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Emergent neutrality in consumer-resource dynamics.

ABSTRACT: Neutral theory assumes all species and individuals in a community are ecologically equivalent. This controversial hypothesis has been tested across many taxonomic groups and environmental contexts, and successfully predicts species abundance distributions across multiple high-diversity communities. However, it has been critiqued for its failure to predict a broader range of community properties, particularly regarding community dynamics from generational to geological timescales. Moreover, it is unclear whether neutrality can ever be a true description of a community given the ubiquity of interspecific differences, which presumably lead to ecological inequivalences. Here we derive analytical predictions for when and why non-neutral communities of consumers and resources may present neutral-like outcomes, which we verify using numerical simulations. Our results, which span both static and dynamical community properties, demonstrate the limitations of summarizing distributions to detect non-neutrality, and provide a potential explanation for the successes of neutral theory as a description of macroecological pattern.

SUBMITTER: D'Andrea R

PROVIDER: S-EPMC7446820 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Emergent neutrality in consumer-resource dynamics.

D'Andrea Rafael R Gibbs Theo T O'Dwyer James P JP

PLoS computational biology 20200730 7

Neutral theory assumes all species and individuals in a community are ecologically equivalent. This controversial hypothesis has been tested across many taxonomic groups and environmental contexts, and successfully predicts species abundance distributions across multiple high-diversity communities. However, it has been critiqued for its failure to predict a broader range of community properties, particularly regarding community dynamics from generational to geological timescales. Moreover, it is ...[more]

PMID: 32730245

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Project description:BackgroundThe dominant paradigm for modeling the complexities of interacting populations and food webs is a system of coupled ordinary differential equations in which the state of each species, population, or functional trophic group is represented by an aggregated numbers-density or biomass-density variable. Here, using the metaphysiological approach to model consumer-resource interactions, we formulate a two-state paradigm that represents each population or group in a food web in terms of both its quantity and quality.Methodology and principal findingsThe formulation includes an allocation function controlling the relative proportion of extracted resources to increasing quantity versus elevating quality. Since lower quality individuals senescence more rapidly than higher quality individuals, an optimal allocation proportion exists and we derive an expression for how this proportion depends on population parameters that determine the senescence rate, the per-capita mortality rate, and the effects of these rates on the dynamics of the quality variable. We demonstrate that oscillations do not arise in our model from quantity-quality interactions alone, but require consumer-resource interactions across trophic levels that can be stabilized through judicious resource allocation strategies. Analysis and simulations provide compelling arguments for the necessity of populations to evolve quality-related dynamics in the form of maternal effects, storage or other appropriate structures. They also indicate that resource allocation switching between investments in abundance versus quality provide a powerful mechanism for promoting the stability of consumer-resource interactions in seasonally forcing environments.Conclusions/significanceOur simulations show that physiological inefficiencies associated with this switching can be favored by selection due to the diminished exposure of inefficient consumers to strong oscillations associated with the well-known paradox of enrichment. Also our results demonstrate how allocation switching can explain observed growth patterns in experimental microbial cultures and discuss how our formulation can address questions that cannot be answered using the quantity-only paradigms that currently predominate.

Project description:BackgroundVariability in the ecological impacts of invasive species across their geographical ranges may decrease the accuracy of risk assessments. Comparative functional response analysis can be used to estimate invasive consumer-resource dynamics, explain impact variability, and thus potentially inform impact predictions. The European green crab (Carcinus maenas) has been introduced on multiple continents beyond its native range, although its ecological impacts appear to vary among populations and regions. Our aim was to test whether consumer-resource dynamics under standardized conditions are similarly variable across the current geographic distribution of green crab, and to identify correlated morphological features.MethodsCrabs were collected from multiple populations within both native (Northern Ireland) and invasive regions (South Africa and Canada). Their functional responses to local mussels (Mytilus spp.) were tested. Attack rates and handling times were compared among green crab populations within each region, and among regions (Pacific Canada, Atlantic Canada, South Africa, and Northern Ireland). The effect of predator and prey morphology on prey consumption was investigated.ResultsAcross regions, green crabs consumed prey according to a Type II (hyperbolic) functional response curve. Attack rates (i.e., the rate at which a predator finds and attacks prey), handling times and maximum feeding rates differed among regions. There was a trend toward higher attack rates in invasive than in native populations. Green crabs from Canada had lower handling times and thus higher maximum feeding rates than those from South Africa and Northern Ireland. Canadian and Northern Ireland crabs had significantly larger claws than South African crabs. Claw size was a more important predictor of the proportion of mussels killed than prey shell strength.DiscussionThe differences in functional response between regions reflect observed impacts of green crabs in the wild. This suggests that an understanding of consumer-resource dynamics (e.g., the per capita measure of predation), derived from simple, standardized experiments, might yield useful predictions of invader impacts across geographical ranges.

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Emergent neutrality in consumer-resource dynamics.

Publications

Emergent neutrality in consumer-resource dynamics.

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