Lay Summaries

The summaries below are provided by our authors to help put their research into context for the wider scientific community and the general public. Lay summaries for the current issue are here. You can also find all the previous lay summaries by issue, as well as summaries for articles on Early View, in the lay summaries archive.

Lay summaries for the current issue.

 

You can also find all the previous lay summaries by issue, as well as summaries for articles on Early View, in the lay summaries archive.

 

 

How bark properties promote invertebrate diversity in tree logs during early decay

Juan Zuo, Matty P. Berg , Roy Klein, Jasper Nusselder, Gert Neurink, Orsi Decker, Mariet M. Hefting, Ute Sass-Klaassen, Richard S. P. van Logtestijn, Leo Goudzwaard, Jurgen van Hal1, Frank J. Sterck, Lourens Poorter, Johannes H. C. Cornelissen One incubation plot of LOGLIFE experiment in Hollandse Hout, province of Flevoland, the Netherlands. Photograph by J. Zuo.

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Temperate forests accumulate large numbers of tree logs, which play important roles for biodiversity. They host a large number of organisms that need decaying bark or wood for food, shelter or reproduction. Among these organisms, invertebrates are a vital group with a fascinating diversity and an important role in the decay process of dead trees itself. The factors that determine invertebrate community composition in logs are still not clear. In recently dead tree trunks, the attached bark is of critical importance. The large variation in bark structure and tissue quality observed among tree species may determine invertebrate community composition by providing variation in resources and habitats.

We investigated the effects of bark properties, during the early decay stage of logs, on invertebrate community structure of 11 common, temperate tree species in the LOGLIFE ‘common garden’ experiment, in which logs of all these trees were placed in the same forest plots at the same time. We measured several bark properties and studied their effects on six animal groups: earthworms, woodlice, centipedes, millipedes, flies/midges and beetles. We hypothesized that, across tree species, the more different the bark properties were between two species, the more the composition of the animal community would differ as well.

Our tree species varied greatly in seven different bark properties, which had profound effects on the abundance of specific invertebrate groups. The greater the overall difference in the bark properties between tree species, the more dissimilar were the animal communities they supported, and the richer they were together in different invertebrate families. Bark properties have important effects on the composition and diversity of invertebrate communities in recently dead and decaying tree trunks. Our findings indicate that functional diversity in bark properties in decaying logs is likely a good indicator, better than tree species per se, of animal diversity in forests.

Image caption: One incubation plot of LOGLIFE experiment in Hollandse Hout, province of Flevoland, the Netherlands. Photograph by J. Zuo.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Relative importance of soil properties and microbial community for soil functionality

Manuel Delgado-Baquerizo, Jasmine Grinyer, Peter B. Reich and Brajesh K. SinghImage provided by authors.

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Soil ecosystem functionality is usually divided into two groups of functions: broad (i.e. widely conducted by all or most living organisms) and specialized (i.e. conducted by particular groups of organisms). The most widely accepted theories in soil ecology suggest that broad (e.g. respiration) and specialized (e.g. denitrification – reduction of nitrate, ultimately to nitrogen) functions are affected differently by resource availability and microbial communities in terrestrial ecosystems. However, we lack solid empirical data to quantify the relative importance of microbial communities and soil properties in regulating soil functions. Here we conducted a manipulative experiment and used statistical modeling to evaluate the role of soil properties and microbial communities in driving broad and specialized functioning. Our results provide direct experimental evidence that soil microbial community plays an important role in determining the rates of both broad (soil respiration) and specialized (denitrification) functions. In particular, our findings indicate that for broad functioning, soil properties such as total carbon can play a bigger role than the microbial community composition. Contrary to this, bacterial community composition drove the rates of specialized functioning, regardless of soil properties. These results support the most widely accepted soil ecological theories that suggest that broad functions such as soil respiration, which are a product of widely distributed processes across living microorganisms, are limited by both resource availability and microbial abundance. But specialized functioning, which is conducted by particular groups of organisms, may be highly sensitive to changes in microbial community. Such evidence helps advance our understanding of different drivers of soil ecosystem functioning, which will be crucial to developing an ecologically-relevant theory about belowground ecosystem functioning.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Are dive bottom durations good indicators of fur seal foraging success?

Morgane Viviant, Tiphaine Jeanniard-du-Dot, Pascal Monestiez, Matthieu Authier and Christophe GuinetArctic fur seal. Photograph by Christophe Guinet, CEBC UMR 7372 ULR-CNRS.

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Foraging models applied to air breathing divers predict that diving predators should optimize the time spent foraging at the bottom of dives, depending on prey encounter rate, distance to the prey patch (depth) and physiological constraints. This hypothesis was tested in free-ranging diving Antarctic fur seal Arctocephalus gazelle, equipped with accelerometers or Hall sensors that recorded mouth-opening events, an indicator of feeding events. 82 % of mouth-openings, defined as prey catch attempts, occurred at the bottom of dives. In accordance with model predictions, fur seals increased their foraging time at the bottom of dives with increasing diving depth, irrespective of the number of mouth-openings events. For dives shallower than 55 m, the mean bottom duration of dives without mouth-opening events was shorter than for dives with mouth-opening events. However, this difference was only due to the occurrence of V-shaped dives with very short bottom durations (0 or 1 s). When those V-shaped dives are removed, bottom duration was no longer related to the presence of prey capture attempts. Thus, the decision to abandon foraging is likely related to other information about prey availability than mouth-opening events (i.e. visual, sensory or acoustic cues), that seals might start collecting during the descent phase. For dives deeper than 55 meters, seals keep on foraging at bottom to maintain a greater diving efficiency as there is no longer any benefit of giving up. Most dives occurred at shallower depths (30-55 m) than the depth of highest foraging efficiency (i.e. of greatest number of mouth-opening events detected per dive, below 60 m). This is likely related to physiological constraints linked to deeper dives. These findings suggests that foraging decisions are more complex than predicted by current theory and highlight the importance of the information collected by the predator during the descent as well as physiological constraints.

Image caption: Arctic fur seal. Photograph by Christophe Guinet, CEBC UMR 7372 ULR-CNRS.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Stable isotopes reveal the ecology of tropical butterfly larvae.

Erik van Bergen, Henry S. Barlow, Oskar Brattström, Howard Griffiths, Ullasa Kodandaramaiah, Colin P. Osborne and Paul M. BrakefieldEcologists at work. Photo provided by author.

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Despite many ecological studies, our understanding of the larval ecology of many tropical butterfly species is very limited. In contrast to adults, caterpillars are mainly active at night and are notoriously hard to spot in the wild. This seriously hampers investigations of the evolution of feeding ecology and potential co-evolutionary interactions between host plants and butterflies. One group of butterfly species that is particularly interesting in the context of plant-herbivore co-evolution is the subtribe Mycalesina (Nymphalidae). These tropical butterflies feed mainly on grasses as larvae and have radiated dramatically in Sub-Saharan Africa, Madagascar and Asia with over 300 extant species.

The commonest form of photosynthesis is called C3, but tropical grasses often have a variant called C4, and the evolutionary history of mycalesine butterflies is expected to be closely tied to the rapid replacement of C3 vegetation by C4 grasslands in the Late Miocene-Pliocene. In contrast to C3 host plants, these C4 grasses tend to have a higher physical toughness and lower nutritional values. Therefore, insect herbivores, such as mycalesine larvae, are expected to avoid C4 grasses when C3 host plants are available. In addition, one would predict that novel feeding adaptations, for instance in jaw morphology or digestive physiology, may have evolved in mycalesines in response to the ecological dominance of C4 grasses in open savannah habitats.

Stable isotope analyses represent an unexploited opportunity to increase our understanding of the larval ecology of mycalesine butterflies. The environmental conditions to which a caterpillar is exposed are imprinted into the exoskeleton of the adult during metamorphosis. By measuring the ratios of several stable isotopes we can recover the information that is ‘recorded’ in leg material (=exoskeleton) of adult butterflies, which are relatively easy to capture in the wild. Here, we show that stable isotopes of carbon provide information about the type of host plant, C3 or C4, which was used by the larvae. In addition, stable isotopes of oxygen reveal how much water vapour was present in the atmosphere during larval development.

The isotopic composition of leg tissue in mycalesine butterflies shows that species that inhabit open C4 grass-dominated environments are quite opportunistic in their larval host plant choice. Nevertheless, we observe that during the dry season, larvae are more likely to use high quality C3 grasses and are exposed to lower levels of water vapour in the atmosphere. Finally, our data reveal that the ability to process C4 grasses is clustered within related groups of mycalesine species, suggesting that C4 grass processing adaptations may have evolved in this subtribe.

Image caption: Ecologists at work. Photo provided by author.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently

Inga TM Bödeker, Björn D Lindahl, Åke Olson and Karina E ClemmensenThe soil profile of the boreal forest near Sala in middle Sweden in which the field study was conducted. The soil has a 10-25 cm thick organic layer on top of the mineral soil. Photo by KEC.

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Communities of litter saprotrophic (decomposer) and mycorrhizal fungi are vertically separated within boreal forest soil profiles, with litter saprotrophs normally confined to the fresh litter on the surface and mycorrhizal fungi dominating the deeper soil layers. It is unclear whether this depth partitioning is maintained exclusively by substrate-mediated niche partitioning, or by competition for space and resources. Improved understanding of the mechanisms driving spatial partitioning of these fungal guilds is critical, as they may affect carbon and nutrient cycling in different ways.

We utilized the spatial separation of litter saprotrophic and mycorrhizal fungal communities to – under field settings – test the potential of these fungal guilds to colonize and exploit organic matter outside their normally realized niche. Natural substrates of three qualities – fresh or partly decomposed litter or humus – were incubated in mesh-bags in both their own and in ‘foreign’ locations in the soil profile. After one and two growing seasons we determined fungal community composition and decomposition activities in the substrates.

During the first growing season, all organic substrates were mainly colonized by fungi native to the soil horizon in which the substrates were incubated. This demonstrated the potential of both fungal guilds to colonize all substrates, and suggests that their colonization under natural circumstances is restricted by competitive interactions. Litter substrates also decomposed more slowly when colonized by root-associated communities than when colonized by saprotrophs, suggesting that ectomycorrhizal fungi are less efficient than saprotrophic fungi in decomposing aboveground litter substrates.

During the second growing season, certain basidiomycetes from both guilds were particularly efficient in localizing and exploiting their native organic substrates although displaced in the vertical profile. This resulted in a complete catch-up in decomposition of litter even when placed in the humus, showing that fungal communities – rather than microenvironmental conditions - were the primary drivers of slow decomposition of litter during the first season. Humus substrates were only slightly decomposed by both fungal guilds, and based on the present study we cannot resolve whether competitive interactions between fungal guilds are important for long-term soil C storage.

Overall, fungal community development during the course of the experiment was determined to similar degrees by vertical placement and by substrate quality. While the importance of substrate quality on decomposer communities and their activities has long been acknowledged, our results suggest that competition and monopolization of spatial domains (as tested by the placement treatment) play a more important role in structuring fungal communities at small scales than previously thought. In natural ectomycorrhiza-dominated forest ecosystems, preferred substrates and territorial distribution of these fungal guilds thus coincide, and competition appears to reinforce the vertical, substrate-dependent partitioning and stabilize vertical community stratification.

At the ecosystem level these findings suggest that ectomycorrhizal fungi through competitive interactions have the potential to indirectly regulate litter decomposition rates by restraining activities of more efficient litter saprotrophs. Vice versa, in situations where the competitive strength of mycorrhizal fungi is compromised – for example after forest clear-cuts – saprotrophs may proliferate and accelerate decomposition processes.

Image caption: The soil profile of the boreal forest near Sala in middle Sweden in which the field study was conducted. The soil has a 10-25 cm thick organic layer on top of the mineral soil. Photo by KEC.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Ecosystems, Evolution and Plant Soil Feedbacks

Beyond plant–soil feedbacks: mechanisms driving plant community shifts due to land-use legacies in post-agricultural forests

Eduardo de la Peña, Lander Baeten, Hanne Steel, Nicole Viaene, Nancy De Sutter, An De Schrijver and Kris Verheyen Photograph provided by authors.

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Past human activities have a lasting impact on the composition and functioning of present-day terrestrial ecosystems. Post-agricultural forests are a typical example illustrating the effect of agricultural legacies on the current composition of the ecosystem. Diversity studies show that a common feature of European post-agricultural woodlands is the absence or low frequency of species that characterize the understorey of ancient forests, e.g. wood anemones, oxlips, bluebells, relative to ancient forests that have been forested for centuries. In this study we shed light on the mechanisms that explain why this happens. From previous studies we know that agricultural activities modify not only the nutrient content of soils (e.g. concentration of nitrogen and phosphorus) but also the soil community i.e. soil bacteria, fungi and nematodes. We also know that changes in these soil attributes may have cascading effects on organisms occurring aboveground by mediation of the plant community. We hypothesized that these processes could explain the poor establishment of typical species of ancient understories in post-agricultural sites. With this in mind, we first compared soil nutrients, the soil and the aboveground invertebrate community associated with the same plant species in ancient and post-agricultural sites; then we tested in the field and in the lab how soil conditions affect plant growth and the interactions of plants with insect herbivores. The results of our study show that ancient and post-agricultural soils clearly differed in composition, however the invertebrate species occurring aboveground did not differ in the sites compared. Surprisingly plants growing in post-agricultural sites showed higher abundances of invertebrate herbivores and consequently suffered more leaf herbivory than the same plants growing in ancient woodland soil. Nutrient analyses of soil and plants showed that increased levels of phosphorus (and to a lesser extent, nitrogen) made plants more nutritious for insect herbivores. Our study demonstrates that soil legacies of previous land use not only affect plant growth but also increase herbivore impact and abundance, which we propose as an additional and novel mechanism to explain the shifts in species composition of the understorey.

Image caption: Photograph provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Ecosystems, Evolution and Plant Soil Feedbacks

Rapid evolution of plants and soil microbes

Casey P. terHorst and Peter C. ZeePhotograph provided by authors.

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Ecologists have long appreciated the value of diversity in natural plant communities. Diverse communities function better. Yet, our understanding of the factors that control diversity in communities remains incomplete. We have recently begun to appreciate the important role of microbes in human health; plants too both rely on and battle with microbes in the soil. Plant diversity can affect the soil microbial community, but the microbes also affect plant diversity, in a feedback known as plant-soil feedback (PSF). Because of their short generation times and strong effects on each other’s ecology, plants and microbes can evolve on the scale of weeks to years. Here we review evidence of how changes in plant and microbial traits affect diversity and ecological dynamics in the community. Genetic variation in plant traits and subsequent evolution of those traits can affect traits and species composition of soil microbial communities. Soil microbial communities can, in turn, alter the evolutionary trajectory of plant traits. Finally, we consider how interactions between ecology and evolution might enhance or mitigate the effects of PSF in driving the diversity of natural plant communities.

Image caption: Photograph provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Advances and challenges in the study of ecological networks

Evolutionary history imprinted on species interaction

Guadalupe PeraltaThe leaf veins resemble the shape of species phylogeny which underlies the plant-leafminer interaction. Photo by G. Peralta.

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In ecosystems, organisms interact with each other in diverse ways, forming complex webs of relationships. It is well known that the occurrence of interactions among species of a community depends on species co-occurrence and also on their abundance. However, apart from these factors, it has been suggested that the evolutionary history of species might also determine the interactions that occur within a community. If this was the case, information on species relatedness could improve our understanding of the mechanisms driving community structure and dynamics. In addition, if species relatedness is informative of the interactions that species have, this could be used as a tool for determining and predicting the effects that global environmental changes could have on communities. For instance, the effects of an invasive species could be forecast, and potentially reduced, if we could predict how that species would fit into the assemblage of interactions of the invaded community (i.e. if based on the relatedness of the invasive species with other species we could predict its partners).

Therefore, in this paper I review the ecological literature in which species relatedness has been tested as a potential driver of the ensemble of interactions and its structure. It has been shown that species relatedness can affect different aspects of community structure differently and this imprint can also vary depending on the interaction type (e.g. antagonistic vs. mutualistic interactions).

Thus, the evidence confirms that species interactions bear the stamp of their evolutionary history. Understanding the influence that species relatedness has on community assembly can help us to predict how communities might change and how they will function in the future.

Image caption: The leaf veins resemble the shape of species phylogeny which underlies the plant-leafminer interaction. Photo by G. Peralta.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Neighboring resources can affect the attractiveness of resources occurring in the neighborhood

Thomas A. Verschut, Paul G. Becher, Peter Anderson and Peter A. Hambäck  Photo credit: Sébastien Lebreton.

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Plants often differ in their quality as a food resource for insects. As many insects find food through smell, a plant with a very attractive smell will attract a higher number of insects than a plant with a less attractive smell. However, when an attractive plant grows next to an unattractive plant it can lead to an increased number of insects visiting the unattractive plant, which is known as associational susceptibility. Moreover, an attractive plant could also lower the number of visits to the less attractive plant, which is known as associational resistance. These associational effects have been commonly observed for pollinators visiting flowers and herbivorous insects feeding on different plant species. However, it is not fully understood how mixtures of different resources lead to different outcomes of associational effects.

We tested how the density and frequency of different resources could lead to associational susceptibility or associational resistance using the common fruit fly, Drosophila melanogaster. Fruit flies are strongly attracted to fermenting fruits, which contain odours that are also found in balsamic vinegar. Therefore, we used balsamic vinegar to mimic food resources that differed in their attractiveness. With these resources we created patches containing different frequencies of attractive and less attractive resources.

Firstly, we found that attractiveness of a resource patch depends on which resources it contains, but that there is threshold at which increasing the number of resources does not result in a higher attractiveness of the patch. Secondly, we found that fruit flies are always more attracted to the resource that smells most attractive in the patch. Because a higher number of flies visited the more attractive resource in the mixed patches, compared to when the more attractive resource occurred on its own, it experienced associational susceptibility. Moreover, the less attractive resource experienced associational resistance, as the number of fly visits was lower in mixed patches. The strength of this interaction increased with a decreasing frequency of the more attractive resource. These findings can have important implications for managing plants in mixed environments and can help to predict the relative numbers of insects visiting plants growing in the same area.

Image caption: Photo credit: Sébastien Lebreton.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Advances and challenges in the study of ecological networks

Who interacts with whom? A common framework for identifying linkage rules across different types of interactions

Ignasi Bartomeus, Dominique Gravel, Jason M. Tylianakis, Marcelo A. Aizen, Ian A. Dickie and Maud Bernard-Verdier Eucera bee visiting Cistus salvifolius. Curro Molina.

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To understand ecological communities of plants and animals, we need more than a list of species. We need to know how the species interact. In fact, most important ecological processes are mediated by an interaction. Take for instance a flowering plant and a bee. Only their interaction allows both bees and plants to reproduce. Other interactions involve predators and their prey, or herbivores and plants.

We know that big fish eat small fish and that pollinators with long tongues tend to visit plants with deep flowers. However, quantifying who interacts with whom is not an easy task. For example, predators eat prey smaller than themselves, but not if the prey becomes too small for them. Similarly, pollinators with short tongues cannot reach deep flowers, but long-tongued pollinators may not be constrained to any type of flower.

In this paper, we review recent advances in predicting interactions from species co-occurrence and develop a probabilistic model for inferring trait matching. We model the probability that two species interact based on the matching of their traits while taking into account species abundances. The model presented uses empirical data to understand why two species interact or not. We exemplify its use with three case studies, but the model can be applied to a great range of mutualistic and antagonistic interactions, from grasshoppers chewing on plant leaves to pollinators drinking nectar. Understanding the linkage rules is important to predict how the web of life is organized, especially in the face of the human-induced environmental changes we are experiencing.

Image caption: Eucera bee visiting Cistus salvifolius. Curro Molina.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Ecosystems, Evolution and Plant Soil Feedbacks

The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems

Daniel Revillini, Catherine A. Gehring and Nancy Collins JohnsonMushrooms growing. Image provided by authors.

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Plants release energy from photosynthesis into the soil, supporting the growth of microorganisms that live independently in the soil or form direct physical associations with plant roots. The microorganisms can, in turn, influence plant survival, growth, and reproduction. These plant-soil feedbacks can positively or negatively affect plant productivity and diversity, but many investigations of their importance have been conducted in the glasshouse and/or examined only a subset of the microbial communities that occur in soil. In addition, studies of plant-soil feedback have rarely been linked to broader theories of host plant-microbe resource exchange.

In this paper, we expand our consideration of plant-soil feedbacks in three ways. First, we review what is known about three-way interactions among plants, fungi that form symbiotic nutritional associations with roots (mycorrhizas) and soil bacteria. We then consider how local adaptation arising from the exchange of goods and services among interacting plants and microbes can influence plant-soil feedback. Finally, we incorporate the optimal resource allocation model into plant-soil feedback theory to predict how plant-soil feedbacks will change with two anthropogenic environmental changes, nitrogen deposition and climate change induced drought.

Our review suggests that soil bacteria, particularly plant growth-promoting bacteria, should be incorporated into plant-soil feedback studies involving mycorrhizas because of their synergistic influence on nutrient uptake, hormone production and pathogen defense by host plants. Over evolutionary time, resource availability may be a powerful force that optimizes the acquisition of limiting resources and creates advantageous associations among plants and their resident microorganisms. This force is expected to generate local adaptation and also influence the direction and intensity of soil feedback. Through its focus on limiting resources, the optimal resource allocation model produces testable predictions about the direction and strength of plant-soil feedback across gradients of the availability of resources supplied by plants (photosynthate) and microbes (nutrients and water).

Image caption: Mushrooms growing. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Energy expenditure of adult green turtles at sea

Manfred R. Enstipp, Katia Ballorain, Stéphane Ciccione, Tomoko Narazaki, Katsufumi Sato and Jean-Yves GeorgesAdult green turtle foraging at a seagrass meadow in Mayotte. Credit: Manfred Enstipp.

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All living organisms must obtain food from the environment to provide energy for their daily lives. Understanding how much energy organisms need for their various activities is a central topic studied by eco-physiologists. In the case of marine turtles, knowing their energy needs during the different phases of their life at sea is essential for their conservation, which critically depends on successful reproduction. In these reptiles, reproduction is typically associated with long-distance migration and only occurs every few years. It is an enormous physical task and requires substantial energy reserves, which are build up at the foraging grounds. If a turtle has insufficient energy reserves, it will not be able to engage in costly reproduction, with consequences for population/conservation status.

Using a novel technique (attaching small accelerometry dataloggers to turtles), we studied activity patterns and energy expenditure of adult green turtles foraging year-round at a seagrass meadow in Mayotte and during simulated migration (displacing a turtle from its nesting beach) off Mohéli, in the south-western Indian Ocean. We found a clearly structured activity pattern for turtles at the foraging site that persisted throughout the year. During daylight hours turtles foraged on the shallow seagrass meadow (many short/shallow dives), while at night they rested on the inner reef slope (few long/deep dives). Energy expenditure at the foraging site during the austral summer was low (~1.6 times the value at rest) and declined even further with decreasing water temperatures during the austral winter. By contrast, upon its oceanic release, the displaced turtle swam continuously towards its nesting beach, conducting shallow/short dives during the day, which, mostly at night, were interspersed with few deep/long dives. Energy expenditure during this simulated migration was greatly increased to ~3 times the value at rest, indicating the costliness of such undertaking. Using a novel technique, we were able to study the energy needs of adult green turtles in great detail and under natural conditions. We show that continuous feeding during daylight hours at their foraging site, at low energetic costs, allows these turtles to gradually build up energy reserves needed for migration and reproduction.

Image caption: Adult green turtle foraging at a seagrass meadow in Mayotte. Credit: Manfred Enstipp.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Author-suggested reviewers: Gender differences and influences on the peer review process at an ecology journal

Charles Fox, C. Sean Burns, Anna Muncy and Jennifer MeyerImage from  “What is a journal and a peer reviewed article?” (Northeastern Illinois University Ronald Williams Library)

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Peer review is the primary method by which journals evaluate the quality and importance of submitted manuscripts. Identifying suitable reviewers, and then recruiting them to review, is one of the most challenging parts of an editor’s job. Authors should know best who is qualified to review their papers; thus, to help editors find suitable reviewers, many journals allow or require authors to suggest names of preferred and non-preferred reviewers. However, authors also have a strong incentive to suggest reviewers that they expect to review their paper positively.

In this study, we examine the reviewers that are suggested by authors as preferred (those that authors would like to review their manuscript) and non-preferred (those that authors request not be invited to review their paper), the use of these suggestions by editors, and their influence on the peer review process and outcomes at the journal Functional Ecology. We also examined how gender of the participants (author, editor and reviewer) influences the role of preferred reviewers in the peer review process.

Most authors suggest preferred reviewers, but few suggest non-preferred reviewers. Most author-preferred reviewers are male, but the proportion of women among author suggestions increased from a low of 15% in 2004 to a high of 25% in 2014. Male and female authors did not differ in how likely they were to suggest preferred reviewers, but female authors suggest more female reviewers (~28%, averaged across years) than do male authors (~21%). Women that were suggested as preferred reviewers were more likely to be chosen by editors as desired reviewers than were men suggested by authors. We found no evidence that editor gender, seniority or length of service as an editor for Functional Ecology affected how likely they were to use author-suggested reviewers.

Of reviewers invited to review, those that were suggested by authors were more likely to respond to the editors' review invitations but were not more likely to agree to review. Most strikingly, author-preferred reviewers rated papers much more positively than did editor-selected reviewers, and papers reviewed by author-preferred reviewers were much more likely to be invited for revision than were papers reviewed by editor-selected reviewers. This difference was not influenced by the gender of the participants in the process.

Suggesting preferred reviewers clearly benefits authors – preferred reviewers rate papers significantly more positively (on average) than do editor-selected reviewers, improving the chances that a paper will be published. We thus recommend that authors always suggest preferred reviewers if given the option to do so by a journal. Journals and editors, by contrast, should consider who proposed the reviewer, and possible biases, when deciding whether to use author-suggested reviewers and when evaluating reviewer comments and scores. Highly-selective journals – those whose decisions emphasize broad general interest, significance and novelty – might consider eliminating the practice of allowing or requiring authors to suggest their own reviewers.

Image caption: Image from “What is a journal and a peer reviewed article?” (Northeastern Illinois University Ronald Williams Library).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Advances and challenges in the study of ecological networks

Everything is connected: new tools for understanding and managing forests

Darren M.Evans, James J. N. Kitson, David H. Lunt, Nigel A. Straw & Michael. J. O. PocockSampling for forest insects to create ecological networks can be hazardous when invasive species with urticating hairs (such as Thaumetopoea processionea) are present (note masks and gloves are removed for the photograph). Photo: DM Evans.

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Forests hold a large proportion of global biodiversity and terrestrial carbon stocks and are under significant threats and pressures globally. In the UK, forests are managed mainly for commercial and amenity uses but many are vulnerable to a growing number of diseases (such as Chalara dieback of ash Hymenoscyphus fraxineus and Dothistroma needle blight Dothistroma septosporum) and/or non-native invasive insects (such as Oak processionary moth Thaumetopoea processionea and Asian longhorn beetle Anoplophora glabripennis). There is considerable interest by ecologists and land managers to not only determine the ecological consequences of losing tree species as a result of pests and diseases, but to find new ways of making forests more resilient to environmental change. However, this requires a much better understanding of the complex ways in which trees, insects and other organisms interact within forests than is currently available.

In this Extended Spotlight, we examine how recent advances in both molecular and community ecology can be combined to create highly-resolved species-interaction networks that can better inform the management of terrestrial ecosystems. Ecological networks describe the interactions between species and provide a powerful way of examining the underlying structure of communities as well as ecosystem functioning and stability. Here, we visualize the known interactions between all British tree genera, their herbivores and their associated parasitoids and show that considerable herbivore-parasitoid data is incomplete or missing. To overcome this problem (or when creating a network from scratch) we show how new DNA sequencing technology provides enormous potential for creating bigger, better networks as well as determining hitherto difficult to observe species interactions.

By combining ‘DNA metabarcoding’ with ecological network analysis we provide a novel framework by which forests can be studied and managed. For example, species-interaction data can be used to examine the robustness of forests to tree species loss, for targeted insect pest management and even for planning more resilient forests for the future. Overall, we demonstrate how these approaches can be merged to create important new tools for understanding large-scale ecological and evolutionary processes.

Image caption: Sampling for forest insects to create ecological networks can be hazardous when invasive species with urticating hairs (such as Thaumetopoea processionea) are present (note masks and gloves are removed for the photograph). Photo: DM Evans.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Leaf functional traits are decoupled among eucalyptus genotypes under ambient and elevated CO2

Chris J. Blackman, Michael J. Aspinwall, Víctor Resco de Dios, Renee Smith and David T. Tissue Eucalptus. Photo provided by authors.

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In leaves, high rates of photosynthesis are typically associated with high levels of leaf water supply and demand, high levels of leaf nitrogen and low levels of investment in leaf mass per unit area (LMA). These trait associations are thought to contribute to defining ‘fast’ vs. ‘slow’ performance strategies in plants. While the consistency of these trait relationships varies among different groups of species, the level of trait coordination among genotypes (genetically distinct individuals) of a single species remains largely unknown.

In this study we examined the level of coordination in leaf functional traits among 14 genotypes of a widespread and iconic species of eucalypt (Eucalyptus camaldulensis spp. Camaldulensis) grown in a sunlit glasshouse under well-watered and fertilised conditions. We also examined the effect of growth under variable concentrations of atmospheric CO2 in an effort to understand how rising levels of CO2 may affect patterns of leaf functional trait coordination among genotypes.

We found that leaf functional traits related to photosynthesis (e.g. net photosynthesis and photosynthetic biochemistry), leaf water transport (e.g. leaf venation and stomatal traits) and leaf economics (e.g. LMA and leaf nitrogen) were unrelated to each other among genotypes grown in ambient CO2 (aCO2). However, close associations were observed among suites of traits within each functional ‘group’. We also found that plant growth in elevated CO2 (eCO2) did not substantially alter patterns of trait coordination among genotypes, even though the level and direction of the eCO2 response varied among traits.

Our findings clearly indicate that different suites of leaf functional traits can vary independently of each other, even among genotypes of a single species. A major implication of this result is that leaf functional traits may be free to respond to changes in the environment in different ways, without being constrained by strong linkages to other traits. However, our results also suggest that eCO2 does not seem to be a very strong selective agent in altering patterns of trait coordination among genotypes.

Image caption: Eucalptus. Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Plants helping plants: a relationship that evolves with age

Jose A Navarro-Cano, Marta Goberna, Alfonso Valiente-Banuet and Miguel VerdúThe nurse shrub Ononis tridentata with its beneficiary plant species on a gypsum outcrop in SE Spain (photo credit: Jose A. Navarro Cano).

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Plant facilitation, the mechanism by which one plant species (nurse) gives benefits to the activity or presence of other plant species (beneficiaries) has been reported in areas of high abiotic stress throughout the world. Here, we deal with the topic of plant facilitation in a gypsum ecosystem controlled by soil toxicity and water-stress, through the seldom-explored approach of the evolution of plant nursing abilities with nurse age. We assessed by a manipulative experiment and observational data whether the same nurse plant facilitates species with contrasted functional traits along its lifespan. We hypothesized that early-successional species, with lower nutritional requirements, emerge better below younger nurses whereas late-successional species, which require mature ecosystem conditions, need older nurses. Our results show that facilitation allows the establishment of both plant functional types beneath the same nurse, but in a different temporal sequence determined by nurse age, which determine a reverse stress gradient. Our research adds the time perspective to the nursing ability of some species thus enabling the assembly of both “early-” and “late-successional species” below the same nurse plant species. In light of our results we suggest a revision of the role of facilitative interactions in community assembly rules under severe abiotic stress conditions.

Image caption: The nurse shrub Ononis tridentata with its beneficiary plant species on a gypsum outcrop in SE Spain (photo credit: Jose A. Navarro Cano).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Reproductive effort alters immune parameters measured post-partum in European rabbits under semi-natural conditions

Heiko G. Rödel, Manuela Zapka, Volker Stefanski and Dietrich von HolstEuropean rabbit mother (with coloured aluminium ear tag) closing the entrance of the burrow (left) including the nest with her offspring after nursing. Photo by Heiko G. Rödel.

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Reproduction is energetically costly, and mothers’ resource allocation to reproduction might compromise other physiological functions such as the immune system. These interactions between reproductive effort and immune function have been frequently explored in birds, but hardly in mammals under natural conditions.

We studied such purported negative associations between reproductive effort and immunity in female European rabbits in a field enclosure. To this end, we explored whether mothers’ reproductive effort, measured as litter mass and size and whether the females had given birth to another litter shortly before, were associated with different maternal immune parameters measured post-partum.

We found that mothers with higher reproductive effort showed lower concentrations of white blood cells, in particular of neutrophils and lymphocytes, supporting the existence of a negative association between reproduction and immunity. However, there was also evidence for a positive association between reproductive effort and immune parameters measured from serum, such as immunoglobulin G concentrations and the functionality of the complement system (proteins that enhance the ability of antibodies and phagocytes to deal with pathogens). These parameters were increased in mothers with higher litter size or mass. Interestingly, corresponding negative or positive associations with respect to the immune parameters considered were also apparent when comparing changes in immune parameters and reproductive effort on the individual level – that is, when focussing on females which repeatedly reproduced within the breeding season, and either increased or decreased their reproductive effort during consecutive reproductive events.

In conclusion, the findings of our study underline differential responses of different branches of the maternal post-partum immune system to variation in mothers’ reproductive effort. On the one hand, our females might compromise at least some cellular immune parameters for reproduction. On the other hand, we hypothesize that positive associations such as between immunoglobulin G and reproductive effort could be favoured by evolution, as a higher number of pups requires an intensified transfer of maternal immune parameters via placenta or colostrum and milk to protect the offspring during early postnatal life.

Image caption: European rabbit mother (with coloured aluminium ear tag) closing the entrance of the burrow (left) including the nest with her offspring after nursing. Photo by Heiko G. Rödel.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Nutrient utilization traits vary systematically with intraspecific cell size plasticity

Martino E. Malerba, Kirsten Heimann, Sean R. ConnollyImage provided by authors.

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Analyzing how species respond to changes in the environment is at the heart of ecology. Growth, age, nutrient uptake etc. are species traits used to measure these responses and interpret impacts of environmental conditions on the species composition of ecosystems (reefs, rainforests, etc.). However, these traits can be quite variable, even for the same species (this variation is often termed “intraspecific trait plasticity”). For instance, individuals of the same plant species can display very different traits depending on the environmental conditions they are growing in.

Small one-celled algae (phytoplankton) are known to thrive and bloom primarily due to large nutrient inputs (e.g. nitrogen) into our waterways and seas. Almost all life on earth is directly or indirectly dependent on phytoplankton primary productivity. Today we know that differences in species traits are very important to understand phytoplankton ecology. But virtually nothing is known about how variable traits are within the same phytoplankton species. For instance, we know that cells can change their volume, depending on physiological and environmental conditions. What we do not know is whether the traits of a species change together with the size of a cell.

 

In this study we considered the growth of populations of a single phytoplankton species reared under different nutrient (i.e. nitrate and ammonium) conditions. We found that cells with different nutrient histories exhibit different traits. More importantly, we also found a systematic change between the traits of a species and the mean cell size in the population. This means that environmental conditions favouring smaller or larger cells would also influence the traits of a species. Not accounting for the effects of cell size and previous nutrient history can substantially reduce our ability to understand and predict the dynamics of a species. These results highlight the importance of size plasticity in ecology and suggest that intraspecific variability might play an important role in shaping natural communities.

 

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Experimentally manipulating the harmful products of respiration

Rebecca E. Koch and Geoffrey E. Hill The house finch (Haemorhous mexicanus) is one of the several species in which paraquat has been used as a physiological ROS generator within the field of oxidative stress ecology. Photo credit to co-author Geoff Hill.

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Life requires that energy stored in molecules such as sugars and fats be released and converted into forms of energy that can run cellular processes. Such energy release is inherently inefficient, however, such that some energy is dissipated as heat and some energy ends up changing oxygen molecules into charged particles known as free radicals, which can damage cellular components like membranes and DNA. The amount of free radicals produced in cellular respiration varies among individuals and species, with important consequences for health and fitness—as a matter of fact, free radical damage has been implicated as a major factor in the process of aging. To study processes like free radical damage, scientists require methods to stimulate the production of free radicals or inhibit counter-acting molecules known as antioxidants. By experimentally simulating high levels of free radicals within an animal’s body, we can learn how some individuals are better able to withstand free radical damage and prevent its harmful effects. We reviewed all of the methods for manipulating free radicals that are available to scientists working with vertebrates in an ecological context. We conclude that the toxic herbicides paraquat and diquat are the most effective agents for causing more free radicals to be released by the cells of an animal. These compounds are poisons because they can induce a fatal release of free radicals in humans and other animals. However, if small and carefully regulated doses are used, then free radical release can be stimulated at a less than a lethal level. The other most effective means to increase free radicals in animal cells is to suppress the action of antioxidants. Currently, chemical suppression is possible in some animals, but new genetic techniques that can shut down targeted genes will likely soon become the best means of manipulating free radicals. With the right tools, biologists can tackle fundamental problems like the role of free radical buildup in the process of aging.

Image caption: The house finch (Haemorhous mexicanus) is one of the several species in which paraquat has been used as a physiological ROS generator within the field of oxidative stress ecology. Photo credit to co-author Geoff Hill.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Food, temperature, and endurance: Effects of food deprivation on the thermal sensitivity of physiological performance

Anthony L. Gilbert and Donald B. MilesMale Urosaurus ornatus. Image provided by authors.

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Lizards are a group of terrestrial vertebrates at great risk from changes in global climate because their physiology is dependent on environmental temperature. The focus of research that attempts to estimate lizard responses to climate change has traditionally relied only on changes in temperature, while neglecting other simultaneous changes to the environment. In arid desert ecosystems, warmer temperatures will alter precipitation patterns, further reducing the scant rainfall these areas already receive. As a result, reduced primary productivity is expected to limit prey abundance for a multitude of predators. Physiology, while dependent on temperature, can also be influenced by energetic state, and this is a relationship that has not received much attention especially in lizards and with respect to rapidly changing climates. We examined whether the relationship between physiology and temperature for the tree lizard (Urosaurus ornatus) is affected by food availability. We estimated locomotor performance (endurance capacity), thermal preference, and the thermal sensitivity of locomotor performance for fasted and fed groups of U. ornatus to evaluate the effect of food deprivation on thermal physiology.

We found that food-deprived lizards exhibited reduced endurance running capacity, lowered preferred body temperatures, and a thermal sensitivity of performance favorable for cooler body temperatures compared to fed lizards. This indicates that lizards that are unable to forage effectively will restrict themselves to cooler regions of their habitat and be at a physiological disadvantage for being active at warmer periods of the day. This will further restrict foraging opportunities and intensify energetic imbalance. Our work demonstrates an energetic mechanism by which changes in climate could lead to shifts in lizard activity and ultimately demographic instability and extinction.

Image caption: Male Urosaurus ornatus. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Ecosystems, Evolution and Plant Soil Feedbacks

How plants interact with soil biota in a changing world

Wim H. van der Putten, Mark A. Bradford, E. Pernilla Brinkman, Tess F.J. van de Voorde and G.F. (Ciska) VeenExperiment in progress. Photo provided by authors.

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Soil contains thousands of organisms that can interact with growing plants. In the past, ecologists have developed a method to study the combined effects of all these soil organisms. This method is named plant-soil feedback and considers soil literally as a black box. However, when we want to understand how soil organisms really interact with plants, we need to collect more detailed information about the roles of the various organisms in the soil. The challenge, therefore, is to open the black box of soil. This is essential in order to forecast how changes in the global environment, such as climate warming, land use change, biodiversity loss and invasive species influence plant-soil interactions and, consequently, vegetation composition. In the present article, we review published studies in order to develop a novel tool for opening the black box of soil. This novel tool is named the plant-soil feedback triangle. Basically, there are three major groups of soil organisms: symbionts that co-operate with plants, decomposers that turn plant residues into mineral nutrients, and enemies that cause plant diseases. We visualize soil as a triangle with symbionts, decomposers, and enemies as the three corners. The net effects of these three groups of soil organisms can be depicted in the triangle, so that we can visualize if the net effects of soil biota mean that plants will promote or decrease their own growth conditions in soil. As most studies have been carried out in highly controlled conditions in a greenhouse, we appeal for new studies that test plant-soil feedback effects in the field. In those experiments, it may be assessed what is the contribution of plant-soil feedback to patterns and processes that can be observed in the field. This approach will also enable ecologists to determine the contribution of soil biota relative to that of herbivores, plant competition or facilitation, and changes in soil chemistry or physics.

Image caption: Experiment in progress. Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Trade-offs among endurance capacity, reproduction, and immunity in lizards

Jerry F. Husak, Haley A. Ferguson and Matthew B. Lovern Lizard. Image provided by authors.

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Because resources are limited, investment of acquired energetic resources into a particular trait denies those same resources from being allocated to another trait, resulting in life-history trade-offs. Classic life-history traits such as reproduction and immunity clearly influence fitness and have been the primary focus of ecological research. However, performance traits such as locomotor capacity are also key to fitness and are energetically expensive, yet they are seldom integrated into life-history studies. We manipulated diet and forced allocation of resources to performance, via exercise training, to examine trade-offs among endurance capacity, growth, immune function, and investment in reproduction. Captive green anole lizards were assigned to one of four treatment combinations across two factors (diet restricted or not and endurance trained or not) over the course of nine weeks. Our results show that training enhances endurance performance, regardless of diet treatment, due to increased heart size and volume of red blood cells. Both diet restriction and training dramatically suppressed reproduction and immune function, but there were opposing effects of diet restriction and training on growth: diet restriction decreased it, but training increased it. Elevated stress hormone levels from training were associated with suppression of immunity, and decreased fat stores from diet restriction were associated with suppressed reproduction in both sexes. By forcing allocation of resources to performance with exercise training, we revealed that performance enhancement comes at a cost, suggesting that locomotor performance is an important part of energy allocation decisions and thus a key component of life-history trade-offs.

Image caption: Lizard. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Losing reduces bite force in crickets

Catriona Condon and Simon P. LailvauxAcheta domesticus. Photo provided by authors.

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In many animal species, males fight over access to females or resources that females need. Although actually coming to blows is rare because no-one involved wants to be injured, fights can escalate and become physical if they cannot be resolved through other means such as mutual display. When this happens, a male’s chances of winning a fight is often based on how strong or fast he is. Because many animals bite each other during aggressive interactions, bite force would seem to be an important determinant of a male’s ability to win a fight, and evidence suggests that this is indeed the case for a variety of animal species from lizards to insects. However, other factors can affect the chance of winning a fight, including fight experience, and studies have shown that animals that have recently lost a fight are more likely to lose subsequent fights. This suggests that fighting ability based on, for example, bite force, actually decreases in animals that lose fights. Such a decrease would be surprising because while maximum bite force can potentially be affected by factors including size, diet, and head shape, in the short term an animal’s maximum bite ability would be expected to change very little, and thus his fighting ability should remain relatively constant.

We measured bite force and staged male combat contests in the cricket Acheta domesticus to answer two questions: first, whether individual bite force affects male combat outcomes; and second, whether losing a fight affects a male’s ability to bite and therefore fight. We found that bite force does indeed influence fight outcomes in A. domesticus, with animals that bite harder relative to their opponents being more likely to win an initial male combat bout. When we made males fight a second bout shortly after, we found that animals that lost either the first or both rounds of combat indeed decreased their bite force compared to animals that won just the first round, that won both rounds, or that never fought and therefore never lost. Animals that lose fights therefore show reduced bite force.

Image caption: Acheta domesticus. Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Inbreeding and neighbouring vegetation drive drought-induced die-off within juniper populations

Francisco Lloret and Cristina García Juniper in different conditions. Image provided by authors.

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Massive forest die-off events in response to increasingly frequent and prolonged droughts have been reported worldwide during recent decades. Prolonged and more intensive droughts are expected to hit Mediterranean ecosystems hard, and these effects are already reported to be aggravated by anthropogenic warming. To date, we have a reasonably good understanding of the ecological (plant-plant interactions) and physiological mechanisms (reduced levels of evapotranspiration) that underlie forest responses to drought, yet the role of population genetic diversity remains unclear.

The genetic population literature has already documented the deleterious effects of increased inbreeding levels in both plants and animals, where high levels of inbreeding tend to correlate with declining population trends. Increased inbreeding usually arises as a consequence of frequent mating among relatives, for example due to small population sizes in deforested landscapes, and they typically entail a poor performance of highly inbred individuals compared to less inbred ones. Therefore, we would expect that individual inbreeding would influence the ability of individuals to cope with an extreme climate event, such a prolonged drought.

Specifically, we tested whether the level of individual inbreeding played a role in the response of Mediterranean juniper trees (Juniperus phoenicea) inhabiting a semi-arid ecosystem after a prolonged drought event. As expected the level of individual inbreeding negatively affected both vegetative and reproductive responses to drought, and less inbred individuals were more likely to remain unaffected than highly inbred ones. Additionally we found that neighboring vegetation alleviated the negative effects of drought, with trees growing in open sites showing increased levels of canopy damage. These results reveal the need to integrate ecological and genetic factors when studying forest responses to climate extremes.

Image caption: Juniper in different conditions. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Perspective

Are leaves more vulnerable to cavitation than branches?

Shi-Dan Zhu, Hui Liu, Qiu-Yuan Xu, Kun-Fang Cao and Qing Ye The tropical wet forest in southwestern China (photo was taken by Shi-Dan Zhu).

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Cavitation, blockage of a plant’s water conducting cells (xylem) by air, can be initiated by the entry of air through conduit pit membranes, causing embolized (air-blocked) conduits, when tension in the xylem increases during water stress. Cavitation is of importance to plants because it reduces hydraulic conductivity, which in turn impairs photosynthesis and growth. A number of studies have examined the vulnerability to drought-induced cavitation in both leaves and branches of woody plants, and a general finding is that branches are more resistant to cavitation than their terminal leaves. This is consistent with the hydraulic vulnerability segmentation hypothesis, which proposes that leaves are preferentially sacrificed to protect the hydraulic safety of branches. However, several studies have shown that leaves can be less vulnerable to cavitation than branches, indicating a Lack of Vulnerability Segmentation in these species (i.e., LVS species). Therefore, it is intriguing to evaluate how general vulnerability segmentation is in species from habitats with different climatic conditions.

Here we compiled branch and leaf hydraulic trait data for 69 broadleaved woody species from four different biomes (i.e., tropical rain forest; tropical seasonal forest; temperate seasonal forest; and Mediterranean shrub/woodland). The results showed that vulnerability segmentation was common for species from arid regions, with exceptions for some LVS species from humid regions displaying more hydraulically vulnerable branches than their leaves. Although leaves of LVS species might lose their function as “safety valves” to protect branches from hydraulic failure, they may adopt certain compensatory hydraulic strategies (e.g., wider leaf hydraulic safety margins, better water status, and greater xylem hydraulic conductivity) to achieve water balance. Therefore, with robust cavitation-resistant leaves and effective hydraulic compensatory strategies, LVS species could maintain water supply and functionality of leaves, thus giving them a competitive advantage in the face of potential drought events, such as the strong rainfall seasonality in humid regions.

Image caption: The tropical wet forest in southwestern China (photo was taken by Shi-Dan Zhu).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Land use change in the Amazon rainforest favors generalist fungi

Rebecca C Mueller, Jorge LM Rodrigues, Klaus Nüsslein and Brendan JM BohannanImage provided by authors.

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Land use change, such as conversion of native forests to agriculture, has been shown to have significant negative impacts on the biodiversity of plants and animals. Many studies have also documented the loss of specialist species and the proliferation of generalist, or “weedy” species; however, whether land use change has similar effects on microbial communities is still unclear. Because soil microbial communities are responsible for a wide range of ecosystem functions, such as nutrient cycling, understanding their responses could provide insights into the long-term effects of large-scale deforestation.

Using long-term plots established within multiple land use types in the Amazon rainforest, we quantified the response of soil fungal communities to land use change. We sampled pastures created by the deforestation of primary forest, and secondary forests generated by natural re-colonization of abandoned pastures by forest plants. We measured fungal richness and composition and identified factors associated with shifts in community composition across multiple land use types. In addition, we used distribution patterns of fungi to determine if widely distributed, generalist species were favored by land use change.

Fungal richness was significantly lower in pasture soils compared to primary forests, and the composition of the fungal community differed significantly between primary forest and pastures. Distance to primary forests was the strongest correlate of community composition in pastures, indicating that primary forests can act as reservoirs for re-colonization by native fungi. Generalist fungi were strongly favored in all pasture sites, regardless of time since conversion. The two secondary forests showed variable patterns of richness, composition, and the overall abundance of generalist fungi, suggesting that community recovery is unpredictable.

Similar to patterns documented in plants and animals, we found that fungal richness declined in pastures, with significant shifts in community composition and an associated increase in generalist species. Together, these findings suggest that the increased prevalence of generalists is a consistent response to disturbance across broad taxonomic groups.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The carbon to phosphorus critical ratio of soil microbial community demand

Petr Čapek, Petr Kotas, Stefano Manzoni and Hana ŠantrůčkovaImage provided by authors.

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Nutrient limitation of soil microbial communities is considered to play an important role in ecosystem functioning. The soil microbial community controls the decomposition of dead plant material and therefore its nutrient limitation is commonly included in mathematical models of ecosystem functioning. However, it is not always easy to recognize nutrient limitation. Therefore, guidelines to recognize nutrient limitation were defined. These guidelines are based on ecological stoichiometry theory. According to this theory, there exists a critical carbon (C) to nutrient (E) ratio of substrate that the microbial community feeds on. Above the critical ratio (C:ECR), nutrients are considered to be in insufficient amount and thus limiting. The C to phosphorus (P) critical ratio (C:PCR) that determines P limitation of the soil microbial community is largely unknown and thus it is the subject of our experimental study. Our results show that C:PCR may be extremely variable. Some soil microbial communities can have C:PCR below 30, whereas others can have C:PCR above 400. The C:PCR cannot be simply predicted for microbial communities. There are very likely many factors that affect soil microbial communities C:PCR. More studies would be needed to disentangle the controls over C:PCR. However, one unexpected result of our study is that soil microbial communities are able to store P compounds inside their cells that allow them to temporarily grow without presence of P in soil. This may represent a widely adopted strategy of soil microorganisms.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Effects of single and mixed infections of bean pod mottle virus and soybean mosaic virus on hosts and vectors

Maria Fernanda G. V. Peñaflor, Kerry E. Mauck, Kelly J. Alves, Consuelo M. De Moraes and Mark C. Mescher Arthropod vectors of viruses that infect soybean plants. Left: larval (above) and adult stages of the Mexican bean beetle, Epilachna varivestis Mulsant (Coleoptera:Coccinellidae), which transmits Bean pod mottle virus (BPMV).  Right: the soybean aphid,Aphis glycines Matsumura (Hemiptera: Aphididae), which transmits Soybean mosaicvirus (SMV). Images by Hannier Pulido (Epilachna varivestis) and Kerry Mauck (Aphis glycines).

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Plant-infecting viruses have significant impacts on human agriculture and also play important roles in the ecology of natural plant populations. Most plant viruses are transmitted by arthropod vectors, especially insects, and their spread thus depends on the nature and frequency of interactions among plants and vectors. Recent work has shown that such interactions can be influenced by virus-induced changes in ecologically relevant plant traits, such as plant nutritional and defense chemistry or plant-derived visual and olfactory cues that influence the foraging and feeding behavior of herbivorous arthropods. In many cases, the effects of viruses on such traits, and the associated changes in patterns of plant-vector interactions, appear conducive to virus transmission.

However, little is known about the ecological implications of co-infection of the same host plant by two or more viruses, even though multiple infections are common in both natural and agricultural ecosystems. To explore this issue, we documented the effects of single and mixed infection of soybean plants by bean pod mottle virus (BPMV) and soybean mosaic virus (SMV) on key biochemical plant traits and on the behaviour and performance of a beetle vector of BPMV (Epilachna varivestis) and an aphid vector of SMV (Aphis glycines). Our primary goals were to understand how virus-induced changes in plant phenotypes might influence (i) the acquisition and transmission of each virus by its respective vector in single infections, (ii) the likelihood of secondary infection for plants singly infected with either virus, and (iii) the implications of co-infection for virus transmission by vectors. We documented significant effects of each virus on ecologically relevant host-plant traits and on the preferences and performance of its respective vector (as well as effects of SMV on plant palatability for the BPMV vector E. varivestis). However, most of these effects were not observed in plants with co-infections. These results suggest that co-infection can, in at least some cases, attenuate the effects of individual viruses on plant-vector interactions and, to the extent that such effects are adaptive for the virus, may thereby reduce disease transmission.

Image caption: Arthropod vectors of viruses that infect soybean plants. Left: larval (above) and adult stages of the Mexican bean beetle, Epilachna varivestis Mulsant (Coleoptera:Coccinellidae), which transmits Bean pod mottle virus (BPMV). Right: the soybean aphid,Aphis glycines Matsumura (Hemiptera: Aphididae), which transmits Soybean mosaicvirus (SMV). Images by Hannier Pulido (Epilachna varivestis) and Kerry Mauck (Aphis glycines).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Group foraging decisions in nutritionally differentiated environments

Matthew J Hansen, Timothy M Schaerf, Stephen J Simpson and Ashley J W WardImage provided by authors.

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Food in the environment is temporally and spatially variable and much work in behavioural ecology looks at how animals adjust their foraging behaviour in order to adapt to this variation. However, food also varies in its macro-nutrient composition and studies of foraging behaviour will be more accurate if they acknowledge the extent to which animals can detect and regulate their intake of food based on these differences in food composition. Whilst theory is developing around this subject, only very recently has this theory been extended to group foraging behaviour, and there have been few empirical studies on how the distribution of macro-nutrients in the environment affects vertebrate foraging behaviour. Therefore, we monitored the movements of 8 mosquitofish as they foraged in two environments that contain equal amounts of available energy but differ in their distribution of macro-nutrients. We show that fish will distribute themselves within an environment in relation to the distribution of specific macro-nutrients. Also, fish make foraging decisions based on the macronutrient composition of patches, such that they stay longer in patches with a higher concentration of protein and lower concentration of carbohydrate. This study confirms the importance of considering the macro-nutrient composition of foods when considering the movement decisions of foraging groups, and thus has important consequences for developing more accurate foraging models that take into account the distribution of macro-nutrients in the environment. The results suggest the spatial distribution of nutrients on a landscape scale could influence grouping patterns and social interactions, thus affecting population dynamics.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Ecosystems, Evolution and Plant Soil Feedbacks

Evolution of nitrogen limitation: who you are, but not where you are, matters

Rachel Wooliver, Alix A. Pfennigwerth, Joseph K. Bailey, and Jennifer A. SchweitzerImage provided by authors.

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Nitrogen is considered to be the primary resource that limits plant growth, yet not all species respond similarly to increased soil nitrogen. That is, species’ abilities to use greater amounts of soil nitrogen for growth vary in both magnitude and direction. While some species are able to grow more, others may actually grow less as soil nitrogen increases, representing a ‘competitive’ to ‘conservative’ nitrogen-use spectrum. Species’ placements along this spectrum could help ecologists predict which species will fare better or worse as anthropogenic nitrogen deposition to terrestrial systems continues.

The ‘worldwide economics spectrum’ theory proposes an evolutionary trade-off between competitive and conservative strategies, with two opposing forces at work: 1) evolution by natural selection, with higher-resource environments selecting for more competitive resource use strategies, and 2) functional constraints, where species’ physiological characteristics limit their responses to nitrogen. Using evolutionary modeling methods and a global dataset of species’ growth responses to nitrogen addition, we aimed to determine if current variation in nitrogen use strategies among 125 plant species is consistent with the worldwide economics spectrum theory. We hypothesized that species that 1) have evolved in less stressful environments (for example, low latitudes that are warmer, wetter and nitrogen rich), and 2) are considered to be more functionally competitive (for example, annual species that can exploit short-term nitrogen fluxes), would grow more in response to nitrogen addition.

While on average species more than doubled their biomass with increased soil nitrogen, more than one in four responded negatively or not at all. Closely related species responded similarly, and models incorporating natural selection towards competitive nitrogen strategies best described our data. Importantly, we found that plant functional characteristics, more so than environmental characteristics, explain the evolution of nitrogen use strategies. In conclusion, who you are (defined by your close relatives and your functional characteristics) may be more important than where you are (defined by your resource environment) in determining plant species success as anthropogenic nitrogen deposition continues.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Nutrient inputs affect foodwebs in estuaries

Fiona Y. Warry, Paul Reich, Perran L. M. Cook, Ralph Mac Nally , James R. Thomson, Ryan J. Woodland The mouth of Wingan Inlet, Victoria, Australia; an estuary receiving relatively low inorganic nitrogen loads. Source: F. Y. Warry.

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Excess nitrogen and phosphorus from river catchments can be transported to estuaries where they can alter how these ecosystems function. The effects of elevated nutrients can include altered plant assemblage composition, plant growth and water quality which will have flow on effects for consumers such as fish. However, the effects of nutrient levels entering an estuary will be modulated by the degree of tidal exchange and freshwater flow.

We used stable isotopes of nitrogen and carbon to investigate the effect of nutrient loading on estuarine fish assemblages. The stable isotope composition of fish muscle tissue can be used to indicate its diet and therefore determine how foodwebs, or parts of foodwebs, are arranged. We used metrics derived from carbon and nitrogen stable isotope values of fish and plant tissue collected from nine estuaries to assess how foodwebs were influenced by nitrogen and phosphorous inputs.

The part of the estuarine foodweb occupied by fish became more diverse with increasing inorganic nitrogen inputs. This means fish were utilizing a larger range of nutrition sources, relative to those that were available to them. Total nitrogen and total phosphorous levels had little influence on foodweb arrangement.

The nitrogen loads received by some of our estuaries were high by global standards and were within ranges where seagrass commonly dies because it is overgrown by macroalgae (‘seaweeds’). Macroalgae can take up nutrients more quickly than seagrass so can thrive under high nutrient conditions. However, seagrass remained in all our estuaries possibly due to short water residence times. Other research in our estuaries has shown that overall there is more vegetation when inorganic nitrogen levels increase. Therefore, fish may be able to feed on a more diverse range of prey because greater amounts of vegetation may increase the productivity of small invertebrate prey, and/or fish have more shelter from predation so can be more adventurous in their feeding. The nutrient content of plants may also increase in estuaries with higher inorganic nitrogen levels, increasing their palatability to grazers with flow on effects to fish. Our results demonstrate the crucial role of nitrogen for estuarine foodweb function.

 

Image caption: The mouth of Wingan Inlet, Victoria, Australia; an estuary receiving relatively low inorganic nitrogen loads. Source: F. Y. Warry.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Review

Drivers of individual differences in the ability to transmit pathogens

Kimberly L. VanderWaal and Vanessa O. EzenwaIndividual variation in pathogen transmission potential has been examined by the authors for several savanna wildlife species, including giraffe, in central Kenya. Photo credit: Kimberly VanderWaal.

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In many outbreaks of infectious diseases, a relatively small number of individuals are responsible for the majority of new cases. One of the most famous examples is ‘Typhoid Mary’, who was responsible for 28 outbreaks of typhoid fever in the early 20th century, but there is evidence for “super-spreaders” in many other human and animal disease outbreaks, including HIV, Ebola, brucellosis and West Nile Virus. A general rule-of-thumb is that 20% of infected individuals are responsible for infecting 80% of new cases. Because this phenomenon has key implications for predicting and controlling the spread of infectious diseases, understanding the underlying mechanisms that drive individual variation in pathogen transmission potential has emerged as an important research frontier in both epidemiology and disease ecology.

In this review, we explore the impact of behavior and physiology on variation in the number of new infections produced by an individual, which we define as V. V can be affected by behavioral differences among individuals, such as gregariousness or other personality traits, and by physiological differences, including differences in immune factors, nutrition, and sex. In general, these mechanisms interact with three components that determine V: contact rates between individuals, likelihood of transmission given contact, and the length of time an individual remains infectious. Here, we synthesize scientific literature from multiple fields, and show that behavioral and physiological mechanisms have typically been examined in isolation, yielding an incomplete picture of the drivers of individual differences in transmission potential. Our review emphasizes the need for a more holistic approach for analyzing V. We also describe new tools and methods for assembling the disparate processes that contribute to individual variation in transmission potential in order to gain an improved understanding of the spread of infectious diseases in natural populations.

Image caption: Individual variation in pathogen transmission potential has been examined by the authors for several savanna wildlife species, including giraffe, in central Kenya. Photo credit: Kimberly VanderWaal.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

A time to kill: What determines when wolves kill moose?

Lucas M. Vander Vennen, Brent R. Patterson, Arthur R. Rodgers, Scott Moffatt, Morgan L. Anderson and John M. FryxellA wolf in northern Ontario (photo credit: Lucas M. Vander Vennen).

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The opposing goals of predators and prey can lead to dynamic behavioural interactions, wherein predators attempt to increase predation success and prey try to decrease predation risk. These interactions give rise to many of the predator-prey behaviours we see today, but our understanding of these patterns is often limited by knowledge of what influences predator success and prey risk. Here we look at predator and prey interactions between wolves and moose over the course of the 24-hour daily cycle. We use data from GPS collars to investigate what factors drive the rates at which wolves kill moose. We found wolf-killed moose using wolf collar data, and examine how the temporal pattern of these kills is related to wolf movement, moose movement, and ambient light conditions throughout the period of the 24-hour cycle. We found that kill rate is very well explained by the combined movement speeds of wolves and moose, such that higher movement rates correspond to higher kill rates. This relationship has often been applied to these types of interactions, but our work represents the first field-based test. Interestingly, this effect of movement speed is almost entirely driven by wolves, with very little input from moose. Wolves moved over ten times faster than moose, and so had a much greater influence on their overall combined velocity. Kill rates were not influenced by light conditions, but instead were almost entirely driven by wolf movement rates. While moose may have influence on predation through behavioural adjustments (e.g. vigilance or selecting habitats that provide protection during risky times of day), this indicates that the prey in this system are not able to adjust their predation risk by being active at different times of the day.

Image caption: A wolf in northern Ontario (photo credit: Lucas M. Vander Vennen).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Using nutritional geometry to study the effects of parental diet on offspring

Russell Bonduriansky, Aidan Runagall-McNaull, Angela J. CreanNeriid flies feeding on damaged tree bark in Sydney, Australia.

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You’ve probably heard that you are what you eat, and may even have heard that you are what your parents ate. But the truth is that we still know very little about how an individual’s diet affects the viability, health and features of its offspring.

Part of the problem is that past studies have compared the effects of just two or three kinds of food. They have also tended to focus on the effects of mother’s diet, typically ignoring the father altogether.

But we all know that diets are complex and variable, and their effects can be decidedly nonlinear: two sausage rolls a month might make no noticeable difference to your health, but ten sausage rolls a month might do serious damage. Moreover, recent studies have shown that what fathers eat (for example, how much fat they consume) can indeed affect their offspring, but very few attempts have been made to compare the effects of nutrients in maternal and paternal diets.

We tackled these gaps in knowledge using an approach called “nutritional geometry,” which involves raising experimental subjects on many different diets consisting of different nutrient ratios and concentrations. Nutritional geometry has been used in many previous studies to determine how individuals are affected by their own diet, but we used this approach for the first time to investigate how parental diet affects offspring, and we did this for both maternal and paternal diets. For this experiment, we used a beautiful Australian neriid fly that has served for several years as our “guinea pig” in research on the effects of diet within and across generations.

All this work paid off: We found that macronutrients (protein and carbohydrate) in maternal and paternal diets can have very different (indeed, sometimes opposite) effects on offspring. We were also able to show that the effects of parental diets can be highly non-linear, and that different dietary nutrients can interact in their effects on offspring. We hope that our work will inspire other researchers to use nutritional geometry in studies on the effects of parental diet.

Image caption: Neriid flies feeding on damaged tree bark in Sydney, Australia.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

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