Parasitic plant-host interactions: plant performance and indirect effects on parasite-feeding herbivores

Ecology, July, 1996 by Michelle A. Marvier

INTRODUCTION

The ecological literature has increasingly emphasized the importance of parasites in shaping the dynamics of both plant and animal communities (Gibson and Watkinson 1992, see reviews in Dobson and Hudson 1986, Minchella and Scott 1991, Dobson and Crawley 1994). In particular, generalist parasites such as avian malaria and rinderpest appear to have strong effects on the community structure of their multiple host species (Dobson and Hudson 1986, van Riper et al. 1986). However, one group of common generalist parasites has received little attention from ecologists: the parasitic plants. Parasitic angiosperms are especially attractive models of generalist parasites because they are large and easily manipulated, and because the hosts they attack can be very similar to them both in size and physiological needs. Water, nitrogen, fixed carbon compounds, and minerals are moved unidirectionally from host to parasite through a physical connection, the haustorium (Stewart and Press 1990, Seel et al. 1992). Variation in quality among host species provides the possibility of species-specific effects of plant parasitism, including active choice of some host species by a foraging parasite (Kelly 1990). Host species have been shown to vary both in their ability to tolerate parasitic plant attack and in their capacity to support parasite growth and reproduction, although only a handful of studies have tested for these effects (e.g., Atsatt and Strong 1970, Snogerup 1982, Gibson and Watkinson 1989, Kelly 1990).

However, to fully appreciate the ecological effects of many host-parasite interactions, it is necessary to look beyond direct effects and account for less obvious indirect effects (see review in Price et al. 1986) For example, viral, bacterial, fungal, and metazoan parasites can mediate host vulnerability to predation (Moore 1983, Temple 1987, Hudson et al. 1992, Hechtel et al. 1993) and herbivory (Hammond and Hardy 1988, Linhart 1991). While such studies have examined the indirect effects of parasitism on host - consumer interactions, little work has sought to quantify other indirect interactions involving parasite species, including host effects on parasite - consumer interactions. Further, in studies of microscopic parasites, it is often difficult to fully understand the mechanistic basis for indirect effects (e.g., van Riper et al. 1986, Hudson et al. 1992). In the work reported here, I extend past studies of parasite ecology by simultaneously considering the direct interactions between a parasitic plant and its host plant species as well as the indirect effects of host plant quality on parasite - herbivore interactions.

The intimate relationship between parasitic plants and their hosts, including the direct transfer of compounds from host to parasite, makes it likely that the identity of the host species will strongly influence animals feeding upon parasitic plants, as well as the parasites themselves. The herbivore in my study system may be especially affected by host variation because it is directly linked to the parasitic plant's vascular system. While it has been suggested that plant parasites may indirectly benefit by attacking hosts that supply compounds that defend the parasite from herbivory (Atsatt 1977, Stermitz and Harris 1987, Martin Cordero et al. 1993), there have been few experimental tests of this idea (but see Harvey 1966, Stermitz et al. 1989). Yet the major nutrient requirements and effects of secondary compounds are relatively well understood for plant parasites and for aphids. Therefore, I have combined information on host plant chemistry with experimental studies of host - parasite - herbivore interactions to assess not only the overall strength of different interactions, but also their chemical basis.

A very different motivation for this study is to extend our general understanding of tritrophic interactions. While there has been much speculation about the significance of tritrophic interactions, studies generally either focus on whole trophic levels or are taxonomically limited. The vast majority of species-level studies focus on the interactions among a plant, an insect herbivore, and an insect predator or parasitoid (reviewed in Price et al. 1980, Hare 1992). Host plant - parasitic plant-herbivore interactions represent a novel system well suited for the study of interactions among three trophic levels. While it has long been predicted that these interactions should be analogous to those observed in plant-insect herbivore-parasitoid studies (Atsatt 1977), little work has sought to compare interaction patterns in these two systems.

Here I report the results of a greenhouse study on the direct interactions of a hemiparasitic, or partially autotrophic, plant with three of its major host plant species as well as the indirect effects of this parasitic interaction on an aphid herbivore of the parasite. I chose to begin my investigations of these host - parasite - herbivore interactions with greenhouse studies in order to reduce background variation and thus more easily identify important effects and interactions. I address three aspects of this tritrophic interaction: First, do different host species directly affect the performance of the parasitic plant? Second, do larger parasites directly diminish host growth, and do host species differ in their tolerance of parasitism? Finally, are herbivores that feed on parasitic plants indirectly affected by the identity of the parasite's host?