The population biology of two species of eyefluke, Diplostomum gasterostei and Tylodelphys clavata, in perch

Incidence, intensity and frequency distributions of infections in perch, Perca fluviatilis , with the eyeflukes Tylodelphys clavata and Diplostomum gasterostei were studied in a lake at monthly intervals over a period of two years. T. clavata had appeared in the lake immediately prior to the study, and its levels of infection continued to rise throughout the period of investigation whereas those of D. gasterostei remained relatively steady. The main period of infection of fish by both species of parasites was late summer, but a second and minor infection took place in spring. In the first year after its introduction T. clavata exhibited a seasonal cycle in incidence and intensity of infection and disappeared from fish in summer, but in the second year this cycle was masked by increased variation in development times and lack of synchrony throughout the parasite population. It is concluded that T. clavata has a life span of one year or less and that the parasites die within the fish, mainly in summer. D. gasterostei in contrast has a life span of at least one year, and disappearance of the parasite from the population is probably due to death of some heavily infected fish, although it was not possible to determine if this was due directly to the presence of the parasite.     

Location-dependent infection of fish parasites in Lake Constance

Perch Perca fluviatilis and roach Rutilus rutilus were caught at various locations around Lake Constance (Bodensee). Infection of perch and roach with the eyeflukes Diplostomum spathaceum and Tylodelphis clavata was greatest in the western location (Bottighofen). The varied occurrence of parasite species at different locations indicated that maximum interchange between fish populations was slight. Whitefish Coregonus lavaretus migrating up the River Rhine were less infected with both the tapeworm Proteocephalus exiguus and the copepod Ergasilus sieboldi than whitefish from the middle of the lake. Some of the parasites had already left their hosts. Newly established infections were not found in migrating whitefish.     

Parasite community and mortality of overwintering young-of-the-year roach (Rutilus rutilus)

The composition and development of the parasite community of overwintering young-of-the-year (YOY) roach (Rutilus rutilus) was studied in outdoor artificial ponds. Cumulative mortality of the roach from November until May was about 20%. The prevalences of the epizoic ciliates Trichodina sp. and Apiosoma sp., and of the monogeneans Dactylogyrus suecicus, Dactylogyrus nanus, and Gyrodactylus sp. in general tended to peak in the beginning of April at a water temperature of about 8 C. However, mean parasite intensity remained constant over this interval. Prevalence of metacercariae of the digeneans Diplostomum cf. spathaceum and Tylodelphys clavata remained constant with values around 60% and 10%, respectively. Larvae of the nematode Philometra obturans and the cestode Ligula intestinalis and females of the copepod Neoergasilus japonicus were found sporadically. A concept of 2 thresholds, a critical condition factor (attained by a temperature-induced energy deficiency), and a condition-dependent critical infection intensity, which determine winter mortality of YOY, is suggested.     

Interspecific dominance amongst three species of coarse fish in Slapton Ley, Devon

Marked changes in the relative numbers of roach Rutilus rulilus (L.), rudd Scardinius erylhroplhalmus (L.) and perch Perca fIuviatilis L. , in Slapton Ley, Devon, have been observed over the period 1967–1978. Historically, the lake had been dominated by rudd and perch; significant numbers of roach were not thought to be present until 1967. From then onwards the roach population exhibited a considerable expansion, apparently replacing the rudd, which had virtually disappeared by 1974. In 1975 extensive mortalities of roach were caused by the pseudophyllidean cestode Ligula intestinalis L. During 1976 and 1977 larger number of rudd, belonging to the 1975 and 1976 year classes, were present, suggesting that the roach mortalities might be giving the rudd a chance to recover. However, very few rudd were present during 1978, possibly because lower incidences of ligulosis during 1976–1978 had allowed the roach to recover from the main outbreak of the disease in 1975, and to replace the rudd for the second time. Evidence from trap catches indicated that the perch population had shown a consistent decline between 1970 and 1977. The major phase of this decrease occurred between 1971 and 1973, when the roach population was increasing the most rapidly. Comparisons were made with changes in fish populations in other localities. The major reason for the changes observed was thought to be a competitive relationship between the plankton feeding younger stages, with roach being the dominant species, although other factors may also have been involved.     

The adaptation of digestive enzymes to temperature, season and diet in roach, Rutilus rutilus and rudd Scardinius erythrophthalmus; Proteases

The seasonal changes of proteolytic activity in the gut content of roach R. rutilus and rudd S. erythrophthalmus in four Tyrolean lakes and the adaptation of the proteases to constant temperatures and different natural diets were studied. In rudd proteolytic activity remains nearly constant throughout the year. In roach proteolytic activity increases and then decreases during the first three months after the thaw in spring. This period appears to be endogenously controlled and is followed by a second stage in which proteolytic activity is influenced by environmental factors. Under natural conditions both species have a higher proteolytic activity when feeding on animals than on detritus. Under laboratory conditions there is a slight maximum at an environmental temperature of 16° C when the fish had been fed on meal worms. With plant food a significant dependence of proteolytic activity on environmental temperature was only found in roach.     

The influence of simulated aquatic macrophytes on the zooplankton consumption rate of juvenile roach, Rutilus rutilus, rudd, Scardinius erythrophthalmus, and perch, Perca fluviatilis

Laboratory experiments showed that, of zooplanktivorous roach, rudd and perch, in the absence of any environmental structure roach were the most efficient feeders, but high densities of simulated submerged marcrophytes elevated perch to this position; rudd matched the performances of perch and roach only at intermediate structure densities. These changes in efficiency rankings with increased structure were the result of overall decreases in the performances of roach and rudd. Simulated water lilies and emergent reeds had their own influences on consumption rate. These effects were largely mediated through relationships between structure density and swimming speed; roach and rudd, not perch, showed reduced swimming speeds in the more structured environments. Observations of the routine behaviour of the fish suggest that their assessment of predation risk may be an important factor in determining their activity level and hence foraging strategy.     

A search for introgressive hybridization in the rudd, Scardinius erythrophthalmus (L.), and the roach, Rutilus rutilus (L.)

Rudd, roach and their hybrids from an interbreeding population at Norwich were examined electrophoretically for seven enzymes; an examination of pharyngeal teeth supplemented the data. The rudd were compared to rudd from Lake Trawsfynydd, Wales, a lake free from roach. No differences were observed between the rudd from the two localities and no evidence was found of introgression within the fish from Norwich.     

Long term studies on the population biology of two specie of eyefluke, Diplostomum gasterostei and Tylodelphys clavata (Digenea: Diplostomatidae), concurrently infecting the eyes of perch, Perca fluviatilis

Changes in the size of the infrapopulations of metacercariae of Diplostomum gasterostei and Tylodelphys clavata were studied in a small lake for a period of seven years in perch Perca fluviatilis . Tylodelphys clavata appeared in the lake at the commencement of the study and its subsequent population increase and changes were typical of those of a species recently established in a new habitat. Population size increased slowly at first, then rapidly, then declined again as population density approached equilibrium level. By contrast, the population size of D. gasterostei declined throughout the study. Two processes were responsible for the decline: a decrease in the proportion of fish carrying heavy infections which was continuous throughout the seven years and a dramatic decline in recruitment rate in young fish during the last two years. In earlier years recruitment rate had changed annually and changes in overall infrapopulation size had largely reflected the recruitment rate two years previously. It was concluded that these two processes were independent of each other and related to changes in the population density of other species of eyeflukes. The decline in the proportion of heavily infected fish was significantly negatively correlated with the increase in population density of T. clavata and the decline in recruitment rate in young fish was coincident with the appearance and infrapopulation increase of T. podicipina metacercariae in the eyes of young perch. It is suggested that these two species interact negatively with D. gasterostei and are currently partitioning the perch habitat between themselves.     

The occurrence and life history of Asymphylodora kubanicum (Platyhelminthes: Digenea: Monorchidae) in the Worcester-Birmingham canal, with special reference to the feeding habits of the definitive host, Rutilus rutilus

Two hundred roach and over 400 molluscs were examined over a one year period to investigate the occurrence and life history of Asymphylodora kubanicum in the Worcester-Birmingham canal. Larval stages, infective to the fish definitive host, were present in molluscs throughout the year but did not show a seasonal fluctuation in numbers. Parasites in the intestine of the roach showed a marked annual cycle of occurrence and maturation: low winter infection levels preceded a dramatic increase in infection during the spring and summer. Maturation of the parasite population was rapid during the spring and summer and in late summer and early autumn the parasites laid their eggs and subsequently died. The death of parasites after egg-laying resulted in the low winter infection level during which time little recruitment occurred.
Roach became infected mainly in their third year when molluscs become a dominant component of their diet. Thereafter the older fishes (<2+) are all equally susceptible to infection, but the larger (older) fishes become more heavily infected because of the greater consumption of molluscs per fish. The sex of the fish made no difference to infection with the parasite.     

Host immunization shapes interspecific associations in trematode parasites

1. Individuals of free-living organisms are commonly infected by multiple parasite species. Under such circumstances, positive or negative associations between the species are possible because of direct or indirect interactions, details in parasite transmission ecology and host-mediated factors. One possible mechanism underlying these processes is host immunity, but its role in shaping these associations has rarely been tackled experimentally.
2. In this study, we tested the effect of host immunization on associations between trematode parasites infecting eyes of fish. We first analysed the associations between three species ( Diplostomum spathaceum , Diplostomum gasterostei and Tylodelphys clavata ) in wild hosts, roach ( Rutilus rutilus ) and perch ( Perca fluviatilis ). Second, using rainbow trout ( Oncorhynchus mykiss ) as a model fish species, we experimentally investigated how sequential immunization of the host (i.e. one parasite species infects and immunizes the host first) could affect the associations between two of the species.
3. The results indicated that most of the associations were positive in wild hosts, which supports between-individual variation in host susceptibility, rather than competitive exclusion between the parasite species. However, positive associations were more common in roach than in perch, possibly reflecting differences in ecological conditions of exposure between the host species. The experimental data showed that positive associations between two of the species were eroded by host immunization against one of the parasite species.
4. We conclude that sequential immunization of hosts has a marked effect on interspecific parasite associations and basically can determine if positive associations are detected or not. This implies that correlative results suggesting non-interactive community structure in general may be obscured by the sequence of previous parasite exposure and corresponding dynamics of host immunization.     

Observations on the occurrence of Diplostomum spathaceum and Schistocephalus sp. in ninespine sticklebacks (Pungitius pungitius) from the Belcher Islands, Northwest Territories, Canada

All 175 ninespine sticklebacks, Pungitius pungitius (Linné), collected from the Belcher Islands were parasitized by Diplostomum spathaceum (Rudolphi) and 43% by Schistocephalus sp. D. spathaceum metacercariae were mostly confined to a dorso-ventral band encircling the lens of the eye, and were concentrated in the anterio-dorsal sector of this band. The central area of the lens was thus relatively free of diplostomula, probably minimizing interference with the vision of the fish. The frequency distribution of D. spathaceum abundance in P. pungitius was closely approximated by a negative binomial, while that for Schistocephalus was best fitted by a Poisson. None of the fish condition factors examined appeared related to the intensity of the parasitic infections.     

Polymorphism of A, B and C loci of lactate dehydrogenase in European fish species of the Cyprinidae family

In 24 fish species of the Cyprinidae family, belonging to 21 genera, isoenzyme patterns of lactate dehydrogenase (LDH) were determined, which could be classified in the majority of cases into 3 main groups. Isoenzyme patterns in natural hybrids of roach and rudd, roach and bream, roach and bleak were also analysed. In bitterling, polymorphism was observed in B locus of LDH. In white bream polymorphism exists in the A locus. In bream, rudd, silver carp and barbel polymorphism was found in C loci. Isoenzyme patterns indicate that in each case the polymorphism is genetically controlled by two alleles at a single locus. The populations investigated were in Hardy-Weinberg equilibrium. No significant differences were found in the activity of liver LDH in various polymorphic types of C loci of bream and rudd.     

Parasite fauna of introduced pumpkinseed fish Lepomis gibbosus: first British record of Onchocleidus dispar (Monogenea)

A survey of pumpkinseed Lepomis gibbosus from a stillwater fishery in southern England revealed infections by the ancyrocephalid monogenean Onchocleidus dispar at 100% prevalence. Host specificity of O. dispar to North American centrarchid fish suggests that it is a non-native parasite, introduced to Britain with L. gibbosus. Mean intensity of O. dispar was significantly higher in male (25.5 parasites) compared to female (15) and immature (7) hosts, but was not influenced by host standard length or sampling time. This sex-biased parasitism is likely to be related to both ecological and physiological factors, such as differential exposure to infective stages during nest building, or higher susceptibility to infection due to enhanced host stress levels. O. dispar significantly dominated the external surfaces and the outer gill arches. Analysis of the spatial distribution of the parasite between the 9 regions of gill surface determined that as density increased, higher numbers of parasites were found on the anterior and central gill regions compared to posterior (distal) regions. Apparent microhabitat selection is discussed in terms O. dispar life cycle, maximising oxygen availability, avoiding unstable areas and increasing intraspecific contact. The absence of O. dispar in the gills of roach, rudd and gudgeon sampled from the same fishery supports the assumption that this parasite is currently of little threat to native fish populations.     

The adaptation of digestive enzymes to temperature, season and diet in roach, Rutilus rutilus L. and rudd Scardinius erythrophthalmus L. 1. Amylase

Seasonal changes of the amylolytic activity in the gut content of roach and rudd in four Tyrolean lakes and the adaptation of the amylase to four acclimation temperatures and to different natural foods were studied. In roach amylolytic activity varied with the environmental temperature. Between September and October, however, enzyme activity shifted to a higher level where it remained for the entire cold season. In rudd, which has almost the same seasonal pattern of amylolytic activity as the roach, the activity of the enzyme is independent of environmental temperature. This suggests an endogenous rhythm of enzyme activity. Under natural conditions the roach, but not the rudd, has a higher amylolytic activity when feeding on animals and a lower activity when feeding on detritus. The laboratory experiments revealed no significant differences in amylase activity between fish feeding on animals and those feeding on plants, although in both species the enzymatic activity was lowest when Chara served as food.     

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.)

The introduction, establishment and subsequent history of a population of Ligula intestinalis in roach, Rutilus rutilus , of a small lake was studied over a period of seven years. The introduction is believed to be a natural, chance colonization achieved by the return of Great Crested Grebes as permanent residents. Within two years the parasite had infected 33% of the roach between 60–120 mm in size. It exhibited a pronounced seasonal cycle in infection. Fish were often infected when only a few months old in autumn, and young fish and parasites over-wintered together. Parasite growth resumed in the following summer, when some further infections occurred. The majority of infected fish died in or before their second winter, possibly as a result of selective predation, but a small proportion survived into a third year. Dispersion of the parasite was close to random for most of the time. Multiple infections and slight over-dispersion occurred only in summer months. Infections were scarcer in large fish, due partly to selective mortality of infected fish and partly to a change in the host diet. The pattern of seasonal infection compared favourably with other localities, but prevalence and intensity of infection were consistently lower, parasite dispersion closer to random and multiple infections much scarcer than elsewhere. Infection levels and parasite growth rates varied from year to year, but these annual fluctuations were irregular and showed no consistent pattern. The Ligula population exhibited both regulatory and destabilizing features and there was no definite evidence that it was stable. It is suggested that Ligula is an opportunist species. It is endemic in some sites but in others, especially small lakes, the populations are unregulated and unstable and so persist for short periods only in a non-equilibrium state.     

The ecological interaction between arctic charr, Salvelinus alpinus (L.), and the plerocercoid stage of Diphyllobothrium ditremum

Six hundred and two arctic charr, Salvelinus alpinus , from a small lake (30 ha) were examined for infection with plerocercoids of Diphyllobothrium ditremum the only species of this genus present; 466 (77.4%) harboured the parasite in an overdispersed infection. The prevalence of infection increased with age and reached 100% at 7+ years for males and 8+ years for females. The rate of infection appeared to be related to the feeding biology of the charr which did not change within the age span studied. The rate of increase in density of infection (plerocercoids per fish) decreased with age as did the degree of overdispersion. It is concluded that the infection probably induces mortality in the fish population, and that such mortality is dependent on parasite density.     

Ontogenetic changes in haemoglobins in roach, Rutilus rutilus (L.) and rudd, Scardinius erythrophthalmus (L.)

The haemoglobins and globins of the roach, Rutilus rutilus (L.) and the rudd, Scardinius erythrophthalmus (L.) have been studied by starch gel electrophoresis. At all stages of development studied, the roach and rudd haemoglobins give a similar electrophoretic pattern, the young fish of about 2 cm standard length possessing three separate haemoglobins, of which two bands only persist in the adult. The evolutionary significance of multiple haemoglobins in fishes is briefly discussed.     

Long-term stability in the population levels of the eyefluke Tylodelphys podicipina (Digenea: Diplostomatidae) in perch

Annual changes in the population size of the metacercariae of Tylodelphys podicipina in the eyes of perch in a small eutrophic lake were studied over ten years by following changes in prevalence, abundance and overdispersion of parasites throughout the life of each year class of fish. The population increased rapidly in the first two years after its introduction to the lake, but for the next six years fluctuated within very narrowly constrained limits before declining as a result of a catastrophic decline in the perch population. No evidence of parasite-induced host mortality was found: the decline in parasite abundance throughout the life of each year class was due to density-independent parasite mortality within the fish as a result of natural variation in the life span of the metacercariae. Levels of infection in the first year of a year class were determined principally by transmission processes, as transmission could only occur over a very brief period when release of cercariae from parent generation snails coincided with the presence of perch fry. Transmission appeared to be density-independent, and infection levels in perch to be determined by the dimensions of the transmission' window' and subsequently modified by parasite mortality. No evidence of host responses or any other regulatory factor of fish origin was found, and the infrapopulations in perch appear to be non-equilibrial and unstable. Although the possibility of regulatory processes acting on infrapopulations of the parasite in other hosts remains, the importance of transmission windows in determining infrapopulation levels in fish is emphasized.     

Reproductive and growth strategies of the red roach, Rutilus arcasii (Steindachner, 1866), in two contrasting tributaries of the River Duero, Spain

The life-histories of red roach were assessed in the R. Moros and the R. Ucero, two contrasting tributaries of the R. Duero. Growth occurred from April to October and Ucero red roach were larger than those in the Moros from their second year onwards. Condition increased with gonad development and abruptly decreased after spawning in both populations. The condition of Ucero fish recovered during the summer, but that of the Moros fish remained low. The same year classes (1980 and 1982) dominated both populations. River Moros red roach spawned in a 4-week period between the end of April and early June, while the spawning season of Ucero red roach lasted until August. The length to fecundity relationship was similar for both populations, and fecundity and ovum size increased with fish length. The life-history traits of these red roach populations are discussed in relation to current life-history theories.