Trade-offs, temporal variation, and species coexistence in communities with intraguild predation

Intraguild predation/parasitism (IGP: competing species preying on or parasitizing each other) is widespread in nature, but the mechanisms by which intraguild prey and predators coexist remain elusive. Theory predicts that a trade-off between resource competition and IGP should allow local niche partitioning, but such trade-offs are expressed only at intermediate resource productivity and cannot explain observations of stable coexistence at high productivity. Coexistence must therefore involve additional mechanisms beside the trade-off, but very little is known about the operation of such mechanisms in nature. Here I present the first experimental test of multiple coexistence mechanisms in a natural community exhibiting IGP. The results suggest that, when resource productivity constrains the competition-IGP trade-off, a temporal refuge for the intraguild prey can not only promote coexistence, but also change species abundances to a pattern qualitatively different from that expected based on the trade-off or a refuge alone. This is the first empirical study to demonstrate a mechanism for why communities with IGP do not lose species diversity in highly productive environments. These results have implications for diversity maintenance in multi-trophic communities, and the use of multiple natural enemies in biological control.     

Interaction rules affect species coexistence in intransitive networks

Intransitive communities, those in which species' abilities cannot be ranked in a hierarchy, have been the focus of theoretical and empirical research, as intransitivity could help explain the maintenance of biodiversity. Here we show that models for intransitive competition embedding slightly different interaction rules can produce opposite patterns. In particular, we find that interactions in which an individual can be outcompeted by its neighbors, but cannot outcompete its neighbors, produce negative frequency dependence that, in turn, promotes coexistence. Whenever the interaction rule is modified toward symmetry (the individual and the neighbors can outcompete each other) the negative frequency dependence vanishes, producing different coexistence levels. Macroscopically, we find that asymmetric interactions yield highest biodiversity if species compete globally, while symmetric interactions favor highest biodiversity if competition takes place locally.     

Dominant species identity, not community evenness, regulates invasion in experimental grassland plant communities

While there has been extensive interest in understanding the relationship between diversity and invasibility of communities, most studies have only focused on one component of diversity: species richness. Although the number of species can affect community invasibility, other aspects of diversity, including species identity and community evenness, may be equally important. While several field studies have examined how invasibility varies with diversity by manipulating species identity or evenness, the results are often confounded by resource heterogeneity, site history, or disturbance. We designed a mesocosm experiment to examine explicitly the role of dominant species identity and evenness on the invasibility of grassland plant communities. We found that the identity of the dominant plant species, but not community evenness, significantly impacted invasibility. Using path analysis, we found that community composition (dominant species identity) reduced invasion by reducing early-season light availability and increasing late-season plant community biomass. Nitrogen availability was an important factor for the survival of invaders in the second year of the experiment. We also found significant direct effects of certain dominant species on invasion, although the mechanisms driving these effects remain unclear. The magnitude of dominant species effects on invasibility we observed are comparable to species richness effects observed in other studies, showing that species composition and dominant species can have strong effects on the invasibility of a community.     

The invasibility of marine algal assemblages: role of functional diversity and identity

The emergence of the biodiversity-ecosystem functioning debate in the last decade has renewed interest in understanding why some communities are more easily invaded than others and how the impact of invasion on recipient communities and ecosystems varies. To date most of the research on invasibility has focused on taxonomic diversity, i.e., species richness. However, functional diversity of the communities should be more relevant for the resistance of the community to invasions, as the extent of functional differences among the species in an assemblage is a major determinant of ecosystem processes. Although coastal marine habitats are among the most heavily invaded ecosystems, studies on community invasibility and vulnerability in these habitats are scarce. We carried out a manipulative field experiment in tide pools of the rocky intertidal to test the hypothesis that increasing functional richness reduces the susceptibility of macroalgal communities to invasion. We selected a priori four functional groups on the basis of previous knowledge of local species characteristics: encrusting, turf, subcanopy, and canopy species. Synthetic assemblages containing one, two, three, or four different functional groups of seaweeds were created, and invasion by native species was monitored over an eight-month period. Cover and resource availability in the assemblages with only one functional group showed different patterns in the use of space and light, confirming true functional differences among our groups. Experimental results showed that the identity of functional groups was more important than functional richness in determining the ability of macroalgal communities to resist invasion and that resistance to invasion was resource-mediated.     

Spatial arrangement of competitors influences coexistence of reef-building corals

Spatial aggregation among strong competitors has been identified as a putative mechanism promoting the coexistence of weak competitors in intensely competitive communities. With notable exceptions in plant communities, few investigators have tested this hypothesis experimentally. In this study, we manipulated the spatial arrangement of corals to test whether within-patch aggregation of a strong coral competitor enhances the success of a weaker coral competitor. Corals grown in simple aggregated arrangements, where the number and type of competitors were held constant, grew almost twice as much as those in non-aggregated arrangements. These growth results suggest that species coexistence is promoted by aggregation within competitive neighborhoods. Thus spatial aggregation may be one of several important mechanisms contributing to the persistence of weak competitors and species coexistence on coral reefs.     

Consequences of dominance: a review of evenness effects on local and regional ecosystem processes

The composition of communities is strongly altered by anthropogenic manipulations of biogeochemical cycles, abiotic conditions, and trophic structure in all major ecosystems. Whereas the effects of species loss on ecosystem processes have received broad attention, the consequences of altered species dominance for emergent properties of communities and ecosystems are poorly investigated. Here we propose a framework guiding our understanding of how dominance affects species interactions within communities, processes within ecosystems, and dynamics on regional scales. Dominance (or the complementary term, evenness) reflects the distribution of traits in a community, which in turn affects the strength and sign of both intraspecifc and interspecific interactions. Consequently, dominance also mediates the effect of such interactions on species coexistence. We review the evidence for the fact that dominance directly affects ecosystem functions such as process rates via species identity (the dominant trait) and evenness (the frequency distribution of traits), and indirectly alters the relationship between process rates and species richness. Dominance also influences the temporal and spatial variability of aggregate community properties and compositional stability (invasibility). Finally, we propose that dominance affects regional species coexistence by altering metacommunity dynamics. Local dominance leads to high beta diversity, and rare species can persist because of source-sink dynamics, but anthropogenically induced environmental changes result in regional dominance and low beta diversity, reducing regional coexistence. Given the rapid anthropogenic alterations of dominance in many ecosystems and the strong implications of these changes, dominance should be considered explicitly in the analysis of consequences of altered biodiversity.     

Small-scale grassland assembly patterns differ above and below the soil surface

The existence of deterministic assembly rules for plant communities remains an important and unresolved topic in ecology. Most studies examining community assembly have sampled aboveground species diversity and composition. However, plants also coexist belowground, and many coexistence theories invoke belowground competition as an explanation for aboveground patterns. We used next-generation sequencing that enables the identification of roots and rhizomes from mixed-species samples to measure coexisting species at small scales in temperate grasslands. We used comparable data from above (conventional methods) and below (molecular techniques) the soil surface (0.1 x 0.1 x 0.1 m volume). To detect evidence for nonrandom patterns in the direction of biotic or abiotic assembly processes, we used three assembly rules tests (richness variance, guild proportionality, and species co-occurrence indices) as well as pairwise association tests. We found support for biotic assembly rules aboveground, with lower variance in species richness than expected and more negative species associations. Belowground plant communities were structured more by abiotic processes, with greater variability in richness and guild proportionality than expected. Belowground assembly is largely driven by abiotic processes, with little evidence for competition-driven assembly, and this has implications for plant coexistence theories that are based on competition for soil resources.     

Stronger predation in the tropics shapes species richness patterns in marine communities

Species interactions are widely assumed to be stronger at lower latitudes, but surprisingly few experimental studies test this hypothesis, and none ties these processes to observed patterns of species richness across latitude. We report here the first experimental field test that predation is both stronger and has a disproportionate effect on species richness in the tropics relative to the temperate zone. We conducted predator-exclusion experiments on communities of sessile marine invertebrates in four regions, which span 32 degrees latitude, in the western Atlantic Ocean and Caribbean Sea. Over a three-month timescale, predation had no effect on species richness in the temperate zone. In the tropics, however, communities were from two to over ten times more species-rich in the absence of predators than when predators were present. While micro-and macro-predators likely compete for the limited prey resource in the tropics, micropredators alone were able to exert as much pressure on the invertebrate communities as the full predator community. This result highlights the extent to which exposure to even a subset of the predator guild can significantly impact species richness in the tropics. Patterns were consistent in analyses that included relative and total species abundances. Higher species richness in the absence of predators in the tropics was also observed when species occurrences were pooled across two larger spatial scales, site and region, demonstrating a consistent scaling relationship. These experimental results show that predation can both limit local species abundances and shape patterns of regional coexistence in the tropics. When preestablished diverse tropical communities were then exposed to predation for different durations, ranging from one to several days, species richness was always reduced. These findings confirmed that impacts of predation in the tropics are strong and consistent, even in more established communities. Our results offer empirical support for the long-held prediction that predation pressure is stronger at lower latitudes. Furthermore, we demonstrate the magnitude to which variation in predation pressure can contribute to the maintenance of tropical species diversity.     

Abiotic constraints eclipse biotic resistance in determining invasibility along experimental vernal pool gradients.

Effective management of invasive species requires that we understand the mechanisms determining community invasibility. Successful invaders must tolerate abiotic conditions and overcome resistance from native species in invaded habitats. Biotic resistance to invasions may reflect the diversity, abundance, or identity of species in a community. Few studies, however, have examined the relative importance of abiotic and biotic factors determining community invasibility. In a greenhouse experiment, we simulated the abiotic and biotic gradients typically found in vernal pools to better understand their impacts on invasibility. Specifically, we invaded plant communities differing in richness, identity, and abundance of native plants (the "plant neighborhood") and depth of inundation to measure their effects on growth, reproduction, and survival of five exotic plant species. Inundation reduced growth, reproduction, and survival of the five exotic species more than did plant neighborhood. Inundation reduced survival of three species and growth and reproduction of all five species. Neighboring plants reduced growth and reproduction of three species but generally did not affect survival. Brassica rapa, Centaurea solstitialis, and Vicia villosa all suffered high mortality due to inundation but were generally unaffected by neighboring plants. In contrast, Hordeum marinum and Lolium multiflorum, whose survival was unaffected by inundation, were more impacted by neighboring plants. However, the four measures describing plant neighborhood differed in their effects. Neighbor abundance impacted growth and reproduction more than did neighbor richness or identity, with growth and reproduction generally decreasing with increasing density and mass of neighbors. Collectively, these results suggest that abiotic constraints play the dominant role in determining invasibility along vernal pool and similar gradients. By reducing survival, abiotic constraints allow only species with the appropriate morphological and physiological traits to invade. In contrast, biotic resistance reduces invasibility only in more benign environments and is best predicted by the abundance, rather than diversity, of neighbors. These results suggest that stressful environments are not likely to be invaded by most exotic species. However, species, such as H. marinum, that are able to invade these habitats require careful management, especially since these environments often harbor rare species and communities.     

Coexistence of intraguild predators and prey in resource-rich environments

The prevalence of intraguild predation (IGP) in productive environments has long puzzled ecologists. Theory predicts the exclusion of intraguild prey from such environments, but data consistently defy this expectation. This suggests that coexistence mechanisms at high resource productivity may differ from those at lower productivity. Here I present a mathematical model that investigates multiple coexistence mechanisms. I incorporate two biological features widely observed in IGP communities: intraspecific interference via cannibalism or superparasitism, and temporal refuges arising from differential sensitivities to abiotic variation. I develop predictions based on three aspects of the IG prey-IG predator interaction: mutual invasibility, transient dynamics, and long-term abundances. These predictions specify the conditions under which coexistence mechanisms reinforce vs. deter one another: when a competition-IGP trade-off allows coexistence at intermediate productivity a temporal refuge for the intraguild prey always allows coexistence at high productivity, but intraspecific interference does so only at a net fitness cost to the intraguild predator. Intraspecific interference that benefits the intraguild predator not only reduces tradeoff-mediated coexistence at intermediate productivity, but also undermines the refuge's coexistence-enhancing effect at high productivity. Different mechanism combinations yield characteristic signatures in time series data during transient dynamics. By judicious measurement of parameters and examining time series for critical signatures, one can elucidate the mechanisms that allow IGP to prevail in resource-rich environments.     

Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence

We investigated the roles of resource availability and phenotypic plasticity in promoting ecological character displacement (i.e., trait evolution stemming from resource competition between species). Because ecological character displacement generates new populations that differ in resource use, this process should only occur when exploitable resources are available. We tested this hypothesis in two species of spadefoot toads (Spea bombifrons and S. multiplicata) whose tadpoles use phenotypic plasticity to develop into either an omnivore morph, which specializes on detritus, or a physically distinctive carnivore morph, which specializes on shrimp. Both species grow best on shrimp, but when reared together, S. bombifrons outcompetes S. multiplicata for shrimp and S. multiplicata outcompetes S. bombifrons for detritus. We found that when each species occurred alone in the field, they produced similar proportions of omnivores and carnivores. When the two species occurred together, however, they underwent ecological character displacement in larval development, with S. multiplicata producing mostly omnivores, and S. bombifrons producing mostly carnivores. We combined observations of natural populations with experiments to evaluate whether such character displacement was only possible when both shrimp and detritus were relatively abundant. Mixed-species ponds contained abundant detritus and shrimp, in contrast with nearby pure-species ponds, which were deficient in one resource. Experiments revealed that S. multiplicata competed poorly when detritus was rare and that S. bombifrons competed poorly when shrimp was rare. In nature, when one of these two resources was scarce, one species was missing, perhaps through competitive exclusion by the species that was the superior competitor for the remaining resource. Thus, ecological character displacement and, therefore, coexistence of close competitors, was only possible when diverse resources were available. Finally, even if exploitable resources are available, character displacement is not guaranteed to transpire if species cannot utilize such resources expeditiously. Phenotypic plasticity provides a general and important mechanism for facilitating resource partitioning. Thus, by facilitating shifts in resource use, phenotypic plasticity and ecological opportunity may often interact to promote divergence and coexistence of competitors.     

Conditions for coexistence of freshwater mussel species via partitioning of fish host resources

Riverine freshwater mussel species can be found in highly diverse communities where many similar species coexist. Mussel species potentially compete for food and space as adults, and for fish host resources during the larval (glochidial) stage. Resource partitioning at the larval stage may promote coexistence. A model of resource utilization was developed for two mussel species and analyzed to determine conditions for coexistence. Mussel species were predicted to coexist when they differed in terms of their success in contacting different fish host species; very similar strategies offered limited possibilities for coexistence. Differences in the mussel species’ maximum infestation loads on the fish hosts that coincided with differences in their fish host contact success promoted coexistence. Mussel species with a given set of trade-offs in fish host use were predicted to coexist only for a subset of relative fish host abundances, so a shift in relative fish host abundances could result in the loss of a mussel species. An understanding of the conditions for freshwater mussel species coexistence can help explain high mussel diversity in rivers and guide ongoing conservation activities.     

The importance of quantifying propagule pressure to understand invasion: an examination of riparian forest invasibility

The widely held belief that riparian communities are highly invasible to exotic plants is based primarily on comparisons of the extent of invasion in riparian and upland communities. However, because differences in the extent of invasion may simply result from variation in propagule supply among recipient environments, true comparisons of invasibility require that both invasion success and propagule pressure are quantified. In this study, we quantified propagule pressure in order to compare the invasibility of riparian and upland forests and assess the accuracy of using a community's level of invasion as a surrogate for its invasibility. We found the extent of invasion to be a poor proxy for invasibility. The higher level of invasion in the studied riparian forests resulted from greater propagule availability rather than higher invasibility. Furthermore, failure to account for propagule pressure may confound our understanding of general invasion theories. Ecological theory suggests that species-rich communities should be less invasible. However, we found significant relationships between species diversity and invasion extent, but no diversity-invasibility relationship was detected for any species. Our results demonstrate that using a community's level of invasion as a surrogate for its invasibility can confound our understanding of invasibility and its determinants.     

A Two-Part Measure of Degree of Invasion for Cross-Community Comparisons

Abstract:  Invasibility is a critical feature of ecological communities, especially for management decisions. To date, invasibility has been measured in numerous ways. Although most researchers have used the richness (or number) of exotic species as a direct or indirect measure of community invasibility, others have used alternative measures such as the survival, density, or biomass of either a single or all exotic species. These different measures, even when obtained from the same communities, have produced inconsistent results and have made comparisons among communities difficult. Here, we propose a measure of the degree of invasion (DI) of a community as a surrogate for community invasibility. The measure is expressed as 2 independent components: exotic proportion of total species richness and exotic proportion of total species abundance (biomass or cover). By including richness and abundance, the measure reflects that the factors that control invasibility affect both of these components. Expressing exotic richness and abundance relative to the richness and abundance of all species in a community makes comparisons across communities of different sizes and resource availability possible and illustrates the importance of dominance of exotic species relative to natives, which is a primary management concern associated with exotic species.     

Mass effects mediate coexistence in competing shrews

Recent developments in metacommunity theory have raised awareness that processes occurring at regional scales might interfere with local dynamics and affect conditions for the local coexistence of competing species. Four main paradigms are recognized in this context (namely, neutral, patch-dynamics, species-sorting, and mass-effect), which differ according to the role assigned to ecological or life-history differences among competing species, as well as to the relative time scale of regional vs. local dynamics. We investigated the patterns of regional and local coexistence of two species of shrews (Crocidura russula and Sorex coronatus) sharing a similar diet (generalist insectivores) over four generations, in a spatially structured habitat at the altitudinal limit of their distributions. Local populations were small, and regional dynamics were strong, with high rates of extinction and recolonization. Niche analysis revealed significant habitat differentiation on a few important variables, including temperature and availability of winter resting sites. In sites suitable for both species, we found instances of local coexistence with no evidence of competitive exclusion. Patterns of temporal succession did not differ from random, with no suggestion of a colonization-competition trade-off. Altogether, our data provide support for the mass-effect paradigm, where regional coexistence is mediated by specialization on different habitat types, and local coexistence by rescue effects from source sites. The strong regional dynamics and demographic stochasticity, together with high dispersal rates, presumably contributed to mass effects by overriding local differences in specific competitive abilities.     

Competition, predation and coexistence in a three trophic system

Simple ecological models that mostly operate with population densities using continuous variables, explain quite well the behavior of real populations. In this work we propose and discuss the continuous dynamics of a system of three species, which belongs to the well-known family of Lotka–Volterra models. In particular, the proposed model includes direct effects such as predation and competition among species, and indirect effects such as refuge. The model is proposed to explain recent studies about a group of crustacean (amphipods of genus Hyallela) found in all the plain streams and shallow lakes of the American continent. The studied system includes three compartments: algae, a strictly herbivore amphipod and an omnivore (herbivore and carnivore) one. The analysis of the model shows that there are stable extinction equilibria throughout all the parameters’ space. There are also equilibria with stable coexistence of the three species and two interesting binary equilibria: one with stable coexistence of algae and herbivore and other with coexistence between algae and omnivore amphipods. The presence of Allee effect in the algae growth and the existence of refuge for the herbivore amphipod (prey) determine a bottom-up control.     

Spatially stochastic settlement and the coexistence of benthic marine animals

For sessile organisms, dispersal and recruitment are typically spatially stochastic, but there is little understanding of how this variability scales up to influence processes such as competitive coexistence. Here we argue that coexistence of benthic marine animals is enhanced by stochastic differences between species in the spatial distribution of larval settlement. Differentiation of settlement distributions among competitors results in intraspecifically aggregated settlement, which can reduce overall interspecific competition and increase overall intraspecific competition. We test for the components of this mechanism using a pair of subtidal invertebrates, and we find that the mean interspecific effect of the dominant competitor is substantially reduced by natural settlement variability. Using a simulation parameterized with experimental data, we find that variable settlement could play an important role in long-term coexistence between these species. This mechanism may apply broadly to benthic marine communities, which can be highly diverse and typically exhibit large settlement fluctuation over a range of scales.     

Turbulence and phytoplankton diversity: A general model of the “paradox of plankton”

The principle of “competitive exclusion” predicts that no two species can occupy the same ecological niche at the same time and place (Hardin, 1960). Hutchinson (1953, 1961) suggested that the vast diversity of phytoplankton observed in many aquatic environments presents an apparent contradiction to this principle. Since all phytoplankton compete for the same basic resources, and since the euphotic zones of most natural waters are relatively homogeneous, such coexisting plankters appear to be simultaneously occupying the same niche. In this paper we present simulation results from a mathematical model wherein we examine the hypothesis that physical turbulence in an aquatic system can mollify interactive pressures between plankton populations and allow coexistence of species competing for the same resources. Using Bella's (1972) highly simplified model as a point of departure, we develop a new model, explicitly incorporating gross physiological mechanisms, to investigate the effects of both advective and turbulent components of water movement on the growth of three competing phytoplankton species. We observed that, in the absence of water motion, no two species were able to coexist, while under the hypothetical conditions of advection without turbulence (laminar flow), just two species were able to occur contemporaneously. Coexistence of all three species was achieved only with the addition of a random turbulent component to the model's hydrodynamic function. Moreover, this general coexistence was observed only when the major turbulent frequency approached the turnover rate of phytoplankton populations. We suggest that there is a limited region of periodicities and magnitudes for hydrodynamic energy in which phytoplankton can coexist, and that most natural aquatic environments fall within this region. We further speculate that, in general, the coupling of physical and biological processes in nature may be influenced by the relative frequency characteristics of those processes.     

Diversity-invasibility across an experimental disturbance gradient in Appalachian Forests

Research examining the relationship between community diversity and invasions by nonnative species has raised new questions about the theory and management of biological invasions. Ecological theory predicts, and small-scale experiments confirm, lower levels of nonnative species invasion into species-rich compared to species-poor communities, but observational studies across a wider range of scales often report positive relationships between native and nonnative species richness. This paradox has been attributed to the scale dependency of diversity-invasibility relationships and to differences between experimental and observational studies. Disturbance is widely recognized as an important factor determining invasibility of communities, but few studies have investigated the relative and interactive roles of diversity and disturbance on nonnative species invasion. Here, we report how the relationship between native and nonnative plant species richness responded to an experimentally applied disturbance gradient (from no disturbance up to clearcut) in oak-dominated forests. We consider whether results are consistent with various explanations of diversity-invasibility relationships including biotic resistance, resource availability, and the potential effects of scale (1 m2 to 2 ha). We found no correlation between native and nonnative species richness before disturbance except at the largest spatial scale, but a positive relationship after disturbance across scales and levels of disturbance. Post-disturbance richness of both native and nonnative species was positively correlated with disturbance intensity and with variability of residual basal area of trees. These results suggest that more nonnative plants may invade species-rich communities compared to species-poor communities following disturbance.     

Coexistence of the niche and neutral perspectives in community ecology

The neutral theory for community structure and biodiversity is dependent on the assumption that species are equivalent to each other in all important ecological respects. We explore what this concept of equivalence means in ecological communities, how such species may arise evolutionarily, and how the possibility of ecological equivalents relates to previous ideas about niche differentiation. We also show that the co-occurrence of ecologically similar or equivalent species is not incompatible with niche theory as has been supposed, because niche relations can sometimes favor coexistence of similar species. We argue that both evolutionary and ecological processes operate to promote the introduction and to sustain the persistence of ecologically similar and in many cases nearly equivalent species embedded in highly structured food webs. Future work should focus on synthesizing niche and neutral perspectives rather than dichotomously debating whether neutral or niche models provide better explanations for community structure and biodiversity.