Emergent trade-offs among plasticity strategies in mixotrophs.

Marine mixotrophs combine phagotrophy and phototrophy to acquire the resources they need for growth. Metabolic plasticity, the ability for individuals to dynamically alter their relative investment between different metabolic processes, allows mixotrophs to efficiently exploit variable environmental conditions. Different mixotrophs may vary in how quickly they respond to environmental stimuli, with slow-responding mixotrophs exhibiting a significant lag between a change in the environment and the resulting change metabolic strategy. In this study, we develop a model of mixotroph metabolic strategy and explore how the rate of the plastic response affects the seasonality, competitive fitness, and biogeochemical role of mixotroph populations. Fast-responding mixotrophs are characterized by more efficient resource use and higher average growth rates than slow-responding mixotrophs because any lag in the plastic response following a change in environmental conditions creates a mismatch between the mixotroph's metabolic requirements and their resource acquisition. However, this mismatch also results in increased storage of unused resources that support growth under future nutrient-limited conditions. As a result of this trade-off, mixotroph biomass and productivity are maximized at intermediate plastic response rates. Furthermore, the trade-off represents a mechanism for coexistence between fast-responding and slow-responding mixotrophs. In mixed communities, fast-responding mixotrophs are numerically dominant, but slow-responding mixotrophs persist at low abundance due to the provisioning effect that emerges as a result of their less efficient resource acquisition strategy. In addition to increased competitive ability, fast-responding mixotrophs are, on average, more autotrophic than slow-responding mixotrophs. Notably, these trade-offs associated with mixotroph response rate arise without including an explicit physiological cost associated with plasticity, a conclusion that may provide insight into evolutionary constraints of metabolic plasticity in mixotrophic organisms. When an explicit cost is added to the model, it alters the competitive relationships between fast- and slow-responding mixotrophs. Faster plastic response rates are favored by lower physiological costs as well as higher amplitude seasonal cycles.

Environment-dependent metabolic investments in the mixotrophic chrysophyte Ochromonas.

Mixotrophic protists combine photosynthesis and phagotrophy to obtain energy and nutrients. Because mixotrophs can act as either primary producers or consumers, they have a complex role in marine food webs and biogeochemical cycles. Many mixotrophs are also phenotypically plastic and can adjust their metabolic investments in response to resource availability. Thus, a single species's ecological role may vary with environmental conditions. Here, we quantified how light and food availability impacted the growth rates, energy acquisition rates, and metabolic investment strategies of eight strains of the mixotrophic chrysophyte, Ochromonas. All eight Ochromonas strains photoacclimated by decreasing chlorophyll content as light intensity increased. Some strains were obligate phototrophs that required light for growth, while other strains showed stronger metabolic responses to prey availability. When prey availability was high, all eight strains exhibited accelerated growth rates and decreased their investments in both photosynthesis and phagotrophy. Photosynthesis and phagotrophy generally produced additive benefits: In low-prey environments, Ochromonas growth rates increased to maximum, light-saturated rates with increasing light but increased further with the addition of abundant bacterial prey. The additive benefits observed between photosynthesis and phagotrophy in Ochromonas suggest that the two metabolic modes provide nonsubstitutable resources, which may explain why a tradeoff between phagotrophic and phototrophic investments emerged in some but not all strains.

Acquired Phototrophy as an Evolutionary Path to Mixotrophy.

AbstractAcquired photosynthesis transforms genotypically heterotrophic lineages into autotrophs. Transient acquisitions of eukaryotic chloroplasts may provide key evolutionary insight into the endosymbiosis process-the hypothesized mechanism by which eukaryotic cells obtained new functions via organelle retention. Here, we use an eco-evolutionary model to study the environmental conditions under which chloroplast retention is evolutionarily favorable. We focus on kleptoplastidic lineages-which steal functional chloroplasts from their prey-as hypothetical evolutionary intermediates. Our adaptive dynamics analysis reveals a spectrum of evolutionarily stable strategies ranging from phagotrophy to phototrophy to obligate kleptoplasty. Our model suggests that a low-light niche and weak (or absent) trade-offs between chloroplast retention and overall digestive ability favor the evolution of phototrophy. In contrast, when consumers experience strong trade-offs, obligate kleptoplasty emerges as an evolutionary end point. Therefore, the preevolved trade-offs that underlie an evolving lineage's physiology will likely constrain its evolutionary trajectory.

Predator switching strength controls stability in diamond-shaped food web models.

In food web models that include more than one prey type for a single predator, it is common for the predator's functional response to include some form of switching-preferential consumption of more abundant prey types. Predator switching promotes coexistence among competing prey types and increases diversity in the prey community. Here, we show how the dynamics of a diamond-shaped food web model of a marine plankton community are sensitive to a parameter that sets the strength of predator switching. Stronger switching destabilizes the model's coexistence equilibrium and leads to the appearance of limit cycles. Stronger switching also increases the evenness of the asymptotic prey community and promotes synchrony in the dynamics of disparate prey types. Given the dependence of model behavior on the strength of predator switching, it is important that modelers carefully consider the parameterization of functional responses that include switching.

Cascading effects of prey identity on gene expression in a kleptoplastidic ciliate.

Kleptoplastidic, or chloroplast stealing, lineages transiently retain functional photosynthetic machinery from algal prey. This machinery, and its photosynthetic outputs, must be integrated into the host's metabolism, but the details of this integration are poorly understood. Here, we study this metabolic integration in the ciliate Mesodinium chamaeleon, a coastal marine species capable of retaining chloroplasts from at least six distinct genera of cryptophyte algae. To assess the effects of feeding history on ciliate physiology and gene expression, we acclimated M. chamaeleon to four different types of prey and contrasted well-fed and starved treatments. Consistent with previous physiological work on the ciliate, we found that starved ciliates had lower chlorophyll content, photosynthetic rates, and growth rates than their well-fed counterparts. However, ciliate gene expression mirrored prey phylogenetic relationships rather than physiological status, suggesting that, even as M. chamaeleon cells were starved of prey, their overarching regulatory systems remained tuned to the prey type to which they had been acclimated. Collectively, our results indicate a surprising degree of prey-specific host transcriptional adjustments, implying varied integration of prey metabolic potential into many aspects of ciliate physiology.

Evidence for evolutionary adaptation of mixotrophic nanoflagellates to warmer temperatures.

Mixotrophs, organisms that combine photosynthesis and heterotrophy to gain energy, play an important role in global biogeochemical cycles. Metabolic theory predicts that mixotrophs will become more heterotrophic with rising temperatures, potentially creating a positive feedback loop that accelerates carbon dioxide accumulation in the atmosphere. Studies testing this theory have focused on phenotypically plastic (short-term, non-evolutionary) thermal responses of mixotrophs. However, as small organisms with short generation times and large population sizes, mixotrophs may rapidly evolve in response to climate change. Here, we present data from a 3-year experiment quantifying the evolutionary response of two mixotrophic nanoflagellates to temperature. We found evidence for adaptive evolution (increased growth rates in evolved relative to acclimated lineages) in the obligately phototrophic strain, but not in the facultative phototroph. All lineages showed trends of increased carbon use efficiency, flattening of thermal reaction norms, and a return to homeostatic gene expression. Generally, mixotrophs evolved reduced photosynthesis and higher grazing with increased temperatures, suggesting that evolution may act to exacerbate mixotrophs' effects on global carbon cycling.

Fertilization by coral-dwelling fish promotes coral growth but can exacerbate bleaching response.

Many corals form close associations with a diverse assortment of coral-dwelling fishes and other fauna. As coral reefs around the world are increasingly threatened by mass bleaching events, it is important to understand how these biotic interactions influence corals' susceptibility to bleaching. We used dynamic energy budget modeling to explore how nitrogen excreted by coral-dwelling fish affects the physiological performance of host corals. In our model, fish presence influenced the functioning of the coral-Symbiodiniaceae symbiosis by altering nitrogen availability, and the magnitude and sign of these effects depended on environmental conditions. Although our model predicted that fish-derived nitrogen can promote coral growth, the relationship between fish presence and coral tolerance of photo-oxidative stress was non-linear. Fish excretions supported denser symbiont populations that provided protection from incident light through self-shading. However, these symbionts also used more of their photosynthetic products for their own growth, rather than sharing with the coral host, putting the coral holobiont at a higher risk of becoming carbon-limited and bleaching. The balance between the benefits of increased symbiont shading and costs of reduced carbon sharing depended on environmental conditions. Thus, while there were some scenarios under which fish presence increased corals' tolerance of light stress, fish could also exacerbate bleaching and slow or prevent subsequent recovery. We discuss how the contrast between the potentially harmful effects of fish predicted by our model and results of empirical studies may relate to key model assumptions that warrant further investigation. Overall, this study provides a foundation for future work on how coral-associated fauna influence the bioenergetics of their host corals, which in turn has implications for how these corals respond to bleaching-inducing stressors.

Prey type constrains growth and photosynthetic capacity of the kleptoplastidic ciliate Mesodinium chamaeleon (Ciliophora).

Kleptoplastidic, or chloroplast-stealing, lineages offer insight into the process of acquiring photosynthesis. By quantifying the ability of these organisms to retain and use photosynthetic machinery from their prey, we can understand how intermediaries on the endosymbiosis pathway might have evolved regulatory and maintenance mechanisms. Here, we focus on a mixotrophic kleptoplastidic ciliate, Mesodinium chamaeleon, noteworthy for its ability to retain functional chloroplasts from at least half a dozen cryptophyte algal genera. We contrasted the performance of kleptoplastids from blue-green and red cryptophyte prey as a function of light level and feeding history. Our experiments showed that starved M. chamaeleon cells are able to maintain photosynthetic function for at least 2 weeks and that M. chamaeleon containing red plastids lost chlorophyll and electron transport capacity faster than those containing blue-green plastids. However, likely due to increased pigment content and photosynthetic rates in red plastids, M. chamaeleon had higher growth rates and more prolonged growth when feeding on red cryptophytes. For example, M. chamaeleon grew rapidly and extensively when fed the blue-green cryptophyte Chroomonas mesostigmatica, but this growth appeared to hinge on high levels of feeding supporting photosynthetic activity. In contrast, even starved M. chamaeleon containing red plastids from Rhodomonas salina could achieve high photosynthetic rates and extensive growth. Our findings show that plastid origin impacts the maintenance and magnitude of photosynthetic activity, though whether this is due to variation in ciliate control or gradual loss of plastid function in ingested prey cells remains unknown.

High-seas fish wars generate marine reserves.

The effective management of marine fisheries is an ongoing challenge at the intersection of biology, economics, and policy. One way in which fish stocks-and their habitats-can be protected is through the establishment of marine reserves, areas that are closed to fishing. Although the potential economic benefits of such reserves have been shown for single-owner fisheries, their implementation quickly becomes complicated when more than one noncooperating harvester is involved in fishery management, which is the case on the high seas. How do multiple self-interested actors distribute their fishing effort to maximize their individual economic gains in the presence of others? Here, we use a game theoretic model to compare the effort distributions of multiple noncooperating harvesters with the effort distributions in the benchmark sole owner and open access cases. In addition to comparing aggregate rent, stock size, and fishing effort, we focus on the occurrence, size, and location of marine reserves. We show that marine reserves are a component of many noncooperative Cournot-Nash equilibria. Furthermore, as the number of harvesters increases, (i) both total unfished area and the size of binding reserves (those that actually constrain behavior) may increase, although the latter eventually asymptotically decreases; (ii) total rents and stock size both decline; and (iii) aggregate effort used (i.e., employment) can either increase or decrease, perhaps nonmonotonically.

Social tipping points in animal societies.

Animal social groups are complex systems that are likely to exhibit tipping points-which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions-yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization-populations, communities, ecosystems-may help to reveal principles that transcend traditional disciplinary boundaries.

Preferential Plastid Retention by the Acquired Phototroph Mesodinium chamaeleon.

The ciliate genus Mesodinium contains species that rely to varying degrees on photosynthetic machinery stolen from cryptophyte algal prey. Prey specificity appears to scales inversely with this reliance: The predominantly phototrophic M. major/rubrum species complex exhibits high prey specificity, while the heterotrophic lineages M. pulex and pupula are generalists. Here, we test the hypothesis that the recently described mixotroph M. chamaeleon, which is phylogenetically intermediate between M. major/rubrum and M. pulex/pupula, exhibits intermediate prey preferences. Using a series of feeding and starvation experiments, we demonstrate that M. chamaeleon grazes and retains plastids at rates which often exceed those observed in M. rubrum, and retains plastids from at least five genera of cryptophyte algae. Despite this relative generality, M. chamaeleon exhibits distinct prey preferences, with higher plastid retention, mixotrophic growth rates and efficiencies, and starvation tolerance when offered Storeatula major, a cryptophyte that M. rubrum does not appear to ingest. These results suggest that niche partitioning between the two acquired phototrophs may be mediated by prey identity. M. chamaeleon appears to represent an intermediate step in the transition to strict reliance on acquired phototrophy, indicating that prey specificity may evolve alongside degree of phototrophy.

Acquired phototrophy stabilises coexistence and shapes intrinsic dynamics of an intraguild predator and its prey.

In marine ecosystems, acquired phototrophs - organisms that obtain their photosynthetic ability by hosting endosymbionts or stealing plastids from their prey - are omnipresent. Such taxa function as intraguild predators yet depend on their prey to periodically obtain chloroplasts. We present a new theory for the effects of acquired phototrophy on community dynamics by analysing a mathematical model of this predator-prey interaction and experimentally verifying its predictions with a laboratory model system. We show that acquired phototrophy stabilises coexistence, but that the nature of this coexistence exhibits a 'paradox of enrichment': as light increases, the coexistence between the acquired phototroph and its prey transitions from a stable equilibrium to boom-bust cycles whose amplitude increases with light availability. In contrast, heterotrophs and mixotrophic acquired phototrophs (that obtain < 30% of their carbon from photosynthesis) do not exhibit such cycles. This prediction matches field observations, in which only strict ( > 95% of carbon from photosynthesis) acquired phototrophs form blooms.

Multiple Friends with Benefits: An Optimal Mutualist Management Strategy?

Most mutualisms in nature involve interactions between multispecies mutualist guilds and multiple partner species. While mechanisms such as niche partitioning can explain part of this diversity, the presence of low-quality partners, which produce relatively low returns on investment compared with other guild members, is not well understood. Here, we consider a novel explanation for this persistence: that low-quality partners are actively maintained by their hosts as part of a growth-maximizing strategy, even in the presence of higher-quality alternatives. We use a model inspired by the interaction between host trees and ectomycorrhizal fungi to demonstrate that when the environment is variable, trees maintain low-quality fungal partners that they would not otherwise maintain in constant environments. This active investment, which emerges as a response to saturating returns on investment in higher-quality partners, could contribute to the maintenance of diversity in multispecies mutualisms.

Nonhierarchical Dispersal Promotes Stability and Resilience in a Tritrophic Metacommunity.

Community interactions (e.g., predation, competition) can be characterized by two factors: their strengths and how they are structured between and within species. Both factors play a role in determining community dynamics. In addition to trophic interactions, dispersal acts as an interaction between separate populations. As with other interactions, the structure of dispersal can affect the stability of a system. However, the primary structure that has been studied in consumer-resource models has been hierarchical dispersal, where between-patch dispersal rates increase with trophic level. Here we use analytical, numerical, and simulation approaches on a two-patch, three-species metacommunity model to investigate the relationship between structure and community stability and resilience. We show that metacommunity stability is greater in systems with both weak and strong dispersal rates. Our system is stabilized by the formation of patterns when predators disperse frequently and herbivores disperse rarely, and via asynchrony when both predators and herbivores disperse infrequently. Our results show how interaction strengths within both trophic and spatial networks shape metacommunity stability.

Mycorrhizal co-invasion and novel interactions depend on neighborhood context.

Biological invasions are a rapidly increasing driver of global change, yet fundamental gaps remain in our understanding of the factors determining the success or extent of invasions. For example, although most woody plant species depend on belowground mutualists such as mycorrhizal fungi and nitrogen-fixing bacteria, the relative importance of these mutualisms in conferring invasion success is unresolved. Here, we describe how neighborhood context (identity of nearby tree species) affects the formation of belowground ectomycorrhizal partnerships between fungi and seedlings of a widespread invasive tree species, Pseudotsuga menziesii (Douglas-fir), in New Zealand. We found that the formation of mycorrhizal partnerships, the composition of the fungal species involved in these partnerships, and the origin of the fungi (co-invading or native to New Zealand) all depend on neighborhood context. Our data suggest that nearby ectomycorrhizal host trees act as both a reservoir of fungal inoculum and a carbon source for late-successional and native fungi. By facilitating mycorrhization of P. menziesii seedlings, adult trees may alleviate mycorrhizal limitation at the P. menziesii invasion front. These results highlight the importance of studying biological invasions across multiple ecological settings to understand establishment success and invasion speed.

Habitat damage, marine reserves, and the value of spatial management.

The biological benefits of marine reserves have garnered favor in the conservation community, but "no-take" reserve implementation is complicated by the economic interests of fishery stakeholders. There are now a number of studies examining the conditions under which marine reserves can provide both economic and ecological benefits. A potentially important reality of fishing that these studies overlook is that fishing can damage the habitat of the target stock. Here, we construct an equilibrium bioeconomic model that incorporates this habitat damage and show that the designation of marine reserves, coupled with the implementation of a tax on fishing effort, becomes both biologically and economically favorable as habitat sensitivity increases. We also study the effects of varied degrees of spatial control on fisheries management. Together, our results provide further evidence for the potential monetary and biological value of spatial management, and the possibility of a mutually beneficial resolution to the fisherman-conservationist marine reserve designation dilemma.

Nonrandom extinction patterns can modulate pest control service decline.

Changes in biodiversity will mediate the consequences of agricultural intensification and expansion for ecosystem services. Regulating services, like pollination and pest control, generally decline with species loss. In nature, however, relationships between service provision and species richness are not always strong, partially because anthropogenic disturbances purge species from communities in nonrandom orders. The same traits that make for effective service providers may also confer resistance or sensitivity to anthropogenic disturbances, which may either temper or accelerate declines in service provision with species loss. We modeled a community of predators interacting with insect pest prey, and identified the contexts in which pest control provision was most sensitive to species loss. We found pest populations increased rapidly when functionally unique and dietary-generalist predators were lost first, with up to 20% lower pest control provision than random loss. In general, pest abundance increased most in the scenarios that freed more pest species from predation. Species loss also decreased the likelihood that the most effective service providers were present. In communities composed of species with identical traits, predators were equally effective service providers and, when competing predators went extinct, remaining community members assumed their functional roles. In more realistic trait-diverse communities, predators differed in pest control efficacy, and remaining predators could not fully compensate for the loss of their competitors, causing steeper declines in pest control provision with predator species loss. These results highlight diet breadth in particular as a key predictor of service provision, as it affects both the way species respond to and alter their environments. More generally, our model provides testable hypotheses for predicting how nonrandom species loss alters relationships between biodiversity and pest control provision.

Mesodinium.

In this Quick guide, Holly Moeller and Matthew Johnson introduce Mesodinium, a genus of algae with a propensity for 'stealing' photosynthetic machinery from its prey.

Fungal Fight Club: phylogeny and growth rate predict competitive outcomes among ectomycorrhizal fungi.

Ectomycorrhizal fungi are among the most prevalent fungal partners of plants and can constitute up to one-third of forest microbial biomass. As mutualistic partners that supply nutrients, water, and pathogen defense, these fungi impact host plant health and biogeochemical cycling. Ectomycorrhizal fungi are also extremely diverse, and the community of fungal partners on a single plant host can consist of dozens of individuals. However, the factors that govern competition and coexistence within these communities are still poorly understood. In this study, we used in vitro competitive assays between five ectomycorrhizal fungal strains to examine how competition and pH affect fungal growth. We also tested the ability of evolutionary history to predict the outcomes of fungal competition. We found that the effects of pH and competition on fungal performance varied extensively, with changes in growth media pH sometimes reversing competitive outcomes. Furthermore, when comparing the use of phylogenetic distance and growth rate in predicting competitive outcomes, we found that both methods worked equally well. Our study further highlights the complexity of ectomycorrhizal fungal competition and the importance of considering phylogenetic distance, ecologically relevant traits, and environmental conditions in predicting the outcomes of these interactions.