Using exclusion rate to unify niche and neutral perspectives on coexistence

The competitive exclusion principle is one of the most influential concepts in ecology. The classical formulation suggests a correlation between competitor species similarity and competition severity, leading to rapid competitive exclusion where species are very similar; yet neutral models show that identical species can persist in competition for long periods. Here, we resolve the conflict by examining two components of similarity – niche overlap and competitive similarity – and modeling the effects of each on exclusion rate (defined as the inverse of time to exclusion). Studying exclusion rate, rather than the traditional focus on binary outcomes (coexistence versus exclusion), allows us to examine classical niche and neutral perspectives using the same currency. High niche overlap speeds exclusion, but high similarity in competitive ability slows it. These predictions are confirmed by a well‐known model of two species competing for two resources. Under ecologically plausible scenarios of correlation between these two factors, the strongest exclusion rates may be among moderately similar species, while very similar and highly dissimilar competitors have very low exclusion rates. Adding even small amounts of demographic stochasticity to the model blurs the line between deterministic and probabilistic coexistence still further. Thus, focusing on exclusion rate, instead of on the binary outcome of coexistence versus exclusion, allows a variety of outcomes to result from competitive interactions. This approach may help explain species coexistence in diverse competitive communities and raises novel issues for future work.     

Coexistence through mutualist‐dependent reversal of competitive hierarchies

Mechanisms that allow for the coexistence of two competing species that share a trophic level can be broadly divided into those that prevent competitive exclusion of one species within a local area, and those that allow for coexistence only at a regional level. While the presence of aphid‐tending ants can change the distribution of aphids among host plants, the role of mutualistic ants has not been fully explored to understand coexistence of multiple aphid species in a community. The tansy plant (Tanacetum vulgare) hosts three common and specialized aphid species, with only one being tended by ants. Often, these aphids species will not coexist on the same plant but will coexist across multiple plant hosts in a field. In this study, we aim to understand how interactions with mutualistic ants and predators affect the coexistence of multiple species of aphid herbivores on tansy. We show that the presence of ants drives community assembly at the level of individual plant, that is, the local community, by favoring one ant‐tended species, Metopeurum fuscoviride, while preying on the untended Macrosiphoniella tanacetaria and, to a lesser extent, Uroleucon tanaceti. Competitive hierarchies without ants were very different from those with ants. At the regional level, multiple tansy plants provide a habitat across which all aphid species can coexist at the larger spatial scale, while being competitively excluded at the local scale. In this case, ant mutualist‐dependent reversal of the competitive hierarchy can drive community dynamics in a plant–aphid system.     

A COEVOLUTIONARY ISOMORPHISM APPLIED TO LABORATORY STUDIES OF COMPETITION

Some empirical consequences of an isomorphism between the Lotka-Volterra competitive model and a coevolutionary competitive model are developed. In both the Lotka-Volterra and coevolutionary models, four competitive outcomes are possible: 1) species one wins, 2) species two wins, 3) indeterminate outcome, and 4) stable coexistence. These two models are isomorphic in the sense that the inequalities associated with a particular competitive outcome of the Lotka-Volterra model correspond in a one-to-one manner with similar inequalities associated with the same competitive outcome of the coevolutionary model. The inequalities of the Lotka-Volterra model involve the competition coefficients themselves, while the inequalities of the coevolutionary model involve the genetic variances and covariances of the competition coefficients. The isomorphism suggests some alternative interpretations of the results of classical laboratory studies of competition. The Lotka-Volterra (or ecological) hypotheses postulate that the competition coefficients are constant and that genetic considerations play no role in determining the competitive outcome. By contrast, the evolutionary hypotheses derived from the coevolutionary model postulate that the competition coefficients are variables and that the genetic variances and covariances of the competition coefficients determine the competitive outcome. The isomorphism is applied to competitive exclusion and coexistence, and to competitive indeterminacy in Tribolium. In particular, the evolutionary hypotheses isomorphic to the two classical explanations of competitive indeterminacy, the demographic stochasticity and genetic founder effect hypotheses, are constructed. The theory developed here and in a previous paper (Pease, 1984) provides one perspective on the relation among the Lotka-Volterra competition theory, quantitative genetics, competitive exclusion, the reversal of competitive dominance, coexistence, competitive indeterminacy in Tribolium, and experiments investigating the relation between genetic variability and the rate of evolution of fitness.     

Testing for effects of climate change on competitive relationships and coexistence between two bird species

Climate change is expected to have profound ecological effects, yet shifts in competitive abilities among species are rarely studied in this context. Blue tits (Cyanistes caeruleus) and great tits (Parus major) compete for food and roosting sites, yet coexist across much of their range. Climate change might thus change the competitive relationships and coexistence between these two species. Analysing four of the highest-quality, long-term datasets available on these species across Europe, we extend the textbook example of coexistence between competing species to include the dynamic effects of long-term climate variation. Using threshold time-series statistical modelling, we demonstrate that long-term climate variation affects species demography through different influences on density-dependent and density-independent processes. The competitive interaction between blue tits and great tits has shifted in one of the studied sites, creating conditions that alter the relative equilibrium densities between the two species, potentially disrupting long-term coexistence. Our analyses show that long-term climate change can, but does not always, generate local differences in the equilibrium conditions of spatially structured species assemblages. We demonstrate how long-term data can be used to better understand whether (and how), for instance, climate change might change the relationships between coexisting species. However, the studied populations are rather robust against competitive exclusion.     

Cellular automaton models for competition in patchy environments: Facilitation, inhibition, and tolerance

We have developed cellular automaton models for two species competing in a patchy environment. We have modeled three common types of competition: facilitation (in which the winning species can colonize only after the losing species has arrived) inhibition (in which either species is able to prevent the other from colonizing) and tolerance (in which the species most tolerant of reduced resource levels wins). The state of a patch is defined by the presence or absence of each species. State transition probabilities are determined by rates of disturbance, competitive exclusion, and colonization. Colonization is restricted to neighboring patches. In all three models, disturbance permits regional persistence of species that are excluded by competition locally. Persistence, and hence diversity, is maximized at intermediate disturbance frequencies. If disturbance and dispersal rates are sufficiently high, the inferior competitor need not have a dispersal advantage to persist. Using a new method for measuring the spatial patterns of nominal data, we show that none of these competition models generates patchiness at equilibrium. In the inhibition model, however, transient patchiness decays very slowly. We compare the cellular automaton models to the corresponding mean-field patch-occupancy models, in which colonization is not restricted to neighboring patches and depends on spatially averaged species frequencies. The patch-occupancy model does an excellent job of predicting the equilibrium frequencies of the species and the conditions required for coexistence, but not of predicting transient behavior.     

Population size dependence, competitive coexistence and habitat destruction

1. Spatial dynamics can lead to coexistence of competing species even with strong asymmetric competition under the assumption that the inferior competitor is a better colonizer given equal rates of extinction. Patterns of habitat fragmentation may alter competitive coexistence under this assumption.
2. Numerical models were developed to test for the previously ignored effect of population size on competitive exclusion and on extinction rates for coexistence of competing species. These models neglect spatial arrangement.
3. Cellular automata were developed to test the effect of population size on competitive coexistence of two species, given that the inferior competitor is a better colonizer. The cellular automata in the present study were stochastic in that they were based upon colonization and extinction probabilities rather than deterministic rules.
4. The effect of population size on competitive exclusion at the local scale was found to have little consequence for the coexistence of competitors at the metapopulation (or landscape) scale. In contrast, population size effects on extinction at the local scale led to much reduced landscape scale coexistence compared to simulations not including localized population size effects on extinction, especially in the cellular automata models. Spatially explicit dynamics of the cellular automata vs. deterministic rates of the numerical model resulted in decreased survival of both species. One important finding is that superior competitors that are widespread can become extinct before less common inferior competitors because of limited colonization.
5. These results suggest that population size–extinction relationships may play a large role in competitive coexistence. These results and differences are used in a model structure to help reconcile previous spatially explicit studies which provided apparently different results concerning coexistence of competing species.     

Competitive exclusion through reproductive interference

A simple differential equation model was developed to describe the competitive interaction that may occur between species through reproductive interference. The model has the form comparable to Volterra's competition equations, and the graphical analysis of the outcome of the two-species interaction based on its zero-growth isoclines proved that: (1) The possible outcome in this model, as in usual models of resource competition, is either stable coexistence of both species or gradual exclusion of one species by the other, depending critically upon the values of the activity overlapping coefficient c_ij; (2) but, for the same c_ij-values, competitive exclusion is much more ready to occur here than in resource competition; (3) and moreover, the final result of the competition is always dependent on the initial-condition due to its non-linear isoclines, i.e., even under the parameter condition that generally allows both species to coexist, an extreme bias in intial density to one species can readily cause subsequent complete exclusion of its counterparts. Thus, it may follow that the reproductive interference is likely to be working in nature as an efficient mechanism to bring about habitat partitioning in either time or space between some closely related species in insect communities, even though they inhabit heterogeneous habitats where resource competition rarely occurs so that they could otherwise attain steady coexistence.     

Disturbance, interspecific interaction and diversity in metapopulations

Metapopulation diversity patterns depend on the relations among the timescales of local biological interactions (predation, competition), the rates of dispersal among local populations and the patterns of disturbance. We investigate these relationships using a family of simple non-linear Markov chain models. We consider three models for interspecific competition; if the species are identified with early and late successional species, the models describe the facilitation, inhibition and tolerance models of ecological succession. By adding a third competing species we also compare transitive competitive hierarchies and intransitive competitive networks. Finally, we examine the effects of predation in mediating coexistence among competing prey species. In each model we find circumstances in which biotic or abiotic disturbance can increase both local and regional diversity, but those circumstances depend on the various timescales in the model in ways that arc neither obvious nor trivial.     

Trait adaptation promotes species coexistence in diverse predator and prey communities

Species can adjust their traits in response to selection which may strongly influence species coexistence. Nevertheless, current theory mainly assumes distinct and time‐invariant trait values. We examined the combined effects of the range and the speed of trait adaptation on species coexistence using an innovative multispecies predator–prey model. It allows for temporal trait changes of all predator and prey species and thus simultaneous coadaptation within and among trophic levels. We show that very small or slow trait adaptation did not facilitate coexistence because the stabilizing niche differences were not sufficient to offset the fitness differences. In contrast, sufficiently large and fast trait adaptation jointly promoted stable or neutrally stable species coexistence. Continuous trait adjustments in response to selection enabled a temporally variable convergence and divergence of species traits; that is, species became temporally more similar (neutral theory) or dissimilar (niche theory) depending on the selection pressure, resulting over time in a balance between niche differences stabilizing coexistence and fitness differences promoting competitive exclusion. Furthermore, coadaptation allowed prey and predator species to cluster into different functional groups. This equalized the fitness of similar species while maintaining sufficient niche differences among functionally different species delaying or preventing competitive exclusion. In contrast to previous studies, the emergent feedback between biomass and trait dynamics enabled supersaturated coexistence for a broad range of potential trait adaptation and parameters. We conclude that accounting for trait adaptation may explain stable and supersaturated species coexistence for a broad range of environmental conditions in natural systems when the absence of such adaptive changes would preclude it. Small trait changes, coincident with those that may occur within many natural populations, greatly enlarged the number of coexisting species.     

Coexistence of species competing for shared resources

In this paper we develop a mathematical model in which any number of competing species can coexist on four resources which regenerate according to an algebraic relationship. We show that previous attempts to prove that n species cannot coexist on fewer that n resources (the “competitive exclusion principle”) all make use of the very restrictive assumption that the specific growth rates of all competing species are linear functions of resource densities. When this restriction is relaxed, it becomes possible to find situations in which n species can coexist on fewer than n resources. On the basis of this and other observations we conclude that the competitive exclusion principle should be considered to apply only to coexistence at fixed densities.     

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.     

Compartmentalization and niche differentiation: causal patterns of competition and coexistence

The current major models of coexistence of species on the same resources are briefly summarized. It is then shown that analysis of supposedly competitive systems in terms of the physical four dimensions of phase-space is sufficient to understand the causes for coexistence and for competitive exclusion. Thus, the multiple dimensions of niche theory are reduced to factors which define the magnitudes of the phase-spatial system, in particular the boundaries of population spaces and of periods of activity. Excluding possible cooperative interaction between consumers, it appears that coexistence of species on thesame kind of limiting resource is possible only in cases of compartmentalization either in space, or in time, of resource consumption, i.e. if each consumer species disposes of a separate resource supply. Three criteria were found to be decisive for successful compartmentalization (i.e. for coexistence): 1. the vector of the resource flow; 2. relative mobility between consumers and resource units; 3. dependence or independence of resource flow on previous consumption. The traditional terminology of niche theory and of competition theory in general proved to be inadequate for analytical treatment of problems of coexistence.     

Phylogenetic community structure metrics and null models: a review with new methods and software

Competitive exclusion and habitat filtering influence community assembly, but ecologists and evolutionary biologists have not reached consensus on how to quantify patterns that would reveal the action of these processes. Currently, at least 22 α‐diversity and 10 β‐diversity metrics of community phylogenetic structure can be combined with nine null models (eight for β‐diversity metrics), providing 278 potentially distinct approaches to test for phylogenetic clustering and overdispersion. Selecting the appropriate approach for a study is daunting. First, we describe similarities among metrics and null models across variance in phylogeny size and shape, species abundance, and species richness. Second, we develop spatially explicit, individual‐based simulations of neutral, competitive exclusion, or habitat filtering community assembly, and quantify the performance (type I and II error rates) of all 278 metric and null model combinations against each assembly process. Many α‐diversity metrics and null models are at least functionally equivalent, reducing the number of truly unique metrics to 12 and the number of unique metric + null model combinations to 72. An even smaller subset of metric and null model combinations showed robust statistical performance. For α‐diversity metrics, phylogenetic diversity and mean nearest taxon distance were best able to detect habitat filtering, while mean pairwise phylogenetic distance‐based metrics were best able to detect competitive exclusion. Overall, β‐diversity metrics tended to have greater power to detect habitat filtering and competitive exclusion than α‐diversity metrics, but had higher type 1 error in some cases. Across both α‐ and β‐diversity metrics, null model selection affected type I error rates more than metric selection. A null model that maintained species richness, and approximately maintained species occurrence frequency and abundance across sites, exhibited low type I and II error rates. This regional null model simulates neutral dispersal of individuals into local communities by sampling from a regional species pool. We introduce a flexible new R package, metricTester, to facilitate robust analyses of method performance.     

From elaborate to compact seasonal plant epidemic models and back: is competitive exclusion in the details?

Seasonality, or periodic host absence, is a central feature in plant epidemiology. In this respect, seasonal plant epidemic models take into account the way the parasite overwinters and generates new infections. These are termed primary infections. In the literature, one finds two classes of models: high-dimensional elaborate models and low-dimensional compact models, where primary infection dynamics are explicit and implicit, respectively. Investigating a compact model allowed previous authors to show the existence of a competitive exclusion principle. However, the way compact models derive from elaborate models has not been made explicit yet. This makes it unclear whether results such as competitive exclusion extend to elaborate models as well. Here, we show that assuming primary infection dynamics are fast in a standard elaborate model translates into a compact form. Yet, it is not that usually found in the literature. Moreover, we numerically show that coexistence is possible in this original compact form. Reversing the question, we show that the usual compact form approximates an alternate elaborate model, which differs from the earlier one in that primary infection dynamics are density dependent. We discuss to which extent these results shed light on coexistence within soil- and air-borne plant parasites, such as within the take-all disease of wheat and the grapevine powdery mildew cryptic species complexes, respectively.     

Limited niche differentiation within remarkable co‐occurrences of congeneric species: Monomorium ants in the Australian seasonal tropics

Niche theory predicts that few closely related species can co‐occur because such species tend to be ecologically similar and niche differentiation is required to avoid competitive exclusion. We analyse the co‐occurrence of a remarkable 10–15 species of the ant genus Monomorium occurring within single 10 × 10 m plots in a tropical savanna of northern Australia. Most of the species are undescribed, so we use genetic analysis to validate our species demarcations. We document nest dispersion patterns, and investigate differentiation in the three primary niche dimensions: space, time and food. We also examine species differences in competitive abilities, by describing rates of foraging activity, foraging ranges, worker aggression, and levels of behavioural dominance. Analyses of nest and forager distributions showed very limited evidence of spatial segregation within plots. The great majority of species foraged either exclusively or primarily during daylight hours. Body size and isotopic analyses indicated very limited dietary differentiation. Such limited niche partitioning occurred despite the species differing markedly in their competitive abilities as measured by rates of resource discovery, recruitment and monopolization. Our findings defy the traditional assumption that multiple closely related and ecologically similar species of highly interactive taxa cannot co‐occur. It seems very likely that species coexistence in our study system is determined to a very large degree by stochastic processes relating to dispersal and establishment, as predicted by neutral theory. However, neutral theory assumes competitive equivalence, whereas we found very marked differences in the competitive abilities of our co‐occurring species. We suggest that competitive exclusion is prevented by the modular nature of ant colonies, with competition limiting colony performance but not preventing occurrence. We conclude that other factors that allow species persistence, and not just competitive equivalence, can allow dispersal and establishment processes to drive species coexistence.     

Spatial heterogeneity, source-sink dynamics, and the local coexistence of competing species

Patch occupancy theory predicts that a trade-off between competition and dispersal should lead to regional coexistence of competing species. Empirical investigations, however, find local coexistence of superior and inferior competitors, an outcome that cannot be explained within the patch occupancy framework because of the decoupling of local and spatial dynamics. We develop two-patch metapopulation models that explicitly consider the interaction between competition and dispersal. We show that a dispersal-competition trade-off can lead to local coexistence provided the inferior competitor is superior at colonizing empty patches as well as immigrating among occupied patches. Immigration from patches that the superior competitor cannot colonize rescues the inferior competitor from extinction in patches that both species colonize. Too much immigration, however, can be detrimental to coexistence. When competitive asymmetry between species is high, local coexistence is possible only if the dispersal rate of the inferior competitor occurs below a critical threshold. If competing species have comparable colonization abilities and the environment is otherwise spatially homogeneous, a superior ability to immigrate among occupied patches cannot prevent exclusion of the inferior competitor. If, however, biotic or abiotic factors create spatial heterogeneity in competitive rankings across the landscape, local coexistence can occur even in the absence of a dispersal-competition trade-off. In fact, coexistence requires that the dispersal rate of the overall inferior competitor not exceed a critical threshold. Explicit consideration of how dispersal modifies local competitive interactions shifts the focus from the patch occupancy approach with its emphasis on extinction-colonization dynamics to the realm of source-sink dynamics. The key to coexistence in this framework is spatial variance in fitness. Unlike in the patch occupancy framework, high rates of dispersal can undermine coexistence, and hence diversity, by reducing spatial variance in fitness.     

Hominid paleoecology: The competitive exclusion principle and determinants of niche relationships

Some paleonanthropologists invoke the competitive exclusion principle programmatically in support of a single-species (or lineage) hypothesis of hominid evolution. Others apparently accept the association between competitive exclusion and a single species view, and develop multi-species interpretations using only taxonomic concepts. This paper demonstrates that the competitive exclusion principle itself is too assumption-bound to be appropriate for analyzing questions of hominid coexistence. Especially, the principle does not establish the ecological validity of the single-species hypothesis. Contrary to its immediate appearances, the principle has developed historically and analytically to predict and explain the evolution and maintenance of diversity in communities. Used in this manner it constitutes an important basis for the study of hominid paleoecology. Niche concepts necessary to demonstrate this are introduced, and competition and other factors that may have influenced the realized niches of sympatric hominid species are discussed. Nearly all modifications of the competitive exclusion principle that make it more realistic also illuminate factors that generate stable coexistence among competing species. These factors and their organizing theory establish the relevance of a broad data base to the analysis of hominid paleoecology; they should help to guide research on the ecology of early homonid species and their interrelationships.     

Resource use patterns predict long-term outcomes of plant competition for nutrients and light

An 11-year competition experiment among combinations of six prairie perennial plant species showed that resource competition theory generally predicted the long-term outcome of competition. We grew each species in replicated monocultures to determine its requirements for soil nitrate (R*) and light (I*). In six pairwise combinations, the species with the lower R* and I* excluded its competitor, as predicted by theory. In the remaining two pairwise combinations, one species had a lower R*, and the second had a lower I*; these species pairs coexisted, although it is unclear whether resource competition alone was responsible for their coexistence. Smaller differences in R* or I* between competing species led to slower rates of competitive exclusion, and the influence of R* differences on the rate of competitive exclusion was more pronounced on low-nitrogen soils, while the influence of I* differences was more pronounced on high-nitrogen (low-light) soils. These results were not explained by differences in initial species abundances or neutrality. However, only a few of our paired species coexisted under our experimentally imposed conditions (homogeneous soils, high seeding densities, minimal disturbance, regular water, and low herbivory levels), suggesting that other coexistence mechanisms help generate the diversity observed in natural communities.     

How do similarities in spatial distributions and interspecific associations affect the coexistence of Quercus species in the Baotianman National Nature Reserve,Henan, China

Congeneric species often have similar ecological characteristics and use similar resources. These similarities may make it easier for them to co‐occur in a similar habitat but may also lead to strong competitions that limit their coexistence. Hence, how do similarities in congeneric species affect their coexistence exactly? This study mainly used spatial point pattern analysis in two 1 hm² plots in the Baotianman National Nature Reserve, Henan, China, to compare the similarities in spatial distributions and interspecific associations of Quercus species. Results revealed that Quercus species were all aggregated under the complete spatial randomness null model, and aggregations were weaker under the heterogeneous Poisson process null model in each plot. The interspecific associations of Quercus species to non‐Quercus species were very similar in Plot 1. However, they can be either positive or negative in different plots between the co‐occurring Quercus species. The spatial distributions of congeneric species, interspecific associations with non‐Quercus species, neighborhood richness around species, and species diversity were all different between the two plots. We found that congeneric species did have some similarities, and the closely related congeneric species can positive or negative associate with each other in different plots. The co‐occurring congeneric species may have different survival strategies in different habitats. On the one hand, competition among congenerics may lead to differentiation in resource utilization. On the other hand, their similar interspecific associations can strengthen their competitive ability and promote local exclusion to noncongeneric species to obtain more living space. Our results provide new knowledge for us to better understand the coexistence mechanisms of species.     

Evolutionary ecology: when relatives cannot live together

The importance of competition in determining species coexistence has been much debated. A phylogenetic analysis of sedges indicates that competitive exclusion may inhibit co-occurrence among closely related species, but not among more distant relatives.