Asymmetric facilitation can reduce size inequality in plant populations resulting in delayed density‐dependent mortality

Size inequality in plant populations is a ubiquitous feature that has received much attention due to ecological and evolutionary implications. The mechanisms driving size inequality were mainly attributed to different modes of competition (symmetric versus asymmetric), while the potential effects of different modes of facilitation (symmetric versus asymmetric) to this pattern have not yet been fully explored. We employed an individual‐based model to explore the relative roles of both competition and facilitation simultaneously along an environmental stress gradient. Special emphasis was given to the assessment of symmetric facilitation (plants receive benefit from each other equally or proportionally to benefactors’ sizes) and asymmetric facilitation (beneficiary plants receive benefits from benefactor plants that are higher than proportional to the benefactors’ size) in altering plant size inequality. We found that independent of the particular mode of competition, symmetric facilitation generally increased size inequality, whereas asymmetric facilitation decreased it. This pattern was consistent along the stress gradient. Because of their different effects on size inequality, symmetric facilitation accelerated self‐thinning, whereas asymmetric facilitation delayed the onset of density‐dependent mortality, promoting survival under intermediate stress conditions. We compared our model predictions with both 1) a previous modelling study focusing on the effect of (symmetric) facilitation on the size inequality, and 2) re‐analysed data from a published experiment generating asymmetric facilitation of plants against enhanced ultraviolet‐B (UV‐B). Whereas our model predictions and the results of the empirical experiment were consistent, we found that previous theoretical results that solely relied on symmetric facilitation need to be re‐adjusted. Our study showed that combinations of different modes of competition and facilitation can alter size inequality in different ways and with important consequences for the onset of density‐dependent mortality during population development. Explicitly considering different modes and mechanisms of interactions (both facilitation and competition) will improve mechanistic understanding in plant ecology.     

Positive interactions can increase size inequality in plant populations

1.  Large variation in the size of individuals is a ubiquitous feature of natural plant populations. While the role of competition in generating this variation has been studied extensively, the potential effects of positive interactions among plants, which are common in high-stress environments, have not been investigated.
2.  Using an individual-based 'zone-of-influence' model, we investigate the effects of competition, abiotic stress and facilitation on size inequality in plant monocultures. In the model, stress reduces the growth rate of plants, and facilitation ameliorates the effects of stress. Both facilitation and competition occur in overlapping zones of influence. We tested some of the model's predictions with a field experiment using the clonal grass Elymus nutans in an alpine meadow.
3.  Facilitation increased the size inequality of model populations when there was no density-dependent mortality. This effect decreased with density as competition overwhelmed facilitation. The lowest size inequality was found at intermediate densities both with the model and in the field.
4.  When density-dependent mortality was included in the model, stress delayed its onset and reduced its rate by reducing growth rates, so the number of survivors at any point in time was higher under harsh than under more benign conditions. Facilitation increased size inequality during self-thinning.
5.   Synthesis . Our results demonstrate that facilitation interacts with abiotic stress and competition to influence the degree of size inequality in plant populations. Facilitation increased size inequality at low to intermediate densities and during self-thinning.     

Facilitation among plants can accelerate density‐dependent mortality and steepen self‐thinning lines in stressful environments

The speed and slope of plant self‐thinning are all affected by plant–plant interactions across environmental gradients. Possible mechanisms driving the self‐thinning dynamics include the relative strength of root versus shoot competition, and the interplay between competition and facilitation. Although these mechanisms often act in concert, their relative importance has not yet been fully explored. We used both a one‐layer and a two‐layer zone‐of‐influence (ZOI) model to examine how competition and facilitation drive self‐thinning across stress gradients. As a development of the traditional ZOI model, the two‐layer version explicitly models shoot and root growth and neighbor interactions, and thus the overall size‐symmetry of competition is regulated by the relative strength of root versus shoot competition. One‐layer model simulations revealed that increasingly asymmetric competition accelerated thinning, and steepened (slope ranged from about –1 to –4/3) and lowered self‐thinning lines. Stress slowed down density‐dependent mortality considerably when competition was not completely symmetric. Stress significantly decreased the self‐thinning intercept, while facilitation simply counteracted stress effects. Both stress and facilitation showed little effect on the slope. In the two‐layer model, both stress and facilitation affected mortality in the same way as in the one‐layer version when competition was not completely symmetric. Different from the one‐layer model, the two‐layer version showed that the effects of stress and facilitation on the self‐thinning slope were mediated by the asymmetry of competition. As stress increased, the overall asymmetry of competition shifted from asymmetric to symmetric due to increased relative strength of root competition. High stress thus dramatically flattened self‐thinning lines, whereas the inclusion of facilitation counteracted stress and led to steeper self‐thinning lines. Our two‐layer model is based on the current knowledge of plant–plant interactions, and better represents ecological realities. It can help elaborate experiments for testing the role of competition and facilitation in driving plant population dynamics.     

Extreme drought stress shifts net facilitation to neutral interactions between shrubs and sub‐canopy plants in an arid desert

The stress gradient hypothesis (SGH) predicts that the importance or intensity of competition and facilitation will change inversely along abiotic stress gradients. It was originally postulated that increasing environmental stress can induce a monotonic increase in facilitation. However, more recent models predicted that the relationship between severity and interaction exhibits a hump‐shaped pattern, in which positive interactions prevail under moderate stress but decline at the extreme ends of stress gradients. In the present study, we conducted a field experiment along a temporal rainfall gradient for five consecutive years, in order to investigate interactions in a shrub‐herbaceous plant community at the southern edge of the Badain Jaran Desert, and, more specifically, investigated the effects of Calligonum mongolicum, a dominant shrub species, on both abiotic environmental variables and the performance of sub‐canopy plant species. We found that shrubs can improve sub‐canopy water regimes, soil properties, plant biomass, density, cover, and richness and, more importantly, that the positive effect of shrubs on sub‐canopy soil moisture during the summer diminishes as rainfall decreases, a pattern that partly explains the collapse of the positive interaction between shrubs and their understory plants. These results provide empirical evidence that the positive effect of shrubs on understory plant communities in extreme arid environments may decline and become neutral with increasing drought stress.     

Context‐dependent biotic interactions control plant abundance across altitudinal environmental gradients

Many biotic interactions influence community structure, yet most distribution models for plants have focused on plant competition or used only abiotic variables to predict plant abundance. Furthermore, biotic interactions are commonly context‐dependent across abiotic gradients. For example, plant–plant interactions can grade from competition to facilitation over temperature gradients. We used a hierarchical Bayesian framework to predict the abundances of 12 plant species across a mountain landscape and test hypotheses on the context‐dependency of biotic interactions over abiotic gradients. We combined field‐based estimates of six biotic interactions (foliar herbivory and pathogen damage, fungal root colonization, fossorial mammal disturbance, plant cover and plant diversity) with abiotic data on climate and soil depth, nutrients and moisture. All biotic interactions were significantly context‐dependent along temperature gradients. Results supported the stress gradient hypothesis: as abiotic stress increased, the strength or direction of the relationship between biotic variables and plant abundance generally switched from negative (suggesting suppressed plant abundance) to positive (suggesting facilitation/mutualism). For half of the species, plant cover was the best predictor of abundance, suggesting that the prior focus on plant–plant interactions is well‐justified. Explicitly incorporating the context‐dependency of biotic interactions generated novel hypotheses about drivers of plant abundance across abiotic gradients and may improve the accuracy of niche models.     

The interplay between above‐ and below‐ground plant–plant interactions along an environmental gradient: insights from two‐layer zone‐of‐influence models

The changes in plant–plant interactions along environmental gradients have been a focus of recent ecological research. It has been suggested that both above‐ and below‐ground competition and their interplay vary along gradients, but few studies have investigated this idea, and in most cases, the role of facilitation has not been considered, despite its importance in high stress environments. Here we used two‐layer ‘zone‐of‐influence’ models to simulate the effects of facilitation, size‐asymmetry of competition, abiotic stress, resource availability and the balance of root–shoot growth on shoot and root interactions and their interplay along an environmental gradient. In the absence of facilitation, shoot and total competition became weaker, while root competition and the interplay between shoot and root competition were unchanged under increasing stress when root competition was completely symmetric. In contrast, shoot, root, total interactions and the interplay between shoot and root interactions were all negative, and they increased with increasing stress when root competition was size‐symmetric. When facilitation was included in the models, net effects of shoot, root, total interactions and the interplay of root–shoot interactions were very different from those without facilitation, and many were positive under highly stressful conditions. The type of stress (non‐resource or resource) did not significantly influence the simulation results. Our study provides an alternative interpretation of the interplay between above‐ and below‐ground plant–plant interactions across an environmental gradient.     

Effects of positive interactions, size symmetry of competition and abiotic stress on self-thinning in simulated plant populations

Background and Aims

Competition drives self-thinning (density-dependent mortality) in crowded plant populations. Facilitative interactions have been shown to affect many processes in plant populations and communities, but their effects on self-thinning trajectories have not been investigated.

Methods

Using an individual-based ‘zone-of-influence’ model, we studied the potential effects of the size symmetry of competition, abiotic stress and facilitation on self-thinning trajectories in plant monocultures. In the model, abiotic stress reduced the growth of all individuals and facilitation ameliorated the effects of stress on interacting individuals.

Key Results

Abiotic stress made the log biomass – log density relationship during self-thinning steeper, but this effect was reduced by positive interactions among individuals. Size-asymmetric competition also influenced the self-thinning slope.

Conclusions

Although competition drives self-thinning, its course can be affected by abiotic stress, facilitation and competitive symmetry.     

Density dependence,spatial scale and patterning in sessile biota

Sessile biota can compete with or facilitate each other, and the interaction of facilitation and competition at different spatial scales is key to developing spatial patchiness and patterning. We examined density and scale dependence in a patterned, soft sediment mussel bed. We followed mussel growth and density at two spatial scales separated by four orders of magnitude. In summer, competition was important at both scales. In winter, there was net facilitation at the small scale with no evidence of density dependence at the large scale. The mechanism for facilitation is probably density dependent protection from wave dislodgement. Intraspecific interactions in soft sediment mussel beds thus vary both temporally and spatially. Our data support the idea that pattern formation in ecological systems arises from competition at large scales and facilitation at smaller scales, so far only shown in vegetation systems. The data, and a simple, heuristic model, also suggest that facilitative interactions in sessile biota are mediated by physical stress, and that interactions change in strength and sign along a spatial or temporal gradient of physical stress.     

Pollination outcomes reveal negative density‐dependence coupled with interspecific facilitation among plants

Pollination is thought to be under positive density‐dependence, destabilising plant coexistence by conferring fitness disadvantages to rare species. Such disadvantage is exacerbated by interspecific competition but can be mitigated by facilitation and intraspecific competition. However, pollinator scarcity should enhance intraspecific plant competition and impose disadvantage on common over rare species (negative density‐dependence, NDD). We assessed pollination proxies (visitation rate, pollen receipt, pollen tubes) in a generalised plant community and related them to conspecific and heterospecific density, expecting NDD and interspecific facilitation due to the natural pollinator scarcity. Contrary to usual expectations, all proxies indicated strong intraspecific competition for common plants. Moreover interspecific facilitation prevailed and was stronger for rare than for common plants. Both NDD and interspecific facilitation were modulated by specialisation, floral display and pollinator group. The combination of intraspecific competition and interspecific facilitation fosters plant coexistence, suggesting that pollination can be a niche axis maintaining plant diversity.     

Persistence,multiple demographic strategies and conservation in long‐lived Mediterranean plants

Abstract. Persistence by longevity has been rarely considered as an alternative to regeneration by seeding for plants showing multiple demographic strategies. We propose a conceptual model of multiple demographic strategies for long‐lived plants in stable habitats, shifting from regeneration by seeding to persistence by longevity and/or vegetative reproduction, along gradients of abiotic stress or interspecific competition. Regeneration by seeding would be promoted under low abiotic stress or under low competition, whereas persistence by longevity and/or vegetative reproduction would predominate at high levels of abiotic stress or competition. We test this model with two threatened species of the Mediterranean region, the shrub Juniperus communis, a widely distributed species which maintains relict populations in the Mediterranean mountains thanks to great adult longevity and Pinguicula vallisneriifolia, a palaeo‐endemic herb relying on a perennial habit and vegetative reproduction under drought imposed stress or high competition at late successional phases. As a main consequence, multiple demographic strategies enhance a plant's ability to exploit environmental heterogeneity at different spatial (patches, localities, regions within the species’ distribution area) and temporal (individual life span, glacial‐interglacial cycles) scales. The potential of multiple demographic dynamics based on persistence and regeneration must be considered as a major ecological trait determining the long‐term viability of peripheral populations of relict species as well as the inertia against extinction of many threatened endemisms, thereby contributing to the maintenance of the high plant diversity characterizing the Mediterranean region.     

Intraspecific facilitation: a missing process along increasing stress gradients – insights from simulated shrub populations

In recent years many field studies have been conducted to assess the relative importance of facilitation and competition in structuring vegetation communities in different environments. Herein, we present a simulation model which systematically explores the relative importance of intra‐specific facilitation and competition between adult shrubs and seedlings for spatial pattern formation. A grid‐based simulation model was constructed and calibrated using data collected in the field from Sarcopoterium spinosum populations in Israel to simulate population dynamics along a rainfall gradient. A series of simulation experiments was conducted in which manipulations of seedling survival probabilities were carried out to assess the relative importance of these processes in generating spatial patterns. Increased survival probabilities of first‐year shrubs in open areas were used to simulate competition effects, while increased survival probabilities in the vicinity of shrubs were used to simulate facilitation effects. Simulation results were then compared to shrub spatial patterns observed in the field. The results indicate that facilitation is not an important process in generating intra‐specific spatial patterns. Rather, in mesic environments with high precipitation, competition is the dominant process generating spatial patterns, resulting in regular spacing of shrubs, similarly to the patterns observed in the field (L(h) values<0). In arid sites, where precipitation values are lower, and stress conditions are higher, the dominant process generating spatial patterns was random mortality due to drought conditions. The resulting spatial patterns in this case are random (L(h)～0), whereas observed field populations exhibited clumped patterns (L(h)>0). We conclude that as stress conditions increase, the importance of intraspecific neighborhood interactions decrease whereas the importance of environmental factors increase in dictating intra‐specific spatial pattern formation. Consequently in mesic environments intra‐specific competition among adults determines the emerging patterns, while intraspecific facilitation is a negligible process.     

Non‐trophic plant–animal interactions mediate positive density dependence among conspecific saplings

Trophic plant–animal interactions (e.g. browsing by ungulates, insect attack) are an important and well‐studied source of mortality in many tree populations. Non‐trophic tree–animal interactions (e.g. deer antler rubbing) also frequently lead to tree death, and thus have significant effects on forest ecosystem functioning, but they are much less well studied than trophic interactions are. As deer populations have increased in recent decades in the Northern Hemisphere, their impact on tree populations via browsing and antler rubbing will increase. The aim of the study was to illustrate the potential ability of non‐trophic plant–animal interactions to regulate the dynamics of a natural forest. Specifically, we wanted to determine whether and how density and distance‐dependent processes affect sapling mortality caused by an antler rubbing by red deer Cervus elaphus. We used a spatially explicit approach to examine density and distance‐dependent mortality effects in almost two thousand Picea abies saplings over 20 years, based on a fully mapped permanent 14.4 ha plot in a natural subalpine old‐growth spruce forest. Antler rubbing by deer was the main identified cause of sapling mortality, and it showed a strong spatial pattern: positive density dependence of survival among spruce saplings. Deer selectively killed spruce saplings that were isolated from conspecifics. In consequence, non‐trophic plant–deer interactions were a major driver of the spatial pattern of P. abies sapling survival. The other mortality causes (e.g. breaking, overturning) did not show density‐dependent patterns or their effects were much weaker. In the medium and long term, the density‐dependent pattern of sapling mortality due to antler rubbing can alter the tree stand structure. Our results highlight the ecological relevance of non‐trophic plant–animal interactions for forest ecosystem functioning.     

SPATIAL DYNAMICS OF A HIMANTHALIA ELONGATA (FUCALES, PHAEOPHYTA) POPULATION

In dense monospecific stands of plants intraspecific competition usually results in self-thinning, the concurrent increase in biomass and decrease in density over time. Self-thinning may also result in a change in the spatial pattern of individuals, but so far the spatial dynamics of marine plants has not been investigated. The brown alga Himanthalia elongata ( L.) S. F. Gray forms dense monospecific stands on many northern temperate rocky shores, and various attributes (including its simple form) facilitated the study of the spatial dynamics of this species .
The spatial pattern of settling zygotes was examined in the laboratory. In the absence of water movement, substratum heterogeneity, and a point source, zygotes usually settled in clumps rather than randomly. Within the clumps zygotes appeared to be regularly distributed at a scale similar to the size of the zygotes themselves. Furthermore, the clumps themselves seemed to be regularly distributed. On the shore, well-established stands of "button-stage" Himanthalia populations were examined during a period of extensive growth and self-thinning. Individual plants were initially highly regular in spatial pattern but became less so over time. The pattern of plants dying during self-thinning was also highly regular and probably reflected existing spatial regularity. However, using a hypothesis of mortality as a random event, I found that smaller plants had a less than average survival potential, while larger plants had a greater than average chance. A consideration of the spatial pattern of plants alive at the end of the study revealed regularity at a scale of 2–7 mm but a random spatial pattern at larger scales, which might indicate a small sphere of influence of competing individuals. The best predictor of mean nearest neighbor distances in the populations was mean plant diameter .     

The shift from plant–plant facilitation to competition under severe water deficit is spatially explicit

The stress‐gradient hypothesis predicts a higher frequency of facilitative interactions as resource limitation increases. Under severe resource limitation, it has been suggested that facilitation may revert to competition, and identifying the presence as well as determining the magnitude of this shift is important for predicting the effect of climate change on biodiversity and plant community dynamics. In this study, we perform a meta‐analysis to compare temporal differences of species diversity and productivity under a nurse plant (Retama sphaerocarpa) with varying annual rainfall quantity to test the effect of water limitation on facilitation. Furthermore, we assess spatial differences in the herbaceous community under nurse plants in situ during a year with below‐average rainfall. We found evidence that severe rainfall deficit reduced species diversity and plant productivity under nurse plants relative to open areas. Our results indicate that the switch from facilitation to competition in response to rainfall quantity is nonlinear. The magnitude of this switch depended on the aspect around the nurse plant. Hotter south aspects under nurse plants resulted in negative effects on beneficiary species, while the north aspect still showed facilitation. Combined, these results emphasize the importance of spatial heterogeneity under nurse plants for mediating species loss under reduced precipitation, as predicted by future climate change scenarios. However, the decreased water availability expected under climate change will likely reduce overall facilitation and limit the role of nurse plants as refugia, amplifying biodiversity loss.     

Effects of Ultraviolet-B Irradiance on Intraspecific Competition and Facilitation of Plants: Self-Thinning,Size Inequality,and Phenotypic Plasticity

(1) The effects of facilitation on the structure and dynamics of plant populations have not been studied so widely as competition. The UV-B radiation, as a typical environmental factor causing stress, may result in direct stress and facilitation. (2) The effects of UV-B radiation on intraspecific competition and facilitation were investigated based on the following three predictions on self-thinning, size inequality, and phenotypic plasticity: i) Self-thinning is the reduction in density that results from the increase in the mean biomass of individuals in crowded populations, and is driven by competition. In this study, the mortality rate of the population is predicted to decrease from UV-B irradiance. ii) The size inequality of a population increases with competition intensity because larger individuals receive a disproportionate share of resources, thereby leaving limited resources for smaller individuals. The second hypothesis assumes that direct stress decreases the size inequality of the population. iii) Phenotypic plasticity is the ability to alter one’s morphology in response to environmental changes. The third hypothesis assumes that certain morphological indices can change among the trade-offs between competition, facilitation, and stress. These predictions were tested by conducting a field pot experiment using mung beans, and were supported by the following results: (3) UV-B radiation increased the survival rate of the population at the end of self-thinning. However, this result was mainly due to direct stress rather than facilitation. (4) Just as competitor, facilitation was also asymmetric. It increased the size inequality of populations during self-thinning, whereas stress decreased the size inequality. (5) Direct stress and facilitation influence plants differently on various scales. Stress inhibited plant growth, whereas facilitation showed the opposite on an individual scale. Stress increased survival rate, whereas facilitation increased individual variability on the population scale. (6) Trade-offs between competitions, facilitation, and direct stress varied in different growing stages.     

植物邻体间的正相互作用

植物间的正负相互作用是构建植被群落的重要因素,也是群落生态学研究的中心内容之一。近20a来,植物间正相互作用的研究得到快速发展。综述了正相互作用的定义,不同植物群落中的直接、间接正相互作用及其发生机制,正相互作用研究的实验和模型方法,正负相互作用随胁迫梯度的变化及正相互作用对群落构建的影响。探讨了正相互作用研究前景:(1)进一步理解正负相互作用的平衡及其对群落构建的影响;(2)加深对全球变暖背景下的正相互作用的认识;(3)需把正相互作用研究同进化联系起来;(4)充分发挥正相互作用在生态系统中的推动力作用,把正相互作用应用到生态恢复中,为恢复退化生态系统服务。     

The effects of density, spatial pattern, and competitive symmetry on size variation in simulated plant populations

Patterns of size inequality in crowded plant populations are often taken to be indicative of the degree of size asymmetry of competition, but recent research suggests that some of the patterns attributed to size-asymmetric competition could be due to spatial structure. To investigate the theoretical relationships between plant density, spatial pattern, and competitive size asymmetry in determining size variation in crowded plant populations, we developed a spatially explicit, individual-based plant competition model based on overlapping zones of influence. The zone of influence of each plant is modeled as a circle, growing in two dimensions, and is allometrically related to plant biomass. The area of the circle represents resources potentially available to the plant, and plants compete for resources in areas in which they overlap. The size asymmetry of competition is reflected in the rules for dividing up the overlapping areas. Theoretical plant populations were grown in random and in perfectly uniform spatial patterns at four densities under size-asymmetric and size-symmetric competition. Both spatial pattern and size asymmetry contributed to size variation, but their relative importance varied greatly over density and over time. Early in stand development, spatial pattern was more important than the symmetry of competition in determining the degree of size variation within the population, but after plants grew and competition intensified, the size asymmetry of competition became a much more important source of size variation. Size variability was slightly higher at higher densities when competition was symmetric and plants were distributed nonuniformly in space. In a uniform spatial pattern, size variation increased with density only when competition was size asymmetric. Our results suggest that when competition is size asymmetric and intense, it will be more important in generating size variation than is local variation in density. Our results and the available data are consistent with the hypothesis that high levels of size inequality commonly observed within crowded plant populations are largely due to size-asymmetric competition, not to variation in local density.     

Nurse‐plant effects on the seed biology and germination of desert annuals

Nurse‐plants generally have positive effects on understorey species by creating more suitable conditions for stress‐intolerant plants relative to open micro‐habitats. However, long‐term effects of this plant–plant facilitation system have been rarely examined. Seeds of five desert annual species from Atiquipa coastal desert in Southern Peru were used to examine whether different microenvironmental conditions under the nurse‐plants Caesalpinia spinosa Molina (Kuntze) lead to differences in seed biology and germinability of annual plants relative to open, canopy‐free conditions. Seeds collected from plants associated with nurse‐plants were predicted to be (i) larger due to more favourable growing conditions, (ii) more viable and with greater germination rates, (iii) less variable in size and viability due to reduced environmental heterogeneity, and (iv) to germinate faster to avoid apparent competition with other annuals. Seed attribute measurements and germination trials in growth chambers were used to test these predictions. Although the plant abundance of only 2 of 5 species was strongly facilitated by the nurse‐plant, no significant differences were found in seed mass, viability or relative variability between understorey and open micro‐habitats for any of the species. Contrary to our predictions, final seed germination rates of seeds from open micro‐habitats were higher, and the open micro‐habitat treatment was more favourable for germination of seeds from both open and understorey environments. Taken together, these results suggest that plant–plant facilitation does not necessarily affect seed biology traits. Further studies addressing larger distribution ranges and/or density gradients of understorey species will illuminate the potential evolutionary effects of nurse‐plants.