Grazing Optimization, Nutrient Cycling, and Spatial Heterogeneity of Plant-Herbivore Interactions: Should a Palatable Plant Evolve?

Abstract

Abstract. Can the evolution of plant defense lead to an optimal primary production? In a general theoretical model, Loreau (1995) and de Mazancourt et al. (1998de Mazancourt et al. ( , 1999 have shown that herbivory could increase primary production up to a moderate rate of grazing intensity through recycling of a limiting nutrient, provided several conditions are fulfilled. In the present paper, we assume: (1) grazing intensity is controlled by plants through their level of palatability; and (2) plant fitness is determined by its productivity. We explore the conditions under which such an optimal production may be reached through natural selection. We model two competing plant types that differ only in palatability and are distributed in a patchy landscape determined by the plant-herbivore interaction. Patch size is determined by herbivore behavior: herbivores recycle nutrient homogeneously within patches, but recycle nutrient proportionally to consumption between patches. The model shows that a strategy of intermediate palatability can be adaptive in response to a small herbivore that lives on and recycles nutrient around one or a few individual plants. For moderately small herbivores, plant palatability may evolve towards one of two local convergent strategies, depending on the initial conditions. For medium-to large-sized herbivores, the nonpalatable strategy is always selected. We discuss the functional and evolutionary implications of these results, and suggest that the traditional dichotomy describing antagonistic and mutualistic interactions may be misleading.Key words. Antagonism, grazing optimization, group selection, indirect effect, maximum power principle, mutualism, patchy environment, plant defense, plant palatability, primary production, spatial heterogeneity.Received August 5, 1998. Accepted July 12, 1999 Can plant-herbivore interaction be mutualistic? Plant-herbivore interactions have traditionally been considered antagonistic because herbivores have a negative direct effect on plants through biomass consumption. This assumption has been challenged by the grazing optimization hypothesis, which states that herbivores can enhance plant primary production (McNaughton 1979;Hilbert et al. 1981;Dyer et al. 1986): primary production can increase with low grazing intensity and reach an optimum at intermediate grazing, before production decreases again when grazing intensity becomes too high. Several authors have gone further and have suggested that grazing optimization can lead to mutualistic interactions between plants and their herbivores (Owen andWiegert 1981, 1982;Petelle 1982;Vail 1992), based on a few studies that show a positive effect of herbivory on plant fitness (Paige and Whitham 1987; but see Bergelson and Crawley 1992;Paige 1992;Gronemeyer et al. 1997;Lennartsson et al. 1997Lennartsson et al. , 1998. Such a claim has attracted a lot of criticism (Silvertown 1982;Belsky et al. 1993;Mathews 1994). According to Belsky et al. (1993), no plausible explanation of a real benefit for the individu...

Management of water hyacinth (Eichhornia crassipes [Mart.] Solms) using bioagents in the Rift Valley of Ethiopia

“…Plant fresh weight was higher in plants that received only A. alternata than in plants that received weevils and application of weevils augmented with A. alternata, possibly because of no herbivory effect. Direct effects of herbivory on water hyacinth through biomass consumption and fungal pathogens through leaf and stem consumption have also been reported earlier to influence plant biomass (De Mazancourt and Loreau, 2000). Plant fresh weight differed among treatments and was highest in the control treatment (no herbivory and no fungal application).…”

Toward an integration of evolutionary biology and ecosystem science

“…For example, in models with a simplified ecosystem structure comprized of nutrients, producers, consumers and decomposers, grazing by herbivores can maximize the rate of primary production under a wide range of conditions, provided that plant fitness is tied to productivity rather than biomass (Cohen et al 2000;Loreau 2010a). If plant populations vary in their tolerance to grazing, and there is spatial structure in the plant-herbivore community, then evolutionary change in the plants will be mediated by a balance between their spatial aggregation and patch size (de Mazancourt & Loreau 2000). In such a scenario, the optimal level of plant tolerance allowing grazing optimization to occur is difficult to attain by individual level selection alone.…”

Effects of Defense Evolution and Diet Choice on Population Dynamics in a One-Predator–two-Prey System

“…Many studies have analyzed such evolutionary processes (de Jong 1995, Yamamura and Tsuji 1995, Iwasa et al 1996, Loreau and de Mazancourt 1999, de Jong and van der Meijden 2000, but few have considered defense evolution in the context of population dynamics. Matsuda et al (1993), de Mazancourt andLoreau (2000), and de Mazancourt et al (2001) have, however, addressed this issue from the viewpoint of the population dynamics or nutrient dynamics, although Matsuda et al (1993) focused on a two-predator-one-prey system and de Mazancourt and Loreau (2000) and de Mazancourt et al (2001) did not explicitly consider the relationship between the predator behavior response and the prey defense. Edelstein-Keshet and Rausher (1989) and Underwood (1999) analyzed the relationship between the population dynamics of herbivores and plants that, within a single generation, increased their defense level in response to the level of herbivory (induced defense), although they neither explicitly incorporated the population dynamics of plants, nor focused on the evolutionary aspects of defense.…”