Are Trade-Offs Among Species’ Ecological Interactions Scale Dependent? A Test Using Pitcher-Plant Inquiline Species

Trade-offs among species' ecological interactions is a pervasive explanation for species coexistence. The traits associated with trade-offs are typically measured to mechanistically explain species coexistence at a single spatial scale. However, species potentially interact at multiple scales and this may be reflected in the traits among coexisting species. I quantified species' ecological traits associated with the trade-offs expected at both local (competitive ability and predator tolerance) and regional (competitive ability and colonization rate) community scales. The most common species (four protozoa and a rotifer) from the middle trophic level of a pitcher plant (Sarracenia purpurea) inquiline community were used to link species traits to previously observed patterns of species diversity and abundance. Traits associated with trade-offs (competitive ability, predator tolerance, and colonization rate) and other ecological traits (size, growth rate, and carrying capacity) were measured for each of the focal species. Traits were correlated with one another with a negative relationship indicative of a trade-off. Protozoan and rotifer species exhibited a negative relationship between competitive ability and predator tolerance, indicative of coexistence at the local community scale. There was no relationship between competitive ability and colonization rate. Size, growth rate, and carrying capacity were correlated with each other and the trade-off traits: Size was related to both competitive ability and predator tolerance, but growth rate and carrying capacity were correlated with predator tolerance. When partial correlations were conducted controlling for size, growth rate and carrying capacity, the trade-offs largely disappeared. These results imply that body size is the trait that provides the basis for ecological interactions and trade-offs. Altogether, this study showed that the examination of species' traits in the context of coexistence at different scales can contribute to our understanding of the mechanisms underlying community structure.     

Coexistence of nearly neutral species

Aims The neutral theory of biodiversity provides a powerful framework for modeling macroecological patterns and interpreting species assemblages. However, there remain several unsolved problems, including the effect of relaxing the assumption of strict neutrality to allow for empirically observed variation in vital rates and the 'problem of time'—empirically measured coexistence times are much shorter than the prediction of the strictly neutral drift model. Here, we develop a nearly neutral model that allows for differential birth and death rates of species. This model provides an approach to study species coexistence away from strict neutrality.Methods Based on Moran's neutral model, which assumes all species in a community have the same competitive ability and have identical birth and death rates, we developed a model that includes birth–death trade-off but excludes speciation. This model describes a wide range of asymmetry from strictly neutral to nearly neutral to far from neutral and is useful for analyzing the effect of drift on species coexistence. Specifically, we analyzed the effects of the birth–death trade-off on the time and probability of species coexistence and quantified the loss of biodiversity (as measured by Simpson's diversity) due to drift by varying species birth and death rates.Important findings We found (i) a birth–death trade-off operating as an equalizing force driven by demographic stochasticity promotes the coexistence of nearly neutral species. Species near demographic trade-offs (i.e. fitness equivalence) can coexist even longer than that predicted by the strictly neutral model; (ii) the effect of birth rates on species coexistence is very similar to that of death rates, but their compensatory effects are not completely symmetric; (iii) ecological drift over time produces a march to fixation. Trade-off-based neutral communities lose diversity more slowly than the strictly neutral community, while non-neutral communities lose diversity much more rapidly; and (iv) nearly neutral systems have substantially shorter time of coexistence than that of neutral systems. This reduced time provides a promising solution to the problem of time.     

Correlates of inter-specific variation in germination response to water stress in a semi-arid savannah

Within arid plant communities species vary considerably in the ability to germinate under water stress. Attempts to correlate this variation with environmental gradients have remained largely inconclusive. Germinating only at high water potentials can be seen as a form of predictive germination. Predictive germination provides a fitness variance reducing mechanism and is therefore expected to show negative correlations with other variance reducing life-history attributes such as large seed size or dormancy. We predicted that differences in life-history attributes rather than edaphic gradients could explain the variation in germination responses to water stress found in arid plant communities. To test our hypothesis we determined the germination response of 28 species from the arid Kalahari savannah to a gradient of osmotic stress, expressed as the water potential needed to reduce germination by 50%. In addition, we determined the life-history variables seed mass and germination fraction and the habitat variables soil texture preference and association with acacias. The data were analysed using phylogenetically independent contrasts in a multiple regression model.Contrary to our hypothesis we found no increase in the capacity to germinate under osmotic stress with increasing seed mass and an increase with increasing germination fraction. However, we also found no significant effect of the habitat variables. This result may be explained by variation in seedling drought tolerance. Drought tolerance will also have a variance-reducing effect and can be expected to trade-off with fractional germination. Our results suggest that in arid plant communities most variation in the capacity to germinate under water stress expresses different ways to make a living under similar conditions rather than adaptations to environmental gradients.     

Coexistence in a metacommunity: the competition-colonization trade-off is not dead

The competition–colonization trade-off model is often used to explain the coexistence of species. Yet its applicability has been severely criticized, mainly because the original model assumed a strict competitive hierarchy of species and did not allow for any preemptive effect. We considered the impact of relaxing both of these limitations on coexistence. Relaxing trade-off intensity makes coexistence less likely and introduces a minimum colonization rate below which any coexistence is impossible. Allowing for preemption introduces a limit to dissimilarity between species. Surprisingly, preemption does not impede coexistence as one could presume from previous studies, but can actually increase the likelihood of coexistence. Its effect on coexistence depends on whether or not species in the regional pool are strongly limited in their colonization ability. Preemption is predicted to favour coexistence when: (i) species are not strongly limited in their colonization ability; and (ii) the competitive trade-off is not infinitely intense.     

Intraspecific variation and species coexistence

We use a two-species model of plant competition to explore the effect of intraspecific variation on community dynamics. The competitive ability ("performance") of each individual is assigned by an independent random draw from a species-specific probability distribution. If the density of individuals competing for open space is high (e.g., because fecundity is high), species with high maximum (or large variance in) performance are favored, while if density is low, species with high typical (e.g., mean) performance are favored. If there is an interspecific mean-variance performance trade-off, stable coexistence can occur across a limited range of intermediate densities, but the stabilizing effect of this trade-off appears to be weak. In the absence of this trade-off, one species is superior. In this case, intraspecific variation can blur interspecific differences (i.e., shift the dynamics toward what would be expected in the neutral case), but the strength of this effect diminishes as competitor density increases. If density is sufficiently high, the inferior species is driven to extinction just as rapidly as in the case where there is no overlap in performance between species. Intraspecific variation can facilitate coexistence, but this may be relatively unimportant in maintaining diversity in most real communities.     

Signs of stabilisation and stable coexistence

Many empirical studies motivated by an interest in stable coexistence have quantified negative density dependence, negative frequency dependence, or negative plant–soil feedback, but the links between these empirical results and ecological theory are not straightforward. Here, we relate these analyses to theoretical conditions for stabilisation and stable coexistence in classical competition models. By stabilisation, we mean an excess of intraspecific competition relative to interspecific competition that inherently slows or even prevents competitive exclusion. We show that most, though not all, tests demonstrating negative density dependence, negative frequency dependence, and negative plant–soil feedback constitute sufficient conditions for stabilisation of two‐species interactions if applied to data for per capita population growth rates of pairs of species, but none are necessary or sufficient conditions for stable coexistence of two species. Potential inferences are even more limited when communities involve more than two species, and when performance is measured at a single life stage or vital rate. We then discuss two approaches that enable stronger tests for stable coexistence‐invasibility experiments and model parameterisation. The model parameterisation approach can be applied to typical density‐dependence, frequency‐dependence, and plant–soil feedback data sets, and generally enables better links with mechanisms and greater insights, as demonstrated by recent studies.     

Trade-offs and coexistence in microbial microcosms

Trade-offs among the abilities of organisms to respond to different environmental factors are often assumed to play a major role in the coexistence of species. There has been extensive theoretical study of the role of such trade-offs in ecological communities but it has proven difficult to study such trade-offs experimentally. Microorganisms are ideal model systems with which to experimentally study the causes and consequences of ecological trade-offs. In model communities of E. coli B and T-type bacteriophage, a trade-off in E. coli between resistance to bacteriophage and competitive ability is often observed. This trade-off can allow the coexistence of different ecological types of E. coli. The magnitude of this trade-off affects, in predictable ways, the structure, dynamics and response to environmental change of these communities. Genetic factors, environmental factors, and gene-by-environment interactions determine the magnitude of this trade-off. Environmental control of the magnitude of trade-offs represents one avenue by which environmental change can alter community properties such as invasability, stability and coexistence. This revised version was published online in August 2006 with corrections to the Cover Date.     

Dark diversity in dry calcareous grasslands is determined by dispersal ability and stress‐tolerance

Temperate calcareous grasslands are characterized by high levels of species richness at small spatial scales. Nevertheless, many species from a habitat‐specific regional species pool may be absent from local communities and represent the ‘dark diversity’ of these sites. Here we investigate dry calcareous grasslands in northern Europe to determine what proportion of the habitat‐specific species pool is realized at small scales (i.e. how the community completeness varies) and which mechanisms may be contributing to the relative sizes of the observed and dark diversity. We test whether the absence of particular species in potentially suitable grassland sites is a consequence of dispersal limitation and/or a low ability to tolerate stress (e.g. drought and grazing). We analysed a total of 1223 vegetation plots (1 × 1 m) from dry calcareous grasslands in Sweden, Estonia and western Russia. The species co‐occurrence approach was used to estimate the dark diversity for each plot. We calculated the maximum dispersal distance for each of the 291 species in our dataset by using simple plant traits (dispersal syndrome, growth form and seed characteristics). Large seed size was used as proxy for small seed number; tall plant height and low S‐strategy type scores were used to characterise low stress‐tolerance. Levels of small‐scale community completeness were relatively low (more species were absent than present) and varied between the grasslands in different geographic areas. Species in the dark diversity were generally characterized by shorter dispersal distances and greater seed weight (fewer seeds) than species in the observed diversity. Species within the dark diversity were generally taller and had a lower tolerance of stressful conditions. We conclude that, even if temperate grasslands have high levels of small‐scale plant diversity, the majority of potentially suitable species in the regional species pool may be absent as a result of dispersal limitation and low stress‐tolerance.     

Plant resistance to mechanical stress: evidence of an avoidance-tolerance trade-off

External mechanical forces resulting from the pressure exerted by wind or water movement are a major stress factor for plants and may cause regular disturbances in many ecosystems. A plant's ability to resist these forces relies either on minimizing the forces encountered by the plant (avoidance strategy), or on maximizing its resistance to breakage (tolerance strategy). We investigated plant resistance strategies using aquatic vegetation as a model, and examined whether avoidance and tolerance are negatively correlated. We tested the avoidance-tolerance correlation across 28 species using a phylogenetically corrected analysis, after construction of a molecular phylogeny for the species considered. Different species demonstrated contrasting avoidance and tolerance and we demonstrated a significant negative relationship between the two strategies, which suggests an avoidance-tolerance trade-off. Negative relationships may result from costs that each strategy incurs or from constraints imposed by physical laws on plant tissues. The existence of such a trade-off has important ecological and evolutionary consequences. It would lead to constraints on the evolution and variation of both strategies, possibly limiting their evolution and may constrain many morphological, anatomical and architectural traits that underlie avoidance and tolerance.     

The competition-colonization trade-off is dead; long live the competition-colonization trade-off

When applied at the individual patch level, the classic competition-colonization models of species coexistence assume that propagules of superior competitors can displace adults of inferior competitors (displacement competition). But if adults are invulnerable to displacement by propagules (as trees are to seeds), and propagules compete to replace adults that die for reasons independent of the outcome of juvenile competition (a lottery system), a competition-colonization trade-off alone is not able to produce coexistence. However, we show that coexistence is possible if patch density varies spatially, such that it becomes a niche axis. We also show how a dispersal-fecundity trade-off can partition variation in patch density. We discuss the application of these models to empirical systems. An important implication of communities coexisting via variation in patch density is that the amount of habitat loss necessarily interacts with the pattern of loss in affecting extinctions, invasions, and coexistence, in contrast to displacement competition models, for which the spatial pattern of loss is not important or is less important. Finally, with respect to mechanisms promoting coexistence, we suggest that trade-offs between different stages of colonization could be far more common in nature than a trade-off between competitive ability and colonization ability.     

Coexistence and relative abundance in annual plant assemblages: the roles of competition and colonization

Although an interspecific trade-off between competitive and colonizing ability can permit multispecies coexistence, whether this mechanism controls the structure of natural systems remains unresolved. We used models to evaluate the hypothesized importance of this trade-off for explaining coexistence and relative abundance patterns in annual plant assemblages. In a nonspatial model, empirically derived competition-colonization trade-offs related to seed mass were insufficient to generate coexistence. This was unchanged by spatial structure or interspecific variation in the fraction of seeds dispersing globally. These results differ from those of the more generalized competition-colonization models because the latter assume completely asymmetric competition, an assumption that appears unrealistic considering existing data for annual systems. When, for heuristic purposes, completely asymmetric competition was incorporated into our models, unlimited coexistence was possible. However, in the resulting abundance patterns, the best competitors/poorest colonizers were the most abundant, the opposite of that observed in natural systems. By contrast, these natural patterns were produced by competition-colonization models where environmental heterogeneity permitted species coexistence. Thus, despite the failure of the simple competition-colonization trade-off to explain coexistence in annual plant systems, this trade-off may be essential to explaining relative abundance patterns when other processes permit coexistence.     

Evolutionary coexistence in a fluctuating environment by specialization on resource level

Microbial communities in fluctuating environments, such as oceans or the human gut, contain a wealth of diversity. This diversity contributes to the stability of communities and the functions they have in their hosts and ecosystems. To improve stability and increase production of beneficial compounds, we need to understand the underlying mechanisms causing this diversity. When nutrient levels fluctuate over time, one possibly relevant mechanism is coexistence between specialists on low and specialists on high nutrient levels. The relevance of this process is supported by the observations of coexistence in the laboratory, and by simple models, which show that negative frequency dependence of two such specialists can stabilize coexistence. However, as microbial populations are often large and fast growing, they evolve rapidly. Our aim is to determine what happens when species can evolve; whether evolutionary branching can create diversity or whether evolution will destabilize coexistence. We derive an analytical expression of the invasion fitness in fluctuating environments and use adaptive dynamics techniques to find that evolutionarily stable coexistence requires a special type of trade-off between growth at low and high nutrients. We do not find support for the necessary evolutionary trade-off in data available for the bacterium Escherichia coli and the yeast Saccharomyces cerevisiae on glucose. However, this type of data is scarce and might exist for other species or in different conditions. Moreover, we do find evidence for evolutionarily stable coexistence of the two species together. Since we find this coexistence in the scarce data that are available, we predict that specialization on resource level is a relevant mechanism for species diversity in microbial communities in fluctuating environments in natural settings.     

Rules of the seed size game: contests between large‐seeded and small‐seeded species

The coexistence of multiple seed size strategies within plant communities have been considered puzzling, based on a theoretical expectation of the existence of an optimal seed size under each set of specific environmental conditions. A model aimed at explaining the coexistence of different seed sizes has been suggested, where a seed size – seed number tradeoff is connected to a tradeoff between competition and colonization, leading to a competitive advantage in larger‐seeded species and a colonization advantage in smaller‐seeded species. Recently an alternative model has been suggested, based on a tradeoff between stress tolerance and fecundity, associated with the variation from large to small seeds. Here, we examine the role of seed size for recruitment in two‐species contests subjected to various treatments. In a garden experiment seeds of 14 plant species were combined pair‐wise into seven pairs, each with one larger‐seeded species and one smaller‐seeded species. Each species‐pair was sown with sparse and dense seed densities and subjected to different treatments of shading and litter. Recruitment was recorded during two years. Our results showed a general advantage of larger‐seeded species over smaller‐seeded species. This seed size advantage increased in treatments with litter, whereas there were minor effects of shade, and no effect of seed density was found. We thus found little support for a density dependent seed size game as assumed in models of a competition‐colonization tradeoff, whereas our results fit well with a model based on a tradeoff between stress tolerance and fecundity. Our experiment provides novel empirical data to theoretical models on co‐existence between multiple seed size strategies.     

Keystone predation and plant species coexistence: the role of carnivore hunting mode

Plant communities are shaped by bottom-up processes such as competition for nutrients and top-down processes such as herbivory. Although much theoretical work has studied how herbivores can mediate plant species coexistence, indirect effects caused by the carnivores that consume herbivores have been largely ignored. These carnivores can have significant indirect effects on plants by altering herbivore density (density-mediated effects) and behavior (trait-mediated effects). Carnivores that differ in traits, particularly in their hunting mode, cause different indirect effects on plants and, ultimately, different plant community compositions. We analyze a food-web model to determine how plant coexistence is affected by herbivore-consuming carnivores, contrasting those causing only density-mediated effects with those causing trait-mediated effects as well. In the latter case, herbivores can adjust their consumption of a refuge plant species. We derive a general graphical model to study the interplay of density- and trait-mediated effects. We show that carnivores eliciting both effects can sustain plant species coexistence, given intermediate intensities of behavioral adjustments. Coexistence is more likely, and more stable, if the refuge plant is competitively dominant. These results extend our understanding of carnivore indirect effects in food webs and show that behavioral effects can have major consequences on plant community structure, stressing the need for theoretical approaches that incorporate dynamical traits.     

Plant species richness and community productivity: why the mechanism that promotes coexistence matters

This paper stresses that the mechanism of coexistence is the key to understanding the relationship between species richness and community productivity. Using model plant communities, we explored two general kinds of mechanisms based on resource heterogeneity and recruitment limitation, with and without any trade-off between reproductive and competitive abilities. We generated different levels of species richness by changing model parameters, in particular the number of species in the regional pool, the degree of recruitment limitation, and the level of heterogeneity. Different diversity–productivity patterns are obtained with different coexistence mechanisms, indicating there is no reason to expect any general relationship between species richness and productivity. We discuss these results in the context of the within-site and across-site aspects of the relationship between species richness and productivity. Furthermore, we extend these results to hypothesize the relationship between species richness and productivity for other coexistence mechanisms not explicitly considered here.     

Functional Traits in a Species-Rich Grassland and a Short-Term Change in Management: Is There a Competition-Colonization Trade-Off?

The species richness of grasslands generally cannot be fully restored after changes in management. Some species with small statures and basal leaf rosettes can be lost forever. The same species, however, seem to possess the traits necessary for successful re-colonization – they produce small, easily dispersable seeds, numerous seedlings and have lasting seed banks. We tested the hypothesis that plants in species-rich grasslands can be characterized by a negative correlation between their competitive ability and potential for generative regeneration, i.e. by a competition-colonization trade-off. An analysis of the traits of 95 grassland species supported this hypothesis. We then conducted a manipulative experiment in three different meadow communities in the Bílé Karpaty Mts. The experiment involved characterizing species traits during periods of different grassland management regimes in the years 1997–2000 and comparing these with the original management regime, which was restored between 2000 and 2003. We found out that the hypothesis only holds true for the pooled dataset for all three communities. When the individual meadow communities were analyzed separately, plant traits other than those responsible for the competition-colonization trade-off appear to be characteristic of responsive species, e.g. shoot lifespan or phenology. Our results imply that despite the general trade-offs found in large comparative studies, the plant response in a specific community is constrained by the local species pool.     

Competition as a demolition derby: why tolerating competitors is more important than suppressing them

Tolerance and suppression are distinct components of competition among plants, and recognizing how they affect competitive outcomes is important for understanding the mechanisms and consequences of competition. We used simulations informed by experimental trials to ask whether tolerance or suppression of competitors was more important for the survival of native plants experiencing competition with an exotic invasive species. When competition was pairwise, tolerance and suppression contributed equally to competitive rank in simulations. However, when multiple native genotypes competed together against an invader, the ability to tolerate competition was up to 50 times more important than the ability to suppress the invader. In two-competitor communities the chief advantage of suppressing competitors was a global decrease in their abundance, but this advantage did not exist in communities of multiple competitors – which is more representative of natural conditions – because decreased competitor abundance benefited all plants regardless of their competitive ability. We suggest that this concept is analogous to a ‘demolition derby,' an automotive contest where participants attempt to have the last functional vehicle on the playing field. Because strong suppressors share the benefits of eliminating competitors with other remaining competitors, we propose that tolerance of competitors is more beneficial than suppression when competition occurs in a multiplayer scenario – in a demolition derby and in nature. This finding has implications for our understanding of how competition influences plant species coexistence, plant community structure and invasion outcomes.     

Potential mechanisms of coexistence in closely related forbs

The stable coexistence of very similar species has perplexed ecologists for decades and has been central to the development of coexistence theory. According to modern coexistence theory, species can coexist stably (i.e. persist indefinitely with no long‐term density trends) as long as species' niche differences exceed competitive ability differences, even if these differences are very small. Recent studies have directly quantified niche and competitive ability differences in experimental communities at small spatial scales, but provide limited information about stable coexistence across spatial scales in heterogeneous natural communities. In this study, we use experimental and observational approaches to explore evidence for niche and competitive ability differences between two closely related, ecologically similar and widely coexisting annual forbs: Trachymene cyanopetala and T. ornata. We experimentally tested for stabilizing niche differences and competitive ability differences between these species by manipulating species' frequencies, under both well‐watered and water‐stressed conditions. We considered these experimental results in light of extensive field observations to explore evidence of niche segregation at a range of spatial scales. We found little evidence of intra‐specific stabilization or competitive ability differences in laboratory experiments while observational studies suggested niche segregation across pollinator assemblages and small‐scale microclimate heterogeneity. Though we did not quantify long‐term stabilization of coexisting populations of these species, results are consistent with expectations for stable coexistence of similar species via a spatial storage effect allowing niche differences to overcome even small (to absent) competitive ability differences.     

Resistance of a terrestrial plant community to local microhabitat changes

The number of plant and animal species that exist today is estimated to be around 8.7 million. Approximately 300,000 of these species are flora. This extremely high species diversity has been puzzling scientist since the beginning of ecological research because most of these species compete for limited resources that should lead to the exclusion of all but few superior species. This can be seen in a number of coexistence model today that can only maintain at most four species at a time. We have shown recently that by incorporating minute differences in microhabitat to a lattice competition model, about 13 species can coexist from an initial number of 20. Here, we improve the model further by considering that microhabitat differences are not fixed but can change over time which can affect coexistence. A primary driver to this alteration is climate change, both natural and human induced. To show the resistance of a lattice plant community model, a dynamic microhabitat locality is incorporated by changing the spatial and species‐specific heterogeneity of each lattice site. We show that even if the microhabitat locality of each plant species is dynamic, diversity can still be maintained in a lattice plant ecosystem model. This shows that natural communities of terrestrial plants can be resistant to the stress of microhabitat locality changes to a certain extent.     

Eco-Evolutionary dynamics enable coexistence via neighbor-dependent selection

Recent studies suggest that selection can allow coexistence in situations where ecological dynamics lead to competitive exclusion, provided that there is a trade-off between traits optimal for interacting with conspecifics and traits optimal for interacting with heterospecifics. Despite compelling empirical evidence, there is no general framework for elucidating how and when selection will allow coexistence in natural communities. Here we develop such a framework for a mechanism that we term "neighbor-dependent selection." We show that this mechanism can both augment coexistence when ecological conditions allow for niche partitioning and enable coexistence when ecological conditions lead to competitive exclusion. The novel insight is that when ecological conditions lead to exclusion, neighbor-dependent selection can allow coexistence via cycles driven by an intransitive loop; selection causes one species to be a superior interspecific competitor when it is rare and an inferior interspecific competitor when it is abundant. Our framework predicts the conditions under which selection can enable coexistence, as opposed to merely augmenting it, and elucidates the effects of heritability on the eco-evolutionary feedbacks that drive coexistence. Given increasing evidence that evolution operates on ecological timescales, our approach provides one means for evaluating the role of selection and trait evolution in species coexistence.