon are described.     

Dung exploitation by the dung beetle Typhaeus typhoeus (Col., Geotrupidae)

Summary The competitive interactions between roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) were investigated in two habitats, the open water and the waterlily zone. The growth rates of both species in enclosures were lower when confined together than when alone, demonstrating interspecific competition. Allopatric roach had the highest growth rate in both habitats although the open water was preferred. The diets of both species were dominated by zooplankton in both the open water and waterlily zones. In laboratory experiments, roach had significantly higher feeding rates than rudd when fed D. magna and Cyclops sp. The impact of roach on the mean sizes and densities of zooplankton in the enclosures, together with the results from the laboratory study, indicate that roach were competitively superior in the open water. Because of high mortality in the sympatric waterlily enclosure, no conclusions about interspecific competition in this habitat could be drawn. The observed habitat segregation between roach and rudd was at least partly interactive.     

Changes in the fish community and water quality during seven years of stocking piscivorous fish in a shallow lake

SUMMARY 1. Piscivores (annual stocking of 1000 individuals ha^?1 of 0+ pike and a single stocking of 30 kg ha^?1 of large 20–30 cm perch) were stocked in seven consecutive years in a shallow eutrophic lake in Denmark. The stocking programme aimed at changing food‐web structure by reducing zooplanktivorous and benthivorous fish, with resultant effects on lower trophic levels and ultimately water quality. 2. The fish community and water quality parameters (Secchi depth, concentrations of total phosphorus, chlorophyll a and suspended solids) were monitored between 1996 and 2000 and relationships were evaluated between predatory fish and potential prey and between zooplanktivorous or benthivorous fish and water quality parameters. In addition, potential consumption of piscivorous fishes was calculated. 3. The density of fish feeding on larger zooplankton or benthos (roach >15 cm, crucian carp >15 cm) declined distinctly during the study period. This effect was attributed to predation by large (>50 cm) pike. Based on scale readings, we cautiously suggest that the stocking of 0+ pike boosted the adult pike population to produce an unexpected impact in later years. Conversely, no direct impact of stocked 0+ pike was detected on 0+ roach. 4. A major decline in the recruitment strength of 0+ roach was observed in 2000. A combination of (i) the indirect effect of large pike preying on adult roach, with negative effect on roach reproduction and (ii) the direct predation effect of 0+ pike and/or 1+ and 2+ perch recruited in the lake, provides the most likely explanation of this phenomenon. 5. A marked increase in Secchi depth in 2000 and declining trends in suspended solids, chlorophyll‐a and total phosphorus concentrations were observed. These changes may also be attributable to changes in the fish community, although the relationships were not straightforward. 6. This 7‐year study indicates that piscivorous fish may be a significant structuring force in shallow eutrophic lakes, suggesting that stocking piscivores can increase predation pressure on cyprinids. However, the general lack of impact of 0+ pike points to the need of refining current stocking practices in several countries across Europe.     

Growth,Reproduction and Condition of Roach (Rutilus rutilus (L.)), Perch (Perca fluviatilis,L.) and Ruffe (Gymnocephalus cernuus (L.)) in Eutrophic Lake Aydat (France)

The growth, reproduction and condition of adults of the three dominant fish species (roach, Rutilus rutilus, (L.); perch, Perca fluviatilis, L. and ruffe, Gymnocephalus cernuus, (L.)) in the eutrophic Lake Aydat were studied over one year cycle. Compared to published data, the growth of R. rutilus and G. cernuus was about average, while that of P. fluviatilis was below average. Comparing to literature, the fecundity of R. rutilus and G. cernuus was low but their oocytes were large. In contrast, P. fluviatilis had a high fecundity but small oocytes. At the end of summer, an abrupt decrease in the condition was recorded only for perch, probably due to stress as a result of environmental conditions. The sex-ratio was in favour of females for the three studied species but, in contrast to G. cernuus, the sex-ratio of R. rutilus and P. fluviatilis increased significantly also with age. It is concluded that Lake Aydat is a more favourable environment for R. rutilus and G. cernuus than for P. fluviatilis.     

Notes on the Effect of Cutting Bracken (Pteris aquilina L.)

Background: Undisturbed high elevation treelines follow a common growing season isotherm, irrespective of latitude. Small stature plants thrive at much higher elevations because they grow in a favourable microclimate near the ground, whereas trees are aerodynamically coupled to free atmospheric circulation, hence the uniform treeline elevation in a given region.

Aims: I argue that the treeline results from tree architecture and not from a tree-specific inferior physiology. At tissue level, all cold adapted higher plants (including winter crops) face similar temperature related limitations and are constrained by similar thermal thresholds.

Methods: In order to explore this hypothesis, winter rape and winter oat were grown in the field and the daily rate of leaf expansion was measured during early winter, with temperatures similar to those at treeline at the beginning of the growing season (monthly mean temperature of 5 °C).

Results: Leaves of these winter crops only grew when the degree hours above 5 °C for a given day exceeded zero. Rape and oats showed very similar responses. The data support a common temperature threshold for tissue formation in winter crops and treeline trees.

Conclusions: A literature survey revealed lower temperature thresholds (close to freezing point) in arctic and Antarctic algae. It appears that the formation of complex, partly lignified tissue does not happen below 5 °C, whereas such temperatures exert little constraints on photosynthesis. The study illustrates that tissue growth in winter crops can help understand growth of treeline trees, given that both exhibit similar minimum temperature requirements for meristem functioning.     

Use of body-water content to assess the physiological state of roach Rutilus rutilus L. in natural conditions

It is shown that in natural conditions roach have two levels of water content in their organisms during their annual cycle which reflect different physiological states of the fish. During the feeding period, the body-water content is maintained at a low level of 72.6 ± 0.05%, determining the physiological state related to the growth of fishes. In winter, spring, and postspawning periods, the water content in the roach organism is high, 75 ± 0.06%, which reflects the physiological state of survival during periods of the year unfavorable for growth. The water content in the organism of fish is a convenient integrated parameter for assessing the general physiological state of fish in natural conditions.     

Piscivory of 0+ pike (Esox lucius L.) in a small eutrophic lake and its implication for biomanipulation

Stocking 0+ pike in shallow eutrophic lakes as an indirect way to facilitate clear water by increased phytoplankton grazing by zooplankton, has been used in several studies with varying success. Lack of piscivory could be one reason for poor impact of the pike stockings, on reducing the 0+ cyprinid fish population. In relation to this, we present data on food and feeding habits of 936 0+ pike (Esox lucius L.) (2–18 cm) sampled during five years in a small eutrophic lake undergoing biomanipulation. Overall, the food of 0+ pike followed a sequence of diet shifts including microcrustacea, insects, macrocrustacea and finally vertebrates (fish) with increase in pike length. Despite a high abundance of potential prey fish in the lake, in general less than 50% of the pike were piscivorous until a length of 10.1–13.7 cm. As piscivory increased, the principal prey fish (0+ roach) apparently displayed antipredatorial behaviour which decreased their availability for 0+ pike. We conclude that lack of piscivory caused by e.g. anti predator tactics by prey fish, may reduce the impact of 0+ pike stockings in lake restoration projects.

     

Phenotypic modification of roach (Rutilus rutilus L.) infected with Ligula intestinalis L. (Cestoda: Pseudophyllidea).

In European freshwater, cyprinid fish may be heavily infected by plerocercoids of the pseudophyllidea cestode Ligula intestinalis (L.). During their development, these parasites grow rapidly to a large size in the fish's body cavity, characteristically distending the abdomen. In this study, the influence of this tapeworm on roach (Rutilus rutilus L.) morphology was analyzed. Forty-five infected and 45 uninfected roach were collected from the Lavernose-Lacasse gravel pit in Toulouse, south western France and examined for 40 morphological measurements to study phenotypic modification of the body and 14 bilateral characters for an analysis of asymmetry. Results indicate that the degree of bilateral asymmetry does not change between infected and uninfected roach, despite the strong host-morphological modifications such as deformation of the abdomen, fin displacements at the level of the tail, and sagging of the vertebral column. The intensity of abdominal distension and fish morphology changes depends on the total parasite biomass present. Differences were observed in morphology at different levels of infection, which relate to established effects of L. intestinalis on the physiology and behavior of intermediate hosts. These morphological changes induced by the parasite could increase trophic transmission to the definitive avian hosts.     

Size-dependent ontogenetic diet shifts to piscivory documented from stable isotope analyses in an introduced population of largemouth bass

Piscivorous largemouth bass (Micropterus salmoides) have been introduced in several regions outside of their native range in North America, resulting in significant disturbance to native fish communities. This species exhibits an ontogenetic diet shift from zooplanktivory to piscivory as juveniles. An early switch to piscivory allows 0+ bass to increase their growth rate prior to winter, resulting in reduced mortality. However, little is known about the dietary switch at the population level during the first year. We used carbon stable isotope analyses to examine the diets of age 0+ individuals in Lake Izunuma, Japan. The onset of the shift to piscivory occurred at a smaller size than in native or other non-native areas [>40 mm total length (TL)]. We found a positive correlation between TL and δ¹³C throughout summer and autumn. Small individuals had δ¹³C values that were similar to those of zooplankton, whereas large individuals had δ¹³C values that were similar to those of cyprinid prey species. This suggests that the smaller 0+ individuals remain zooplanktivorous until late autumn, whereas the larger individuals shift to piscivory as early as June, soon after the breeding season ends. Our results also suggest that a significant number of 0+ bass failed to switch to piscivory until the winter of their first year, despite the smaller size threshold for the onset of piscivory.     

Diet and growth of asp,Aspius aspius (Linnaeus, 1758), in the Danube River near the confluence with the Sava River (Serbia)

A sample of 198 asp (Aspius aspius) was collected over a 28.5 km long section of the Danube River, upstream and downstream from the mouth of the Sava River, in order to provide information on population structure, diet, growth, and condition of this species. Total body lengths of sampled fish were 90–405 mm, and body weights 5–567 g. The sample was predominantly sub‐adult fish aged 0+ to 4+ years. Sexually immature asp prevailed over the sexually mature asp. The sex ratio (1.4 : 1) was biased toward males. Male asps in the Danube become sexually mature only in their fifth year of life, and the females even later, as no sexually mature females were caught. The diet spectrum consists exclusively of fishes; of seven determined prey species, most important are bleak Alburnus alburnus, roach Rutilus rutilus, and goldfish Carassius auratus. Highest value of the seasonal vacuity index is in November (I_v = 94.1), and the smallest in July (I_v = 35.6). Trophic niche breadth is largest in May (H = 1.40), and smallest in November (H = 0.00). The largest average number of prey items is found in age class 4+ (2.33), the smallest in age class 0+ (1.00). Von Bertalanffy growth parameters are L_∞ = 526.46, K = 0.28, and t₀ = 0.22. The length–weight relationship is described as log W = ?5.16 + 3.03 log L. Fulton’s condition factor increases with fish length, from 0.70 to 0.83. Regarding seasonal fluctuations, this factor begins to increase in late spring, with the trend continuing until autumn, and then decreasing from autumn to spring.