Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation

Abstract

Symbiotic nitrogen (N) fixing trees are absent from old-growth temperate and boreal ecosystems, even though many of these are N-limited. To explore mechanisms that could select against N fixation in N-limited, old-growth ecosystems, we developed a simple resource-based evolutionary model of N fixation. When there are no costs of N fixation, increasing amounts of N fixation will be selected for until N no longer limits production. However, tradeoffs between N fixation and plant mortality or turnover, plant uptake of available soil N, or N use efficiency (NUE) can select against N fixation in N-limited ecosystems and can thereby maintain N limitation indefinitely (provided that there are losses of plant-unavailable N). Three key traits influence the threshold that determines how large these tradeoffs must be to select against N fixation. A low NUE, high mortality (or turnover) rate and low losses of plant-unavailable N all increase the likelihood that N fixation will be selected against, and a preliminary examination of published data on these parameters shows that these mechanisms, particularly the tradeoff with NUE, are quite feasible in some systems. Although these results are promising, a better characterization of these parameters in multiple ecosystems is necessary to determine whether these mechanisms explain the lack of symbiotic N fixers-and thus the maintenance of N limitation-in old-growth forests. evolutionary ecology ͉ model B iological nitrogen (N) fixation-the conversion of atmospheric N 2 gas to biologically useful N-lies at the heart of one of the most intriguing patterns in terrestrial ecosystem ecology: N is thought to limit net primary production (NPP) in many old-growth temperate and boreal forests, despite the existence of numerous N-fixing bacteria in these biomes. Intuition holds that symbiotic N fixers (a symbiosis between a plant and N-fixing bacteria, hereafter ''N fixers'') should have a competitive advantage when N limits NPP and thus should invade and out-compete nonfixing plants (hereafter ''nonfixers'') in N-limited ecosystems. Newly fixed N from their activity would increase N supply, rendering N limitation a transient phenomenon. Yet N limitation is common in old-growth temperate and boreal forests, where no N fixers exist as canopy trees (1, 2). This paradox suggests two fundamental questions about temperate and boreal forests: (i) Why do N fixers not persist beyond early succession? (ii) Why have no old-growth dominant species evolved N-fixing symbioses?The first of these questions addresses a well documented successional pattern: In temperate and boreal ecosystems, N fixers dominate early primary succession but are replaced during the course of succession by nonfixers, even when N may still limit NPP (3-6). Some recent modeling studies have investigated this question (7-10), as outlined below. The second question has received little attention in the literature (but see ref. 11) but is equally important to explaining the paradox of N limitation. Unlike the successional question,...

Evolution of nutrient acquisition: when adaptation fills the gap between contrasting ecological theories

“…The same type of result was found by Menge et al [5] for the evolution of symbiotic nitrogen fixation. This is probably owing to the use of a donor-recipient function for nutrient absorption.…”

“…(c) Perspectives A shortcoming of our model is that nitrogen fixation is not allowed to evolve or to change in a plastic way, while it is well known that the intensity of nitrogen fixation and the distribution of legume species depend on nitrogen availability [5,[39][40][41]. The way we chose to model the capacity of plants to take up nutrients, as well as to describe plant mortality, may seem overly simplistic.…”

“…In most of these studies, the limiting resources for which organisms compete, for example prey, 'disappear' once consumed. Thus far, few studies have tackled the evolution of traits governing the use of a recycled resource [4][5][6], like traits allowing plants to influence nutrient cycling. Such traits are important because they are likely to determine key ecosystem properties [7][8][9].…”

Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems

“…More recently, Menge et al [71,80] developed analytical models of a plant with N-fixing symbioses competing with a non-fixer. They concluded that a lower N use efficiency (less growth per unit of N acquired) can suffice to keep N fixers from entering a N-limited ecosystem dominated by non-fixers [71]-a result consistent with the greater N concentrations observed in legumes [81] and actinorhizal plants in comparison with most non-fixers.…”

Legumes are different: Leaf nitrogen, photosynthesis, and water use efficiency

“…N 2 FP can profoundly influence both ecosystem development and responses to changing climate by alleviating nitrogen shortages that limit capacity of ecosystems to fix and sequester CO 2 (2)(3)(4). A central tenet of traitbased ecology (5,6) is that carbon fixation and transpiration are directly related to leaf nitrogen; in turn, leaf nitrogen is used to drive global models of carbon (and water) exchanges between plants and the atmosphere (7).…”