Chapter 7Host Range of Daphnia Parasites

Introduction

Every parasite has a host, but no parasite can infect all potential hosts. Moreover, parasites are usually very limited in the number of host species they are able to infect. Thus, in describing a parasite's host range, one defines its niche. This description usually resembles a list of host species that a parasite is able to infect. The description of the host range usually does not distinguish the degree to which a parasite is able to infect a host and which hosts it prefers to infect. Therefore, the host range, presented as a list of potential host species, cannot tell us much about the evolution and ecology of a parasite, nor about its consequences for the host. Nevertheless, the host range can be, at least locally, a useful tool for identifying certain parasite species and can sometimes even help identify host species by the presence of their specialist parasites.

Host specificity describes the degree to which a parasite is a specialist. This term is often used together with host range, such that a wide host range indicates a low specificity. However, although host range is often described as a list of potential host species, specificity is often used to describe host–parasite associations from a more quantitative perspective, e.g., which hosts are preferred. Host specificity is very important for both ecological and evolutionary aspects of host–parasite interactions. Biologically speaking, any difference in the degree to which a parasite is associated with different host species indicates some degree of specificity. Thus, specificity may range from extreme forms, such as the ability of a parasite to infect only certain members of one host species, to slight differences in the degree to which the parasite infects or harms different host species. To gain a deeper understanding of a particular system, it is also helpful to take into account the consequences of specificity for the host and for the parasite.

For ecological and evolutionary questions, it is also important to consider from whose point of view one considers specificity. For a parasite, a host is suitable if the parasite is able to reproduce in and transmit from this host species. Hosts that do not allow for secondary infections are of little relevance for the parasite's host range, although the interaction may still be detrimental to the host. A host's perspective is different. A host is part of a host range if it can be infected by the parasite, even if the parasite does not do well in this host. Ecologically, this difference in perspective can be important when considering the spread of parasites and the coexistence of host species.

Understanding Host Ranges of Daphnia Parasites

In his review of "Parasites and Epibionts of Cladocera", Green (1974) stated that, "It seems unlikely that many of the parasites and epibionts of Cladocera will prove to be highly specific in their host preference" (page 490). Although I tend to agree with this statement regarding epibionts (for example, Gilbert and Schröder 2003), I think that we lack the necessary data to conclude that parasites are usually unspecific. Some species (e.g., the microsporidium Octosporea bayeri) are known to be highly host species specific. It is clear that we need more studies to reach a general conclusion on this point.

We currently know little about the host ranges and host specificity of Daphnia parasites. When investigating potential hosts, one must consider a number of questions whose answers are not as clear-cut as the relative ease of studying host specificity in Daphnia might suggest. However, this complexity allows us to dig deeper into aspects of host range evolution, which is certainly a very fascinating topic in evolutionary parasitology. Before I discuss how to estimate host specificity, I will briefly outline some problems that are important from an evolutionary perspective.

Results from field and laboratory studies suggest that infections are often highly dependent on the host clones, on the population from which the hosts and parasites were collected, and on the ecological settings in which the data were gathered. Thus, statements about host specificity must take into account variation within and between species and even within populations. For example, Pasteuria ramosa shows very strong host clone–parasite isolate interaction. Within populations, different clones of D. magna vary widely in their susceptibility to different isolates of P. ramosa and vice versa (Carius et al. 2001) (Figure 5.2). Furthermore, P. ramosa can be locally adapted to its host population (Ebert et al. 1998) such that it grows best in hosts from the population from which it was isolated. On the other hand, P. ramosa is able to infect several Daphnia species and even other Cladocerans (Green 1974; Stirnadel and Ebert 1997). Thus, a conservative approach would classify P. ramosa as being rather unspecific with regard to the host species it is able to infect. P. ramosa is, however, highly specific in its interactions with particular host genotypes, in seeming contrast to its apparently wide host range. The reason for this discrepancy is currently not clear. One possibility is that the P. ramosa species is composed from many lines, each with a narrow host range, but all together having a very wide range. However, the alternative, that single P. ramosa genotypes are able to infect only certain host clones within a species as well as certain clones from other species (narrow within host species range but wide range across host species), cannot be excluded, although it seems to go against the intuition of many evolutionary parasitologists. These two hypotheses can be easily distinguished experimentally.

From an ecological perspective, host specificity may not only be defined by the ability of the parasite to infect a host but also by its effect on the host. For example, Caullerya mesnili is able to infect D. galeata and D. hyalina. However, in D. haylina it is rather benign, whereas it is highly virulent in D. galeata (Bittner 2001). Thus, virulence is specific to D. galeata.

Finally, it should be noted that literature reports of the same parasite species in different Daphnia species or the same parasite species in different localities are often not very trustworthy unless they are combined with detailed taxonomic and/or molecular investigations. Because parasites are usually not very rich in morphological characters, it is easy to pool different species into one taxon. It seems likely to me that many currently described parasite species will turn out to be a group of species.

How to Describe and Test Host Ranges

A practical way to judge a parasite's ability to infect different host species based on field data is to compare the prevalence of infections when both hosts are present in the same lake or pond. This method, however, is rather conservative. Bittner (2001) used it to assess the host specificity of seven parasite species, all of which appeared to be somewhat host specific. Using the appropriate statistical test, she found firm support for specificity for only one parasite species. Some of the other parasite species that had appeared to be host specific occurred only rarely or were found only when the other host species was absent, which made a proper comparison impossible. Stirnadel and Ebert (1997) used the same method to classify the specificity of parasites from three populations, each of which had D. magna, D. pulex, and D. longispina occurring in sympatry. Gurleya vavrai was the only parasite unambiguously classified as specific (infecting D. pulex and D. longispina but not D. magna), whereas Metschnikowia bicuspidata, P. ramosa, and an unknown fungal parasite were clearly able to infect all three Daphnia species. Some parasites appeared specific in one pond but unspecific in another pond. Whether these findings are explained by local genetic differences or misidentification of parasites (presence of cryptic species) is not clear. Again, low statistical power for the less common parasites prevented us from reaching firm conclusions for a number of parasite species.

A slightly different approach was used by Bengtsson and Ebert (1998) and by Ebert et al. (2001) in a Daphnia metapopulation context. In these studies, specificity was judged on replication across numerous rock pool populations. If two Daphnia species occur together in a number of rock pools and one of them is significantly more often infected by a certain parasite species, one may conclude that the parasite is specific to this host. Bengtsson and Ebert (1998) found that none of the parasite species they observed were specific to one of the two host species. However, the microsporidium Larssonia sp. showed consistently higher prevalence in D. pulex than in D. longispina whenever both host species were sympatric in a rock pool. Furthermore, Larssonia sp. seemed to have a stronger fitness-reducing effect on D. pulex than on D. longispina. Ebert et al. (2001) found that White Fat Cell Disease and two microsporidians, Ordospora colligata and Octosporea bayeri, were specific to D. magna (not infecting D. longispina and D. pulex). Spirobacillus cienkowskii and Larssonia sp. (possibly the same species as in Bengtsson and Ebert 1998) infected all three Daphnia species. The numerous epibiont species found in rock-pool Daphnia infected all available host species and were even seen to colonize hosts from other taxa, e.g., insect larvae. For the other parasites, no clear statement could be made.

Conclusions

The available evidence suggests that Daphnia parasites differ strongly in the degree to which they are associated with different host species or host clones. Host ranges indicate only the number of host species a certain parasite species is able to infect and can include anything from one to many host species, as well as hosts of different genera or families. Considering specificity from a quantitative perspective, which takes into account quantitative differences in the susceptibility of hosts, every parasite probably shows some degree of specificity. Because the current statistical methods are conservative and some parasites are rare, I believe that more detailed investigation will reveal more examples of specific parasites. Laboratory experiments can best elucidate the host range of parasites with well-defined transmission mechanisms. Parasites that do not transmit horizontally under controlled conditions must be studied by field observation.

References

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