Towards a mechanistic understanding of variation in aquatic food chain length.

Ecologists have long sought to understand variation in food chain length (FCL) among natural ecosystems. Various drivers of FCL, including ecosystem size, resource productivity and disturbance, have been hypothesised. However, when results are aggregated across existing empirical studies from aquatic ecosystems, we observe mixed FCL responses to these drivers. To understand this variability, we develop a unified competition-colonisation framework for complex food webs incorporating all of these drivers. With competition-colonisation tradeoffs among basal species, our model predicts that increasing ecosystem size generally results in a monotonic increase in FCL, while FCL displays non-linear, oscillatory responses to resource productivity or disturbance in large ecosystems featuring little disturbance or high productivity. Interestingly, such complex responses mirror patterns in empirical data. Therefore, this study offers a novel mechanistic explanation for observed variations in aquatic FCL driven by multiple environmental factors.

Transgressive segregation in mating traits drives hybrid speciation.

Hybridization can rapidly generate novel genetic variation, which can promote ecological speciation by creating novel adaptive phenotypes. However, it remains unclear how hybridization, creating novel mating phenotypes (e.g., mating season, genitalia shapes, sexual displays, mate preferences), affects speciation especially when the phenotypes do not confer adaptive advantages. Here, based on individual-based evolutionary simulations, we propose that transgressive segregation of mating traits can drive incipient hybrid speciation. Simulations demonstrated that incipient hybrid speciation occurred most frequently when the hybrid population received moderate continued immigration from parental lineages causing recurrent episodes of hybridization. Recurrent hybridization constantly generated genetic variation, which promoted the rapid stochastic evolution of mating phenotypes in a hybrid population. The stochastic evolution continued until a novel mating phenotype came to dominate the hybrid population, which reproductively isolates the hybrid population from parental lineages. However, too frequent hybridization rather hindered the evolution of reproductive isolation by inflating the variation of mating phenotypes to produce phenotypes allowing mating with parental lineages. Simulations also revealed conditions for the long-term persistence of hybrid species after their incipient emergence. Our results suggest that recurrent transgressive segregation of mating phenotypes can offer a plausible explanation for hybrid speciation and radiations that involved little adaptive ecological divergence.

Range expansions of sexual versus asexual organisms: Effects of reproductive assurance and migration load.

It is generally considered that sexual organisms show faster evolutionary adaptation than asexual organisms because sexuals can accumulate adaptive mutations through recombination. Yet, empirical evidence often shows that the geographic range size of sexual species is narrower than that of closely related asexual species, which may seem as if asexuals can adapt to more varied environments. Two potential explanations for this apparent contradiction considered by the existing theory are reproduction assurance and migration load. Here, we consider both reproductive assurance and migration load within a single model to comparatively examine their effects on range expansions of sexuals and asexuals across an environmental gradient. The model shows that higher dispersal propensity decreases sexuals' disadvantage in reproductive assurance while increasing their disadvantage in migration load. Moreover, lower mutation rate constrains adaptation more strongly in asexuals than in sexuals. Thus, high dispersal propensity and high mutation rates promote that asexuals have wider range sizes than sexuals. Intriguingly, our model reveals that sexuals can have wider geographic range sizes than asexuals under low dispersal propensity and low mutation rates, a pattern consistent with a few exceptional empirical cases. Combining reproductive assurance and migration load provides a useful perspective to better understand the relationships between species' mating systems and their geographic ranges.

Increased Floral Rewards due to Local Adaptation Drives Plant Ecological Speciation via Learned Preferences of Pollinators.

AbstractIn animal-pollinated plants, the growth environment and pollination environment are two important agents of natural selection. However, their simultaneous effects on plant speciation remain underexplored. Here, we report a theoretical finding that if plants' local adaptation to the growth environment increases their floral rewards for pollinators, it can strongly facilitate ecological speciation in plants. We consider two evolving plant traits, vegetative and floral signal traits, in a population genetic model for two plant populations under divergent selection from different growth environments. The vegetative trait determines plants' local adaptation. Locally adapted plants reward pollinators better than maladapted plants. By associative learning, pollinators acquire learned preferences for floral signal traits expressed by better-rewarding plants. If pollinators' learned preferences become divergent between populations, floral signal divergence occurs and plants develop genetic associations between vegetative and floral signal traits, leading to ecological speciation via a two-allele mechanism. Interestingly, speciation is contingent on whether novel floral signal variants arise before or after plant populations become locally adapted to the growth environment. Our results suggest that simultaneous selection from growth and pollination environments might be important for the ecological speciation of animal-pollinated plants.

The Relationship between Vector Species Richness and the Risk of Vector-Borne Infectious Diseases.

AbstractInfectious diseases can impact human welfare and impede wildlife management. Much recent research explores whether biodiversity increases or decreases infectious disease risk. Here, we theoretically study the relationship between vector species richness and the risk of vector-borne diseases using an epidemiological model of a single host and multiple vectors. The model considers that vectors are involved in interspecific feeding interference that causes transmission interference and in interspecific recruitment competition that mediates susceptible vector regulation. The model reveals three possible shapes of the vector richness-disease risk relationship: monotonic amplification, hump-shaped, and monotonic dilution patterns. The monotonic amplification pattern occurs across a wide parameter region. The hump-shaped and monotonic dilution patterns are found when transmission interference is strong and recruitment competition is weak. Unexpectedly, susceptible vector regulation not only promotes dilution but can strengthen amplification if coupled with strong transmission interference. Our results suggest that vector richness might be more likely to cause amplification rather than dilution, and shifts in the community mean trait values of vectors could also affect disease risk along the vector richness gradient.

The effects of resource subsidy duration in a detritus-based stream ecosystem: A mesocosm experiment.

Most resource subsidies are temporally variable, dynamically affecting the consumer populations, community structures and ecosystem functions of recipient ecosystems. Temporally variable resource subsidies are characterized by the duration, magnitude, timing and frequency of resource subsidy inputs. These different characteristics may have different mechanisms by which to affect recipient ecosystems. Few studies have examined the duration of resource subsidy inputs on recipient ecosystems, although there exist previous studies focusing on magnitude, timing and frequency. We provide the first experimental test of the effects of subsidy duration on a stream ecosystem by using an outdoor mesocosm experiment, in which we directly manipulated the subsidy duration (pulsed vs. prolonged) of terrestrial invertebrate input into the mesocosm. Given the same overall amount of terrestrial invertebrate subsidy was added, a prolonged subsidy allowed large-stage fish to effectively monopolize the subsidy over small-stage fish, which led small-stage fish to maintain their predation pressure on in-situ prey, that is, benthic invertebrates. On the other hand, a pulsed subsidy allowed small-stage fish to increase their feeding rate of the subsidy and to become away from foraging in-situ prey. Consequently, weaker indirect positive effects on in-situ benthic prey and leaf break-down rate were found with the prolonged versus pulsed subsidy. However, these indirect effects varied by the dominant benthic prey species, which differed in edibility for fish. Such predator-specific vulnerability of benthic prey can be important in mediating trophic cascades in detritus-based stream food webs. Phenological events that generate temporal subsidies (e.g. salmon spawning run and arthropod emergence) can be synchronized (pulsed) or desynchronized (prolonged) within and among species, depending on the degree of spatial and temporal environmental heterogeneity. The effects of subsidy duration would thus be important to better understand ecological processes in spatially and temporally coupled ecosystems.

Hybridization can promote adaptive radiation by means of transgressive segregation.

Understanding the mechanisms of rapid adaptive radiation has been a central problem of evolutionary ecology. Recently, there is a growing recognition that hybridization between different evolutionary lineages can facilitate adaptive radiation by creating novel phenotypes. Yet, theoretical plausibility of this hypothesis remains unclear because, for example, hybridization can negate pre-existing species richness. Here, we theoretically investigate whether and under what conditions hybridization promotes ecological speciation and adaptive radiation using an individual-based model to simulate genome evolution following hybridization between two allopatrically evolved lineages. The model demonstrated that transgressive segregation through hybridization can facilitate adaptive radiation, most powerfully when novel vacant ecological niches are highly dissimilar, phenotypic effect size of mutations is small and there is moderate genetic differentiation between parental lineages. These results provide a theoretical basis for the effect of hybridization facilitating adaptive radiation.

Resource waves: phenological diversity enhances foraging opportunities for mobile consumers.

Time can be a limiting constraint for consumers, particularly when resource phenology mediates foraging opportunity. Though a large body of research has explored how resource phenology influences trophic interactions, this work has focused on the topics of trophic mismatch or predator swamping, which typically occur over short periods, at small spatial extents or coarse resolutions. In contrast many consumers integrate across landscape heterogeneity in resource phenology, moving to track ephemeral food sources that propagate across space as resource waves. Here we provide a conceptual framework to advance the study of phenological diversity and resource waves. We define resource waves, review evidence of their importance in recent case studies, and demonstrate their broader ecological significance with a simulation model. We found that consumers ranging from fig wasps (Chalcidoidea) to grizzly bears (Ursus arctos) exploit resource waves, integrating across phenological diversity to make resource aggregates available for much longer than their component parts. In model simulations, phenological diversity was often more important to consumer energy gain than resource abundance per se. Current ecosystem-based management assumes that species abundance mediates the strength of trophic interactions. Our results challenge this assumption and highlight new opportunities for conservation and management. Resource waves are an emergent property of consumer-resource interactions and are broadly significant in ecology and conservation.

Inaccurate Color Discrimination by Pollinators Promotes Evolution of Discrete Color Polymorphism in Food-Deceptive Flowers.

Many plant species employing a food-deceptive pollination strategy show discrete or continuous floral polymorphism within their populations. Previous studies have suggested that negative frequency-dependent selection (NFDS) caused by the learning behavior of pollinators was responsible for the maintenance of floral polymorphism. However, NFDS alone does not explain why and when discrete or continuous polymorphism evolves. In this study, we use an evolutionary simulation model to propose that inaccurate discrimination of flower colors by pollinators results in evolution of discrete flower color polymorphism. Simulations showed that associative learning based on inaccurate discrimination in pollinators caused disruptive selection of flower colors. The degree of inaccuracy determined the number of discrete flower colors that evolved. Our results suggest that animal behavior based on inaccurate discrimination may be a general cause of disruptive selection that promotes discrete trait polymorphism.

Mycoloop: chytrids in aquatic food webs.

Parasites are ecologically significant in various ecosystems through their role in shaping food web structure, facilitating energy transfer, and controlling disease. Here in this review, we mainly focus on parasitic chytrids, the dominant parasites in aquatic ecosystems, and explain their roles in aquatic food webs, particularly as prey for zooplankton. Chytrids have a free-living zoosporic stage, during which they actively search for new hosts. Zoospores are excellent food for zooplankton in terms of size, shape, and nutritional quality. In the field, densities of chytrids can be high, ranging from 10(1) to 10(9) spores L(-1). When large inedible phytoplankton species are infected by chytrids, nutrients within host cells are transferred to zooplankton via the zoospores of parasitic chytrids. This new pathway, the "mycoloop," may play an important role in shaping aquatic ecosystems, by altering sinking fluxes or determining system stability. The grazing of zoospores by zooplankton may also suppress outbreaks of parasitic chytrids. A food web model demonstrated that the contribution of the mycoloop to zooplankton production increased with nutrient availability and was also dependent on the stability of the system. Further studies with advanced molecular tools are likely to discover greater chytrid diversity and evidence of additional mycoloops in lakes and oceans.

Roles of alternative prey for mesopredators on trophic cascades in intraguild predation systems: a theoretical perspective.

Declines of apex predators can cause dramatic increases of smaller predators and ensuing collapses of their prey. However, recent empirical evidence finds that the disappearance of apex predators does not reduce but can increase prey populations. This poses a great challenge in managing species interactions involving mesopredator release. Here we analyze a mathematical model to explain variable consequences of apex predator loss and to develop management guidelines for prey conservation. The model formulates an intraguild predation system (apex predators, mesopredators, and their shared prey) with mesopredators supplied with additional alternative prey. We show that apex predator loss causes only negative effects on shared prey without alternative prey but has either negative or positive effects with alternative prey. Moreover, when alternative prey is highly abundant, apex predator loss causes strong mesopredator release and reduces shared prey greatly. Finally, the model suggests that a viable management strategy to restore shared prey under much uncertainty about a target system is to allocate a limited control effort not only to both predators but also to alternative prey. Alternative prey for mesopredators may be a crucial ingredient that controls the cascading dynamics of intraguild predation systems and should be considered as an important management target.

Predation on pollinators promotes coevolutionary divergence in plant-pollinator mutualisms.

Coevolution of plants and pollinators has been suggested as a mechanism driving diversification of plant-pollinator mutualisms. There is increasing recognition that predators or competitors can influence the abundance and behavior of pollinators and indirectly affect the fitness of plants. However, existing theories on plant-pollinator diversification focus exclusively on mutualistic interactions between plants and pollinators. Here we used simulations to evaluate whether predation on pollinators promotes coevolutionary diversification of plant-pollinator mutualisms. We developed an individual-based simulation model in which the blooming season of plants and the active seasons of pollinators and predators can evolve. In simulations without predators, plant-pollinator coevolution caused diversification in blooming/active seasons for both plants and pollinators, but this diversification resulted in polymorphisms, not speciation. The introduction of predators promoted a split of plant and pollinator populations into reproductively isolated subpopulations with corresponding blooming and active seasons or a directional shift of blooming and active seasons, increasing the possibility of plant-pollinator cospeciation. This result suggests that predation on pollinators can promote sympatric and allopatric divergence of plant-pollinator mutualisms. Joint action of antagonistic and mutualistic interactions may be fundamentally important for diversification in coevolutionary interactions.

The effect of chronic seaweed subsidies on herbivory: plant-mediated fertilization pathway overshadows lizard-mediated predator pathways.

Flows of energy and materials link ecosystems worldwide and have important consequences for the structure of ecological communities. While these resource subsidies typically enter recipient food webs through multiple channels, most previous studies focussed on a single pathway of resource input. We used path analysis to evaluate multiple pathways connecting chronic marine resource inputs (in the form of seaweed deposits) and herbivory in a shoreline terrestrial ecosystem. We found statistical support for a fertilization effect (seaweed increased foliar nitrogen content, leading to greater herbivory) and a lizard numerical response effect (seaweed increased lizard densities, leading to reduced herbivory), but not for a lizard diet-shift effect (seaweed increased the proportion of marine-derived prey in lizard diets, but lizard diet was not strongly associated with herbivory). Greater seaweed abundance was associated with greater herbivory, and the fertilization effect was larger than the combined lizard effects. Thus, the bottom-up, plant-mediated effect of fertilization on herbivory overshadowed the top-down effects of lizard predators. These results, from unmanipulated shoreline plots with persistent differences in chronic seaweed deposition, differ from those of a previous experimental study of the short-term effects of a pulse of seaweed deposition: while the increase in herbivory in response to chronic seaweed deposition was due to the fertilization effect, the short-term increase in herbivory in response to a pulse of seaweed deposition was due to the lizard diet-shift effect. This contrast highlights the importance of the temporal pattern of resource inputs in determining the mechanism of community response to resource subsidies.

IsoWeb: a bayesian isotope mixing model for diet analysis of the whole food web.

Quantitative description of food webs provides fundamental information for the understanding of population, community, and ecosystem dynamics. Recently, stable isotope mixing models have been widely used to quantify dietary proportions of different food resources to a focal consumer. Here we propose a novel mixing model (IsoWeb) that estimates diet proportions of all consumers in a food web based on stable isotope information. IsoWeb requires a topological description of a food web, and stable isotope signatures of all consumers and resources in the web. A merit of IsoWeb is that it takes into account variation in trophic enrichment factors among different consumer-resource links. Sensitivity analysis using realistic hypothetical food webs suggests that IsoWeb is applicable to a wide variety of food webs differing in the number of species, connectance, sample size, and data variability. Sensitivity analysis based on real topological webs showed that IsoWeb can allow for a certain level of topological uncertainty in target food webs, including erroneously assuming false links, omission of existent links and species, and trophic aggregation into trophospecies. Moreover, using an illustrative application to a real food web, we demonstrated that IsoWeb can compare the plausibility of different candidate topologies for a focal web. These results suggest that IsoWeb provides a powerful tool to analyze food-web structure from stable isotope data. We provide R and BUGS codes to aid efficient applications of IsoWeb.

Marine subsidies have multiple effects on coastal food webs.

The effect of resource subsidies on recipient food webs has received much recent attention. The purpose of this study was to measure the effects of significant seasonal seaweed deposition events, caused by hurricanes and other storms, on species inhabiting subtropical islands. The seaweed represents a pulsed resource subsidy that is consumed by amphipods and flies, which are eaten by lizards and predatory arthropods, which in turn consume terrestrial herbivores. Additionally, seaweed decomposes directly into the soil under plants. We added seaweed to six shoreline plots and removed seaweed from six other plots for three months; all plots were repeatedly monitored for 12 months after the initial manipulation. Lizard density (Anolis sagrei) responded rapidly, and the overall average was 63% higher in subsidized than in removal plots. Stable-isotope analysis revealed a shift in lizard diet composition toward more marine-based prey in subsidized plots. Leaf damage was 70% higher in subsidized than in removal plots after eight months, but subsequent damage was about the same in the two treatments. Foliage growth rate was 70% higher in subsidized plots after 12 months. Results of a complementary study on the relationship between natural variation in marine subsidies and island food web components were consistent with the experimental results. We suggest two causal pathways for the effects of marine subsidies on terrestrial plants: (1) the "fertilization effect" in which seaweed adds nutrients to plants, increasing their growth rate, and (2) the "predator diet shift effect" in which lizards shift from eating local prey (including terrestrial herbivores) to eating mostly marine detritivores.

Timescale hierarchy determines the indirect effects of fluctuating subsidy inputs on in situ resources.

Empirical studies have shown that temporally fluctuating inputs of resource subsidies can indirectly increase or decrease the abundance of in situ resources by affecting generalist consumers that feed on both subsidies and in situ resources. By mathematical modeling, we develop a theoretical framework that can explain these variable consumer-mediated indirect effects. We show that the hierarchy of timescales among fluctuations in the subsidy input rate and consumers' reproductive and aggregative numerical responses predict the signs of the indirect effects. These predictions are consistent with field observations from a variety of natural systems. Our results suggest that the timescale hierarchy of ecological processes is fundamentally important for understanding and predicting indirect effects in nonequilibrium food web dynamics.

Speciation reversal and biodiversity dynamics with hybridization in changing environments.

A considerable fraction of the world's biodiversity is of recent evolutionary origin and has evolved as a by-product of, and is maintained by, divergent adaptation in heterogeneous environments. Conservationists have paid attention to genetic homogenization caused by human-induced translocations (e.g. biological invasions and stocking), and to the importance of environmental heterogeneity for the ecological coexistence of species. However, far less attention has been paid to the consequences of loss of environmental heterogeneity to the genetic coexistence of sympatric species. Our review of empirical observations and our theoretical considerations on the causes and consequences of interspecific hybridization suggest that a loss of environmental heterogeneity causes a loss of biodiversity through increased genetic admixture, effectively reversing speciation. Loss of heterogeneity relaxes divergent selection and removes ecological barriers to gene flow between divergently adapted species, promoting interspecific introgressive hybridization. Since heterogeneity of natural environments is rapidly deteriorating in most biomes, the evolutionary ecology of speciation reversal ought to be fully integrated into conservation biology.

ECOSYSTEM SIZE, BUT NOT DISTURBANCE, DETERMINES FOOD-CHAIN LENGTH ON ISLANDS OF THE BAHAMAS.

Ecologists have long struggled to explain variation in food-chain length among natural ecosystems. Food-chain length is predicted to be shorter in ecosystems subjected to greater disturbance because longer chains are theoretically less resilient to perturbation. Moreover, food-chain length is expected to be longer in larger ecosystems because increasing ecosystem size increases species richness and stabilizes predator-prey interactions, or increases total resource availability. Here we test the roles of disturbance and ecosystem size in determining the food-chain length of terrestrial food webs on Bahamian islands. We found that disturbance affected the identity of top predators, but did not change food-chain length because alternative top predators occupied similar trophic positions. On the other hand, a 106 -fold increase in ecosystem size elevated food-chain length by one trophic level. We suggest that the effect of disturbance on food-chain length is weak when alternate top predators are trophic omnivores and have similar trophic positions. This and previous work in lakes suggest that ecosystem size may be a strong determinant of food-chain length in both aquatic and terrestrial ecosystems.

Intraguild predation promotes complex alternative states along a productivity gradient.

Intraguild predation is the simplest, ubiquitous form of trophic omnivory, known to greatly influence the structure and functioning of natural and managed food webs. Although alternative states are fundamental to intraguild predation dynamics, only necessary conditions for alternative states have been previously reported. Using simple models, we found complex but systematic patterns in which different alternative states occur along a productivity gradient, and clarified the sufficient conditions to separate these patterns. We found that two quantities known to control the necessary conditions also determine the sufficient conditions: (1) relative energy transfer efficiency through alternative trophic pathways to an intraguild predator, and (2) relative resource exploitation ability between intraguild prey and predator. These governing quantities suggest how body size and stoichiometric relations between intraguild prey and predators can influence the possibility of alternative states. Our results indicate that food webs involving intraguild predation have a high potential of complex alternative states, and their management can be highly precarious.

Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses.

Within an organism, lipids are depleted in (13)C relative to proteins and carbohydrates (more negative delta(13)C), and variation in lipid content among organisms or among tissue types has the potential to introduce considerable bias into stable isotope analyses that use delta(13)C. Despite the potential for introduced error, there is no consensus on the need to account for lipids in stable isotope analyses. Here we address two questions: (1) If and when is it important to account for the effects of variation in lipid content on delta(13)C? (2) If it is important, which method(s) are reliable and robust for dealing with lipid variation? We evaluated the reliability of direct chemical extraction, which physically removes lipids from samples, and mathematical normalization, which uses the carbon-to-nitrogen (C:N) ratio of a sample to normalize delta(13)C after analysis by measuring the lipid content, the C:N ratio, and the effect of lipid content on delta(13)C (Deltadelta(13)C) of plants and animals with a wide range of lipid contents. For animals, we found strong relationships between C:N and lipid content, between lipid content and Deltadelta(13)C, and between C:N and Deltadelta(13)C. For plants, C:N was not a good predictor of lipid content or Deltadelta(13)C, but we found a strong relationship between carbon content and lipid content, lipid content and Deltadelta(13)C, and between and carbon content and Deltadelta(13)C. Our results indicate that lipid extraction or normalization is most important when lipid content is variable among consumers of interest or between consumers and end members, and when differences in delta(13)C between end members is <10-12 per thousand. The vast majority of studies using natural variation in delta(13)C fall within these criteria. Both direct lipid extraction and mathematical normalization reduce biases in delta(13)C, but mathematical normalization simplifies sample preparation and better preserves the integrity of samples for delta(15)N analysis.