Reconciling empirical ecology with neutral community models

Neutral community models embody the idea that individuals are ecologically equivalent, having equal fitness over all environmental conditions, and describe how the spatial dynamics and speciation of such individuals can produce a wide range of patterns of distribution, diversity, and abundance. Neutral models have been controversial, provoking a rush of tests and comments. The debate has been spurred by the suggestion that we should test mechanisms. However, the mechanisms and the spatial scales of interest have never clearly been described, and consequently, the tests have often been only peripherally relevant. At least two mechanisms are present in spatially structured neutral models. Dispersal limitation causes clumping of a species, which increases the strength of intraspecific competition and reduces the strength of interspecific competition. This may prolong coexistence and enhance local and regional diversity. Speciation is present in some neutral models and gives a donor-controlled input of new species, many of which remain rare or are short lived, but which directly add to species diversity. Spatial scale is an important consideration in neutral models. Ecological equivalence and equal fitness have implicit spatial scales because dispersal limitation and its emergent effects operate at population levels, and populations and communities are defined at a chosen spatial scale in recent neutral models; equality is measured relative to a metacommunity, and this necessitates defining the spatial scale of that metacommunity. Furthermore, dispersal has its own scales. Thorough empirical tests of neutral models will require both tests of mechanisms and pattern-producing ability, and will involve coupling theoretical models and experiments.     

Interpreting beta‐diversity components over time to conserve metacommunities in highly dynamic ecosystems

The concept of metacommunity (i.e., a set of local communities linked by dispersal) has gained great popularity among community ecologists. However, metacommunity research mostly addresses questions on spatial patterns of biodiversity at the regional scale, whereas conservation planning requires quantifying temporal variation in those metacommunities and the contributions that individual (local) sites make to regional dynamics. We propose that recent advances in diversity‐partitioning methods may allow for a better understanding of metacommunity dynamics and the identification of keystone sites. We used time series of the 2 components of beta diversity (richness and replacement) and the contributions of local sites to these components to examine which sites controlled source‐sink dynamics in a highly dynamic model system (an intermittent river). The relative importance of the richness and replacement components of beta diversity fluctuated over time, and sample aggregation led to underestimation of beta diversity by up to 35%. Our literature review revealed that research on intermittent rivers would benefit greatly from examination of beta‐diversity components over time. Adequately appraising spatiotemporal variability in community composition and identifying sites that are pivotal for maintaining biodiversity at the landscape scale are key needs for conservation prioritization and planning. Thus, our framework may be used to guide conservation actions in highly dynamic ecosystems when time‐series data describing biodiversity across sites connected by dispersal are available.     

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.     

Bird metacommunities in temperate South American forest: vegetation structure, area, and climate effects

Spatial structure in metacommunities and their relationships to environmental gradients have been linked to opposing theories of community assembly. In particular, while the species sorting hypothesis predicts strong environmental influences, the neutral theory, the mass effect, and the patch dynamics frameworks all predict differing degrees of spatial structure resulting from dispersal and competition limitations. Here we study the relative influence of environmental gradients and spatial structure in bird assemblages of the Chilean temperate forest. We carried out bird and vegetation surveys in South American temperate forests at 147 points located in nine different protected areas in central Chile, and collected meteorological and productivity data for these localities. Species composition dissimilarities between sites were calculated, as well as three indices of bird local diversity: observed species richness, Chao estimate of richness, and Shannon diversity. A stepwise multiple regression and partial regression analyses were used to select a small number of environmental factors that predicted bird species diversity. Although diversity indices were spatially autocorrelated, environmental factors were sufficient to account for this autocorrelation. Moreover, community dissimilarities were not significantly related to distance between sites. We then tested a multivariate hypothesis about climate, vegetation, and avian diversity interactions using a structural equation modeling (SEM) approach. The SEM showed that climate and area of fragments have important indirect effects on avian diversity, mediated through changes in vegetation structure. Given the scale of this study, the metacommunity framework provides useful insights into the mechanisms driving bird assemblages in this region. Taken together, the weak spatial structure of community composition and diversity, as well as the strong environmental effects on bird diversity, support the interpretation that species sorting has a predominant role in structuring avian assemblages in the region.     

Metacommunity organization of soil microorganisms depends on habitat defined by presence of Lobelia siphilitica plants

We tested regional-scale spatial patterns in soil microbial community composition for agreement with species sorting and dispersal limitation, two alternative mechanisms behind different models of metacommunity organization. Furthermore, we tested whether regional metacommunity organization depends on local habitat type. We sampled from sites across Ohio and West Virginia hosting populations of Lobelia siphilitica, and compared the metacommunity organization of soil microbial communities under L. siphilitica to those in adjacent areas at each site. In the absence of L. siphilitica, bacterial community composition across the region was consistent with species sorting. However, under L. siphilitica, bacterial community composition was consistent with dispersal limitation. Fungal community composition remained largely unexplained, although fungal communities under L. siphilitica were both significantly different in composition and less variable in composition than in adjacent areas. Our results show that communities in different local habitat types (e.g., in the presence or absence of a particular plant) may be structured on a regional scale by different processes, despite being separated by only centimeters at the local scale.     

Species dispersal rates alter diversity and ecosystem stability in pond metacommunities

Metacommunity theory suggests that relationships between diversity and ecosystem stability can be determined by the rate of species dispersal among local communities. The predicted relationships, however, may depend upon the relative strength of local environmental processes and disturbance. Here we evaluate the role of dispersal frequency and local predation perturbations in affecting patterns of diversity and stability in pond plankton metacommunities. Pond metacommunities were composed of three mesocosm communities: one of the three communities maintained constant "press" predation from a selective predator, bluegill sunfish (Lepomis macrochirus); the second community maintained "press" conditions without predation; and the third community experienced recurrent "pulsed" predation from bluegill sunfish. The triads of pond communities were connected at either no, low (0.7%/d), or high (20%/d) planktonic dispersal. Richness and composition of zooplankton and stability of plankton biomass and ecosystem productivity were measured at local and regional spatial scales. Dispersal significantly affected diversity such that local and regional biotas at the low dispersal rate maintained the greatest number of species. The unimodal local dispersal-diversity relationship was predator-dependent, however, as selective press predation excluded species regardless of dispersal. Further, there was no effect of dispersal on beta diversity because predation generated local conditions that selected for distinct community assemblages. Spatial and temporal ecosystem stability responded to dispersal frequency but not predation. Low dispersal destabilized the spatial stability of producer biomass but stabilized temporal ecosystem productivity. The results indicate that selective predation can prevent species augmentation from mass effects but has no apparent influence on stability. Dispersal rates, in contrast, can have significant effects on both species diversity and ecosystem stability at multiple spatial scales in metacommunities.     

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.     

Spatial clustering of habitat structure effects patterns of community composition and diversity

Natural ecosystems often show highly productive habitats that are clustered in space. Environmental disturbances are also often nonrandomly distributed in space and are either intrinsically linked to habitat quality or independent in occurrence. Theoretical studies predict that configuration and aggregation of habitat patch quality and disturbances can affect metacommunity composition and diversity, but experimental evidence is largely lacking. In a metacommunity experiment, we tested the effects of spatially autocorrelated disturbance and spatial aggregation of patch quality on regional and local richness, among-community dissimilarity, and community composition. We found that spatial aggregation of patch quality generally increased among-community dissimilarity (based on two measures of beta diversity) of communities containing protozoa and rotifers in microcosms. There were significant interacting effects of landscape structure and location of disturbances on beta diversity, which depended in part on the specific beta diversity measures used. Effects of disturbance on composition and richness in aggregated landscapes were generally dependent on distance and connectivity among habitat patches of different types. Our results also show that effects of disturbances in single patches cannot directly be extrapolated to the landscape scale: the predictions may be correct when only species richness is considered, but important changes in beta diversity may be overlooked. There is a need for biodiversity and conservation studies to consider the spatial aggregation of habitat quality and disturbance, as well as connectivity among spatial aggregations.     

The influence of environmental spatial structure on the life-history traits and diversity of species in a metacommunity

Several models have been proposed to understand how so many species can coexist in ecosystems. Despite evidence showing that natural habitats are often patchy and fragmented, these models rarely take into account environmental spatial structure. In this study we investigated the influence of spatial structure in habitat and disturbance regime upon species’ traits and species’ coexistence in a metacommunity. We used a population-based model to simulate competing species in spatially explicit landscapes. The species traits we focused on were dispersal ability, competitiveness, reproductive investment and survival rate. Communities were characterized by their species richness and by the four life-history traits averaged over all the surviving species. Our results show that spatial structure and disturbance have a strong influence on the equilibrium life-history traits within a metacommunity. In the absence of disturbance, spatially structured landscapes favour species investing more in reproduction, but less in dispersal and survival. However, this influence is strongly dependent on the disturbance rate, pointing to an important interaction between spatial structure and disturbance. This interaction also plays a role in species coexistence. While spatial structure tends to reduce diversity in the absence of disturbance, the tendency is reversed when disturbance occurs. In conclusion, the spatial structure of communities is an important determinant of their diversity and characteristic traits. These traits are likely to influence important ecological properties such as resistance to invasion or response to climate change, which in turn will determine the fate of ecosystems facing the current global ecological crisis.     

Evaluating the long-term metacommunity dynamics of tree hole mosquitoes

Four different conceptual models of metacommunities have been proposed, termed "patch dynamics," "species sorting", "mass effect", and "neutral". These models simplify thinking about metacommunities and improve our understanding of the role of spatial dynamics both in structuring communities and in determining local and regional diversity. We tested whether mosquito communities inhabiting water-filled tree holes in southeastern Florida, U.S.A., displayed any of the characteristics and dynamics predicted by the four models. The densities of the five most common species in 3-8 tree holes were monitored every two weeks during 1978-2003. We tested relationships between habitat variables and species densities, spatial synchrony, the presence of life history trade-offs, and species turnover. Dynamics showed strong elements of species sorting, but with considerable turnover, as predicted by the patch dynamics model. Consistent with patch dynamics, there was substantial asynchrony in dynamics for different tree holes, substantial species turnover in space and time, and an occupancy/colonization trade-off. Substantial correlations of density and occupancy with tree hole volume were consistent with the species-sorting model, but unlike this model, species did not have permanent refuges. No evidence of mass effects was found, and correlations between habitat variables and dynamics were inconsistent with neutral models. Our results did not match a single model and therefore caution against overly simplifying metacommunity dynamics by using one dynamical characteristic to select a particular metacommunity perspective.     

Consumptive and nonconsumptive effects of predators on metacommunities of competing prey

Although predators affect prey both via consumption and by changing prey migration behavior, the interplay between these two effects is rarely incorporated into spatial models of predator-prey dynamics and competition among prey. We develop a model where generalist predators have consumptive effects (i.e., altering the likelihood of local prey extinction) as well as nonconsumptive effects (altering the likelihood of colonization) on spatially separated prey populations (metapopulations). We then extend this model to explore the effects of predators on competition among prey. We find that generalist predators can promote persistence of prey metapopulations by promoting prey colonization, but predators can also hasten system-wide extinction by either increasing local extinction or reducing prey migration. By altering rates of prey migration, predators in one location can exert remote control over prey dynamics in another location via predator-mediated changes in prey flux. Thus, the effect of predators may extend well beyond the proportion of patches they visit. In the context of prey metacommunities, predator-mediated shifts in prey migration and mortality can shift the competition-colonization trade-off among competing prey, leading to changes in the prey community as well as changes in the susceptibility of prey species to habitat loss. Consequently, native prey communities may be susceptible to invasion not only by exotic prey species that experience reduced amounts of mortality from resident predators, but also by exotic prey species that exhibit strong dispersal in response to generalist native predators. Ultimately, our work suggests that the consumptive and nonconsumptive effects of generalist predators may have strong, yet potentially cryptic, effects on competing prey capable of mediating coexistence, fostering invasion, and interacting with anthropogenic habitat alteration.     

The effect of positive interactions on community structure in a multi-species metacommunity model along an environmental gradient

Positive interactions are widely recognized as playing a major role in the organization of community structure and diversity. As such, recent theoretical and empirical works have revealed the significant contribution of positive interactions in shaping species’ geographical distributions, particularly in harsh abiotic conditions. In this report, we explore the joint influence of local dispersal and an environmental gradient on the spatial distribution, structure and function of communities containing positive interactions. While most previous theoretical efforts were limited to modelling the dynamics of single pairs of associated species being mutualist or competitor, here we employ a spatially explicit multi-species metacommunity model covering a rich range of interspecific interactions (mutualism, competition and exploitation) along an environmental gradient. We find that mutualistic interactions dominate in communities with low diversity characterized by limited species dispersal and poor habitat quality. On the other hand, the fraction of mutualistic interactions decreases at the expense of exploitation and competition with the increase in diversity caused by higher dispersal and/or habitat quality. Our multi-species model exemplifies the ubiquitous presence of mutualistic interactions and the role of mutualistic species as facilitators for the further establishment of species during ecosystem assembly. We therefore argue that mutualism is an essential component driving the origination of complex and diverse communities.     

Quantifying the dynamics of marine invertebrate metacommunities: What processes can maintain high diversity with low densities in the Mediterranean Sea?

The Mediterranean Sea hosts 5.6% of the world benthic invertebrate species on 0.82% of the ocean surface. Mediterranean ecosystems are also characterized by low densities (and biomasses) compared to other oceanic ecosystems, a feature often attributed to their oligotrophic environment. Oligotrophic conditions can induce lower growth rates and higher mortality rates, and a stronger competition for food between individuals. A theoretical model was developed in order to study the diversity vs. density patterns in coastal benthic invertebrate species. This model describes their minimal population dynamics including basic processes (growth, mortality, reproduction and effects of competitive interactions between individuals) and incorporating fluxes of larvae (finally recruited as juveniles) between a mosaic of local habitats. Populations are therefore structured in a metacommunity. The connectivity between local communities is ensured by passive pelagic larval dispersal. In the Mediterranean Sea, because of the microtidal regime, the connectivity between coastal habitats is lower and more variable than in macrotidal basins. Mathematical properties of the model revealed that competitive interactions (intra- and interspecific competitions) have a stabilizing effect on interacting organisms when gains by recruitment are higher than losses by mortality. In addition, low mortality rates and low connectivity which decreases negative local interactions maintains high regional species diversity with low local densities. This property suggested that oligotrophy cannot be the only factor leading to the high diversity–low density pattern observed in the Mediterranean Sea.     

Latitudinal variation in local interactions and regional enrichment shape patterns of marine community diversity

While communities are shaped by both local interactions and enrichment from the regional species pool, we propose a hypothesis that the balance of these forces shifts with latitude, with regional enrichment dominating at high latitudes and local interactions dominating at low latitudes. To test this hypothesis, we conducted a latitudinal-scale experiment with marine epifaunal communities. In four regions of the North Atlantic Ocean and Caribbean Sea, we used mimics of ecosystem engineers to manipulate biogenic structural complexity. We iteratively evaluated diversity patterns of experimental communities up to one year after deployment. Additional data were also collected from one of our tropical sites 2.5 years after initial deployment. As hypothesized, we found a reciprocal latitudinal gradient in the effects of the structurally complex mimics and regional enrichment. In the tropics, local diversity was always higher in association with the mimics than in exposed areas that were more open to predation. This effect was consistent across two spatial scales and beyond the one-year timescale of the experiment. In temperate communities, no consistent effects of the mimics on diversity were observed. However, the proportion of species from the regional species pool that were present at the local scale increased from the tropics to the temperate zone, consistent with the hypothesis that higher-latitude communities may experience greater influence from the regional species pool than communities at low latitudes. This study represents the first large-scale experimental demonstration that suggests that the relative impact of local interactions and regional enrichment on community diversity may depend on latitude.     

A chemical trait creates a genetic trade-off between intra- and interspecific competitive ability

The importance of non-resource-based mechanisms of competition between plant species has been increasingly recognized, but little is known about how genetic variation and evolutionary changes in the underlying competitive traits might affect species coexistence. I found that genetic variation in sinigrin concentration, a putative allelopathic agent in Brassica nigra, affected the fitness of three heterospecific neighbor species but did not affect neighboring B. nigra individuals. Investment in sinigrin led to a negative genetic correlation between intra- and interspecific competitive ability, which over many generations could provide a strong stabilizing force maintaining both species and genetic diversity in this system.     

A nearly neutral model of biodiversity

S. P. Hubbell's unified neutral theory of biodiversity has stimulated much new thinking about biodiversity. However, empirical support for the neutral theory is limited, and several observations are inconsistent with the predictions of the theory, including positive correlations between traits associated with competitive ability and species abundance and correlations between species diversity and ecosystem functioning. The neutral theory can be extended to explain these observations by allowing species to differ slightly in their competitive ability (fitness). Here, we show that even slight differences in fecundity can greatly reduce the time to extinction of competitors even when the community size is large and dispersal is spatially limited. In this case, species richness is dramatically reduced, and a markedly different species abundance distribution is predicted than under pure neutrality. In the nearly neutral model, species co-occur in the same community not because of, but in spite of, ecological differences. The more competitive species with higher fecundity tend to have higher abundance both in the metacommunity and in local communities. The nearly neutral perspective provides a theoretical framework that unites the sampling model of the neutral theory with theory of biodiversity affecting ecosystem function.     

The unified neutral theory of biodiversity: do the numbers add up?

Hubbell's unified neutral theory is a zero-sum ecological drift model in which population sizes change at random in a process resembling genetic drift, eventually leading to extinction. Diversity is maintained within the community by speciation. Hubbell's model makes predictions about the distribution of species abundances within communities and the turnover of species from place to place (beta diversity). However, ecological drift cannot be tested adequately against these predictions without independent estimates of speciation rates, population sizes, and dispersal distances. A more practical prediction from ecological drift is that time to extinction of a population of size N is approximately 2N generations. I test this prediction here using data for passerine birds (Passeriformes). Waiting times to speciation and extinction were estimated from genetic divergence between sister populations and a lineage-through-time plot for endemic South American suboscine passerines. Population sizes were estimated from local counts of birds in two large forest plots extrapolated to the area of wet tropical forest in South America and from atlas data on European passerines. Waiting times to extinction (ca. 2 Ma) are much less than twice the product of average population size (4.0 and 14.4 x 10(6) individuals in South America and Europe) and generation length (five and three years) for songbirds, that is, 40 and 86 Ma, respectively. Thus, drift is too slow to account for turnover in regional avifaunas. Presumably, other processes, involving external drivers, such as climate and physiographic change, and internal drivers, such as evolutionary change in antagonistic interactions, predominate. Hubbell's model is historical and geographic, and his perspective importantly links local and regional process and pattern. Ecological reality can be added to the mix while retaining Hubbell's concept of continuity of communities in space and time.     

Spatial scale and species identity influence the indigenous-alien diversity relationship in springtails

Although theory underlying the invasion paradox, or the change in the relationship between the richness of alien and indigenous species from negative to positive with increasing spatial scale, is well developed and much empirical work on the subject has been undertaken, most of the latter has concerned plants and to a lesser extent marine invertebrates. Here we therefore examine the extent to which the relationships between indigenous and alien species richness change from the local metacommunity to the interaction neighborhood scales, and the influences of abundance, species identity, and environmental favorability thereon, in springtails, a significant component of the soil fauna. Using a suite of modeling techniques, including generalized least squares and geographically weighted regressions to account for spatial autocorrelation or nonstationarity of the data, we show that the abundance and species richness of both indigenous and alien species at the metacommunity scale respond strongly to declining environmental favorability, represented here by altitude. Consequently, alien and indigenous diversity covary positively at this scale. By contrast, relationships are more complex at the interaction neighborhood scale, with the relationship among alien species richness and/or density and the density of indigenous species varying between habitats, being negative in some, but positive in others. Additional analyses demonstrated a strong influence of species identity, with negative relationships identified at the interaction neighborhood scale involving alien hypogastrurid springtails, a group known from elsewhere to have negative effects on indigenous species in areas where they have been introduced. By contrast, diversity relationships were positive with the other alien species. These results are consistent with both theory and previous empirical findings for other taxa, that interactions among indigenous and alien species change substantially with spatial scale and that environmental favorability may play a key role in explaining the larger scale patterns. However, they also suggest that the interactions may be affected by the identity of the species concerned, especially at the interaction neighborhood scale.     

Mixed but not admixed: a spatial analysis of genetic variation of an invasive ascidian on natural and artificial substrates

Following the introduction to a new area (pre-border dispersal), post-border processes determine the success in the establishment of non-indigenous species (NIS). However, little is known on how these post-border processes shape the genetic composition of NIS at regional scales. Here, we analyse genetic variation in introduced populations along impacted coastlines to infer demographic and kinship dynamics at the post-border stage. We used as a model system the ascidian species Microcosmus squamiger that has been introduced worldwide. This species can colonize and grow fast on man-made artificial structures, impacting activities such as mariculture. However, it can also establish itself on natural substrates, thus altering natural communities and becoming an ecological problem. We genotyped 302 individuals from eight populations established on natural and artificial substrates in the north-western Mediterranean Sea, using six microsatellite loci. We then compared the resulting genotypes with those found within the native range of the species. We found high levels of genetic diversity and allelic richness in all populations, with an overall deficit of heterozygotes. Autocorrelation analyses showed that there was no within-population genetic structure (at a scale of tens of metres); likewise, no significant differentiation in pairwise comparisons between populations (tens of kilometres apart) and no isolation-by-distance pattern was found. The results suggest that M. squamiger has a natural capacity for high dispersal from one patch of hard substrate to another and no differences whatsoever could be substantiated between natural and artificial substrates. Interestingly, two groups of genetically differentiated individuals were detected that were associated with the two ancestral source areas of the worldwide expansion of the species. Individual assignment tests showed the coexistence of individuals of these two clusters in all populations but with little interbreeding among them as the frequency of admixed individuals was only 15 %. The mechanism responsible for maintaining these genetic pools unmixed is unknown, but it does not appear to compromise post-border colonization of introduced populations.