Structural blueprint and ontogeny determine the adaptive value of the plastic response to competition in clonal plants: a modelling approach

Local competitive interactions strongly influence plant community dynamics. To maintain their performance under competition, clonal plants may plastically modify their network architecture to grow in the direction of least interference. The adaptive value of this plastic avoidance response may depend, however, on traits linked with the plant’s structural blueprint and ontogeny. We tested this hypothesis using virtual populations. We used an Individual Based Model to simulate competitive interactions among clones within a plant population. Clonal growth was studied under three competition intensities in plastic and non-plastic individuals. Plasticity buffered the negative impacts of competition at intermediate densities of competitors by promoting clone clumping. Success despite competition was promoted by traits linked with (1) the plant’s structural blueprint (weak apical dominance and sympodial growth) and (2) ontogenetic processes, with an increasing or a decreasing dependence of the elongation process on the branch generation level or length along the competition intensity gradient respectively. The adaptive value of the plastic avoidance response depended on the same traits. This response only modulated their importance for clone success. Our results show that structural blueprint and ontogeny can be primary filters of plasticity and can have strong implications for evolutionary ecology, as they may explain why clonal plants have developed many species-specific plastic avoidance behaviours.     

Intraspecific interactions in the annual legume Medicago minima are shaped by both genetic variation for competitive ability and reduced competition among kin

Documenting if plants exhibit kin competition avoidance in intraspecific plant interactions is relevant both to improve crop growth, and to understand diversity and composition in natural plant communities. However, a number of confounding mechanisms complicates detecting kin competition avoidance from experiments comparing plants growing with kin and non-kin neighbors. We conducted complementary greenhouse experiments using genotypes from four populations of the annual Medicago minima, which in a previous study showed higher survival when interacting with kin relative to non-kin. We show that genotypes vary in kin competition avoidance, and in competitive ability, but find no indication of complementary resource use. Importantly, from our first experiment of root growth behavior, we know that some genotypes exhibit kin competition avoidance. Yet, the variation in competitive ability we find in our second experiment, where plants grow in mini communities together with either kin or unrelated genotypes, can alone explain the variation we observe in growth and biomass among communities. In our case, the genotypes with highest competitive ability were also those that showed kin competition avoidance. This confounding effect obscured the disentangling of mechanisms underlying difference in growth between kin and non-kin interactions. When silencing root exudates by adding activated carbon to a subset of our genotype combinations, we found increased size asymmetry of plants grown together, and mostly in kin communities. This suggests that plants recognize the identity of neighbors via root exudates, and compete less with neighbors recognized as kin. To detect kin competition avoidance we suggest designing experiments that pair unrelated genotypes with similar competitive abilities. Such design, combined with silencing root exudates would be powerful to detect whether plants show kin competition avoidance or not.     

Plastic and constant developmental traits contribute to adaptive differences in co-occurring Polygonum species

Adaptive differences among species are often thought to result from developmentally constant trait differences that enhance fitness in alternative environments. Species differences in patterns of individual phenotypic plasticity can also have ecological consequences. Indeed, functionally related constant and plastic traits may interact to determine the phenotype's adaptive value in particular conditions. We compared juvenile shade avoidance traits (height and its components, internode length and node number) across two field density treatments in Polygonumpersicaria and P. hydropiper, annual plant species that co‐occur in pastures comprised of a mosaic of plant densities. We used selection analyses to test trait contributions to fitness in alternative density treatments. Seedlings of both species expressed plasticity for internode elongation in response to density; P. persicaria plants increased internode length and consequently height significantly more in high density than did those of P. hydropiper. As predicted by the shade avoidance hypothesis, increased height was adaptive for both species in high density stands, so P. persicaria plants had higher fitness in this environment. By contrast, node numbers were relatively constant across density treatments in both species: P. hydropiper seedlings consistently produced more nodes than did those of P. persicaria. This constant trait difference contributed to P. hydropiper's greater relative fitness at low density, where more nodes and hence leaves enable plants to better exploit available light. Differences between species in these juvenile shade‐avoidance traits did not result from the evolutionary constraints of lack of heritable variation or costs of plasticity. We discuss how these interspecific trait differences may have been generated by divergent selective histories resulting from differences in herbivore resistance. These results illustrate how adaptive differences in both plastic and constantly expressed traits may jointly contribute to ecological distribution, including coexistence in patchy habitats.     

Physiological regulation and functional significance of shade avoidance responses to neighbors

Plants growing in dense vegetations compete with their neighbors for resources such as water, nutrients and light. The competition for light has been particularly well studied, both for its fitness consequences as well as the adaptive behaviors that plants display to win the battle for light interception. Aboveground, plants detect their competitors through photosensory cues, notably the red:far-red light ratio (R:FR). The R:FR is a very reliable indicator of future competition as it decreases in a plant-specific manner through red light absorption for photosynthesis and is sensed with the phytochrome photoreceptors. In addition, also blue light depletion is perceived for neighbor detection. As a response to these light signals plants display a suite of phenotypic traits defined as the shade avoidance syndrome (SAS). The SAS helps to position the photosynthesizing leaves in the higher zones of a canopy where light conditions are more favorable. In this review we will discuss the physiological control mechanisms through which the photosensory signals are transduced into the adaptive phenotypic responses that make up the SAS. Using this mechanistic knowledge as a starting point, we will discuss how the SAS functions in the context of the complex multi-facetted environments, which plants usually grow in.Key words: competition, shade avoidance, hormones, cell wall, adaptive plasticity, photoreceptor, light     

植物亲缘识别的研究进展

植物的亲缘识别(kin recognition)指植物通过识别周边个体与自己的亲缘关系, 调整自身的生长生态策略、促进亲缘个体的生存与繁衍。研究表明, 植物主要通过特定的叶片挥发物、根系分泌物、感光载体等途径, 识别周边个体与自己的亲缘关系, 改变自身形态学策略(如根系大小、根冠比、种子数量等)或者生理代谢策略(次生代谢物质、防御蛋白等), 调整与周边个体的竞争强度, 缓和与近亲缘个体之间的竞争, 加强与远亲缘或非亲缘个体的竞争。同时亲缘识别的强度也受环境因子(养分等)的影响。结合目前的研究进展, 该文分析了导致亲缘识别的研究结果存在差异或争议的主要原因, 认为主要与实验材料的选择、亲缘关系的界定标准、环境条件及测定的指标不统一有关。将来的研究应重点从生理生化、分子、代谢水平上深入研究植物亲缘识别的机理。     

Recent advance of kin recognition in plant

Plants have the ability to discriminate kin members from strangers in competitive interactions and show altruistic behavior towards related individuals. Studies have showed that plants recognize their neighbors and adjust their ecological strategy mainly through leaf volatiles, root secretions and photographic carrier. The target plants can modify their morphological traits (root size, root:shoot ratio, seed numbers etc.) or metabolism characteristics (secondary metabolites, defense-related proteins etc.) when groups of plants shared common resources, so as to minimize competition with close relatives. The density of kin recognition is influenced by environmental conditions. The main reasons for controversial experimental results of kin recognition are associated with plant materials, standard of kin selection, ecological factors and measured indices. Further studies are required to understand the mechanisms of kin interactions in plants from physiological, biochemical, molecular and metabolic levels.     

Struggling for Light: DELLA Regulation During Plant-Plant Interactions

We recently described how DELLA proteins are involved in plant growth responses to neighbors in dense stands. These responses that are called shade avoidance include enhanced stem and petiole elongation and are a classic example of adaptive phenotypic plasticity. Although much is known about neighbor detection, much less is known about the signal transduction network downstream of these signals. We will discuss here how a group of growth-supressors, called DELLA proteins, are functionally regulated upon the detection of neighbors. DELLA proteins are degraded upon binding of gibberellin (GA) to its receptor, thus releasing the restraint of GA responses. We discuss here that GA positively regulates shade avoidance by reducing DELLA protein levels. Furthermore, we will show that this is an essential step in shade avoidance, but also that reduced DELLA abundance alone is not sufficient to induce these growth responses. It is concluded that GA-dependent DELLA degradation is one essential step in the signal transduction network from light-mediated neighbor detection towards adaptive shoot elongation responses.Key Words: arabidopsis, canopy, DELLA, eco-devo, gibberellin, light, phenotypic plasticity, phytochrome, shade avoidance     

Nitrogen Relationships of Vigna mungo in Pure Stands and in Celosia argentea Mixtures

Dynamics of the nitrogen relationships of Vigna mungo in pureand in mixed stands with Celosia argentea, a common weed ofleguminous crops in certain regions of India, were investigated.The weed significantly depressed nodulation and reduced thedry matter and nitrogen yield of the legume which was lowestat the highest density of the weed. A significant amount ofnitrogen transfer occurred from the legume in the weed mixtureswhich appeared to be taken up by the weed plants. Therefore,weed plants benefited from their association with the legumeby accumulating more dry matter and nitrogen in the legume mixtures.The possible competitive or biochemical interference of theweed with nitrogen relationships of the legume in mixtures isdiscussed. Vigna mungo, Celosia argentea, pure stands, mixed stands, total nitrogen, interference     

Environmental Heterogeneity and Population Differentiation in Plasticity to Drought in <Emphasis Type="Italic">Convolvulus Chilensis</Emphasis> (Convolvulaceae)

Plant populations may show differentiation in phenotypic plasticity, and theory predicts that greater levels of environmental heterogeneity should select for higher magnitudes of phenotypic plasticity. We evaluated phenotypic responses to reduced soil moisture in plants of Convolvulus chilensis grown in a greenhouse from seeds collected in three natural populations that differ in environmental heterogeneity (precipitation regime). Among several morphological and ecophysiological traits evaluated, only four traits showed differentiation among populations in plasticity to soil moisture: leaf area, leaf shape, leaf area ratio (LAR), and foliar trichome density. In all of these traits plasticity to drought was greatest in plants from the population with the highest interannual variation in precipitation. We further tested the adaptive nature of these plastic responses by evaluating the relationship between phenotypic traits and total biomass, as a proxy for plant fitness, in the low water environment. Foliar trichome density appears to be the only trait that shows adaptive patterns of plasticity to drought. Plants from populations showing plasticity had higher trichome density when growing in soils with reduced moisture, and foliar trichome density was positively associated with total biomass. Co-ordinating editor: F. Stuefer     

Plasticity of physiology in Lobelia: testing for adaptation and constraint

Phenotypic plasticity is thought to be a major mechanism allowing sessile organisms such as plants to adapt to environmental heterogeneity. However, the adaptive value of many common plastic responses has not been tested by linking these responses to fitness. Even when plasticity is adaptive, costs of plasticity, such as the energy necessary to maintain regulatory pathways for plastic responses, may constrain its evolution. We used a greenhouse experiment to test whether plastic physiological responses to soil water availability (wet vs. dry conditions) were adaptive and/or costly in the congeneric wildflowers Lobelia cardinalis and L. siphilitica. Eight physiological traits related to carbon and water uptake were measured. Specific leaf area (SLA), photosynthetic rate (A), stomatal conductance (gs), and photosynthetic capacity (Amax) responded plastically to soil water availability in L. cardinalis. Plasticity in Amax was maladaptive, plasticity in A and g(s) was adaptive, and plasticity in SLA was adaptively neutral. The nature of adaptive plasticity in L. cardinalis, however, differed from previous studies. Lobelia cardinalis plants with more conservative water use, characterized by lower g(s), did not have higher fitness under drought conditions. Instead, well-watered L. cardinalis that had higher g(s) had higher fitness. Only Amax responded plastically to drought in L. siphilitica, and this response was adaptively neutral. We detected no costs of plasticity for any physiological trait in either L. cardinalis or L. siphilitica, suggesting that the evolution of plasticity in these traits would not be constrained by costs. Physiological responses to drought in plants are presumed to be adaptive, but our data suggest that much of this plasticity can be adaptively neutral or maladaptive.     

Testing adaptive plasticity to UV: costs and benefits of stem elongation and light-induced phenolics

On exposure to ultraviolet radiation (UV), many plant species both reduce stem elongation and increase production of phenolic compounds that absorb in the UV region of the spectrum. To demonstrate that such developmental plasticity to UV is adaptive, it is necessary to show that the induced phenotype is both beneficial in inductive environments and maladaptive in non-inductive environments. We measured selection on stem elongation and phenolic content of seedlings of Impatiens capensis transplanted into ambient-UV and UV-removal treatments. We extended the range of phenotypes expressed, and thus the opportunity for selection in each UV treatment, by pretreating seedlings with either a low ratio of red:far-red wavelengths (R:FR), which induced stem elongation and reduced phenolic concentrations, or high R:FR, which had the opposite effect on these two phenotypic traits. Reduced stem length relative to biomass was advantageous for elongated plants under ambient UV, whereas increased elongation was favored in the UV-removal treatment. Selection favored an increase in the level of phenolics induced by UV in the ambient-UV treatment, but a decrease in phenolics in the absence of UV. These results are consistent with the hypotheses that reduced elongation and increased phenolic concentrations serve a UV-protective function and provide the first explicit demonstration in a wild species that plasticity of these traits to UV is adaptive. The observed cost to phenolics in the absence of UV may explain why many species plastically upregulate phenolic production when exposed to UV, rather than evolve constitutively high levels of these compounds. Finally, pretreatment with low R:FR simulating foliar shade did not exacerbate the fitness impact of UV exposure when plants had several weeks to acclimate to UV. This observation suggests that the evolution of adaptive shade avoidance responses to low R:FR in crowded stands will not be constrained by increased sensitivity to UV in elongated plants when they overtop their neighbors.     

Is photomorphogenic shade avoidance adaptive? Perspectives from population biology

Photomorphogenic shade avoidance responses provide an ideal model system for integrating genetic, physiological and population biology approaches to the study of adaptive plasticity. The adaptive plasticity hypothesis predicts that shade avoidance phenotypes induced by low ratios of red to far-red light (R:FR) will have high relative fitness in dense stands, but will suffer a fitness disadvantage at low density. Experiments with transgenic and mutant plants in which photomorphogenic genes are disabled, as well as phenotype manipulation by means of altered R:FR, strongly support the shade avoidance hypothesis. The observation of photomorphogenic ecotypes in different selective environments also suggests that the shade avoidance response has undergone adaptive evolution. Quantitative genetic variation in R:FR sensitivity has been detected in wild populations, indicating that the evolutionary potential exists for response to natural selection. However, evolutionary response may be constrained by genetic correlations among developmentally linked traits. Therefore it cannot be assumed that an observed suite of photomorphogenic responses represents an adaptive optimum for every trait.     

Plant adaptation to dynamically changing environment: the shade avoidance response

The success of competitive interactions between plants determines the chance of survival of individuals and eventually of whole plant species. Shade-tolerant plants have adapted their photosynthesis to function optimally under low-light conditions. These plants are therefore capable of long-term survival under a canopy shade. In contrast, shade-avoiding plants adapt their growth to perceive maximum sunlight and therefore rapidly dominate gaps in a canopy. Daylight contains roughly equal proportions of red and far-red light, but within vegetation that ratio is lowered as a result of red absorption by photosynthetic pigments. This light quality change is perceived through the phytochrome system as an unambiguous signal of the proximity of neighbors resulting in a suite of developmental responses (termed the shade avoidance response) that, when successful, result in the overgrowth of those neighbors. Shoot elongation induced by low red/far-red light may confer high relative fitness in natural dense communities. However, since elongation is often achieved at the expense of leaf and root growth, shade avoidance may lead to reduction in crop plant productivity. Over the past decade, major progresses have been achieved in the understanding of the molecular basis of shade avoidance. However, uncovering the mechanisms underpinning plant response and adaptation to changes in the ratio of red to far-red light is key to design new strategies to precise modulate shade avoidance in time and space without impairing the overall crop ability to compete for light.     

Simulated warming differentially affects the growth and competitive ability of Centaurea maculosa populations from home and introduced ranges

Climate warming may drive invasions by exotic plants, thereby raising concerns over the risks of invasive plants. However, little is known about how climate warming influences the growth and competitive ability of exotic plants from their home and introduced ranges. We conducted a common garden experiment with an invasive plant Centaurea maculosa and a native plant Poa pratensis, in which a mixture of sand and vermiculite was used as a neutral medium, and contrasted the total biomass, competitive effects, and competitive responses of C. maculosa populations from Europe (home range) and North America (introduced range) under two different temperatures. The warming-induced inhibitory effects on the growth of C. maculosa alone were stronger in Europe than in North America. The competitive ability of C. maculosa plants from North America was greater than that of plants from Europe under the ambient condition whereas this competitive ability followed the opposite direction under the warming condition, suggesting that warming may enable European C. maculosa to be more invasive. Across two continents, warming treatment increased the competitive advantage instead of the growth advantage of C. maculosa, suggesting that climate warming may facilitate C. maculosa invasions through altering competitive outcomes between C. maculosa and its neighbors. Additionally, the growth response of C. maculosa to warming could predict its ability to avoid being suppressed by its neighbors.     

Density dependence across multiple life stages in a temperate old-growth forest of northeast China

Recent studies on species coexistence suggest that density dependence is an important mechanism regulating plant populations. However, there have been few studies of density dependence conducted for more than one life-history stage or that control for habitat heterogeneity, which may influence spatial patterns of survival and mask density dependence. We explored the prevalence of density dependence across multiple life stages, and the effects of controlling for habitat heterogeneity, in a temperate forest in northeast China. We used generalized linear mixed-effects models to test for density-dependent mortality of seedlings and spatial point pattern analysis to detect density dependence for sapling-to-juvenile transitions. Conspecific neighbors had a negative effect on survival of plants in both life stages. At the seedling stage, we found a negative effect of conspecific seedling neighbors on survival when analyzing all species combined. However, in species-level analyses, only 2 of 11 focal species were negatively impacted by conspecific neighbors, indicating wide variation among species in the strength of density dependence. Controlling for habitat heterogeneity did not alter our findings of density dependence at the seedling stage. For the sapling-to-juvenile transition stage, 11 of 15 focal species showed patterns of local scale (<10 m) conspecific thinning, consistent with negative density dependence. The results varied depending on whether we controlled for habitat heterogeneity, indicating that a failure to account for habitat heterogeneity can obscure patterns of density dependence. We conclude that density dependence may promote tree species coexistence by acting across multiple life-history stages in this temperate forest.     

Population regulation in Bromus rubens and B. mollis: Life cycle components and competition

Summary A series of Bromus rubens and B. mollis populations were sampled in the coastal range and northern part of the Central Valley of California in order to study their population ecology in demographic terms. Quantitative estimates were obtained on plants collected directly in nature, and their progenies in controlled environments with randomized block design in the greenhouse.Two parameters of population growth — the intrinsic rate of increase, r, and the carrying capacity, K-were estimated by using the logistic model (r=ln R and K=equilibrium population size). It was found that B. mollis is a relatively K-type species, while B. rubens is a relatively r-type species.The effects of density on competition between individuals in pure and mixed populations of B. mollis and B. rubens were studied. In both species, increasing density induced greater mortality and a striking plastic reduction in the size and reproductive potential of the individuals. Further, B. rubens showed a relatively greater mortality and less plastic response to densities than B. mollis in both pure and mixed stands. Two different types of plasticity were considered: one in response to changing density (d-plasticity); and the other in response to changing enironmental conditions (e-plasticity). High plasticity in one of them need not imply that the other one is high too. B. rubens showed higher e-plasticity, but lower d-plasticity than B. mollis.The relationships between r, K and competitive ability were discussed. Two types of K-strategy were distinguished: one involving greater nonreproductive effort with longer life span, or lowered mortality (Type-I) and the other with density-induced adjustments in body size along with survival in higher numbers (Type-II). Different populations of these two Bromus species showed different values of r and K (Type-II) and different competitive abilities. It was found that higher r was usually accompanied by lower K (Type-II), while higher K (Type-II) was accompanied by lower competitive ability, which in turn is correlated with higher d-plasticity. In general, coexistence was predicted on the basis of estimates derived from the interspecific competition experiments.     

Feeding behavior of bollworm and tobacco budworm (Lepidoptera: Noctuidae) larvae in mixed stands of nontransgenic and transgenic cotton expressing an insecticidal protein

Feeding behavior of third-instar bollworm, Helicoverpa zea (Boddie), and tobacco budworm, Heliothis virescens (F.), was observed in pure and mixed stands of nontransgenic and transgenic cotton (BTK), Gossypium hirsutum L., expressing an insecticidal protein CryIA(c) from a bacterium, Bacillus thuringiensis Berliner subsp. kurstaki. Five plant stands composed of BTK and non-BTK plants were evaluated; two pure stands and three mixed stands. Percentage ratios of BTK to non-BTK plants in the stands were 100:0, 75:25, 50:50, 25:75 and 0:100, respectively. In all stands with BTK plants, fewer bollworm and tobacco budworm larvae were found on BTK plants than non-BTK plants 24 h after infestation with third instars. At 48 h, significantly fewer tobacco budworm larvae, but not fewer bollworm larvae, were found on BTK plants. However, the number of larvae of either insect did not increase on non-BTK plants compared with the initial infestation density of three larvae per plant. The number of obacco budworm injured flower buds, and capsules was lower in all plant stands containing BTK plants compared with the pure stand of non-BTK at 48 h after infestation. Higher numbers of larvae on non-BTK plants were possibly the result of larval intoxication, reduced feeding, and increased plant abandonment and death on BTK plants rather than a classical feeding preference. Unexpectedly, the number of flower buds and capsules injured by bollworm and tobacco budworm when averaged per plant for all plants in a stand, differed little among the 75:25, 50:50 and 25:75 plant mixtures. These data suggest that larvae of both species frequently moved among plants, feeding indiscriminately on BTK and non-BTK plants.     

Light spectral quality, phytochrome and plant competition

The light environment experienced by plants in natural vegetation is strongly dependent upon interactions with neighbors. For plants in dense stands, reduced irradiance can lead to reductions in growth and fitness. Spectral light quality is also altered beneath a leaf canopy, and can serve as an important signal of competition for light. Recent physiological studies indicate that plants can perceive the quality of light reflected from neighbors as an accurate predictor of future competition, and respond morphologically even before they are directly shaded. These findings have important implications for plant population biology, and provide a valuable opportunity for the study of adaptive plasticity.     

Competition between two naturalized dandelions,Taraxacum officinale weber andTaraxacum laevigatum DC., in mixed cultures with different levels of soil moisture

Taraxacum officinala andTaraxacum laevigatum were grown in mixed stands at various plant densities and mixing ratios with various levels of soil moisture to formulate the effect of soil moisture on the competitive relationship between the species. In pure stands, the mean plant weight—plant density relation for each level of soil moisture could be described by the reciprocal equation of the crowding effect. On the other hand, the response of mean plant weight to soil moisture content followed the reciprocal equation for a repulsive growth factor at the respective levels of plant density. By introducing the density conversion factor, the results of mixed stands could be successfully formulated from similar reciprocal equations. The dependence of density conversion factor on soil moisture content was also formulated. From these relations, a comprehensive formula was developed to describe the effects of plant density and soil moisture content on the growth of two species in mixed stands. Changes in the biomass in mixed stands were, examined by means of calculations based on the experimental results.     

Blue light regulated shade avoidance

Most plants grow in dense vegetation with the risk of being out-competed by neighboring plants. These neighbors can be detected not only through the depletion in light quantity that they cause, but also through the change in light quality, which plants perceive using specific photoreceptors. Both the reduction of the red:far-red ratio and the depletion of blue light are signals that induce a set of phenotypic traits, such as shoot elongation and leaf hyponasty, which increase the likelihood of light capture in dense plant stands. This set of phenotypic responses are part of the so called shade avoidance syndrome (SAS). This addendum discusses recent findings on the regulation of the SAS of Arabidopsis thaliana upon blue light depletion. Keller et al. and Keuskamp et al. show that the low blue light attenuation induced shade avoidance response of seedling and rosette-stage A. thaliana plants differ in their hormonal regulation. These studies also show there is a regulatory overlap with the R:FR-regulated SAS.