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bioRxiv2018

Live imaging of Aiptasia larvae, a model system for studying coral bleaching, using a simple microfluidic device

Coral reefs, and their associated diverse ecosystems, are of enormous ecological importance. In recent years, coral health has been severely impacted by environmental stressors brought on by human activity and climate change, threatening the extinction of several major reef ecosystems. Reef damage is mediated by a process called coral bleaching where corals, sea anemones, and other cnidarians lose their photosynthetic algal symbionts (genus Symbiodinium) upon stress induction, resulting in drastically decreased host energy harvest and, ultimately, coral death. The mechanism by which this critical cnidarian-algal symbiosis is lost remains poorly understood. Here, we report Traptasia, a simple microfluidic device with multiple traps designed to isolate and image individual live larvae of Aiptasia, a sea anemone model organism, and their algal symbionts over extended time courses. Aiptasia larvae are ~100 m in length, deformable, and highly motile, posing particular challenges for long-term imaging. Using a trap design optimized via fluid flow simulations and polymer bead loading tests, we trapped Aiptasia larvae containing algal symbionts and demonstrated stable imaging for >10 hours. We visualized algal migration within Aiptasia larvae and observed algal expulsion under an environmental stressor. To our knowledge, this device is the first to enable live imaging of cnidarian larvae and their algal symbionts and, in further implementation, could provide important insights into the cellular mechanisms of coral bleaching under different environmental stressors. The device is simple to use, requires minimal external equipment and no specialized training to operate, and can easily be adapted to study a variety of large, motile organisms.

ecology↗

bioRxiv2018

Variable costs of eavesdropping a green leaf volatile on two plant species in a common garden experiment

Herbivore-induced plant volatile (HIPV)-mediated eavesdropping by plants is a well-documented, inducible phenomenon that has practical agronomic applications for enhancing plant defense and pest management. However, as with any inducible phenomenon, responding to volatile cues may incur physiological and ecological costs that limit plant productivity. In a common garden experiment, we tested the hypothesis that exposure to a single HIPV would decrease herbivore damage at the cost of reduced plant growth and reproduction. Lima bean (Phaseolus lunatus) and pepper (Capsicum annuum) plants were exposed to a persistent, low-dose ([~]10ng/hour) of the green leaf volatile cis-3-hexenyl acetate (z3HAC), which is an HIPV and damage-associated volatile. z3HAC-treated pepper plants were shorter, had less aboveground and belowground biomass, and produced fewer flowers and fruits relative to controls while z3HAC-treated lima bean plants were taller and produced more leaves and flowers than did controls. Natural herbivory was reduced in z3HAC-exposed lima bean plants, but not in pepper. Cyanogenic potential, a putative direct defense mechanism in lima bean, was lower in young z3HAC-exposed leaves, suggesting a growth-defense tradeoff from z3HAC exposure alone. Plant species-specific responses to an identical volatile cue have important implications for agronomic costs and benefits of volatile-mediated inter-plant communication under field conditions.

ecology↗

bioRxiv2018

Chronic infections can shape epidemic exposure: Pathogen co-occurrence networks in the Serengeti lions

Pathogens are embedded in a complex network of microparasites that can collectively or individually alter disease dynamics and outcomes. Chronic pathogens, for example, can either facilitate or compete with subsequent pathogens thereby exacerbating morbidity and mortality. Pathogen interactions are ubiquitous in nature, but poorly understood, particularly in wild populations. We report here on ten years of serological and molecular data in African lions, leveraging comprehensive demographic and behavioral data to utilize pathogen networks to test if chronic infections shape infection by acute pathogens. We combine network and community ecology approaches to assess broad network structure and characterize associations between pathogens across spatial and temporal scales. We found significant non-random structure in the lion-pathogen co-occurrence network and identified potential facilitative and competitive interactions between acute and chronic pathogens. Our results provide a novel insight for untangling the complex associations underlying pathogen co-occurrence networks.

ecology↗

bioRxiv2018

The equivocal \"mean age of parents in a cohort\"

The mean age at childbirth is an important notion in demography, ecology and evolution, where it is used as a measure of generation time. A standard way to quantify it is to compute the mean age of the parents of all offspring produced by a cohort, and the resulting measure is thought to represent the mean age at which a typical parent produces offspring. In this note, I explain why this interpretation is problematic. I also introduce a new measure of the mean age at reproduction and show that it can be very different from the mean age of parents of offspring of a cohort. In particular, the mean age of parents of offspring of a cohort systematically overestimates the mean age at reproduction, and can even be greater than the expected lifespan of parents.

ecology↗

bioRxiv2018

Sex makes them sleepy: change in host reproductive status induces diapause in parasitoids

When organisms coevolve, any change in one species can induce phenotypic changes in traits and ecology of the other species. The role such interactions play in ecosystems is central, but their mechanistic bases remain underexplored. Upper trophic level species have to synchronize their life-cycle to both abiotic conditions and to lower trophic level species phenology and phenotypic variations. We tested the effect of host seasonal strategy on parasitoid diapause induction by using a holocyclic clone of the pea aphid Acyrthosiphon pisum producing asexual and sexual morphs that are viviparous females (i.e. laying embryos) and oviparous females (laying eggs), respectively, the latter being only present at the end of the growing season. Aphidius ervi parasitoids from populations of contrasted climatic origin (harsh vs. mild winter areas) were allowed to parasitize each morph in a split-brood design and developing parasitoids were next reared under either fall-like or summer-like temperature-photoperiod conditions. We next examined aspects of the host physiological state by comparing the relative proportion of forty-seven metabolites and lipid reserves in both morphs produced under the same conditions. We found that oviparous morphs are cues per se for diapause induction; parasitoids entered diapause at higher levels when developing in oviparous hosts (19.4 {+/-} 3.0%) than in viviparous ones (3.6 {+/-} 1.3%), under summer-like conditions (i.e., when oviparous aphids appear in the fields). This pattern was only observed in parasitoids from the harsh winter area since low diapause levels were observed in the other population, suggesting local adaptations to overwintering cues. Metabolomics analyses show parasitoids response to be mainly influenced by the hosts physiology, with higher proportion of polyols and sugars, and more fat reserves being found in oviparous morphs. Host quality thus varies across the seasons and represents one of the multiple environmental parameters affecting parasitoid diapause. Our results underline strong coevolutionary processes between hosts and parasitoids in their area of origin, likely leading to phenological synchronization, and we point out the importance of such bottom-up effects for trait expression, and for the provision of ecosystem services such as biological control in the context of climate change.

ecology↗

bioRxiv2018

Dispersers are more likely to follow mucus trails in the land snail Cornu aspersum

Dispersal, i.e. movement leading to gene flow, is a fundamental although costly life history trait. The use of indirect social information may help mitigate these costs, yet in many cases little is known about the proximate sources of such information, and how dispersers and residents may differ in their information use. Land gastropods, which have a high cost of movement and obligatorily leave information potentially exploitable by conspecifics during movement (through mucus trails), are a good model to investigate links between dispersal costs and information use. We used Y-mazes to see whether dispersers and residents differed in their trail-following propensity, in the snail Cornu aspersum. Dispersers followed mucus trails more frequently than expected by chance, contrary to non-dispersers. Ignoring dispersal status during tests would lead to falsely conclude to no trail-following for the majority of ecologically realistic scenarios. Trail following by dispersers may reduce dispersal costs by reducing energy expenditure and helping snails find existing patches. Finally, we point that ignoring the potential for collective dispersal provided by trail-following abilities may lead to wrong inferences on the demographic and genetic consequences of dispersal.

ecology↗

bioRxiv2018

Temporal and spatial variation in distribution of fish environmental DNA in England’s largest lake

Environmental DNA offers great potential as a biodiversity monitoring tool. Previous work has demonstrated that eDNA metabarcoding provides reliable information for lake fish monitoring, but important questions remain about temporal and spatial repeatability, which is critical for understanding the ecology of eDNA and developing effective sampling strategies. Here, we carried out comprehensive spatial sampling of Englands largest lake, Windermere, during summer and winter to 1) examine repeatability of the method, 2) compare eDNA results with contemporary gill-net survey data, 3) test the hypothesis of greater spatial structure of eDNA in summer compared to winter due to differences in water mixing between seasons, and 4) compare the effectiveness of shore and offshore sampling for species detection. We find broad consistency between results from three sampling events in terms of species detection and abundance, with eDNA detecting more species than established methods and being significantly correlated to rank abundance determined by long-term data. As predicted, spatial structure was much greater in the summer, reflecting less mixing of eDNA than in the winter. For example Arctic charr, a deep-water species, was only detected in deep, mid-lake samples in the summer, while littoral or benthic species such as minnow and stickleback were more frequently detected in shore samples. By contrast in winter, the eDNA of these species was more uniformly distributed. This has important implications for design of sampling campaigns, for example, deep-water species could be missed and littoral/benthic species overrepresented by focusing exclusively on shoreline samples collected in the summer.

ecology↗

bioRxiv2018

Adaptive metabolic strategies explain diauxic shifts and promote species coexistence

Bacteria are able to adapt to different environments by changing their \"metabolic strategies\", i.e. the ways in which they uptake available resources from the environment. For example, in a celebrated experiment Jacques Monod showed that bacteria cultured in media containing two different sugars consume them sequentially, resulting in bi-phasic growth curves called \"diauxic shifts\". From the theoretical point of view, microbial communities are commonly described using MacArthurs consumer-resource model, which describes the population dynamics of species competing for a given set of resources. In this model, however, metabolic strategies are treated as constant parameters. Here, we introduce adaptive metabolic strategies in the framework of consumer-resource models, allowing the strategies to evolve to maximize each species relative fitness. By doing so, we are able to describe quantitatively, and without invoking any specific molecular mechanisms for the metabolism of the microbial species, growth curves of the bakers yeast Saccharomyces cerevisiae measured in a controlled experimental set-up, with galactose as the primary carbon source. We also show that metabolic adaptation enables the community to self-organize, allowing species to coexist even in the presence of few resources, and to respond optimally to a time-dependent environment. A connection between the Competitive Exclusion Principle and the metabolic theory of ecology is also discussed.

ecology↗

bioRxiv2018

Competition among Aedes aegypti larvae

Adult Aedes aegypti mosquitoes are important vectors of human disease. The size of the adult female affects her success, fitness, and ability to transmit diseases. The size of the adults is determined during the aquatic larval stage. Competition among larvae for food influences the size of the pupa and thus the adult. In these experiments, the food level (mg/larva) and the density (larvae/vial) both affect intraspecific competition, which shows up as the interaction of the two factors. Furthermore, the total food per vial affects the nature of competition among the larvae, also apparent in the interaction of food and density. Male larvae are affected by the percent of males in the vial, but females are not. Seven biologically significant dependent variables were examined, and the data analyzed by multivariate analysis of variance to gain insight into the relationships among the variables and the effects of these factors on the larvae as they grew in small containers. Male and female larvae compete differently from one another for the particulate yeast cells in this experiment; female larvae outcompete males through larger size and by retaining cells within their gut at low total food levels. Under conditions of more intense competition, the pupal masses of both males and females are smaller, so the effect of competition is a reduced apparent food level. The age at pupation is also affected by food and density. Across the twenty treatment combinations of food/larva and larvae/vial, female larvae grew as though there were six different ecological environments while male larvae grew as though there were only four different environments. No interference competition was observed. Eradication efforts aimed at adult populations of this mosquito may inadvertently increase the size and robustness of the next generation of larvae, resulting in a subsequent adult population increase in the second generation.

ecology↗

bioRxiv2018

Geographically Opposing Responses of Sea Urchin Recruitment to Changes in Ocean Climate

Sea urchins are voracious herbivores that influence the ecological structure and function of nearshore ecosystems throughout the world. Like many species that produce planktonic larvae, their recruitment is thought to be particularly sensitive to climatic fluctuations in temperature that directly or indirectly affect adult reproduction and larval transport and survival. Yet how climate alters sea urchin populations in space and time by modifying larval recruitment and year-class strength on the time-scales that regulate populations remains understudied. Using a, spatially replicated weekly-biweekly dataset spanning 27 years and 1100 km of coastline, we characterized seasonal, interannual, and spatial patterns of larval settlement of the purple sea urchin (Strongylocentrotus purpuratus). We show that large spatial differences in temporal patterns of larval settlement were associated with different responses to fluctuations in ocean temperature and climate. Importantly, we found a strong correlation between larval settlement and regional year class strength suggesting that such temporal and spatial variation in settlement plays an important role in controlling population dynamics. These results provide strong evidence over extensive temporal and spatial domains that climatic fluctuations shape broad-scale patterns of larval settlement and subsequent population structure of an important marine herbivore known to control the productivity, community state and provisioning services of marine ecosystems.

ecology↗

bioRxiv2018

Estimating parameters from multiple time series of population dynamics using Bayesian inference

O_LIEmpirical time series of interacting entities, e.g. species abundances, are highly useful to study ecological mechanisms. Mathematical models are valuable tools to further elucidate those mechanisms and underlying processes. However, obtaining an agreement between model predictions and experimental observations remains a demanding task. As models always abstract from reality one parameter often summarizes several properties. Parameter measurements are performed in additional experiments independent of the ones delivering the time series. Transferring these parameter values to different settings may result in incorrect parametrizations. On top of that, the properties of organisms and thus the respective parameter values may vary considerably. These issues limit the use of a priori model parametrizations.\nC_LIO_LIIn this study, we present a method suited for a direct estimation of model parameters and their variability from experimental time series data. We combine numerical simulations of a continuous-time dynamical population model with Bayesian inference, using a hierarchical framework that allows for variability of individual parameters. The method is applied to a comprehensive set of time series from a laboratory predator-prey system that features both steady states and cyclic population dynamics.\nC_LIO_LIOur model predictions are able to reproduce both steady states and cyclic dynamics of the data. Additionally to the direct estimates of the parameter values, the Bayesian approach also provides their uncertainties. We found that fitting cyclic population dynamics, which contain more information on the process rates than steady states, yields more precise parameter estimates. We detected significant variability among parameters of different time series and identified the variation in the maximum growth rate of the prey as a source for the transition from steady states to cyclic dynamics.\nC_LIO_LIBy lending more flexibility to the model, our approach facilitates parametrizations and shows more easily which patterns in time series can be explained also by simple models. Applying Bayesian inference and dynamical population models in conjunction may help to quantify the profound variability in organismal properties in nature.\nC_LI

ecology↗

bioRxiv2018

Global cooling & the rise of modern grasslands: Revealing cause & effect of environmental change on insect diversification dynamics

Utilising geo-historical environmental data to disentangle cause and effect in complex natural systems is a major goal in our quest to better understand how climate change has shaped life on Earth. Global temperature is known to drive biotic change over macro-evolutionary time-scales but the mechanisms by which it acts are often unclear. Here, we model speciation rates for Orthoptera within a phylogenetic framework and use this to demonstrate that global cooling is strongly correlated with increased speciation rates. Transfer Entropy analyses reveal the presence of one or more additional processes that are required to explain the information transfer from global temperature to Orthoptera speciation. We identify the rise of C4 grasslands as one such mechanism operating from the Miocene onwards. We therefore demonstrate the value of the geological record in increasing our understanding of climate change on macro-evolutionary and macro-ecological processes.

ecology↗

bioRxiv2018

Quorums enable optimal pooling of independent judgements

Majority-voting and the Condorcet Jury Theorem pervade thinking about collective decision-making. Thus, it is typically assumed that majority-voting is the best possible decision mechanism, and that scenarios exist where individually-weak decision-makers should not pool information. Condorcet and its applications implicitly assume that only one kind of error can be made, yet signal detection theory shows two kinds of errors exist, false positives and false negatives. We apply signal detection theory to collective decision-making to show that majority voting is frequently sub-optimal, and can be optimally replaced by quorum decision-making. While quorums have been proposed to resolve within-group conflicts, or manage speed-accuracy trade-offs, our analysis applies to groups with aligned interests undertaking single-shot decisions. Our results help explain the ubiquity of quorum decision-making in nature, relate the use of sub- and super-majority quorums to decision ecology, and may inform the design of artificial decision-making systems.\n\nImpact StatementTheory typically assumes that majority voting is optimal; this is incorrect - majority voting is typically sub-optimal, and should be replaced by sub-majority or super-majority quorum voting. This helps explain the prevalence of quorum-sensing in even the simplest collective systems, such as bacterial communities.

ecology↗

bioRxiv2018

Development of an eDNA method for monitoring fish communities: ground truthing in diverse lakes with characterised fish faunas

O_LIAccurate, cost-effective monitoring of fish is required to assess the quality of lakes under the European Water Framework Directive (WFD). Recent studies have shown that environmental DNA (eDNA) metabarcoding is an effective and non-invasive method, which can provide semi-quantitative information on fish communities in large lakes.\nC_LIO_LIThis study further investigated the potential of eDNA metabarcoding as a tool for WFD status assessment by collecting and analysing water samples from eight Welsh lakes and six meres in Cheshire, England, with well described fish faunas. Water samples (N = 252) were assayed using two mitochondrial DNA regions (Cytb and 12S rRNA).\nC_LIO_LIeDNA sampling indicated the presence of very similar species in the lakes compared to those expected on the basis of existing and historical information. In total, 24 species were detected with a total of 111 species occurrences in the lakes studied using eDNA. Secondly, there was a significant positive correlation between expected faunas and eDNA data in terms of confidence of species occurrence (Spearmans r = 0.74, df = 109, p <; 0.001). Thirdly, eDNA data can estimate relative abundance with the standard five-level classification scale (\"DAFOR\"). Lastly, four ecological fish communities were characterised using eDNA data which agrees with the pre-defined lake types according to environmental characteristics.\nC_LIO_LISynthesis and applications. This study provides further evidence that eDNA metabarcoding could be a powerful and non-invasive monitoring tool for WFD purpose in a wide range of lake types, considerably outperforming other methods for community level analysis.\nC_LI

ecology↗

bioRxiv2018

Empirical analysis and modelling of Argos Doppler location errors in Romania

BackgroundAdvances in wildlife tracking technology have allowed researchers to understand the spatial ecology of many terrestrial and aquatic animal species. Argos Doppler is a technology that is widely used for wildlife tracking owing to the small size and low weight of the Argos transmitters. This allows them to be fitted to small-bodied species. The longer lifespan of the Argos units in comparison to units outfitted with miniaturized global positioning system (GPS) technology has also recommended their use. In practice, large Argos location errors often occur due to communication conditions such as transmitter settings, local environment, and the behavior of the tracked individual.\n\nMethodsConsidering the geographic specificity of errors and the lack of benchmark studies in Eastern Europe, the research objectives were: (1) to evaluate the accuracy of Argos Doppler technology under various environmental conditions in Romania, (2) to investigate the effectiveness of straightforward destructive filters for improving Argos Doppler data quality, and (3) to provide guidelines for processing Argos Doppler wildlife monitoring data. The errors associated with Argos locations in four geographic locations in Romania were assessed during static, low-speed and high-speed tests. The effectiveness of the Douglas Argos distance angle filter algorithm was then evaluated to ascertain its effect on the minimization of localization errors.\n\nResultsArgos locations received in the tests had larger associated horizontal errors than those indicated by the operator of the Argos system, including under ideal reception conditions. Positional errors were similar to those obtained in other studies outside of Europe. The errors were anisotropic, with larger longitudinal errors for the vast majority of the data. Errors were mostly related to speed of the Argos transmitter at the time of reception, but other factors such as topographical conditions and orientation of antenna at the time of the transmission also contributed to receiving low-quality data. The Douglas-Argos filter successfully excluded the largest errors while retaining a large amount of data when the threshold was set to the local scale (2 km).\n\nDiscussionFilter selection requires knowledge about the movement patterns and behavior of the species of interest, and the parametrization of the selected filter typically requires a trial and error approach. Selecting the proper filter reduces the errors while retaining a large amount of data. However, the post-processed data typically includes large positional errors; thus, we recommend incorporating Argos error metrics such as error ellipse or use complex modeling approaches when working with filtered data.

ecology↗

bioRxiv2018

Pollinator size and its consequences: Predictive allometry for pollinating insects

O_LIBody size is an integral functional trait that underlies pollination-related ecological processes, yet it is often impractical to measure directly. Allometric scaling laws have been used to overcome this problem. However, most existing models rely upon small sample sizes, geographically restricted sampling and have limited applicability for non-bee taxa. Predictive allometric models that consider biogeography, phylogenetic relatedness and intraspecific variation are urgently required to ensure greater accuracy.\nC_LIO_LIHere, we measured body size, as dry weight, and intertegular distance (ITD) of 391 bee species (4035 specimens) and 103 hoverfly species (399 specimens) across four biogeographic regions: Australia, Europe, North America and South America. We updated existing models within a Bayesian mixed-model framework to test the power of ITD to predict interspecific variation in pollinator dry weight in interaction with different co-variates: phylogeny or taxonomy, sexual dimorphism and biogeographic region. In addition, we used ordinary least squares (OLS) regression to assess intraspecific dry weight - ITD relationships for 10 bee and five hoverfly species.\nC_LIO_LIIncluding co-variates led to more robust interspecific body size predictions for both bees (Bayesian R2: 0.946; {Delta}R2 0.047) and hoverflies (Bayesian R2: 0.821; {Delta}R2 0.058) relative to models with ITD alone. In contrast, at the intraspecific level, our results demonstrate that ITD is an inconsistent predictor of body size for bees (R2: 0.02 - 0.66) and hoverflies (R2: -0.11 - 0.44).\nC_LIO_LITherefore, predictive allometry is more suitable for interspecific comparative analyses than assessing intraspecific variation. Collectively, these models form the basis of the dynamic R package, pollimetry, which provides a comprehensive resource for allometric research concerning insect pollinators worldwide.\nC_LI

ecology↗

bioRxiv2018

Effect of cadmium accumulation on the performance of plants and of herbivores that cope differently with organic defences

Some plants can accumulate in their shoots metals that are toxic to most other organisms. This ability may serve as a defence against herbivores. Although both metal accumulation and the production of organic defences may be costly to the plant, the two mechanisms may interact on their effect on herbivores. However, this interplay between metal-based and classical organic defences remains overlooked.\n\nTo fill this gap, we studied the interactions between tomato (Solanum lycopersicum), a plant that accumulates cadmium, and two spider-mites, Tetranychus urticae and T. evansi that respectively induce and suppress organic plant defences, measurable via the activity of trypsin inhibitors. We exposed plants to different concentrations of cadmium and measured their effect on mites and plants. The oviposition of both spider-mite species was higher on plants exposed to low concentrations of Cd than on control plants but decreased at concentrations above 0.5 mM. Therefore, herbivores with contrasting responses to organic defences responded similarly to metal accumulation by the plants. On the plant, despite clear evidence for Cd accumulation, we did not detect any effect of Cd on traits that reflect the general response of the plant, such as biomass, water content and carbon/nitrogen ratio. Still, we found an effect of Cd supply upon the quantity of soluble sugars and leaf reflectance changes that may reflect structural modifications in the cells. In turn, these changes in plant traits interfered with the performance of spider mites feeding on those plants.\n\nAdditionally, we show that the induction and suppression of plant defences by spider mites was not affected by Cd supply to the plants. Furthermore, the effect of metal supply on spider-mite performance was not affected by previous infestation. Together, our results suggest no interaction between metal-based and organic plant defences, on our system. This may be useful for plants living in heterogeneous environments, as they may use one or the other defence mechanism, depending on their relative performance in each environment. This may be relevant to studies on the interactions between herbivores and plants, from physiology to ecology.

ecology↗

bioRxiv2018

What we (don’t) know about global plant diversity

RationaleThe era of big biodiversity data has led to rapid, exciting advances in theoretical and applied biological, ecological and conservation sciences. While large genetic, geographic and trait databases are available, these are neither complete nor random samples of the globe. Biases in species absence in these databases create problems, reducing our inferential and predictive power.\n\nMethodsWe performed a comprehensive examination of the taxonomic and spatial sampling in the most complete current databases for plant genes, locations, and traits.\n\nResultsOnly 17.7% of the worlds described land plants feature in all three databases, meaning that more than 82% of plant biodiversity lacks representation in at least one database. Species coverage is highest for location data and lowest for genetic data. Bryophytes and orchids stand out taxonomically and the equatorial region stands out spatially as poorly represented in all databases.\n\nConclusionWe have highlighted a number of clades and regions about which we know little functionally, spatially and genetically, on which we should set research targets. The scientific community should recognize and reward the significant value, both for biodiversity science and conservation, of filling in these gaps in our knowledge of the plant tree of life.

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