Lake Maarsseveen Research Articles

Spatiotemporal variation in the distribution of chytrid parasites in diatom host populations

Summary1. Many host–parasite interaction dynamics show distinct seasonality. Parasite population growth and invasion success are generally explained by host density dependence, while the direct influence of environmental factors on parasite life history traits has been underreported.2. In waterbodies, resource availability and environmental conditions change with season (temperature, irradiance and rainfall patterns) and with depth (light, temperature and chemical gradients). Hence, hosts and parasites live in a spatially and temporally variable environment. Such environmental variation leads to structured populations, which in turn have implications for host–parasite interaction dynamics. Nevertheless, time‐series data on the vertical distribution of aquatic hosts and their parasites are rare.3. We present a dataset spanning 1.5 years (2008–2010) of weekly sampling in Lake Maarsseveen (the Netherlands) focussing on the dynamics of the diatom Asterionella formosa and its parasite, the chytrid Zygorhizidium planktonicum, at four depths. Environmental variables measured included ice cover, temperature, global irradiance, light extinction, pH, soluble reactive silicate (SRSi), dissolved nitrate and ortho‐phosphate.4. We observed four host blooms, two in early spring and one each in summer and autumn. Each host bloom was followed by a time‐lagged parasite epidemic. Blooms and epidemics started in the uppermost water layers and showed a time lag in onset date with increasing depth.5. Host abundance was related to SRSi, global irradiance, Schmidt stability and parasite abundance in the upper 10 m, whereas at 15 m only a relationship with parasite abundance prevailed. Parasite abundance was related to host abundance, light extinction, temperature, SRSi, stability and global irradiance within the upper 10 m; again, at 15 m, parasite abundance correlated only with host abundance and disease prevalence.6. Host vertical distribution was less aggregated during isothermal conditions than during thermal stratification, when host abundance was higher in the mixed, photic epilimnion and lower in the dark, colder hypolimnion. Parasite vertical distribution was patchy most of the year. Parasite epidemics seemed to reduce host vertical patchiness as they impacted higher density patches in the photic zone more strongly, a result of both higher host abundance and favourable environmental conditions for the parasite.7. Seasonal variability and vertical gradients in biotic and abiotic factors expose host and parasite individuals to different environmental conditions even within a single population. Environmental variability affects parasite transmission rates through changes in host abundance and through changes in the strength and outcome of host–parasite interactions.

Chytrid infections and diatom spring blooms: paradoxical effects of climate warming on fungal epidemics in lakes

Summary1. We describe the dynamics of host–parasite interactions over a period of more than 30 years between the freshwater diatom Asterionella formosa and two highly virulent chytrid parasites (Rhizophydium planktonicum and Zygorhizidium planktonicum) in Lake Maarsseveen, The Netherlands. This period is characterised by a significant warming trend which is strongest in spring.2. The key spring event in lakes, the diatom bloom, was in many years dominated by Asterionella. We examine whether and how climate warming has affected the prevalence of infection in Asterionella by chytrids.3. In years with cold winters/early springs, a dense Asterionella bloom is followed by epidemic development of disease as high Asterionella densities greatly facilitate transmission of chytrid zoospores. This sequence of events is absent in milder winters.4. Earlier experimental studies have shown that the parasite is almost non‐infective at water temperatures below 3 °C, offering a disease‐free window of opportunity for growth of Asterionella. Climate warming has reduced periods in which water temperature remains <3 °C, narrowing the window of opportunity for uninfected growth. Consequently, Asterionella continuously suffers from infection, albeit at low levels.5. Population reduction as a result of low level infection allows other diatoms to take over as dominant species, possibly through priority effects.6. In mild winters, chytrid infections no longer reach epidemic levels, but remain at low prevalence since transmission is impaired at low host densities. Climate warming thus affects both host and parasite in intricate ways, with the host denied a bloom and consequently the parasite denied an epidemic.7. A shift from Asterionella to a mixed diatom community in years with mild winters may benefit the food web, because of the poor edibility of Asterionella, unless the numerous chytrid zoospores produced during epidemics significantly contribute to zooplankton nutrition.8. Our study demonstrates the potential complexity of climate change impacts on disease. A reduction in the likelihood of epidemic development of a virulent parasite would seem to be of great benefit to the host, but this was not the case. Unexpected, sometimes paradoxical consequences of climate change can be expected and suggest that the view of a ‘warmer hence sicker world’ may not always apply.

Density and depth variations of Daphnia multilocus genotypes during a summer period in Lake Maarsseveen

The genotype composition of a Daphnia population complex during a summer period in Lake Maarsseveen (The Netherlands) was determined by allozyme analysis. The depth distribution, diel vertical migration and several parameters of the total population were measured. Young-of-the-year (0+) perch (Perca fluviatilis) were caught and species and allozyme types of Daphnia in the perch gut were also analysed. During May 1997, the densities of D. hyalina, D. galeata, the back-cross D. g x h – hyalina and the multilocus allozyme genotypes of the hybrid D. g x h decreased, except one multilocus genotype (MMMF). Total population size decreased and the ratio of females with eggs to those without eggs decreased as well. Food limitation during this clear-water phase in the lake is considered responsible. All genotypes, except MMMF, gradually descended in the water column. This drift is thought to be a reaction to the abundantly present 0+ perch or to the kairomones of this fish, although predation on the daphnids was still absent. In June, diel vertical migration started, except again part of the MMMF subpopulation. The other part migrated over a short distance compared with the other taxa and allozyme types. Within two weeks, the upper 5 m of the epilimnion was devoid of Daphnia, and guts of perch were predominantly filled with MMMF. The daphnids in the gut and the lake did not differ in allozyme type composition. By the end of July, population density had increased again. The size and composition of the Daphnia population complex continuously changed during the study period, as did the depth distribution of the components. Different genotypes within the population complex seem to have developed different strategies to cope with starvation and predation and the state at a particular moment can be understood only if past and present factors are considered.

Leptodora kindtii survival in the laboratory

Leptodora kindtii, a pelagic predatory cladoceran, suffers high mortality on transfer to laboratory, which makes the experimental work difficult. We investigated the causes of high mortality, using four variables: water volume, animal density, light intensity, and origin of water for culturing, i.e., water from native or a non-native lake. For the experiments we used Leptodora and water from Lake Loosdrecht and Lake Maarsseveen (The Netherlands). Water was found to be the most important factor; the animals did not necessarily do better in lake water from which they were collected. Water volume and animal density were of limited importance, and light intensity did not affect survival.

GENETIC VARIATION IN ASTERIONELLA FORMOSA (BACILLARIOPHYCEAE): IS IT LINKED TO FREQUENT EPIDEMICS OF HOST‐SPECIFIC PARASITIC FUNGI?1

Understanding of the genetic basis for susceptibility and resistance is still lacking for most aquatic host–parasite systems, for instance, for phytoplankton and their fungal parasites. Fungal parasites can have significant effects on phytoplankton populations, mainly through their ability to decimate algal host populations during epidemics. We used random amplified polymorphic DNA (RAPD) and amplified fragment length polymorphism (AFLP) analysis to study levels of genetic variation within a population of the freshwater diatom Asterionella formosa Hassall in relation to parasitism by the obligate, host‐specific, fungal parasite Zygorhizidium planktonicum Canter. The level of genetic variation within the A. formosa population in Lake Maarsseveen, The Netherlands was found to be high despite the presumed absence or very low frequency of sexual reproduction in this species, the limited gene flow, and the severity of parasite attack that would purge the population from susceptible genotypes. RAPD analysis revealed four distinct banding patterns, with 3 of 21 markers (14%) being polymorphic. In AFLP analysis, every single isolate of A. formosa showed a unique banding pattern, and 120 of the 210 AFLP markers (57%) were found to be polymorphic. Furthermore, character compatibility analysis revealed that sexual reproduction may be one of the mechanisms that generates and maintains genetic variation in the A. formosa population in Lake Maarsseveen. The presence of genetic variation in A. formosa was reflected in infection experiments, which showed that genetically different A. formosa strains differed in their susceptibility to various Z. planktonicum strains and that parasite strains differed in their ability to infect particular host strains.

Density and depth variations of Daphnia multilocus genotypes during a summer period in Lake Maarsseveen

Density and depth variations of Daphnia multilocus genotypes during a summer period in Lake Maarsseveen

Leptodora kindtii survival in the laboratory

Leptodora kindtii, a pelagic predatory cladoceran, suffers high mortality on transfer to laboratory, which makes the experimental work difficult. We investigated the causes of high mortality, using four variables: water volume, animal density, light intensity, and origin of water for culturing, i.e., water from native or a non-native lake. For the experiments we used Leptodora and water from Lake Loosdrecht and Lake Maarsseveen The Netherlands. Water was found to be the most important factor; the animals did not necessarily do better in lake water from which they were collected. Water volume and animal density were of limited importance, and light intensity did not affect survival.

Contrasting migration behaviour of Daphnia pulicaria and D. galeata \boldsymbol× hyalina, in avoidance of predation by 0+perch (Perca fluviatilis)

In spring and early summer, a small population of the large-bodied Daphnia pulicaria coexists with a much larger population of the medium-sized hybrid Daphnia galeata × hyalina in the epilimnion of Lake Maarsseveen (The Netherlands). When large shoals of juvenile perch (Perca fluviatilis) appear in the open water, both species start to migrate vertically. Since D. pulicaria has a larger body-size than D. galeata × hyalina, and is therefore competitive dominant over the hybrid, it is unlikely that both species interact via their common food resource, but they react both to fish predation. However, since they differ in size, and therefore in vulnerability for fish predation, both species adopt different strategies. The smaller bodied, and less vulnerable D. galeata × hyalina exhibits diel vertical migration ascending to the surface at dusk, and staying there during the night. In this way, benefiting from the higher temperatures of the surface layers. In contrast, the large-bodied, and more vulnerable D. pulicaria selects the deep cold hypolimnion water layers as refuge against fish predation. In this way it benefits from a safe habitat, free from fish predators, but on the other hand suffers from low water temperatures, which decrease its fitness. It is likely that the relatively higher temperature in the upper water layers serves as a proximate factor for the downward migration of D. pulicaria.

Relationship between fish kairomone concentration in a lake and phototactic swimming by Daphnia

Light-induced swimming behaviour of Daphnia can lead to diel vertical migration. When this occurs, Daphnia may escape from predation by juvenile 0+ fish. For this to happen, swimming in response to the change in light intensity at dawn and dusk must be enhanced. This enhanced swimming reaction can be elicited by fish-associated kairomone in the laboratory. We studied the effect of these fish-associated kairomones in Lake Maarsseveen, The Netherlands. A bioassay was conducted in which light-induced swimming reactions of Daphnia were used to quantify the kairomone signal strength. In two successive years, 1998 and 1999, water from Lake Maarsseveen was tested weekly in early summer. Samples were taken from the epilimnion at 3 m depth and from the hypolimnion at 15 m depth. Simultaneously, we caught 0+ perch (Perca fluviatilis) with bongo nets to determine its abundance. The length and weight of individuals caught in 1998 were determined to establish a length–weight relationship. Using this relationship and the information on perch density from the trawls, the relative fish biomass was calculated for these two years. It was shown that water from the epilimnion layer increasingly enhanced light-induced swimming reactions until the second week of June, then the effect gradually disappeared. Water from the hypolimnion had no such effect. In 1998, these changes in signal strength correlated with the relative biomass of the 0+ perch, but in 1999, the maximum of the enhancement lagged 2 weeks behind the maximum of the biomass of the 0+ perch. This lag may be due to a different development of the thermocline. We conclude that kairomone concentration may well correlate with 0+ perch biomass and thereby might inform Daphnia not only about the presence, but also about the abundance, of juvenile perch.

The attenuation of ultraviolet and visible radiation in Dutch inland waters

The vertical attenuation coefficients (Kd) of downward ultraviolet (UV) and visible irradiance (PAR) were measured in 19 different inland waters in the Netherlands using a scanning spectroradiometer. Water chemistry variables such as dissolved organic carbon (DOC), absorbance of dissolved matter (ad), chlorophyll-a, and particulate matter were measured to determine the relative contribution of dissolved and particulate components in explaining the variation in Kd. In addition to the field measurements, laboratory measurements were performed to test the relationships between water properties and light attenuation. The attenuation properties of Dutch inland waters vary. In most systems the penetration of UV-B radiation (280–320 nm) is limited to the upper decimetres. Lake Maarsseveen was the clearest waterbody in this study, with KdUVB of 9.1 (m−1). The DOC concentration had limited power in predicting UV attenuation in this study (r2=0.33), because of the large differences in carbon-specific absorption. Ad300 was a much better predictor of UV attenuation (r2=0.75). The relationships obtained in the laboratory experiments can be used to give a good prediction of in situKd values, based on 3 variables (chlorophyll-a, ash weight, and absorption of dissolved matter).

Light-induced migration behaviour ofDaphniamodified by food and predator kairomones

Lake-dwelling waterfleas,Daphnia, often face a dilemma. Food availability is highest, near the water surface, but predation by visually hunting predators is also most severe. Swimming downward at dawn reduces predation risk, but food availability and temperature also decrease with depth. We tested whetherDaphniaprocess information derived from food and predator presence to estimate the costs and benefits of migration, and to determine when it pays to swim down. We studied downward swimming ofD.galeata×hyalinain response to stepwise accelerations of relative increases in the intensity of light at several food and fish kairomone concentrations. Both had a modifying, additive, although independent effect. We studied in six clones the clonal differences of this environmentally induced plasticity of photobehaviour. These clones were caught at two depths at noon during a period of vertical migration in Lake Maarsseveen (the Netherlands), and so presumably differed in vertical migration behaviour. Two clones, one from the epilimnion and one from the hypolimnion, showed a particularly significant difference in migration behaviour.

Differential life history responses of several pelagic Daphnia clones differing in migratory behaviour

Females of the hybrid Daphnia galeata × hyalina were isolated from a natural population in Lake Maarsseveen and from these individuals clones were cultured in the laboratory. Some clones were assumed to be migrating and some non-migrating. Life history experiments were performed with these clones in the presence and absence of fish kairomones. Results show that clones differed in life history strategy in concert with their presumed migration strategies which suggests a link between life history and behaviour. However, no sharp border exists between migrating and non-migrating clones since a gradual response pattern was found for the traits investigated. In the absence of fish kairomones, the relation between length at maturity and number of eggs was found to differ between the clones of the non-migrating and the migrating group. The latter had a lower number of eggs at similar length values. In the presence of fish kairomones, the length–clutch size relation was the same. However, non-migrating clones were smaller at the age at maturity and had fewer eggs. Although clones of both groups were thus found to differ significantly, overlap existed. Age at maturity was found to be the same.

Quantitative effects of fish kairomones and successive light stimuli on downward swimming responses of Daphnia

Swimming in response to light change is considered the proximate mechanism underlying diel vertical migration. This behavioural mechanism is supposed to be tuned to the adaptive needs under natural conditions by the modifying influence of environmental variables, such as predator kairomones. We investigated to what extent fish kairomone level affects downward swimming in response to a continuous relative light intensity increase. At the higher kairomone levels Daphnia had significant higher displacement velocities. Thus, kairomone was perceived quantitatively and behaviour was altered correspondingly. Because the absolute difference in displacement velocity between treatments was small, we assumed that kairomone concentration could not explain much of the seasonal variability in diel vertical migration patterns in Lake Maarsseveen. Therefore, we hypothesised that besides swimming in response to relative changes in light intensity, other aspects of phototaxis were important also. The natural light intensity increase at early morning consists of a continuous increase in the rate of the relative light intensity change, which reach a maximum about 30–45 min before sunrise. After this maximum, the rates of the relative light intensity increase decrease again. Thus far, it was assumed that successive changes in light intensity acted independent on the swimming reaction of the daphnids. In this paper, we present results of experiments with Daphnia swimming in response to a combination of a continuous and an instantaneous increase in light intensity. A continuous relative light increase preceding an instantaneous increase in light intensity (step) enlarged the downward displacement velocity of Daphnia markedly. Hence, successive light stimuli did not act independently. With growing relative light increase rates preceding the step, the displacement velocity increased also. Moreover, the presence of fish kairomone further increased the velocity in response to the light change. Therefore, the rate of the relative change in light intensity is an incomplete description of the stimulus for diel vertical migration behaviour.

Two examples of the interplay between field observations and laboratory experiments from 35 years of research with planktonic organisms

Two studies of complicated ecological phenomena in Lake Maarsseveen (The Netherlands) are presented to illustrate that a combination of field and laboratory analysis might be a successful approach. In the first one, the yearly varying ratio of population abundance of two diatoms, Asterionella formosa and Fragilaria crotonensis during early spring is explained by a combination of abiotic and biotic factors. A fungal parasite blocks population development of the first species at temperatures higher than 3–5 °C . The second species then competes successfully for phosphate and develops a large population. The interaction between Asterionella and the fungus proved to be intricate. Several physiological mechanisms operate together and combined with variable climatic factors makes the prediction of what species will be dominant, impossible. In the second example diel vertical migration of the hybrid Daphnia galeata × hyalina is analysed in the field and the laboratory. Migration is confined to six to seven weeks in June–July when large shoals of juvenile perch are present in the pelagic zone of the lake. These fish exudate a kairomone that enhances the reaction of Daphnia to relative increases in light intensity of dawn. Especially accelerations in rate of relative increases enhance swimming velocity. The extent of enhancement depends, however, on the concentration of the kairomone and on food concentration. A ’Decision Making Mechanism‘ is introduced and the relation between the response mechanism and the adaptive relevance of diel vertical migration is made.Finally considerations about research strategies and the importance of fundamental research are made. It is concluded that the development of limnology and aquatic ecology might be in danger when the present tendency to give prevalence to applied research continues. [KEYWORDS: strategies of plankton research, field observations, laboratory experiments, phytoplankton succession, fungus epidemics, diel vertical migration]

Seasonal dynamics and spatial distribution of chydorid cladocerans in relation to chironomid larvae in the sandy littoral zone of an oligo-mesotrophic lake

The seasonal variation of the principal macro- and meiobenthic taxa in the sandy littoral zone of the oligomesotrophic Dutch Lake Maarsseveen I was studied during two years. Population peaks of the different taxa were clearly separated in time. In early spring there were chironomid density peaks of Stictochironomus sticticus, in one year followed by a Polypedilum maximum. From June–July chydorid cladocerans dominated, with a peak of Monospilus dispar followed by a peak of Rhynchotalona falcata. In autumn the chironomid Cladotanytarsus mancus became dominant, remaining so throughout the winter. To study the spatial heterogeneity of the major macro- and meiofaunal taxa, samples were taken in a grid of 2.5 × 10 m. Distributions of all but one taxon were significantly different from random, with Morisita indices varying from 1.23 (chironomids) to 2.10 (the chydorid Monospilus dispar). Wind-induced disturbance presumably had strong and species-specific effects on littoral macro- and meiobenthic taxa. Chydorid heterogeneity increased immediately following the first autumn storm of the season; this may be explained by the tendency of these organisms to remain attached to detritus particles. Temporal and spatial correlation coefficients between macro- and meiobenthic taxa were generally low, suggesting that interactions between these groups are weak, with distribution patterns that are independent of each other. Among the meiofaunal taxa, positive spatial and temporal correlation coefficients were found; apparently, the similarity in both seasonal dynamics and spatial distribution is larger among the meiofaunal taxa than between macro- and meiofaunal taxa. Also among most of the chironomid species significant positive temporal correlations were found, except for Stictochironomus sticticus and Polypedilum sp.; these species have similar life-cycles, but were during one year temporally separated by several alternating settlement peaks. In the next year, Polypedilum disappeared completely following an extremely strong Stictochironomus settlement peak.

Increased phototaxis in the field leads to enhanced diel vertical migration

Downward and upward displacement velocity of diel vertical migration in Lake Maarsseveen by the hybrid Daphnia galeata × hyalina, was correlated with the relative change in light intensity at dawn and dusk, indicating a phototactic basis for these migrations. The significance of the regression function increased over a period of 4 yr. Changes in environmental factors such as water transparency and food concentration are not responsible.

Micro-environment of chironomid larvae in the littoral and profundal zones of Lake Maarsseveen I, The Netherlands

Micro-environment of chironomid larvae in the littoral and profundal zones of Lake Maarsseveen I, The Netherlands

Temporal and spatial patterns of water mites in Lake Maarsseveen I

The paper analyses the distribution and seasonal changes in numbers of the water mite fauna of Lake Maarsseveen I. Water mites were collected from 1977 until 1986 by dipnet, underwater light trap, hydraulic lift sampler and by frame net. Fifty-two species belonging to the Hydrachnellae and one to the Halacaridae were sampled. The faunal picture obtained is characteristic of mesotrophic to eutrophic lakes.Arrenurus nobilis. Piona paucipora andP. imminuta can be characterised as lake species. The dominant species in the littoral sand flat areHygrobates nigromaculatus andH. trigonicus, at a depth of 0.5–1 m, andMideopsis orbicularis at depths of 2–7 m.Limnesia maculata is also very common on depths between 2 and 7 m. In early summer, however, they prefer shallow water up to 1 m depth.

Distribution and seasonality of desmids in the Maarsseveen Lakes area

The desmid flora of mesotrophic Lake Maarsseveen I, eutrophic Lake Maarsseveen II, as well as the interconnecting broads was studied during the period 1987–1991. Seasonal perodicity of euplanktonicStaurastrum andCosmarium species in the two Maarsseveen lakes fitted the well-known general pattern of desmid abundance peaks in (late) summer time. The deviating seasonality of two euplanktonicClosterium species (C. aciculare andC. acutum var.variabile) could be related to special nutritional demands. The tychoplanktonic desmid flora encountered in the interconnecting system of peat pits and canals proved to be more diversified as the influence of nutrient-poor seepage on the habitat (appearing from conductivity, transparency and the occurrence of particular macrophyte species) was greater. The rare speciesEuastrum germanicum andHeimansia pusilla had been only incidentally recorded in The Netherlands.

Factors governing the spatial and temporal distribution of Chironomid larvae in the Maarsseveen lakes with special emphasis on the role of oxygen conditions

Distribution patterns of the larvae of Chironomidae are compared in three water systems in The Netherlands, which vary in trophic state and oxygen regimes. The life cycles and flying periods of some dominant chironomid species in two of the investigated lakes, Lakes Maarsseveen I and II, are determined by comparing data on the seasonal variations in larval densities with existing literature on Chironomidae in the Maarsseveen lakes. In the oligo-mesotrophic Lake Maarsseveen I (LM I), hypoxic or anoxic conditions in the hypolimnion are observed only at the end of the stratification period. A clear zonation of the chironomid fauna is present in this lake. The littoral zone is dominated byCladotanytarsus gr.mancus andStictochironomus sticticus, the littoriprofundal zone byTanytarsus bathophilus, and the profundal zone byChironomus anthracinus. In comparison with the other species in LM I,T. bathophilus larvae show the most variable distribution patterns over time. Larvae are found in all depths from July to September, but disappear from the hypolimnion as soon as oxygen conditions deteriorate. In the eutrophic Lake Maarsseveen II (LM II), oxygen depletion of the hypolimnion starts immediately after the onset of the thermal stratification in June, and continues until autumnal turnover in November. In this lake, the chironomid community consists primarily ofS. sticticus andCl. gr.mancus, and is confined to the narrow littoral zone. No chironomid larvae are found in the deeper parts of the lake. The eutrophic Lake Gijster in the Brabantse Biesbosch is a deep, man-made reservoir, that is artificially destratified during the summer. In this lakeTanytarsus bathophilus is found in the profundal sediments, whereas almost noChironomus is found in this zone. It is concluded that oxygen conditions existing in the deeper regions of the investigated lakes in large part determine the occurrence and distribution of chironomid species. The distribution ofT. bathophilus is limited by unfavorable oxygen conditions and not by the trophic state of the lake.