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。     

Inclusion of biotic stress (consumer pressure) alters predictions from the stress gradient hypothesis

1.  The stress gradient hypothesis (SGH) predicts a shift from net negative interactions in benign environments towards net positive in harsh environments in ecological communities. While several studies found support for the SGH, others found evidence against it, leading to a debate on how nature and strength of species interactions change along stress gradients, and to calls for new empirical and theoretical work.
2.  In the latest attempt in this journal, it is successfully argued how the SGH should be expanded by considering different life strategies of species (stress tolerance versus competitive ability) and characteristics of abiotic stress (resource versus non-resource based) over wider stress gradients (opposed to low–high contrasts), but the crucial role of biotic stress by consumers is largely ignored in this refinement.
3.  We point out that consumers strongly alter the outcome of species interactions in benign and harsh environments, and show how inclusion of consumer-incurred biotic stress alters the predicted outcome of interactions along resource- and non-resource-based stress gradients for stress-tolerant and competitive benefactors and beneficiaries.
4.   Synthesis. New studies should include stress gradients consisting of both abiotic and biotic components to disentangle their impacts, and to improve our understanding of how species interactions change along environmental gradients.     

Evolution of resource use along a gradient of stress leads to increased facilitation

The stress‐gradient hypothesis (SGH) posits that the relative importance of facilitative interactions versus negative interactions increases as levels of abiotic stress increase. Originally formulated in empirical studies of plant populations, in recent years the SGH has been found to describe how interactions change in response to stress in a wide range of species including algae, mussels and moths. However, there has been little theory attempting to predict patterns from first principles in relation to different types of interactions. Here, we use mathematical models of microbial populations to investigate whether patterns consistent with the SGH arise when species interact through resource use and allelopathy. Evolution alters the degree to which competition for resource use versus facilitation (cross‐feeding) occurs. Our results are consistent with the SGH; species interactions evolve to be more facilitative as average stress intensifies. This occurs because at greater stress the species evolve to become specialists on either of the two resources thereby decreasing overlap in resource use and increasing facilitation through cross‐feeding. In addition, the production of toxic allelopathic compounds decreases as stress intensifies due to density‐dependent effects. Our results suggest that the SGH could arise through fundamental interactions that are common to many organisms and therefore that the SGH could be a more widespread phenomenon than previously recognised.     

Global shifts towards positive species interactions with increasing environmental stress

The study of positive species interactions is a rapidly evolving field in ecology. Despite decades of research, controversy has emerged as to whether positive and negative interactions predictably shift with increasing environmental stress as hypothesised by the stress‐gradient hypothesis (SGH). Here, we provide a synthesis of 727 tests of the SGH in plant communities across the globe to examine its generality across a variety of ecological factors. Our results show that plant interactions change with stress through an outright shift to facilitation (survival) or a reduction in competition (growth and reproduction). In a limited number of cases, plant interactions do not respond to stress, but they never shift towards competition with stress. These findings are consistent across stress types, plant growth forms, life histories, origins (invasive vs. native), climates, ecosystems and methodologies, though the magnitude of the shifts towards facilitation with stress is dependent on these factors. We suggest that future studies should employ standardised definitions and protocols to test the SGH, take a multi‐factorial approach that considers variables such as plant traits in addition to stress, and apply the SGH to better understand how species and communities will respond to environmental change.     

Interaction intensity and importance along two stress gradients: adding shape to the stress-gradient hypothesis

The stress-gradient hypothesis (SGH) predicts that the community-wide prevalence of positive interactions, relative to negative interactions, is greater under more severe environmental conditions. Because the frequency of positive and negative interactions within a community is the aggregate of multiple pair-wise interactions, one approach to testing the SGH is to examine how pair-wise interactions vary along severity gradients. While the SGH suggests that the net outcome of an interaction should monotonically become more positive with increasing environmental severity, recent studies have suggested that the severity-interaction relationship (SIR) may rather be unimodal. We tested which of the proposed shapes of the SIR best fits the variation in the interaction between two species along two types of severity gradients on sub-Antarctic Marion Island. This was done by comparing the performance of the grass Agrostis magellanica in the presence and absence of the cushion plant Azorella selago, along both species’ entire altitudinal ranges (transects spanning 4–8 km), and along a shorter (transect = 0.4 km) wind exposure gradient. Along the altitudinal transects the relative intensity, but not the absolute intensity or the importance, of the Azorella selago–Agrostis magellanica interaction increased with altitude, consistently forming a plateau-shaped SIR with a positive asymptote. Thus, while the performance of Agrostis magellanica was negatively affected by Azorella selago at low altitudes, the grass benefited from growing on the cushion plant under greater environmental severity. Along the wind exposure gradient the intensity of the interaction also became more positive with increasing environmental severity for most performance measures. This suggests that the switch from a net negative to a net positive interaction can occur across both short and long distances. Therefore, this study provides strong evidence for a plateau-shaped SIR, and confirms that the SIR is unimodal along the particular non-resource severity gradients of this study.     

A field test of the stress‐gradient hypothesis along an aridity gradient

Aims: The stress‐gradient hypothesis (SGH) predicts how plant interactions change along environmental stress gradients. We tested the SGH in an aridity gradient, where support for the hypothesis and the specific shape of its response curve is controversial. Location: Almería, Cáceres and Coimbra, three sites in the Iberian Peninsula that encompass the most arid and wet habitats in the distribution range of a nurse shrub species –Retama sphaerocarpa L. (Boiss) – in Europe. Methods: We analysed the effect of Retama on its understorey plant community and measured the biomass and species richness beneath Retama and in gaps. We estimated the frequency (changes in species richness), importance and intensity of the Retama effects, and derived the severity–interaction relationship pattern, analysing how these interaction indices changed along this aridity gradient. Results and conclusions: The intensity and frequency of facilitation by Retama increased monotonically with increasing environmental severity, and the importance tended to have a similar pattern, overall supporting the SGH. Our data did not support predictions from recent revisions of the SGH, which may not apply to whole plant communities like those studied here or when interactions are highly asymmetrical. Facilitation by Retama influenced community composition and species richness to the point that a significant fraction of species found at the most arid end of the gradient were only able to survive beneath the nurse shrub, whereas some of these species were able to thrive in gaps at more mesic sites, highlighting the ecological relevance of facilitation by nurse species in mediterranean environments, especially in the driest sites.     

Testing the role of biotic stress in the stress gradient hypothesis. Processes and patterns in arid rangelands

Since many arid ecosystems are overstocked with domestic herbivores, biotic stress could have a stronger influence in modulating the balance of species interactions than expected from the stress gradient hypothesis (SGH). Here we tested a priori predictions about the effect of grazing on species interactions and fine scale spatial structure of grasses in water‐limited ecosystems. We used detailed vegetation mapping and spatial analysis, and performed a field experiment where the direct and indirect components of positive interactions were disentangled to provide evidence of links between process and pattern. We found associational resistance (biotic refuge) to be the dominant process in grazing situations, while competition, instead of direct facilitation, seemed to govern grass spatial patterns when herbivore pressure was relaxed. These results suggest that facilitation between grasses in arid communities may be related to herbivory rather than nurse plant effects. Associational resistance tends to have the strongest effect on spatial aggregation of species at intermediate grazing pressure. Results suggest that contrary to SGH, this physical clustering of species decreased when grazing pressure reached their maximum levels. Positive associations remained significant only when palatability differences between neighbours is large, suggesting that managing stocking rate is a key factor determining the persistence of herbivory refuges. These refuges are potential foci to initiate population recovery of high quality forage species in arid degraded areas.     

Modelling the niche space of desert annuals needs to include positive interactions

The niche is a necessary consideration when estimating habitable area and geographic range of a species. Modellers often examine the fundamental niche and the environmental requirements for plant species, ignoring interactions among species. In deserts, positive plant interactions are important drivers of biodiversity and structure communities through many mechanistic pathways including modifying environmental conditions. Thus, we tested the hypothesis that desert shrubs increase the geographical extent of some annual species because, through modifying the microclimate, they match the niche requirements of beneficiary species. We used the database of the Global Biodiversity Information Facility to construct MaxEnt species distribution models (SDM) with and without reported benefactor species within the Mojave Desert in California. We chose 20 annual species to be modeled including 10 species that had been previously reported in the literature as being facilitated (beneficiary) and 10 that had no record of being facilitated (unreported). Beneficiary annuals co‐occurred significantly more with benefactor shrubs than the unreported annual species. The inclusion of shrubs into SDMs significantly improved model predictability and geographic range for all the beneficiary annual species, but not for the unreported annual species. Thus, positive interactions are species specific and it is possible to determine annual species dependency on benefactor shrubs at the regional scale. The co‐occurrence of benefactor shrubs and annual species can be used as a proxy for facilitation and recent developments in SDM techniques encourage the inclusion of biotic interactions. Species distribution models should include estimates of facilitation because biotic interactions determine the niche of species and can have implications with a changing climate.     

A dynamic model of facilitation on environmental stress gradients

Theories based on competition for resources in animals and other non‐sessile organisms rarely consider the role of facilitative interactions. Yet these interactions are important for community assembly, especially under stressful environments (e.g. the stress‐gradient hypothesis, SGH). To make an explicit link between species interaction theory and SGH patterns, I used a classic resource competition model promoting coexistence between a beneficiary and its facilitator sharing a common resource along a stress gradient. I compared model outcomes for two fundamentally different mechanisms of facilitation (alleviation of resource versus non‐resource stress), and also tested the effect of a reciprocal cost of facilitation from the beneficiary. I then tested model's biological relevance using experimental data from two tuber moth species (Lepidoptera, Gelechiidae) for which facilitation in resource access was previously established. Simulation outcomes revealed that both the mode of facilitation and the incorporation of facilitation costs affected the shape of the facilitation–stress relationship. These predictions are in line with current SGH observations and experiments on both plants and animals and reconcile the frequently reported variability of this relationship in nature. Moreover, a sensitivity analysis of model's parameters confirmed the robustness of the modelling framework to uncover the mechanisms responsible for observed species interaction–stress patterns. Finally, when parameterized with tuber moth demographic data, model's results corresponded to observed interaction outcomes along resource stress gradients. Overall, having a common model for plants and animals may simplify assumptions in SGH studies, allow contrasting the shapes of different consumer–resource relationships and specifying the conditions that favour one type of interaction outcome over another.     

A case for associational resistance: Apparent support for the stress gradient hypothesis varies with study system

According to the stress gradient hypothesis (SGH), ecological interactions between organisms shift positively as environmental stress increases. In the case of associational resistance, habitat is modified to ameliorate stress, benefitting other organisms. The SGH is contentious due to conflicting evidence and theoretical perspectives, so we adopted a meta-analytic approach to determine if it is widely supported across a variety of contexts, including different kingdoms, ecosystems, habitats, interactions, stressors, and life history stages. We developed an extensive list of Boolean search criteria to search the published ecological literature and successfully detect studies that both directly tested the hypothesis, and those that were relevant but never mentioned it. We found that the SGH is well supported by studies that feature bacteria, plants, terrestrial ecosystems, interspecific negative interactions, adults, survival instead of growth or reproduction, and drought, fire, and nutrient stress. We conclude that the SGH is indeed a broadly relevant ecological hypothesis that is currently held back by cross-disciplinary communication barriers. More SGH research is needed beyond the scope of interspecific plant competition, and more SGH research should feature multifactor stress. There remains a need to account for positive interactions in scientific pursuits, such as associational resistance in tests of the SGH.     

Two alternatives to the stress‐gradient hypothesis at the edge of life: the collapse of facilitation and the switch from facilitation to competition

New evidence demonstrates that facilitation plays a crucial role even at the edge of life in Maritime Antarctica. These findings are interpreted as support for the stress‐gradient hypothesis (SGH) – a dominant theory in plant community ecology that predicts that the frequency of facilitation directly increases with stress. A recent development to this theory, however, proposed that facilitation often collapses at the extreme end of stress and physical disturbance gradients. In this paper, we clarify the current debate on the importance of plant interactions at the edge of life by illustrating the necessity of separating the two alternatives to the SGH, namely the collapse of facilitation, and the switch from facilitation to competition occurring in water‐stressed ecosystems. These two different alternatives to the SGH are currently often amalgamated with each other, which has led to confusion in recent literature. We propose that the collapse of facilitation is generally due to a decrease in the effect of the nurse plant species, whilst the switch from facilitation to competition is driven by environmental conditions and strategy of the response species. A clear separation between those two alternatives is particularly crucial for predicting the role of plant–plant interactions in mediating species responses to global change.     

Positive interactions among competitors can produce species-rich communities

Although positive interactions between species are well documented, most ecological theory for investigating multispecies coexistence remains rooted in antagonistic interactions such as competition and predation. Standard resource-competition models from this theory predict that the number of coexisting species should not exceed the number of factors that limit population growth. Here I show that positive interactions among resource competitors can produce species-rich model communities supported by a single limiting resource. Simulations show that when resource competitors reduce each others' per capita mortality rate (e.g. by ameliorating an abiotic stress), stable multispecies coexistence with a single resource may be common, even while the net interspecific interaction remains negative. These results demonstrate that positive interactions may provide an important mechanism for generating species-rich communities in nature. They also show that focusing on the net interaction between species may conceal important coexistence mechanisms when species simultaneously engage in both antagonistic and positive interactions.     

Fine nurse variations explain discrepancies in the stress‐interaction relationship in alpine regions

Despite a large consensus on increasing facilitation among plants with increasing stress in alpine regions, a number of different outcomes of interaction have been observed, which impedes the generalisation of the ‘stress‐gradient hypothesis’ (SGH). With the aim to reconcile the different viewpoints on the stress‐interaction relationship in alpine environments we hypothesized that fine nurse variations within a single life form (cushion) may explain this pattern variability. To test this hypothesis, we compared the magnitude of the stress‐interaction relationship in a single study area with that observed in existing studies involving cushions, worldwide. We characterized the nurse effects of cushions on the whole plant community at inter‐specific, intra‐specific and intra‐individual levels along a stress gradient in the dry, alpine tropics of Bolivia (4400 m, 4700 m and 4900 m a.s.l). Using a relative index of interaction (RII) we included our data in a meta‐analysis on the nurse effects of cushions along alpine gradients, worldwide. At inter‐specific level, the loose cushion Pycnophyllum was a better nurse than the compact Azorella compacta. However, at intra‐individual level facilitation was higher at the periphery than at the centre of cushions, exceeding in magnitude the variation observed at inter‐specific level. This pattern was associated with higher minimum temperature and lower mortality at the periphery of cushions. The net effects of cushions on plant communities became more positive at higher elevation, corroborating the SGH. Within our single site in Bolivia, fine morphological nurse variations captured a similar variability in the stress‐interaction relationship as that observed in a subset of studies on cushions on a worldwide scale. This suggests that fine variations in nurse traits, in general those not considered in protocols dealing with facilitation or in restoration/conservation management plans, explain in part the current discrepancies among SGH studies in alpine regions.     

A temporal dimension to the stress gradient hypothesis for intraspecific interactions

Space and time are the two fundamental drivers of ecological dynamics. Studies exploring the Stress gradient hypothesis (SGH) – which predicts that the patterns of interspecific interactions shift from negative to positive with increasing environmental severity – conceptualize environmental severity predominantly from a spatial perspective. Here, from a temporal perspective and for intraspecific interactions, we asked: do the predictions of the SGH at the intraspecific level apply to seasonal change in environmental severity? We conducted a field experiment, which was complemented by a two‐year field survey of natural populations of the non‐native biennial forb Alliaria petiolata at the Koffler Scientific Reserve, Ontario, Canada. In both experiment and field survey studies we found statistically significant negative density‐dependent survival in the productive summer period and positive density‐dependent survival over the severe winter period. Effects were stronger in the field experiment than in the survey of natural populations. We suggest that the SGH at the intraspecific level may be applicable to seasonal variation in environmental severity, though our ability to detect its effect in natural communities may depend on other factors such as species dominance and environmental heterogeneity.     

Threshold facilitations of interacting species

The dynamics of species interactions are of central importance for the understanding of ecological coexistence, community structure and the effects of biological invasions. Using bark beetles that colonize the same habitat as an example, we explore species interactions in a resource-based model system with positive feedback between insect abundance and resource availability. The net interspecies interaction was found to be highly dynamic and may alternate in time between competition and mutualism. When both bark beetle species were able to kill trees (“aggressive”), our simulations showed strong facilitations between beetle species. This may lead to escape from control by competition, and increase the frequency of outbreaks of tree-killing. The frequency of net positive interactions varied with interaction strengths and the relative aggressiveness of the species and was highest when both species were strongly aggressive; which predicts disastrous outbreaks if, e.g., the European spruce bark beetle Ips typographus and the North American spruce beetle Dendroctonus rufipennis should become interacting species due to introductions. In imbalanced pairs, the relatively less aggressive species was facilitated more often than the aggressive species. Net positive interactions did not occur for strongly inferior species, but their survival was an increasing function of interaction strength with aggressive species and availability of resources. The benefits for the inferior species in the model are consistent with the structure of one aggressive and several less aggressive or non-aggressive species, which is common in bark beetle communities in many parts of the world.     

Extending the stress‐gradient hypothesis – is competition among animals less common in harsh environments?

The role of positive interactions has become widely accepted as a mechanism shaping community dynamics. Most empirical evidence comes from plant communities and sessile marine organisms. However, evidence for the relative role of positive interactions in organizing terrestrial animal communities is more limited, and a general framework that includes positive interactions among animals is lacking. The ‘stress gradient hypothesis’ (SGH) developed by plant ecologists predicts that the balance between positive and negative interactions will vary along gradients of biotic and abiotic stress, with positive interactions being more important in stressful environments. Paralleling the SGH, stress gradients for terrestrial herbivores could be equated to inverse primary productivity gradients, so we would expect positive interactions to prevail in more stressful, low productivity environments. However, this contradicts the typical view of terrestrial animal ecology that low primary productivity systems will foster intense competition for resources among consumers. Here we use alpine herbivores as a case study to test one of the predictions of the SGH in animal communities, namely the prevalence of positive interactions in low productivity environments. We identify potential mechanisms of facilitation and review the limited number of examples of interspecific interactions among alpine herbivores to assess the role of positive and negative interactions in structuring their communities. A meta‐analysis showed no clear trend in the strength and direction of interactions among alpine herbivores. Although studies were biased towards reporting significant negative inter actions, we found no evidence of competition dominating in harsh environments. Thus, our results only partially support the SGH, but directly challenge the dominant view among animal ecologists. Clearly, a sound theoretical framework is needed to include competition, positive and neutral interactions as potential mechanisms determining the structure of animal communities under differing environmental conditions, and the stress‐gradient hypothesis can provide a solid starting point.     

Nurses experience reciprocal fitness benefits from their distantly related facilitated plants

It is well known that many plants benefit from growing beside a nurse plant of another species, but the possibility that the nurse also benefits has been rarely studied. We hypothesize that positive interactions are maintained not only because of the recruitment benefits for the facilitated plants but also because of fitness benefits for the nurse plant. We tested this hypothesis by comparing seed production, seed predation and seed viability of a dominant nurse plant species (Mimosa luisana) when growing alone and in patches surrounded by its facilitated species. We also tested whether fitness of the nurse species is dependent on the phylogenetic neighborhood formed by their facilitated species using an analysis that accounted for the abundance and pairwise phylogenetic similitude of all species in each patch. Nurses growing associated to their facilitated species produced more seeds (1.86 times) and these seeds were more viable (1.47 times) than those of nurses growing alone. Seed predation did not alter these fitness differences. Seed number and viability increased in phylogenetically diverse neighborhoods. We conclude that distantly related partners are more likely to cause reciprocal increases in fitness, and that such effects contribute to species coexistence.     

Plant–plant facilitation increases with reduced phylogenetic relatedness along an elevation gradient

Environmental conditions can modify the intensity and sign of ecological interactions. The stress gradient hypothesis (SGH) predicts that facilitation becomes more important than competition under stressful conditions. To properly test this hypothesis, it is necessary to account for all (not a subset of) interactions occurring in the communities and consider that species do not interact at random but following a specific pattern. We aim to assess elevational changes in facilitation, in terms of species richness, frequency and intensity of the interaction as a function of the evolutionary relatedness between nurses and their associated species. We sampled nurse and their facilitated plant species in two 1000–2000 m. elevation gradients in Mediterranean Chile where low temperature imposes a mortality filter on seedlings. We first estimated the relative importance of facilitation as a mechanism adding new species to communities distributed along these gradients. We then tested whether the frequency and intensity of facilitation increases with elevation, taking into account the evolutionary relatedness of the nurse species and the facilitated species. We found that nurses increase the species richness of the community by up to 35%. Facilitative interactions are more frequent than competitive interactions (56% versus 44%) and facilitation intensity increased with elevation for interactions involving distantly related lineages. Our results highlight the importance of including an evolutionary dimension in the study of facilitation to have a clearer picture of the mechanisms enabling species to coexist and survive under stressful conditions. This knowledge is especially relevant to conserve vulnerable and threatened communities facing new climate scenarios, such as those located in Mediterranean-type ecosystems.     

The geographic scaling of biotic interactions

A central tenet of ecology and biogeography is that the broad outlines of species ranges are determined by climate, whereas the effects of biotic interactions are manifested at local scales. While the first proposition is supported by ample evidence, the second is still a matter of controversy. To address this question, we develop a mathematical model that predicts the spatial overlap, i.e. co‐occurrence, between pairs of species subject to all possible types of interactions. We then identify the scale of resolution in which predicted range overlaps are lost. We found that co‐occurrence arising from positive interactions, such as mutualism (+/+) and commensalism (+/0), are manifested across scales. Negative interactions, such as competition (?/?) and amensalism (?/0), generate checkerboard patterns of co‐occurrence that are discernible at finer resolutions but that are lost and increasing scales of resolution. Scale dependence in consumer–resource interactions (+/?) depends on the strength of positive dependencies between species. If the net positive effect is greater than the net negative effect, then interactions scale up similarly to positive interactions. Our results challenge the widely held view that climate alone is sufficient to characterize species distributions at broad scales, but also demonstrate that the spatial signature of competition is unlikely to be discernible beyond local and regional scales.     

Community structure and positive interactions in constraining environments

Spatial patterns in plant communities are thought to be controlled by the interplay of species interactions and environmental constraints. To evaluate the role of plant–plant interactions in shaping these communities we quantified species co-occurrence and interaction in seven environmentally distinct communities. These included four different semiarid habitats in southeast Spain, one alpine system in the Sierra Nevada range (Spain), and two sites in Venezuela, a secondary savanna near Caracas (Altos de Pipe), and a sclerophyllous shrubland in the Gran Sabana plateau. We expected that facilitation would be stronger at sites with more spatial associations. The four semiarid sites in Spain and the shrubland in Gran Sabana showed a high degree of positive species associations. Of the other two communities, one showed both positive and negative associations while negative ones predominated in Altos de Pipe. The direct experimental measure of neighbors' effect showed that positive interactions among species prevailed in communities where positive species associations dominated. The appearance of benefactor species in patches increased species richness compared with the surrounding inter-shrub spaces. Our results provide a link between spatial patterns and species interactions, where aggregation points to positive interactions and segregation to competitive or interference effects. Facilitation appears as a relevant process shaping communities under environmental constraints.