Ecology, Epidemiology, and Evolution of Parasitism in Daphnia

  1. Introduction to the Ecology, Epidemiology, and Evolution of Parasitism in Daphnia
  2. Introduction to Daphnia Biology
  3. Some Parasites of Daphnia
  4. Parasitism in Natural Populations
  5. The Effects of Daphnia Parasites on Host Fitness
  6. Host Adaptations against the Costs of Parasitism
  7. Host Range of Daphnia Parasites
  8. Epidemiology
  9. Population Dynamics and Community Ecology
  10. Experiments with Daphnia and Parasites

9 Population Dynamics and Community Ecology

Although much research has examined the effect of parasites on individual hosts, relatively little work has been done to address the impact of parasites on the host population, in particular on host population dynamics. Here I describe what is known about the impact of Daphnia parasites on host population density and persistence. A number of parasites have been shown to reduce host density and to reduce population persistence in experimental populations. Consistent with epidemiological models, the strength of these effects was highest for parasites that also have the strongest effect on reducing host fecundity. Thus far, little is known about the community ecological effects of parasites. The available data suggest, however, that parasites have the potential to influence competition among host species.

  1. Background
  2. Do Parasites Regulate Host Populations?
  3. Do Parasites Influence Host Community Structure?
  4. Factors Structuring Parasite Communities
  5. Conclusions and Open Questions

9.1 Background

Over the last decades, researchers have believed that freshwater zooplankton population dynamics were shaped by inter- and intraspecific competition and by predation. Only recently have parasites been recognized as a factor in the ecology and evolution of plankton communities. In their pioneering work, Canter and Lund (1951, 1953, 1968) showed that a fungal microparasite strongly altered the dominance hierarchy of a phytoplankton community in an English lake. Unfortunately, this work has not stimulated much research in the field. In particular, very little work has addressed the effect of parasites on zooplankton dynamics.

A number of studies using diverse host–parasite systems have shown that parasites can influence their host populations either by reducing host density or even by driving host populations to extinction (Park 1948; Finlayson 1949; Keymer 1981; Kohler and Wiley 1992; Hudson et al. 1998). These studies provide evidence that parasites can regulate their host populations and that some parasites are more likely to do so than others. Thus, one might also expect that zooplankton populations are regulated by their parasites. Ideally, one would like to predict which parasite features affect host population levels and under which conditions parasite effects are seen at the host population level. Several theories have been developed to understand whether variability in the effects of parasites on host fecundity and survival are reflected in host population dynamics (Anderson and May 1978; May and Anderson 1978; Anderson 1979; May and Anderson 1979; Anderson 1982; May and Anderson 1983; Anderson and May 1986; Anderson 1993). A key question is whether processes at the individual level translate to effects at the population level. We have good empirical data on processes at the individual level (e.g., pathogenicity) for a number of host–parasite systems but little on population-level processes.

Mathematical models predict different population dynamics for hosts infected with microparasites that reduce host fecundity versus those infected with parasites that reduce host survival (Anderson 1979, 1982). Host density is predicted to decrease monotonically, with the negative effect that a parasite has on host fecundity (all other things being equal). In contrast, mean host population density is predicted to first decrease and then increase as parasite-induced host mortality rises. This is because (for a given transmission rate parameter) parasites that kill their hosts very rapidly are less likely to be transmitted to other hosts and will, therefore, remain at low prevalence, whereas parasites with little effect on host mortality will have little effect on host demographics. These epidemiological models also predict population fluctuations, positing that host density fluctuations increase as a microparasite shows an increasingly negative effect on host survival and fecundity. According to these models, density fluctuations increase the chance of extinction of small host populations because host density is more likely to drop to zero during population bottlenecks (May 1974; McCallum and Dobson 1995). Epidemiological models, such as those cited above, have often been used to explain empirical results in situations where parasites reduced the density of their hosts or contributed to the extinction of the host population. The same models predict that benign parasites have little effect on host population densities and therefore can be applied equally well to cases where parasites have little or no apparent effect on host population dynamics. Therefore, along with contrasting parasitized with nonparasitized populations, it is important to compare host populations infected by parasites with different effects on host fecundity and survival.

9.2 Do Parasites Regulate Host Populations?

A review of field studies on parasitism in Daphnia populations (see Chapter 4, Generalizations about Parasitism in Natural Populations) reveals very little about the population-level effects of parasites on their hosts. Because there are no replicates or control populations without parasites in field studies, it is difficult to draw conclusions about population-level effects. To my knowledge, only Brambilla (1983) has attempted to analyze his data for possible population-level effects of parasitism. He tested for the effect of the microsporidium Thelohania on the instantaneous birth and death rates in a longitudinal study of a D. pulex population and compared these rates with rates calculated under the assumption that the parasite was absent from the population. The impact of the parasite on birth rate varied widely over the summer and across the year but was generally stronger than it was for the death rate. For nearly all sampling dates, he calculated that the parasites decreased the population growth rate, r, by about 20% on average. He states, however, that the parasite alone probably does not regulate the population growth of its host, because r varied substantially, independent of parasitism (Brambilla 1983). He was not able to carry out laboratory experiments.

Population-level experiments with Daphnia parasites were first proposed by Ebert and Mangin (1995), who showed that D. magna populations infected with the microsporidium Flabelliforma magnivora (in their paper called Tuzetia sp.) had a lower density than uninfected control populations. This parasite is exclusively vertically transmitted under laboratory conditions (horizontal transmission has not been found for this parasite) and was present at a prevalence of 100%. Therefore, one can exclude density-dependent transmission as the regulatory factor. Because exclusively vertically transmitted parasites in asexual populations behave like a deleterious gene (Mangin et al. 1995), the reduced density is a direct consequence of the reduced fecundity and survival of the hosts.

Ebert et al. (2000a) compared the effects of six parasites on the fecundity and survival of individual hosts to their effects on host population density and the host's risk of extinction. Five horizontally transmitted microparasites (two bacteria: White Fat Cell bacterium, Pasteuria ramosa; two microsporidia: Glugoides intestinalis, Ordospora colligata; one fungus: Metschnikowia bicuspidata) and six strains of a vertically transmitted microsporidium (F. magnivora) of D. magna were used. Life table experiments quantified fecundity and survival in individual parasitized and healthy hosts and compared these with the effect of the parasites on host population density and on the likelihood of host population extinction in microcosm populations. Parasite species varied widely in their effects on host fecundity, host survival, host density reduction, and the frequency with which they drove host populations to extinction (Figure 9.1

Figure 9.1
). The fewer offspring an infected host produced, the lower the density of its population. This effect on host density was relatively stronger for vertically transmitted parasite strains than for the horizontally transmitted parasites. There was no clear relationship between the reduction in host density and the effect of parasites on the survival of individual hosts. As predicted by stochastic simulations of an epidemiological model, if a parasite had strong effects on individual host survival and fecundity, the risk of host population extinction was also increased. The same was true for parasite extinctions.

Bittner et al. (2002) showed that the gut parasite Caullerya mesnili is not only able to reduce density in experimental D. galeata cultures severely but also that it is able to drive the host population to extinction. This result is consistent with the study by Ebert et al. (2000a), which showed that C. mesnili is highly virulent, reducing host fecundity strongly and shortening the host's life span substantially. This parasite was also able to alter the outcome of competition among two competing Daphnia species. In the absence of the parasite, D. hyalina was inferior to D. galeata, whereas in its presence, D. hyalina was the superior competitor (Bittner 2001).

In a 27-week time series study of Glugoides intestinalis-infected D. magna cultures, Pulkkinen and Ebert (2004) found no significant reduction in host density, nor did they record a single case of host or parasite extinction. Again, these results are consistent with the predictions and results of Ebert et al. (2000), because G. intestinalis is comparatively avirulent, reducing host fecundity by only about 20% and barely influencing host survival.

In summary, parasites in experimental Daphnia populations have been shown to reduce host density and population survival. In particular, as the theory predicts (Anderson 1982; Ebert et al. 2000), parasites with strong effects on host fecundity are powerful agents for host population regulation. Thus far, all experiments have been conducted under laboratory conditions, i.e., with constant food supply, constant temperature, absence of predators, etc., so that the populations closely reflected an idealized host–parasite system, as many standard epidemiological models envision (Anderson 1979, 1982; Ebert et al. 2000). However, although these experiments have helped us understand the mechanisms of host–parasite epidemiology, they have not answered the question of whether parasites regulate natural Daphnia populations, a question that may require experimental epidemiology under more natural conditions (e.g., mesocosm populations).

9.3 Do Parasites Influence Host Community Structure?

Thus far, we have discussed the impact of parasites on single host species. As a further step, one might ask whether parasites can influence entire host communities. Two characteristics of parasites place them in a prime role to affect community ecology. First, they are often specific in the effect on their hosts, and second, they may exert strong harm on their hosts, influencing the host's competitive ability. A few data suggest that parasites of Daphnia may indeed play a role in the structure of their host's community.

Wolinska et al. (2004) studied parasitism in a pre-alpine lake (Greifensee) in Switzerland. In this lake, D. galeata x hyalina hybrids co-occur with the parental taxa. Interestingly, during the study period, hybrids were the most abundant taxon. The Daphnia community in this lake is parasitized by C.mesnili, which is known to be rather virulent (Bittner et al. 2002). Prevalence reached peaks of 22%, and C. mesnili dramatically reduced Daphnia fecundity. A comparison among the different taxa revealed that hybrids were frequently infected, whereas parental D. galeata (the other parent species, D. hyalina, was rare during the study period) were almost never infected. The authors speculate that the resistance of D. galeata might counterbalance the greater fitness of hybrids. This could stabilize the coexistence of the parental species with the hybrids in Lake Greifensee. It is not clear whether the high susceptibility of the hybrids is a general phenomenon or specific to this population. In any case, the finding adds an important aspect to the puzzling question of hybrid maintenance in natural Daphnia populations and hints at a role of parasites in shaping Daphnia communities.

Bittner (2001) took an experimental approach to study the role of C. mesnili in a two-species community of D. galeata and D. hyalina in Lake Constance. To test whether this parasite, which frequently parasitizes both species, influences their relative competitive ability, Bittner set up a number of population-level experiments in which clones of both Daphnia species competed in the presence and absence of the parasite. Clones were tracked with the help of multi-locus enzyme electrophoresis, and the experiments resulted in a very clear pattern. In the presence of C. mesnili, D. hyalina was the superior competitor, whereas it was inferior in its absence. This finding was consistent across several clones of both species. Of interest, D. hyalina is not completely resistant to the parasite but seems to suffer much less under the costs of parasitism. Bittner's results (2001) show clearly that parasites do have the potential to alter competition in a plankton community. However, although the experiments convincingly demonstrate the mechanism, they do not provide us with a way to judge the importance of this mechanism in natural communities.

In summary, because of their differential effects on different host taxa, parasites have the potential to influence competition in Daphnia communities, much in the same way as they influence clonal competition within a species (Capaul and Ebert 2003; Haag and Ebert 2004) (Figure 6.2

Figure 6.2
). We know little about the strength of this mechanism under natural conditions and about the role of predation in this phenomenon. A combined approach with experimental and observational work in the field may help to clarify the role of parasites in shaping Daphnia communities.

9.4 Factors Structuring Parasite Communities

In several places in this book, I have discussed that parasiteabundance may be negatively influenced by other natural enemies of Daphnia, in particular by planktivorous fish. See the sections "Are There Less Parasites in Lakes with Fish?" in Chapter 4 and "Suggestion for a Lake Model" in Chapter 8 for more details. Predation by visually hunting fish would not only suppress certain parasites species during particular time periods, or completely (Duffy et al. 2005), but would also influence the parasite community by disfavoring parasite species that make their hosts more susceptible to predation, for example, by making their hosts more visible. Although we are starting to understand the dynamics between fish and certain parasites, we do not know anything about the community-level consequences of this relationship.

Another factor that affects parasite communities is interspecific competition. Because hosts are limited resources, within-host competition may be intense and may influence the success of a species on the community level, particularly among parasites with ecologically similar niches (Kuris and Lafferty 1994; Lafferty et al. 1994; Poulin 1998). The best evidence for interspecific competition comes from epibionts rather than endoparasites. Competition was favored as an explanation for the presence/absence patterns of epibionts in two rock-pool metacommunity studies in southern Finland (Green 1957; Ebert et al. 2001). The peritrich Vorticella octava was found to be negatively associated across rock pools with the peritrich Epistylis helenae and the green algae Colacium vesiculosum. All three species primarily colonize the head and dorsal regions of the Daphnia carapace. However, V. octava was found together with E. helenae and C. vesiculosum much less often than chance would suggest, whereas Epistylis and C. vesiculosum occurred independently of each other. This may occur because of the different space requirements of these epibionts on the host's body surface. Colacium has a short stalk, whereas V. octava and E. helenae have long stalks and may form a canopy over Colacium. Moreover, E. helenae has a noncontractile stalk, whereas V. octava has a contractile stalk that, when it contracts, forms a spiral larger than the diameter of the stalk. This contraction may cause a mechanical disturbance to both Colacium and Epistylis and lead to stronger competition (Green 1957). Thus, V. octava may suffer from strong interspecific competition because it interferes mechanically with both E. helenae and C. vesiculosum, whereas the two latter species do not compete as strongly with each other because they are somewhat separated in space.

Earlier, Green (1955) had shown experimentally that peritrichs (species not given) compete with C. vesiculosum and that light is an important factor in determining the outcome of competition between algal epibionts (favored under strong light) and peritrich ciliates (favored under poor light conditions). Across several individuals within a population, this competition leads to a negative correlation between the number of peritrichs and the number of C. vesiculosum (Figure 9.2

Figure 9.2
). The strong variation in epibiont composition across individuals may reflect individual differences in behavior. For example, clones with a phototactic-positive behavior may have more algae than phototactic-negative clones.

These findings clearly demonstrate the strength of within-host competition for shaping entire metapopulation communities. The clearness of the patterns is surprising, however, given that similar strong patterns are rarely seen from other parasites. I speculate that a combination of specific host–epibiont interaction factors play a role here. First, Daphnia molt every few days (1-2 days as juveniles and 3-4 days as adults at 20°C). After molting, the carapace is clean, and epibionts struggle to recolonize it (Threlkeld et al. 1993). Thus, competition for space is reset after every molt, strongly diminishing the role of history (who colonizes first) and leading to stronger homogenization among hosts in the entire population. Second, the low virulence (harm done to the host) caused by epibionts decouples host mortality from the action of epibionts. Third, there is likely to be little or no immune defense of the host against epibionts. All of these factors are different for endoparasites, which are unaffected by host molting but are affected by the immune response of the host and may be virulent for the host. To my knowledge, no study has yet demonstrated parasite competition in plankton hosts.

9.5 Conclusions and Open Questions

It seems rather clear that parasites have the potential to influence host population dynamics and communities and that interspecific competition and ecological factors affecting the host influence parasite communities. What we are lacking are general patterns that would allow us to make predictions for systems we have not yet studied. For this, we need to study not one species or one community at a time but several in parallel. A number of issues have not yet been addressed regarding plankton parasites. Here I suggest a few questions for further research:

  1. Some parasites may alter the outcome of host competition. Which properties of a parasite affect host competition, and which do not?
  2. Is there interspecific competition among endoparasites in plankton hosts?
  3. Are there trade-offs between competition at different levels? For example, a parasite might be a good competitor on a host but is poor in dispersal among hosts or among populations.
  4. Do evolutionary processes (e.g., clonal selection) influence community aspects?