How soil-borne pathogens may affect plant competition

Ecology, Sept, 1997 by Wim H. Van Der Putten, Bas A.M. Peters

INTRODUCTION

Competition is generally regarded as an important ecological factor structuring the composition and diversity of natural communities in space and time (Grace and Tilman 1990). In many cases, direct competition between two species from the same trophic level will be affected by species from other trophic levels. Herbivores, mutualists, and pathogens should be taken into account when considering competition between plants, but the resulting effect may be difficult to predict (Clay 1990). Holt (1977, 1984) presented an example of shifts in relative prey densities mediated by an enemy shared by them, which could not be related to any direct effects between the prey. This was called "apparent competition" (Holt 1977, Connell 1990).

Effects of pathogens have been mentioned in recent literature on plant competition (Clay 1990, Louda et al. 1990), although few examples are presented. This is most likely due to a rather recent interest of ecologists in pathogens as a structuring force in natural vegetation (Burdon 1987). Although Clements (1928) suggested pathogens were involved in changes in the composition of natural vegetation, most examples still originate from the last decade or two (Dobson and Crawley 1994). The majority of these studies concern pathogens that parasitize the aerial parts of plants (e.g., Burdon 1982, 1987, Burdon et al. 1984, De Nooij 1987, Augspurger 1989, Paul 1989, Linders 1994, Castello et al. 1995, Jarosz and Davelos 1995) and refer to a variety of habitats. Very few of these examples on aboveground pathogens, however, concern competition within (Burdon et al. 1984) or between plant species (Paul 1989).

There are fewer examples of soil-borne pathogens in natural vegetation than of aboveground pathogens and their effects on plant competition have not yet been demonstrated. Studies on soil-borne pathogens in natural vegetation are mainly confined to coastal sand dunes (Oremus and Otten 1981, Van der Putten et al. 1993, Zoon et al. 1993, De Rooij-Van der Goes et al. 1995a, b), tropical rain forests (Augspurger 1990), and old fields (Bever 1994). The presence of specific soil pathogens in a successional sere of plants in coastal sand dunes (Van der Putten et al. 1993) should have consequences for competitive interactions among the successive plant species (Crawley 1993). In soybean (Glycine max) the soybean cyst nematode (Heterodera glycines) reduced the competitiveness of its host against the weed common lambsquarters (Chenopodium album) (Chen et al. 1995). This example, although originating from agriculture, supports the hypothesis that soil pathogens may be involved as an indirect factor in interspecific plant competition.

The present study tested the hypothesis that specific soil-borne pathogens affect competitive interactions between plant species. Because effects of soil pathogens on plant competition were not significant in studies of Bever (1994) or in our pilot experiments, the focus of the present work is the influence of experimental conditions affecting the role of soil-borne pathogens in plant competition.

As a model we used the replacement of Ammophila arenaria by Festuca rubra ssp. arenaria, representing one of the first successional stages in coastal sand dunes of northwestern Europe. At sites near the beach, where plants are regularly buried by wind-blown sand, A. arenaria dominates the vegetation, as no other plant is able to survive such extreme conditions (Ranwell 1958). More landward, where both the rate and amount of sand accretion diminish, the vigor of A. arenaria declines (Marshall 1965, Hope-Simpson and Jefferies 1966, Huiskes 1979, Willis 1989) and Festuca rubra ssp. arenaria takes over dominance in the vegetation (Anderson and Taylor 1979, Huiskes 1979). Plant-parasitic nematodes and pathogenic fungi in the root zone of A. arenaria are implicated in this degeneration (Van der Putten et al. 1988, 1990, De Rooij-Van der Goes 1995, De Rooij-Van der Goes et al. 1995a, b) and F. rubra is relatively tolerant to the pathogens of its predecessor (Van der Putten et al. 1993).

According to our hypothesis, A. arenaria will be less competitive against F. rubra ssp. arenaria when grown in unsterilized sand from its own root zone than in this sand after sterilization. As a result, A. arenaria will be relatively less productive in mixtures with F. rubra ssp. arenaria in unsterilized than in sterilized soil from its own root zone. The hypothesis was tested by three greenhouse experiments. Two were pilots to study effects of nutrients and soil moisture on initial growth conditions. The results from these experiments were used to choose nutrient and soil moisture conditions for the competition experiment. An unfertilized control was included to examine whether the applied nutrient solution masks effects of mutualists, such as mycorrhizal fungi.

METHODS

Sampling and treatment of the soil

At the coastal foredune of Voorne, The Netherlands, soil samples were collected from the upper 30-cm soil layer of a site near Haringvlietdam (51 [degrees]52' N, 4 [degrees]4' E) covered by a monospecific stand of A. arenaria. Just landward of this successional stage, F. rubra ssp. arenaria (hereafter called F. rubra) started to invade the vegetation. The site was subject to annual burial by 20-30 cm of wind-blown sand (Van der Putten et al. 1989), so that the collected soil contained mainly 1-yr-old roots of A. arenaria.