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

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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.

 

 

Colour pattern mimicry in flowers- the functional importance of complex floral colour pattern in a food-deceptive orchid

Xiaokai Ma, Jun Shi, Hans Banziger, Yangna Sun, Yanyan Guo, Zhongjian Liu, Steven D. Johnson and Yibo Luo Mimic (silver slipper orchid Paphiopedilum micranthum, centre) and its co-occurring food flowers on a background of their habitat, framed in bee hexagonal vision.  Image courtesy of Xiaokai Ma.

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Mimicry, where one species evolves to resemble another, unrelated species, is a renowned textbook example of natural selection and adaptation. Mimicry is often based on imitation of special visual patterns, such as the gorgeous colour patterns on wings of butterflies and body surface of snakes. Flower mimics, which are widespread among plants, often dupe animal pollinators by providing no reward (i.e. nectar), but imitating the colour of nectar-providing flowers that share the same habitat. Moreover, both the mimics and the food flowers often display complex colour patterns, including contrast between outer and central flower parts, that could be discriminated by pollinators.

To detect whether the colour pattern is the key to flower mimicry, we tested the effects of floral colour patterns in the silver slipper orchid, Paphiopedilum micranthum, on pollinator bumblebee choices and pollination success using behavioural tests in a community context. Using a bee vision model and evolutionary analysis, we also compared the colour patterns of the orchid with those of its relatives, and the food flowers that it mimics.

Our results reveal that orchid pollination success might be enhanced by colour patterns that mimic those of food flowers in the local community. Such mimicry enhances attraction of the orchid to bumblebees. Experimental disruption of the colour pattern clearly hampers decision-making by bumblebees, and this decreases pollination success of the orchid. Evolutionary analysis indicate that the colour pattern of orchid mimics might have been shaped by multiple evolutionary histories, including evolutionary innovation of the outer floral colour and a pre-adaptation of the ancestral centre floral colour.

Our study is novel in its inclusion of colour pattern in the study of floral mimicry in the context of the associated plant community, and provides the first detailed evidence for the functional importance of colour pattern mimicry for a deceptive flower. This finding advances our understanding of the evolutionary processes governing floral deception via the functional significance of colour pattern traits that influence signalling efficacy. This highlights the importance of complex signals in facilitating species interactions.

Image caption: Mimic (silver slipper orchid Paphiopedilum micranthum, centre) and its co-occurring food flowers on a background of their habitat, framed in bee hexagonal vision. Image courtesy of Xiaokai Ma.
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.

Special Feature: The functional role of silicon in plant biology

Molecular evolution of aquaporins and silicon influx in plants

Rupesh Deshmukh and Richard R. BélangerHorsetail plant (Equisetum arvense) in the field (left). Scanning electron micrograph of horsetail leaf (top right) and X-ray microanalysis mapping of silicon presence (bottom right).

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Silicon (Si) is one of the most abundant elements in the earth crust, but whether it is essential for plant growth remains a matter of debate. Plants take up Si through the roots in the form of silicic acid, and can accumulate concentrations as high as 10% on a dry weight basis. Nevertheless, most plants (with the notable exception of horsetail) can complete their life cycle without Si. For this reason, Si is not considered an essential element, in spite of the multiple studies that have shown its beneficial role for plants, especially under conditions of biotic and abiotic stress.

The benefits plants derive from Si are well correlated with their ability to take up Si from the soil, and this ability varies greatly among plant species. In the context of better defining the ecological role of Si in plants, it thus becomes very important to understand which and how plant species can take up silicon.

Si uptake in plants depends on two specific proteins, an influx transporter and an efflux transporter, both with unique characteristics. Recent studies suggest that the presence of an influx transporter is the indispensable key for a plant to be able to absorb Si. Based on DNA sequence analyses and comparisons, influx transporters appear to bear conserved features that allow us to classify plant species as Si-competent or not. While it is unclear how and why plants have acquired or lost this trait, genomic data now offer a reliable molecular tool to predict with accuracy which plant species are predisposed to benefit from Si. This work presents a detailed review of the molecular features inherent to Si influx in plants, a property that has a profound impact on Si biogeochemical cycling and the role of Si in many fundamental aspects of ecology.

Image caption: Horsetail plant (Equisetum arvense) in the field (left). Scanning electron micrograph of horsetail leaf (top right) and X-ray microanalysis mapping of silicon presence (bottom right).
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.

 

How do precipitation gradient and evolutionary history shape the variations in leaf and root traits in the Inner Mongolia grassland?

Junhui Cheng, Pengfei Chu, Dima Chen and Yongfei BaiRoot systems of six grasses widely distributed in the Inner Mongolia grassland.

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The attributes of leaves and roots are fundamental for understanding different strategies that plants use to acquire resources, like water, soil nutrients, and light, in different environmental conditions. This is important because these resource acquisition strategies are essential for species coexistence, community assembly and functioning of terrestrial ecosystems. Species with less dry matter investment per leaf area and root length have high growth rate but short life span, indicating a resource acquisitive strategy. In contrast, species with high dry matter investment per leaf area and root length have low growth rate but long life span, suggesting a resource conservative strategy. It has been assumed that variation in environmental factors (e.g. precipitation and temperature) and evolutionary history (species divergence time on the evolutionary tree) shape both leaf and root traits. The branching architecture of fine roots also affects the functional role of living roots, such as acquisition and transport of water and nutrients. However, few studies have examined the effects of evolutionary history and environmental gradients on species leaf and root traits, or considered how plants are able to access increasingly scarce resources like water and nutrients as climate shifts from relative moist to very arid?

In this study, we examine how leaf and root traits vary across 55 species and 21 plant communities along a 2,000-km transect in the Inner Mongolia grassland, part of the largest contiguous grassland in the world, the Eurasia steppe. Our results suggest that acquisition of soil resources, such as water and nutrients, is a fundamental determinant of plant dry mass investment per root length in arid and semiarid grasslands. Across the transect, species that evolved relatively late tended to have high dry matter investment per leaf area and root length for the first root branching order, and were distributed in dry and infertile habitats, while earlier-evolving species exhibited low dry matter investment per leaf area and root length and were found in wet and fertile habitats. These findings provide new insights for predicting the response of species and ecosystems to changes in temperature and precipitation in arid and semiarid grasslands.

Image caption: Root systems of six grasses widely distributed in the Inner Mongolia grassland.
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.

 

Cold adaptation in insects involves adaptive modifications of the cell membrane phospholipid composition

Stine Slotsbo, Jesper G. Sørensen, Martin Holmstrup, Vladimir Kostal, Vanessa Kellermann and Johannes OvergaardThis photo shows different fruit flies along a cold tolerance gradient, and how the phospholipid fatty acids in the membrane are expected to become more unsaturated with increasing cold tolerance. Photo provided by Heath A. MacMillan.

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Maintaining function and structural integrity of cell membranes is central for the performance and survival of animals. Because temperature influences the physical properties and fluidity of animals’ biological membranes it is hypothesized that temperature stress may compromise membrane function. In accordance with this hypothesis it is often found that acquisition of thermal tolerance following acclimation involves modifications of the cell membrane lipid composition. Each membrane phospholipid consists of a head group attached to two fatty acids, and modification can be in type of head group, types of fatty acids, or a combination of these factors. Membrane modifications are associated with changes in the membranes' physical properties such that appropriate function is secured at the acclimation temperature. Parallel differences in membrane lipid composition have been found between species and between populations of insects that are adapted to different thermal environments. However, there are few large multi-species studies that investigate directly the interspecific association between membrane lipid composition and thermal tolerance in insects.

Here we present the most comprehensive interspecific investigation of phospholipid fatty acids composition within insects (and cold-blooded animals in general). Using 57 species of fruit flies originating from both temperate, subtropical and tropical environments we found clear differences between species in phospholipid fatty acid composition. When we related these differences to species’ cold tolerance, which constitute a powerful proxy for their cold distribution limits, we found that phospholipid fatty acids could explain more than 20 % of the variation in cold tolerance found between species. Considering that a number of other important membrane parameters (phospholipid head group composition and concentration of sterols and other lipid components) were not measured, our finding highlights that phospholipid fatty acids and membrane adaptations in general play a highly significant role in thermal tolerance in insects.

Image caption: This photo shows different fruit flies along a cold tolerance gradient, and how the phospholipid fatty acids in the membrane are expected to become more unsaturated with increasing cold tolerance. Photo provided by Heath A. MacMillan.
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.

 

Macronutrients, weapons and genital traits in male broad horned beetles

Clarissa M. House, Kim Jensen, James Rapkin, Sarah Lane, Kensuke Okada, David J. Hosken and John Hunt Male Gnatocerus cornutus fight using an enlarged mandible which is a secondary sexual trait. Photo credit: Matthew Silk.

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The calorific content and the nutritional composition of food that is acquired from the environment is likely to be vitally important for individual survival, growth and morphology (i.e. the physical characteristics of an animal). This could be especially important if the nutritional requirements of traits differ, such that the optimization of one trait occurs at the expense of another, and therefore trade-offs occur due to nutrient imbalance in the diet that is consumed. In this study we used 24 well-defined, artificial diets to test the sensitivity of a flour beetle, Gnatocerus cornutus, to variation in the calorific content and ratio of two major nutrients, protein (P) and carbohydrates (C) consumed during larval development to adulthood. We found that extreme calorific restriction was fatal or slowed the rate of development. However, beyond a minimum amount of food, the ratio of consumed macronutrients was critically important for the size of the morphological traits that we measured. Male weapons grew most in response to the consumption of P and in particular C whereas the genitalia had the weakest response. Even though different traits grew at different rates the P:C ratio that maximized survival, development rate and the size of all morphological traits was 1:2. This shows that the balance of P:C in the diet that is optimal for survival also optimizes development rate and the size of all morphological traits. Therefore as the nutritional needs of the different traits are similar, the balance of P:C in the diet of this beetle is unlikely to lead to trade-offs. Nonetheless, nutrition will have lasting effects on male fitness as larvae that develop on optimal diets developed fastest and were larger adults with larger weapons and small genitalia, which confers an advantage in male-male competition, access to mates and insemination success.

Image caption: Male Gnatocerus cornutus fight using an enlarged mandible which is a secondary sexual trait. Photo credit: Matthew Silk.
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.

 

Why baby birds differ in the speed at which they grow?

Riccardo Ton and Thomas E. MartinSometimes bird nests are not easily reachable, and creative thinking is required to access their contents. Photo provided by authors.

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Baby songbirds grow at very different speeds. In particular, tropical species tend to grow more slowly than similar species in temperate regions. Understanding why is important because speed of growth can have important consequences for the future and survival of the offspring. Growing slowly can be good and give baby birds time to better develop important organs like the brain, muscles and feathers. However slow growth also increases the probability that a predator like a snake or a hawk will find and eat the babies. Conversely, growing quickly helps a baby bird leave the nest early and avoid predators but with organs of lower quality. Despite these implications for survival, it is still unclear why baby birds differ in the speed at which they grow.

Generally babies of bigger species grow more slowly than those of smaller species. However, songbirds tend not to follow this natural rule. A possible explanation is that metabolism, the set of biochemical reactions that occur in each cell of a living organism, may be the engine propelling growth, but available data on this topic are contradictory. The oxygen that organisms breathe fuels this engine; therefore, if metabolism is the mechanism promoting growth, species that consume more oxygen should grow faster.

To test the hypothesis that metabolic rate may regulate differences in growth, we measured the oxygen consumed by baby birds sleeping on a nest inside a dark chamber for 59 species in three different continents. We sampled fast growing species in Arizona, USA, slow growing species in tropical Malaysia, and species that grow at intermediate speed in South Africa.

We found that, for a given body size, growing baby birds from Arizona consumed substantially more oxygen (had higher metabolism) than species from Malaysia or South Africa. We also found that babies of species consuming more oxygen grew faster compared to those species with lower metabolism. Finally, we observed that when differences in metabolism among species were accounted for, baby songbirds do follow the natural pattern that bigger species grow more slowly. However the reasons why metabolism differs among species and latitudes remain unclear and should be the focus of further studies.

Image caption: Sometimes bird nests are not easily reachable, and creative thinking is required to access their contents. 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.

 

Effects of neonatal size on maturity and escape performance in the Trinidadian guppy

Terry Dial, David Reznick and Elizabeth BrainerdImage provided by authors.

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Newborn offspring are always smaller than the parent, but not all offspring are born the same size or same level of maturity, so what factors ultimately control the evolution of offspring size? Parents balance the tradeoff between offspring size and offspring number, and the optimal balance depends largely on the environment.

In response to high predation pressure by large predatory fish, Trinidadian guppies produce lots of small babies, flooding their environment with numbers. Above waterfall barriers, in environments with low or no predation, guppies produce fewer, larger babies.

To avoid a predator, fish will initiate an escape start by first bending their body into a C-shape and then undulating out of it, away from the threat. In other fish studied, larger individuals are known to produce higher performance escape starts. Thus, it is somewhat paradoxical that an adaptation to living with predators is to produce babies that are born with an inherent size disadvantage, but are they?

Here we measure escape performance of newborn guppies from five populations adapted either to low predation, high predation, or extreme high predation environments. We also measured detailed morphology, both external and internal, to assess whether these offspring possess different body proportions or levels of maturity. We find that those fish responding maximally to our stimulus perform at the upper limit for their size, and that both size and maturity influence this escape performance limit.

The smallest guppies are extremely slow at performing the escape start, even for their size, and these smallest offspring are also less developmentally mature compared with their larger counterparts. Within the Trinidadian guppy, it appears that both size and maturity tradeoff with number of offspring, and that offspring abundance outweighs performance in environments with the highest predation pressure.

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.

 

Wood decomposition inside living trees shows that hollows develop slowly but cause a considerable loss of forest biomass

Zheng Zheng, Shubin Zhang, Carol Baskin, Jerry Baskin, Doug Schaefer and Xiaodong Yang Zhang Shubin is sampling decaying wood from a living tree hollow for measurement of its decay rate by CO2 release, in the Ailao Mountain Forest of China. Picture by Zheng Zheng.

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Living trees with decayed hollows provide nesting places for animals, especially in old-growth forests throughout the world. These hollows are formed by microorganisms that enter wounds in trunks or large branches and then decompose heartwood. Formation of tree hollows appears to be a slow process because tree hollows usually are found in large trees. However, large hollows formed in some trees indicates that wood decomposition rates there can be high compared to tree growth rates, and that hollow trees store less carbon. While abundance and use by animals of tree hollows have been well studied, the rates at which they form have not been measured.

In an old-growth subtropical montane forest preserve in southwest China, we measured decomposition rate of wood within tree hollows. From this we estimated the time required to form them. Wood inside tree hollows decomposed about half as fast as decomposing wood on the forest floor. Decomposition was slower because this wood was drier, and had higher density. Tree hollows enlarged by 2 mm per year on each side horizontally and about 8 times faster than that vertically. At that rate it would take 100 years for hollows to become large enough for nests of a local bee species. In addition, decomposition inside hollow trees means stems of living trees in this forest have lost 8·7% of their biomass.

Image caption: Zhang Shubin is sampling decaying wood from a living tree hollow for measurement of its decay rate by CO2 release, in the Ailao Mountain Forest of China. Picture by Zheng Zheng.
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.

 

Black and yellow plumage signals resistance to oxidative stress in a bird

Amberleigh E. Henschen, Linda A. Whittingham, and Peter O. Dunn Photo by Matt Tillett. Flickr: via Wikimedia Commons. CC BY 2.0.

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Choosing a healthy mate is a vital part of female reproductive success as healthier mates may provide benefits to females, such as a better territory or ‘good genes’ that will be inherited by offspring. Male ornaments can help females choose wisely as these often elaborate traits may honestly advertise male health. In particular, it has been suggested that healthier males will have more effective immune systems and efficient metabolism, which will lead to the production of fewer free radicals (e.g., Oxygen ions and hydrogen peroxide). An excess of free radicals leads to an imbalance in cells called oxidative stress, which can damage cells and lead to poorer quality ornaments. Therefore, it is hypothesized that elaborate male ornaments honestly signal the ability of a male to produce immune responses that do not result in oxidative stress. We tested this hypothesis in the common yellowthroat, a warbler in which males have two ornaments, a black face mask and a yellow bib. These ornaments have been studied in both Wisconsin (WI) and New York (NY) and where females choose mates based on the size of the black mask and the size and color of the yellow bib, respectively. As the yellow bib is an honest indicator of oxidative stress in NY, our aim was to determine if the black mask signals similar information in WI. We assessed oxidative stress in males by measuring how resistant red blood cells from each male were to free radicals as well as oxidative stress in the plasma, or non-cellular portion of the blood. As predicted, we found that males with larger masks had red blood cells with greater resistance to oxidative stress. Furthermore, males with larger and more colorful bibs had lower levels of free radicals in the plasma. These results are consistent with the hypothesis that male ornaments indicate the ability of males to manage oxidative stress, but perhaps not in all components of the blood. Photo caption: Male common yellowthroats have two plumage ornaments, a black mask and yellow bib, which are used by females to choose mates. In this study, the authors found that each ornament was related to different measures of the ability to manage oxidative stress.

Image caption: Photo by Matt Tillett. Flickr: via Wikimedia Commons. CC BY 2.0.
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.

 

Every plant needs good neighbours

Henry E. Creissen, Tove H. Jorgensen and James K.M. BrownFour different Arabidopsis genotypes competing whilst under disease pressure.

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The relationship between plant diversity, ecological stability and ecosystem productivity has been studied extensively in recent decades. Plant herbivores, diseases and insect pests alter such relationships by affecting plant fitness, reducing the growth and competitive ability of diseased plants. This can impact heavily upon plant population and community structure. Yet, despite their importance, experimental tests of mechanisms of pathogen-induced changes to plant competitive ability, productivity and diversity are rare.

We conducted competition experiments involving different genotypes of a small plant (Arabidopsis thaliana) to examine the relationships between population diversity, composition, productivity and stability in diseased and non-diseased plant populations. Plant genotypes varied greatly in both competitive ability and response to two pathogens, a virus and an oomycete. In certain populations we observed compensatory competitive interactions in which some genotypes increased productivity and compensated for the loss of yield by others. These interactions ultimately resulted in increased stability and productivity of the population as a whole. This study shows the importance of pathogen-mediated competition in maintaining plant genotypic diversity and productivity. A key finding is that the genotypic composition of the plant population, specifically the presence and maintenance of resistant genotypes within that population, is responsible for the capacity of the population to maintain productivity, stability and diversity.

As well as increasing our understanding of natural processes occurring in genotypically and phenotypically diverse plant populations, this study has potential applications to agriculture by demonstrating methods that can inform decisions about suitable plant cultivars for cultivation as variety mixtures.

Image caption: Four different Arabidopsis genotypes competing whilst under disease pressure.
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.

 

Feed or fight: Testing the impact of food availability and intraspecific aggression on the functional ecology of an island lizard

Colin M. Donihue, Kinsey M. Brock, Johannes Foufopoulos, and Anthony HerrelPodarcis erhardii from the Greek Islands with tell-tale bite scar on its belly.

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Islands are often considered ideal biological laboratories as they are isolated and vary tremendously in size, structure, and habitats. These factors impose different selective pressures that can drive adaptations of organisms on islands. Our study capitalizes on an island-size gradient in the Greek Archipelago to investigate inter-island divergence in the body size, head shape, and bite force of a lizard, Podarcis erhardii.

We hypothesized that strong bites would be an advantage for lizards on small islands. For example, a strong bite might enable that lizard to eat relatively hard or large insects, so if food resources were sparse on a small island the lizard might not starve. A harder bite might also enable the lizard to win fights with the other individuals competing for the same valuable resources like food, mates, or nesting sites on a small island where lizard densities are often high.

We caught lizards on 11 islands in the Greek Cyclades ranging in size from 0.004 to 450 km2. We measured the lizards’ body and head size, and measured bite force. We then flushed their stomachs to see what they were eating and compared the stomach contents to insects we caught in traps. Finally, we counted the bite scars and lost toes, which typically result from battles with other lizards (see inset picture for an example bite scar).

We found, first, that bite force did increase on small islands. Second, we found that the competition indicators, i.e., bite scars and lost toes, best predicted the pattern in bite force. Hardness of prey in the diet did not vary significantly between lizards on these different islands. These results shed new light on the drivers of body size and performance differences among island populations.

Image caption: Podarcis erhardii from the Greek Islands with tell-tale bite scar on its belly.
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.

 

Individual-level trait diversity indices

Simone Fontana, Owen L. Petchey and Francesco Pomati© Studio Asparagus.

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As humans, we are increasingly concerned about the potential effects of our activities on the structure and functioning of ecosystems. The challenge is to understand if ecosystems will be able to maintain processes and essential functions in a future of lasting human impact (e.g. climate change, pollution). The effects of human-induced environmental change on ecosystem processes might be direct or mediated by changes in the living organisms.

For this reason, researchers are increasingly considering traits (measurable features of individual organisms, e.g. morphological and physiological characteristics) as a powerful way to explain processes in ecological systems. However, traits are generally assumed not to vary at the species level, thus disregarding the importance of differences between individuals belonging to the same species.

Our approach considers both differences among individuals and multiple traits at the same time: each individual is placed within a space defined by every measured trait (axes). Thus a species occupies a ‘cloud’ in trait space, and there are basically three different ways to quantify this cloud; trait richness (= trait space occupied by individuals in a community), trait evenness (= regularity in the distribution of individuals within the trait space) and trait divergence (= how spread-out are individuals within the trait space). These characteristics can in turn be measured by various indices, and we can define how we expect each index to change (increase/decrease) if individual organisms are deleted or moved within the trait space. We tested different indices using simulated and real phytoplankton data, to find those with the most appropriate behaviour (that is, the ones changing as expected as a result of our manipulations). The resulting validated set of indices includes FDis (trait divergence) and two newly proposed metrics: TOP (= Trait Onion Peeling; trait richness) and TED (= Trait Even Distribution, trait evenness).

These three components of trait diversity, used in a complementary approach, may shed light on the importance of differences among individuals in natural ecosystem processes and improve our understanding of the pathways by which environmental changes affect ecosystem functioning through biodiversity change.

Image caption: © Studio Asparagus.
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.

 

Water use by Swedish boreal forests in a changing climate

Thomas B. Hasper, Göran Wallin, Shubhangi Lamba, Marianne Hall, Fernando Jaramillo, Hjalmar Laudon, Sune Linder, Jane L. Medhurst, Mats Räntfors, Bjarni D. Sigurdsson, Johan UddlingSwedish boreal landscape (left; © Thomas B. Hasper) and Flakaliden Whole-Tree Chamber Experiment (right; © Bengt-Olof Vigren).

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The ongoing increases in atmospheric carbon dioxide concentration ([CO2]) and temperature have the potential to alter the flux of water vapor through plant leaf ‘stomata’, tiny and actively regulated pores in the leaf surface. This flux, transpiration, in turn regulates the terrestrial water and energy balance and, thus, influences local and regional hydrology and climate.

Combined stomatal-photosynthesis models employed in ecosystem and climate models predict decreases in stomatal conductance and land evapotranspiration (ET) at elevated [CO2]. This stomatal water-saving response to increased [CO2] has been used to explain the observed increase in global river runoff during the past century. Plant water use is, however, also affected by changes in air temperature, precipitation and land-use, and there is yet no consensus about the contribution of different drivers to temporal trends of ET and river runoff.

In this study, we examined the water-use responses of Swedish boreal forests to climate change by using long-term monitoring as well as experimental data. We used climate and runoff data of large-scale boreal landscapes from the past 50 years to explore historical trends and patterns in ET. In addition, we examined explicit tree water-use responses to elevated [CO2] and/or air temperature in a whole-tree chamber experiment using mature Norway spruce trees.

The results demonstrated that ET increased by 18% over the past half century while river runoff did not significantly change. The increase in ET was related to increasing precipitation and a steady increase in forest standing biomass over this period. The whole-tree experiment showed that Norway spruce trees did not use less water under elevated [CO2] and that elevated air temperature did not increase plant transpiration as decreased stomatal conductance neutralized the effect of higher evaporative demand in warmed air.

Our findings have important implications for projections of the future hydrology of European boreal coniferous forests, indicating that changes in precipitation and standing biomass are more important than effects of elevated [CO2] or temperature on tree transpiration rates.

Image caption: Swedish boreal landscape (left; © Thomas B. Hasper) and Flakaliden Whole-Tree Chamber Experiment (right; © Bengt-Olof Vigren).
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.

 

Nitrogen deposition affects Scots pine stoichiometry

Jordi Sardans, Rocio Alonso, Ivan Janssens, Jofre Carnicer, Stavros Vereseglou, Mathias Rillig, Marcos Fernández-Martínez, Tanja Sanders and Josep Peñuelas Pinus sylvestris forests at the Southern limit of its distribution area, such as in this photo in a Pyrenees valley, are subject to several stresses, from drought to excess light, that threaten their survival. The impacts of these stresses on plant-soil nutrient cycles and nutrient ratios can be crucial for the future of this species in several parts of Europe. Credit Dr. Oriol Grau.

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The spatial and temporal patterns of nitrogen (N) and phosphorus (P) concentrations and of N:P ratios in terrestrial plant communities have been shown to be related to several ecosystem processes. Little is known, however, about the flexibility of N and P concentrations or of N:P ratios in terrestrial plant species along their natural ranges of distribution in response to natural and anthropogenic gradients, or of their ecological significance. Pinus sylvestris (Scots pine) is one of the most important forest species in Eurasia, with a broad distribution extending from Spain to Siberia. This broad distribution across Europe offers a unique opportunity to study the relationships between soil and plant nutrient concentrations, and how these vary with climate, atmospheric N deposition and plant growth. In this study, we investigated needle N and P concentrations, N:P ratios and soil elemental composition and their shifts in response to climatic gradients and atmospheric N deposition in P. sylvestris forests. We also investigated the relationship of these variables with P. sylvestris growth by analyzing a compiled dataset of 2245 stands of P. sylvestris throughout Europe. The results showed that N deposition was positively correlated with needle N concentration and N:P ratio and negatively with needle P concentrations. This was especially pronounced at sites where high levels of N deposition coincided with higher mean annual temperature and higher mean annual precipitation, such as in central Europe. Atmospheric N deposition was also negatively correlated with soil plant-available P and K concentrations. Higher soil-solution nitrate:P ratios coincided with higher needle N:P ratios at higher levels of N deposition. The relationships between needle and soil-solution nutrient concentrations indicated that other elements, such as potassium, could also be involved in soil nutritional disequilibrium. Despite these nutrient imbalances, N deposition was positively related to Pinus sylvestris absolute basal diameter growth.

These results thus indicate a tendency of European P. sylvestris forests to store N in trees and soil in response to N deposition, and strongly suggest a trend toward increased nutrient losses in runoff related to higher soil-solution N concentrations.

Image caption: Pinus sylvestris forests at the Southern limit of its distribution area, such as in this photo in a Pyrenees valley, are subject to several stresses, from drought to excess light, that threaten their survival. The impacts of these stresses on plant-soil nutrient cycles and nutrient ratios can be crucial for the future of this species in several parts of Europe. Credit Dr. Oriol Grau.
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.

Special Feature: The functional role of silicon in plant biology

The Importance of Agriculture in Global Biogenic Silicon Production

Joanna C. Carey and Robinson W. FulweilerCorn farm in central Pennsylvania. Photo: fishhawk via Flickr (CC BY).

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Our human footprint on the Earth is so large that many scientists assert we have ushered in a new geological epoch – the Anthropocene. Human impacts on the Earth are well-documented. We have cut down forests, dammed rivers, overfished the seas, and added enough extra carbon dioxide to our atmosphere to increase global temperatures. We have also fundamentally changed how we grow our food. Industrialized agriculture has altered a range of ecosystem processes, perhaps the most fundamental of which is nutrient cycling. While the impacts of agriculture on the nitrogen and phosphorus cycles are well-described, we know much less about how agriculture has changed the global silicon (Si) cycle.

We care about Si for many reasons. Weathering of silicate rocks plays a key role in regulating atmospheric carbon dioxide concentrations over long time periods. Additionally, Si is an essential nutrient for diatoms, small photosynthetic plankton (think ‘grasses of the sea’) that consume carbon dioxide. Diatoms also support economically, nutritionally, and culturally important marine food webs. Si also turns out to be a ‘quasi-essential’ nutrient for land plants, as it protects them from stressors such as drought, herbivory, and heavy metal toxicity.

Land plants take up dissolved silica and it becomes deposited within their tissues as biogenic Si. Agricultural crops account for approximately 35% of the biogenic silica fixed globally by land plants, not only because of their large biomass, but also because they tend to have high Si concentrations in their tissues. In the last fifty years (1961-2012) biogenic silica production in the ten most productive agricultural crops has more than tripled, and we predict that by 2050 biogenic silica production may increase by another 50%.

Compared to mineral silicates, biogenic silica is considered ‘bio-available’ and is rapidly regenerated and available for subsequent uptake by terrestrial or aquatic organisms. In turn, the substantial increase in biogenic silica production is augmenting the reservoir of biologically available Si on Earth. As a result, the fate of the biogenic silica removed from agricultural areas via plant harvest is important, with implications for global carbon cycling and marine food webs.

Image caption: Corn farm in central Pennsylvania. Photo: fishhawk via Flickr (CC BY).
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.

 

Unseen consequences of losing large wildlife: increases in rodent immune function following large mammal defaunation

Hillary S. Young, Rodolfo Dirzo, Kristofer M. Helgen, Douglas J. McCauley, Charles L Nunn, Paul Snyder, Kari E. Veblen, Serena Zhao and Vanessa O. EzenwaZebras. Photo provided by authors.

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Ecosystems around the world are losing large wildlife due to overexploitation, development of agriculture, and increased human densities. While research has examined the consequences of losing large-bodied animals for the abundance and composition of the smaller animals that remain, little research has considered how these changes affect animal physiology. This is a critical oversight because changes in animal physiology can have enormous consequences for ecosystem functioning and processes, including spread of disease.

We examined the effect of large wildlife removal on immune function in rodents using a large-scale exclosure experiment in Kenya, where high voltage electrified fences have effectively remove all large wildlife from plots for the past 20 years. Examining a suite of immune parameters in the most common mouse species in these plots, we found evidence of significant increases in immune function of rodents when large wildlife are absent. This effect may result from a higher number of parasites in defaunated ecosystems, which drives an increase in need for immune protection. Alternatively, observed changes may result from increased food availability in the landscape when large herbivores are removed, which allows for more energy to be devoted to immune functions. Either way, our research indicates that loss of large wildlife could have major consequences for rodent-borne disease dynamics via changes in immune function. For example, such changes may reduce the likelihood that increased parasite density in landscapes without large wildlife may translate to realized increases in disease prevalence in rodents.

Image caption: Zebras. 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.

Special Feature: Mechanisms and consequences of facilitation in plant communities

Facilitation among plants as an insurance policy for diversity in Alpine communities

Lohengrin A. Cavieres, Carolina Hernández-Fuentes, Angela Sierra-Almeida and Zaal Kikvidze  Laretia acaulis cushion harbouring native grasses in the high alpine of central Chile Andes.

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Positive interactions among plant species occur when the presence of one plant species enhances the chances that another species co-occurs in the same place, indicating that positive interactions may determine biological diversity. Although early research focused on (negative) interactions such as competition and predation as the main factors structuring plant communities and regulating biological diversity, positive interactions have started to gain a place in the ecological literature. However their role in determining diversity at different spatial scales has been poorly explored.

Nurse plants are those that provide shelter to other plant species from environmental severity (e.g. strong winds, extreme low temperature, etc.) or herbivory, and are one of the most commonly recognized examples of positive interactions among plants. It has been suggested that the presence and importance of nurse plants are higher in environmentally severe environments such as alpine or desert habitats, where the mitigation of extreme conditions by the nurse species can be beneficial to many other species.

The majority of the studies addressing the consequences of nurse plants for diversity have compared the diversity of plant assemblages growing within nurses vs. those growing outside them, reporting contrasting results among them. Nonetheless, nurses and their alternative microhabitats (open areas between nurses) are part of the same community. Thus, if nurses allow for the persistence of species that otherwise would be excluded, a net increase in species diversity of the whole community will be generated even if areas under nurse plants contain fewer species than the open areas outside them.

In this study we conducted a bibliographic search using the ISI-Web of Knowledge database and reviewed the literature on alpine plant communities where assessments of the diversity of plants growing within and outside nurse species were available. We found that in most cases, nurse species substantially increased species richness, despite the fact that in some cases they contained lower species numbers than surrounding open areas. Strikingly, nurse species enhanced species richness more in sites with more severe environmental conditions, suggesting that facilitative interactions in alpine habitats act as an insurance policy that sustains diversity under very harsh environmental conditions.

Image caption: Laretia acaulis cushion harbouring native grasses in the high alpine of central Chile Andes.
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.

 

Perturbations in growth trajectory due to early diet affect age-related deterioration in performance

Who-Seung Lee, Pat Monaghan and Neil B. MetcalfeMale (left) and female (right) three-spined sticklebacks.

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Dietary conditions affect the growth rates of organisms, which in turn influences future survival and reproduction. Animals can often compensate for a period of slow growth early in life by accelerating their growth when conditions improve, resulting in normal adult size, but this rapid growth can prove costly in later life. In this study we investigated whether this compensatory growth has long-term consequences for patterns of senescence. Using a small species of fish, the three-spined stickleback (Gasterosteus aculeatus), we showed that a brief period of reduced food availability in early life affected skeletal growth rate not only during the manipulation itself, but also during a subsequent compensatory phase when fish caught up in size with controls. However, fish that had gone through this period of growth acceleration had a faster decline in their swimming performance and a shorter period of breeding over the following two breeding seasons, suggesting that they were ageing faster. This was confirmed by their having a shorter lifespan. The effects were strongest if the acceleration of growth happened just before the breeding season. These results, complementary to those found when growth trajectories were altered by temperature rather than dietary manipulations, show that the costs of accelerated growth can last well beyond the time over which growth rates differ.

Image caption: Male (left) and female (right) three-spined sticklebacks.
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.

 

Flowers avoiding bees? The case of Costus arabicus colour variation sheds light on bee sensorial exclusion hypothesis for hummingbird red-flowers

Pedro Joaquim Bergamo, André Rodrigo Rech, Vinícius L. G. Brito and Marlies SazimaPink flowers of Costus arabicus, presumably avoiding bee-pollination.  Photo credit: Camila Silva Oliveira.

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Floral colour plays a role in plant-pollinator communication by signalling floral resources. Hummingbirds are often associated with red coloured flowers, and there are two tentative hypotheses to explain this association: 1. hummingbirds are attracted to red due its easier detection and, 2. bees are sensorialy excluded from red flowers. The second hypothesis is based on bees' red colour blindness, which leads them to be less frequent and less important than hummingbirds as pollinators of red-reflecting flowers. In this sense, red-reflecting flowers could adopt a "bee avoidance" strategy. Here we empirically tested the above hypotheses. We chose Costus arabicus, which has white- and pink-flowered individuals and is pollinated by both bees and hummingbirds. Specifically, we tested whether differences in red reflectance attracts hummingbirds (expecting more hummingbird visitation of pink flowers) or excludes bees (and then, expecting bee avoidance of pink flowers) and the consequent implications for the plant’s reproduction. Flower colour morphs of C. arabicus differed only in petal red-reflectance. Using vision models, the white flowers were revealed to be easily detected by bees and the pink flowers by hummingbirds. Bees preferentially visited the white flowers, whereas hummingbirds visited both colours at the same rate - both patterns corroborating the bee avoidance hypothesis. Pollen loads deposited on flowers stigmas did not differ between flower colour morphs, indicating that bees and hummingbirds play a similar role in the quantity aspect of pollination. However, bees are more likely to self-pollinate C. arabicus flowers than hummingbirds. We also found that self-pollination limits C. arabicus reproduction, and red-reflecting flowers may enhance the quality aspect of pollination by discouraging bee visitation. Sensory exclusion of bees seems to be the pressure for evolution of red-reflecting flowers, driving specialisation in hummingbird-pollinated flowers due to the costs of bee pollination on plant reproduction.

Image caption: Pink flowers of Costus arabicus, presumably avoiding bee-pollination. Photo credit: Camila Silva Oliveira.
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.

 

Ambient temperature, body condition and sibling rivalry explain feather corticosterone levels in developing black kites

Lidia López-Jiménez, Julio Blas, Alessandro Tanferna, Sonia Cabezas, Tracy Marchant, Fernando Hiraldo and Fabrizio SergioBlack kite feeding its young. Photo credit: Fabrizio Sergio.

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When an animal is psychologically or physically challenged (e.g. upon exposure to inclement weather, disease, food shortage or predators) a number of internal mechanisms that promote survival become activated. In birds, one such mechanism results in the secretion of the hormone corticosterone into the bloodstream. Rises in circulating corticosterone levels elicit a variety of changes in both physiology and behaviour which allow dealing with perturbations as quickly as possible. Recently, the development of a new technique to quantify the amount of corticosterone in feathers has been received with enthusiasm in the field of ecophysiology on account of its potential advantages over more traditional methods such as blood sampling. Feathers develop in specialised areas in the skin called follicles, where they receive a large supply of blood throughout growth (but not afterwards). During this period, numerous materials which circulate at the time, including corticosterone, passively diffuse out of the blood plasma and become sequestered into the forming feather keratin structure. In this sense, feathers have the potential to serve as permanent records of levels of past exposure to perturbations during a comparatively long period (days to weeks). In this study, we aimed to contribute further to the validation of this technique by measuring corticosterone levels in the feathers of the nestling of a raptor species (the black kite, Milvus migrans). Specifically, do these reflect variation between individuals in their responses to a number of potentially challenging environmental, social and physiological variables? As predicted, we found higher feather corticosterone in nestlings that: 1) had been exposed to lower ambient temperatures; 2) had poorer body condition; or 3) had been born in multiple-chick broods, but especially in those hatched lower down the brood hierarchy, which are more prone to suffer aggression from their older siblings during the establishment of dominant-subordinate relationships. Overall, our results underscore the potential of using feather corticosterone to infer levels of exposure to challenging situations in wild birds and their potential power as indicator tools in conservation biology.

Image caption: Black kite feeding its young. Photo credit: Fabrizio Sergio.
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.

 

Multiple environmental drivers structure plant traits at the community level in a pyrogenic ecosystem

Gregory M. Ames, Steven M. Anderson and Justin P. WrightA longleaf pine savanna experiencing a prescribed burn, Fort Bragg, NC. Photo by Gregory Ames, 2012.

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Biodiversity is declining at unprecedented rates and this decline may negatively impact ecosystem functions that we depend on. Preserving functional diversity requires an understanding of how it responds to changes in environmental conditions. Measureable properties of plants that affect performance, i.e. functional traits, provide a measure of functional diversity that is independent of species identity and can be compared across systems containing different species. However, little is known about the relationship between functional traits and environmental forcing, or how local trait variability influences our understanding of this relationship.

We measured traits that are strongly associated with growth and survival strategies of plants in the understory communities of longleaf pine forests that experience periodic fire, to investigate how this strong disturbance interacts with environmental conditions to drive changes in functional traits. We also investigated which environmental factors are most associated with changes in community composition without considering functional traits.

We found that a small set of environmental factors explained a large amount of the variation in key traits, but that the factors explaining community composition and functional traits were different. In particular, we found that functional traits were primarily explained by interactions between environmental factors such as fire, precipitation, and soil texture. This shows that strong environmental gradients cannot be considered independently of one another.

Furthermore, our interpretations of which environmental factors were most important depended on whether or not we used functional trait values from across the landscape or just the local plot-level measurements. This shows that it is essential to account for local variability in species traits when trying to infer relationships with the environment, especially in landscapes with strong disturbance gradients like those imposed by fire.

Our results are important because they show that understanding the response of functional diversity to the environment requires consideration of multiple environmental factors as well as their interactions, as well as the use of locally measured trait values. Incorporating these elements into future trait-based studies will greatly improve our understanding of how functional diversity responds to environmental changes.

Image caption: A longleaf pine savanna experiencing a prescribed burn, Fort Bragg, NC. Photo by Gregory Ames, 2012.
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.

 

Frog habitat preferences do not maximize jumping performance

Allegra Mitchell and Philip J. Bergmann Photo credit: Philip J Bergmann.

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Predicting species responses to a changing climate is difficult because of the dynamic relationship between animals and their environment, but it is necessary to reduce species losses. Amphibians in particular are suffering population declines globally, and understanding how the environment influences their habitat preferences and physical performance is crucial to understanding how these animals will be influenced by climate change. The biology of amphibians makes them especially sensitive to changes in environmental temperature and moisture because they are cold blooded and have highly water-permeable skin. Therefore, changes in environmental temperature and moisture directly affect amphibian body temperature and hydration level. Amphibians should select habitats with the optimal combination of temperature and moisture to perform tasks necessary for survival, like escaping predators or capturing prey. However, interactions between environmental temperature and moisture can influence habitat selection and task performance in different and often unpredictable ways.

In our study, we tested how environmental temperature and moisture influenced temperature and moisture preferences, and jumping performance in Green Frogs (Lithobates clamitans) in the laboratory and the field. We found that frogs in the laboratory selected environmental conditions that minimized water loss through the skin, rather than maximized body temperature to allow them to jump better. Frogs in the field also preferred to be well hydrated, and allowed their body temperatures to be much more variable. Jumping performance was highest at higher temperatures, but higher temperatures also increase dehydration. Therefore, conditions that minimized water loss frequently did not maximize jumping performance, creating a discrepancy between remaining hydrated and moving effectively.

The ecology of Green Frogs may explain this discrepancy because the frogs remain near bodies of water that serve as refuges from both dehydration and many predators. However, when it is warmer and drier, Green Frogs may be more likely to select microhabitats that minimize the risk of dehydration at the expense of their ability to forage and escape from predators. As the climate changes, all amphibians may be at greater risk of dehydration and predation, particularly those that are already declining.

Image caption: Photo credit: Philip J Bergmann.
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.

 

Mercury could reduce parental care behaviour by disrupting parenting hormones in Arctic seabirds

Sabrina Tartu, Paco Bustamante, Frédéric Angelier, Ádám Z. Lendvai, Børge Moe, Pierre Blévin, Claus Bech, Geir W. Gabrielsen, Jan Ove Bustnes, Olivier ChastelUnattended black-legged kittiwake hatchling. Credit: Sabrina Tartu.

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Despite its remote location, the Arctic is a fallout region for long-range transport pollutants, among them mercury, a naturally occurring element that has been enriched in the environment by human activities such as coal combustion and mining. When converted to methylmercury by microbial processes in the ocean, it can accumulate in organisms and magnify along the food web. Consequently, the levels of methylmercury reached in top predators like Arctic seabirds are very elevated. Methylmercury is a toxic element which can have serious health effects on Arctic wildlife. Less known are its effects on free-living animals as an endocrine disruptor, that is, its ability to disrupt the normal functioning of natural hormones. Hormones are chemical substances that act like messenger molecules in the body, and control and regulate the activity of certain cells or organs. To this end, an international team collaborated to assess the effects of mercury contamination on the hormone prolactin and breeding performance in Black-legged kittiwakes from Svalbard, in the high Arctic. Prolactin is a hormone that stimulates lactation in mammals and incubation or chick feeding in birds. Kittiwakes were captured on their nest and a blood sample was taken to measure mercury and prolactin concentrations. It appeared that high mercury levels in male kittiwakes were associated with decreased prolactin secretion and with reduced breeding success. An experimental study was also conducted to see if environmental stress could exaggerate the negative effect of mercury on prolactin secretion. To do so, male kittiwakes were implanted with corticosterone, a stress hormone which naturally rises during unfavorable conditions (e.g. food shortage, predation). Because stress is known to decrease prolactin concentrations, we predicted that mercury and corticosterone would act synergistically and would steepen the mercury- prolactin relationship. Hatching success was significantly lower in corticosterone-implanted males, but contrary to our prediction, mercury and stress did not act synergistically. Results from this study strongly suggest that mercury can impair seabird reproductive performance through a disruption of prolactin secretion and highlights the need to further explore the complex interactions between environmental stressors and anthropogenic contaminants.

Image caption: Unattended black-legged kittiwake hatchling. Credit: Sabrina Tartu.
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.

Special Feature: Mechanisms and consequences of facilitation in plant communities

Functional assessment of animal interactions with shrub-facilitation complexes: a formal synthesis and conceptual framework

Christopher J. Lortie, Alex Filazzola and Diego A. SotomayorA shrub-animal interaction captured using an animal camera at Panoche Hills Ecological Reserve, California.

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Positive interactions between plants in many high-stress ecosystems such as deserts have been commonly studied with shrubs. The term facilitation typically describes these positive interactions between plants, which act unidirectionally from benefactor (shrub) species to beneficiary (usually herbaceous) species, and with benefits examined including increased presence, abundance, and diversity. However, the ecological implications of shrub facilitations for other species are rarely extended to animals. We provide a conceptual framework and quantitative review of the existing research to date on this topic and show that linked positive interactions between plants and animals are important ecologically and that the functional roles of shrubs and animals complement one another in these ecosystems. A transparent, systematic review generated a list of nearly 80 studies that examined positive interactions between a shrub, other plant species, and at least one animal species. In effect, we are proposing that to effectively study the implications of positive interactions between plants and animals for community assembly and resilience, the magic number of interactors is at least three. We then classified all the instances from this defined literature using this approach as either directly between the dominant shrub and the animal species, but still involving at least three species, and not just pairwise, i.e. ‘shrub-animal-plant’, or as indirect, i.e. ‘shrub-plant-animal’. These interaction pathways were evenly split between direct (49%) and indirect (51%) interactions of shrubs with animals. Two critical implications arise from this synthesis exercise. Firstly, positive plant interactions can cascade to animals, and this can be an important simplification in designing experiments because we can begin plant-animal interaction studies with dominant plants. The other dimension of this benefit is a challenge to traditional plant community assembly theory, i.e. you must consider animals too. Secondly, management of even relatively simple, low productivity ecosystems must embrace a networked approach to species. Working with these interacting species must include function in addition to species composition where environmental stress is high, because functional roles can change.

Image caption: A shrub-animal interaction captured using an animal camera at Panoche Hills Ecological Reserve, California.
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.

 

Editor and reviewer gender influence the peer review process but not peer review outcomes at an ecology journal

Charles Fox, C. Sean Burns and Jennifer MeyerIssues of Functional Ecology. Photo Credit: Jennifer Meyer.

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Peer review is a standard and essential component of scientific publishing, but is managed by a narrow and non-random segment of the scientific community – senior editors and editorial boards are disproportionately men, well established (i.e., more senior) scientists, and can write fluently in English. This limited diversity might generate disparities in editorial and peer review that contribute to gender and geographic disparities in scholarly publishing. Here we examine a comprehensive dataset of the peer review process for all papers submitted to this journal, Functional Ecology, from January 2004 to June 2014, to examine how gender, seniority and geographic location of editors and reviewers influence reviewer recruitment and scores given to papers by reviewers.

Functional Ecology editors have been and continue to be majority male, but the number of female editors has increased over time until, in 2014, ~40% of editors handling manuscripts for the journal were women. Reviewers selected by editors to review submissions to the journal were also highly majority male, but the proportion of women selected as reviewers increased over time. This increase is largely caused by an increasing number of female editors because they invited more female reviewers than did male editors. Male editors selected <25% female reviewers, but female editors consistently selected ~30-35% female reviewers. –Similarly, editors over-selected reviewers from their own geographic locality. The proportion of women among selected reviewers decreased with editor seniority when the editor was male but increased with editor seniority when the editor was female. Thus early-career male and female editors differed little in the proportion of women invited to review, but late-career (more senior) male and female editors differed a lot in the proportion of women they invited to review.

Women invited to review were less likely to respond to invitation emails, but were more likely to agree to review if they responded. Men that were invited to review were both less likely to respond to the invitation and more likely to decline if the editor handling the paper was female. In contrast, women responded to invitations similarly regardless of whether the editor inviting them was male or female. Unexpectedly, individuals invited to review were less likely to agree to review if the editor handling the paper, and thus selecting the reviewers, was more senior.

Despite differences between male and female editors, and between male and female reviewers, on aspects of the peer review process, we observed no differences on outcomes – neither review scores given to papers nor final decisions (the proportion of papers rejected) differed between male and female reviewers or male and female editors.

Editor gender, seniority and geographic location affect who is invited to review for Functional Ecology, and how invitees respond to review invitations, but not the final outcome of the peer review process. We suggest that, to increase diversity of reviewer populations, journals should increase gender, age and geographic diversity of their editorial boards.

Image caption: Issues of Functional Ecology. Photo Credit: Jennifer Meyer.
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

Functional characterizations of Ellenberg Indicator Values – a review on ecophysiological determinants

Maik Bartelheimer & Peter PoschlodControlled screening experiment to relate Ellenberg Indicator Values for soil moisture to species plasticity in rooting depth. Photo by Jessica Rossow.

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Ellenberg Indicator Values (EIV) provide a numerical system for Central European plant species to describe their peak occurrence along environmental gradients. EIV are available for the soil factors moisture (M-numbers), nutrients (N-numbers), and soil pH/reaction (R-numbers) as well as for the climatic factors light (L-), temperature (T-), and distance to the Atlantic Ocean with its climate-modifying effects (continentality, C-numbers). By finding correlations of EIVs to morphological or ecophysiological plant properties we hope to identify those properties that determine species distributions along environmental gradients. To identify such determinants this review surveys existing literature containing species comparisons from controlled experiments and combines them with EIV. The picture emerging is that multiple determinants can be identified for nutrient-, reaction- and also moisture-numbers, while only few can be found for light- and especially for continentality- and temperature-numbers.

As an example, for nutrient-numbers 16 different determinants could be identified. These include many that might be expected like ‘specific leaf area’ (a measure of the amount of leaf material deployed per unit area of leaf), ‘seed weight’, and ‘relative growth rate’, but also some that are less obvious, like ‘regrowth after defoliation’, ‘germination response to ammonium nitrate’, and ‘germination temperature requirement’. At the same time, just a single determinant for continentality-numbers could be identified from existing data sets (timing of leaf unfolding and related frost resistance).

Functional characterizations of the different EIV can thus be deduced, which helps us to understand the mechanisms and processes driving the ecological niche of a plant. The approach described is a powerful tool to analyse the ecological significance of different plant properties. In the future, species screenings specifically designed to allow for correlations with EIV have great potential for high explanatory power.

Image caption: Controlled screening experiment to relate Ellenberg Indicator Values for soil moisture to species plasticity in rooting depth. Photo by Jessica Rossow.
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.

 

Tracking woodland water use efficiency under future atmospheric conditions

Teresa E. Gimeno, Kristine Y. Crous, Julia Cooke, Anthony P. O’Grady, Anna Ósvaldsson, Belinda E. Medlyn and David S. Ellsworth A view of the EucFACE study site from the top of a crane inside one of the study rings taken while making a gas-exchange measurement campaigns by Teresa E. Gimeno.

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The most certain prediction for our atmosphere is that carbon dioxide (CO2) concentration will continue to rise, due to fossil fuel burning. Rising CO2 affects the biosphere indirectly because it is the main driver of climate change, but it also has a large direct impact on vegetation because it is the main fuel for plant growth. However, when plants take up CO2, it is accompanied by an inevitable loss of water. This process of transpiration is regulated by the opening and closing of small pores (called stomata) found on the leaf surface of all higher plants. In an atmosphere with more CO2, plants can close stomatal pores to economize on water, while maintaining or even increasing CO2 uptake. This means that plants can increase how efficiently they use water with rising CO2. This increase is particularly relevant for ecosystems where plant growth is limited by water availability, including the vast majority of Australian forests and woodlands.

Previous experiments showed that rising CO2 could increase or decrease water use efficiency depending on plant types and climates. Fortunately, models help to predict optimal water use per unit of CO2 uptake, based on the sensitivity of stomatal pores to the environment. Here we tested the ability of one of these models to predict water use efficiency during carbon uptake in future atmospheric conditions, under variable climatic conditions. To test for optimal stomatal behaviour of the trees, we measured carbon uptake and water use at the tops of mature eucalypt trees under current and future CO2 atmospheric concentrations, over the course of the seasons. Our study was conducted at the EucFACE site, the only existing elevated CO2 experiment in a native Eucalyptus forest. We show that water use efficiency increases proportionally with the rise in CO2 concentration. So in a future global change scenario, mature trees will be more efficient in their water use, but this may only partially mitigate some of the adverse effects of the concomitant rise in temperature.

Image caption: A view of the EucFACE study site from the top of a crane inside one of the study rings taken while making a gas-exchange measurement campaigns by Teresa E. Gimeno.
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.

 

Sperm production characteristics vary with level of sperm competition in Cataglyphis desert ants

Serge Aron, Pascale Lybaert, Claire Baudoux, Morgane Vandervelden and Denis Fournier Cataglyphis hispanica worker ant collecting pollen of Spergularia purpurea (Caryophyllaceae).

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In animal species where females mate with more than one male, ejaculates from different males coexist in the female tract and compete to fertilize ova. Competition among sperm from multiple males is recognized as an important force in the evolution of sperm traits that enhance fertilization success. In contrast to species with weak or no sperm competition, males of species with intense sperm competition usually produce more sperm to out-compete rivals and/or longer sperm cells that swim faster than shorter ones. We studied relationships between levels of sperm competition, sperm production and sperm size in a comparative study of 15 species of Cataglyphis desert ants. The mating system of ants imposes unique selective pressures on male ejaculates that are rarely, if ever, found in other animals. Males disperse with a finite amount of sperm, they typically mate with a single or, rarely, a few females and die shortly afterwards. However, males live posthumously as spermatozoa stored in a little reservoir of the queen (the spermatheca), for several years or more. Thus, the reproductive success of males is limited by the amount of sperm successfully stored in the spermathecae of the queens. A remarkable feature of Cataglyphis ants is that multiple queen-mating (queens can mate with 2 to 14 males) is the ancestral state, and reduction in mating frequency evolved secondarily in some lineages. This provides a unique opportunity to examine how reduction from multiple to single mating influences sperm traits. We counted sperm in the testis of males and showed that they produce more spermatozoa in species experiencing greater levels of sperm competition. In contrast, neither sperm length nor male size is significantly associated with the number of matings of queens. Our comparative analysis provides the first direct evidence that sperm production covaries with the level of sperm competition in a eusocial insect and, more generally, that reduction in sperm competition influences sperm traits in an organism.

Image caption: Cataglyphis hispanica worker ant collecting pollen of Spergularia purpurea (Caryophyllaceae).
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.

 

How are leaf mechanical properties and water use traits coordinated by vein traits?—A case study in Fagaceae

Kiyosoda Kawai and Naoki Okada Hierarchal vein system in Quercus gilva (Fagaceae). Photo credited to authors..

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If you take a stroll into a forest, you will immediately find a variety of leaf shapes there. Broad-leaved (dicotyledonous) flowering plants (Angiosperms) are the most diversified in morphology and this is also true for leaf venation. But, venation in all Angiosperms shares one key property; a hierarchal vein system, i.e. many types (orders) of veins whose diameter and length are dramatically different (see attached image).

This system has been known for a long time, but its functional significance is still discussed. One fascinating explanation has been “division of labor”: thick but short primary and secondary veins transport sugars and water over long distances. On the other hand, thin and net-like minor veins distribute water and collect sugars produced by photosynthesis. But, earlier researches have not paid much attention to another important vein function: mechanical support to keep the light-intercepting leaf stable against gravity.

In this paper, we examined the contribution of leaf veins to leaf mechanical properties and water use and attempted to confirm the “division of labor” hypothesis in Angiosperm venation. For this purpose, we employed 8 Fagaceae species (oak/beech family) with a diversity of leaf shape, leaf habit and venation. We quantified mechanical properties (toughness) of leaves by tearing the leaf lamina and water relations by measuring conductance of leaf and water use efficiency (photo- synthetically gained carbon / loss of water). We measured vein and leaf traits to explain the variation of these functions. For vein traits, we measured vein density (vein length per unit area) for different order veins.

We found that different order veins were associated with different leaf functions. Primary and secondary vein density influenced leaf carbon cost and mechanical properties. In contrast, minor vein density is associated with leaf hydraulics. These results showed that the division of labor occurs in multiple leaf functions among contrasting vein orders. Further our study suggests the possibility that combinations of vein density of different orders could have led to the diversification of multiple leaf functions in the Angiosperms.

Image caption: Hierarchal vein system in Quercus gilva (Fagaceae). Photo credited to 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.

 

Female guppies reduce energetic costs of being harassed by males by becoming more efficient swimmers

Shaun S. Killen, Darren P. Croft, Karine Salin and Safi K. DardenImage provided by authors.

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Females and males of the same species are often in conflict over the frequency and timing of matings. Typically male reproductive success is limited by access to females and males of many species will try to overcome this using a number of behaviours, such as chasing and even attacking females in an attempt to gain a mating. These types of behaviours are considered sexually harassing as males are attempting to coerce females into mating with them. Females can spend a lot of energy avoiding males in these situations and can even be injured. To reduce these costs, one possibility is that females may be able to change their own behaviour or physiology in ways that reduce the negative energetic consequences of harassment, or allows them to more easily escape male coercion.

We studied this likelihood in a laboratory setting by housing female Trinidadian guppies (Poecilia reticulata) for several months with varying levels of male harassment that they would normally encounter in the wild. In the wild male guppies spend a large portion of their time chasing and harassing females in an attempt to mate with them. Females can attempt to avoid this harassment by rapidly swimming away from the male during pursuits.

After five months, females exposed to higher levels of harassment were able to swim much more efficiently, using less energy to swim at a given speed compared to those exposed to lower levels of harassment. It seems that prolonged increases in high-intensity swimming in females, caused by male harassment, leads to changes in the physiology or swimming mechanics of individual fish, which reduce costs of swimming. Indeed, females that experienced lower levels of harassment spent more time swimming with their pectoral fins extended, an indicator of an inefficient swimming technique.

These results show that female guppies can reduce the energetic costs of male sexual harassment through changes in their swimming physiology or technique. Increased swimming efficiency or performance could also allow female guppies to escape male coercion more easily, giving them more control over matings. An exciting opportunity now exists to examine the extent to which this phenomenon occurs in the wild.

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.

Mechanisms and consequences of facilitation in plant communities

Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning

Fabio Bulleri, John F. Bruno, Brian R. Silliman, and John J. StachowiczIntertidal stands of Cystoseira. Photo credit: L. Benedetti-Cecchi.

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Negative species interactions, such as competition, predation or parasitism have been traditionally envisioned as the main forces shaping patterns of species distribution and abundance. Theoretical and empirical research over the last two decades, bringing compelling evidence of the prominent role of positive species interactions (i.e., facilitation and mutualism) in structuring natural communities, has altered this view. Here we take a niche-based view of such positive interactions. The fundamental geographic niche is the physical space in which a species can develop self-sustaining populations if not constrained by negative biotic interactions. The realized niche, in contrast, represents the space actually occupied by a species after accounting for interactions with other species. Previous research has suggested that facilitation or mutualistic interactions can expand species’ realized niches by reducing the impact of negative, niche-shrinking species interactions or, indeed, expand the fundamental niche by allowing species to persist in environments that would otherwise be too physically stressful.

The effects on whole communities of generalized niche expansion due to facilitation have been little explored. In the presence of a foundation species (i.e. species that play a key role in structuring associated communities), facilitation-broadened niches could become less distinct (increased overlap among potential competitors), ultimately altering the intensity of competitive interactions among species. Facilitation, by broadening niches, could therefore limit species coexistence. However, niche overlapping might also be reduced when the foundation species is sufficiently patchy or creates new micro-environments that increase environmental heterogeneity.

Important implications for key areas of ecology arise from this conceptual framework. For instance, the extent to which facilitated species can persist in the face of climate changes by seeking refuge with facilitators depends on the degree of niche overlap and differences in competitive ability among potential beneficiaries. In addition, because facilitation can modify the strength of interactions among species, either by increasing niche overlap or altering environmental heterogeneity, it can also change the fundamental shape of the relationship between species diversity and ecosystem functioning. In summary, a mechanistic understanding of the effects of facilitation on species distribution, biodiversity and ecosystem functioning will require an assessment of how niche-broadening via facilitation changes the degree of niche overlap within a community.

Image caption: Intertidal stands of Cystoseira. Photo credit: L. Benedetti-Cecchi.
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.

 

Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment

Dima Chen, Jianjun Li, Zhichun Lan, Shuijin Hu, and Yongfei BaiSemi-arid grassland in Inner Mongolia of China (Image provided by Qingmin Pan).

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In many areas of the globe and especially in Asia, deposition of atmospheric nitrogen compounds (N) is expected to continue to increase. The dramatic increases in N inputs have wide-ranging ecological impacts on the biotic community, biogeochemical cycles, and greenhouse gas emissions. As one of the largest carbon effluxes between the atmosphere and terrestrial ecosystems, soil respiration plays a vital role in regulating the atmospheric CO2 concentration and climate on Earth. N inputs can affect soil respiration through two mechanisms or pathways: direct N impacts through enhancing soil N availability, and thus increasing plant productivity, and indirect impacts through modifying soil acidity. Yet, few studies have experimentally assessed the relative effects of increased N availability vs. soil acidification on below-ground carbon cycling in natural ecosystems. To address this issue, we conducted a 12-yr N enrichment experiment and a 4-yr complementary acid addition experiment in a semi-arid Inner Mongolian grassland. We found that soil acidification exerts greater control than soil N availability on soil respiration in grasslands experiencing long-term N enrichment, suggesting the need to include soil acidification in predicting terrestrial ecosystem carbon balance under future N deposition scenarios. We also found that N enrichment enhanced soil depletion of base cations such as calcium and magnesium in this semi-arid ecosystem, indicating that researchers and policy makers should also consider the long-term effects of N enrichment on element availability for plants, wildlife, and domestic livestock.

Image caption: Semi-arid grassland in Inner Mongolia of China (Image provided by Qingmin Pan).
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.

 

Mistletoe influences community seedfall patterns

Ana Mellado and Regino ZamoraIn this Mediterranean pineland, parasitized trees, constituting the only (or most abundant) nutritive resource offered on the canopy layer, are particularly noticeable for frugivorous birds. Frugivores respond to mistletoe patchiness by visiting parasitized trees preferentially to unparasitized ones, driving a differential deposition of mistletoe and co-fruiting species seeds towards parasitized trees. Photo by Ugo Mellone.

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Mistletoes are fleshy-fruited parasitic plants that dwell in forest canopies and show a strongly aggregated spatial distribution. Parasitized trees potentially concentrate fruit-eating bird activity in their canopies, where birds find food, places to perch, and protection against predators. Thus, seed-deposition patterns are expected to reflect the heterogeneity associated with the parasite. This becomes especially important in generalist dispersal systems; however, so far, we do not know the implications of mistletoe spatial heterogeneity for the seed-dispersal pattern of other plants that fruit at the same time.

In a Mediterranean pineland, we analyze the impact of Viscum album subsp. austriacum on the seed-deposition pattern of a bird-dispersed plant community, taking into consideration the spatial and temporal variability of environmental factors influencing the birds’ habitat use, such as fruit availability and forest tree density. For four consecutive years, we studied 55 pairs of trees parasitized and unparasitized by mistletoe, analyzing fruit availability, bird visits, and the bird-dispersed seed rain in selected trees.

As expected, fruit-eating birds responded to mistletoe heterogeneity by visiting parasitized trees preferentially to unparasitized ones, generating a differential deposition of mistletoe seeds on tree branches while dispersing seeds of co-fruiting species under the host canopy. Availability of understory fruits remained similar in patches of parasitized and unparasitized trees, but showed strong temporal fluctuations reflected in the seed rain. On the other hand, mistletoe was not only more copious in patches of parasitized trees, but their fruit crops varied little between years, making mistletoes reliable food resources likely to lead to consistency in fruit-deposition patterns.

In conclusion, mistletoes, by patchily growing in the canopy layer and concentrating bird-dispersed seeds underneath, can shape the spatial seed-deposition pattern of fleshy-fruited plants in the forest. Moreover, as seeds constantly reach the same deposition sites over long periods, the soil beneath the host canopy could become hotspots for community regeneration. In degraded areas, such mistletoe effects might be critical, possibly promoting recolonization and vegetation recovery through bird activity.

Image caption: In this Mediterranean pineland, parasitized trees, constituting the only (or most abundant) nutritive resource offered on the canopy layer, are particularly noticeable for frugivorous birds. Frugivores respond to mistletoe patchiness by visiting parasitized trees preferentially to unparasitized ones, driving a differential deposition of mistletoe and co-fruiting species seeds towards parasitized trees. Photo by Ugo Mellone.
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.

 

Interactions under novel global change scenarios: How does ozone affect the triple interaction grass-endophyte-herbivore?

Andrea C. Ueno, Pedro E. Gundel, Marina Omacini, Claudio M. Ghersa, Lowell P. Bush andMaría Alejandra Martínez-GhersaLolium multiflorum and Rhopalosiphum padi.

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As human impact on the environment increases, biological systems, from individuals to ecosystems, are consequently exposed to novel situations. It is especially relevant to understand how symbiosis of plants with beneficial microorganisms will respond to rising atmospheric pollutants.

Tropospheric ozone is a very dynamic pollutant gas associated with human activities that causes oxidative stress on living organisms. At the same time, it has been proposed that episodic exposure to ozone might elicit plant defense mechanisms, increasing tolerance to biotic factors such as herbivory and pathogens. However, we propose that if the plant defense is conferred by a symbiotic microorganism, the opposite effect might be expected. The symbiosis between cool season grasses and fungal endophytes, which live inside the grass leaves, is a defensive mutualism since host plants obtain resistance against herbivory mediated by several fungal alkaloids. Here we show that endophyte-symbiotic and endophyte-free plants of annual ryegrass exposed to ozone for just a few hours were differently affected. We evaluated the effectiveness of the defensive mutualism by exposing the plants to herbivory by aphids. We found that ozone impaired the resistance to aphids in endophyte-symbiotic plants but it slightly increased that of endophyte-free plants. In conclusion, our work suggests that the growing incidence of ozone as a novel stress factor under some global change scenarios could change the rules of certain symbiotic interactions in nature.

Image caption: Lolium multiflorum and Rhopalosiphum padi.
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.

 

Open wide! How and why gape reduces bite force in bats

Sharlene E. SantanaA Stripe-headed Round-eared Bat (Tonatia saurophila). Photo credit: Sharlene Santana.

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As the only flying mammals, bats completely rely on their skull and jaw muscles as major tools for grasping and processing food items. The outstanding diversity of bat diets, spanning fruits and insects of various sizes, to vertebrates and even blood, has resulted in the evolution of a plethora of cranial specializations that allow bats to bite with the appropriate amount of force and at the gapes necessary to consume their preferred foods. Theory predicts, however, that mammals experience trade-offs between their ability to produce a strong bite and to bite at wide gapes. First, opening the jaw at a wide gape stretches the fibers within jaw muscles, which makes their contraction weaker. Second, skull and muscle anatomies that allow for strong bites (e.g., short jaws, short muscle fibers) hinder the production of bite force at wide gapes, whereas anatomies that are more suited for biting at wide gapes (e.g., long jaws, long muscle fibers) are not optimal for producing strong bites.

Very few studies have confirmed these predictions in wild mammals, or harnessed the power of computer models to more deeply investigate this topic. This study documented the variation in bite force at low and wide gapes across free-ranging, tropical bat species, and built 3D computer models of their skulls to identify anatomical traits underlying the relationship between bite force and gape. Using these approaches, we corroborated that bites get weaker as bats have to open their mouth wider, but the drop in bite force varies substantially within and among species. In particular, bats that specialize in eating hard fruits experienced the steepest reduction in bite force at wide gapes. Computer models revealed that larger reductions in bite force at wide gapes are the product of a combination of anatomical features, including a shorter face, a larger temporalis (jaw closing) muscle, and a higher propensity for stretching this muscle during jaw opening. Altogether, these results suggest that gape-mediated changes in bite force can be explained both by behavior and cranial anatomy, and illustrate that these links are relevant for functional analyses of mammal diets.

Image caption: A Stripe-headed Round-eared Bat (Tonatia saurophila). Photo credit: Sharlene Santana.
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.

 

Swimming in UV

Ensiyeh Ghanizadeh Kazerouni, Craig, E. Franklin and Frank SeebacherManly Dam, image provided by authors.

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As pleasant as it is to swim in the sunshine, as humans we know very well how damaging UV radiation from the sun can be. It turns out that we are not the only ones affected by UV radiation: small fish (mosquitofish, Gambusia holbrooki) are too. Here we show that rather than causing sunburn, UV radiation affects the metabolism and capacity to move in fish. For example, exposure to UV-B radiation at relatively low levels reduces swimming endurance of fish by up to 30-40%. This can obviously have serious consequences for foraging behaviour, dispersal, and other ecological functions in these and probably other fish that are exposed to sunshine at the water surface. Luckily, evolution has found a solution to this problem. Fish that are born in summer when the water is warm and UV-B is high are much more resilient to the damage caused by radiation than fish that are born in winter. In other words, the early developmental conditions experienced by fish prepare them for the environment they encounter later in life. There is more to the story, though, because the characteristics of fish as well as many other animals are not fixed even within adults. The process of acclimation means that physiological functions can change reversibly within individuals and thereby lessen potentially negative impacts of environmental conditions. However, our data show that the capacity for acclimation is also dependent on developmental conditions. For example, fish born in summer can cope very well with UV-B but only when chronically exposed to their favourite temperature of 28oC; winter-born fish can barely acclimate at all. Our study reveals how complex the biological effects of environmental change are, with at least two of the major global climate drivers, temperature and UV, interacting in their impact on animals. Similarly, animal responses are a complex mix of genetics and development, which affects average characteristics of animals as well as their mutability later in life. These insights are important because they reveal how animals manage to do well in variable environments, and they will help us predict what the impacts of future climate change will be.

Image caption: Manly Dam, 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.

 

Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on a common milkweed

Tobias Züst and Anurag A. AgrawalThe milkweed aphids Aphis nerii and Aphis asclepiadis sharing their host plant, the common milkweed Asclepias syriaca. T. Züst.

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Herbivorous insect species strongly differ in the number of plants they feed on. Generalist herbivores are often very efficient at consuming plants and reproducing rapidly, but may be susceptible to toxins which the plant produces as defensive compounds. In contrast, specialized herbivores are generally more tolerant of plant toxins, and even may gain the ability to accumulate (sequester) plant toxins in their bodies as a defense against their own enemies. Understanding the effects of plant variation on herbivore performance is thus important for predicting population dynamics of herbivorous insects.

We compared the performance of four aphid species on a set of naturally variable common milkweed plants. Aphids reproduce clonally and the four species vary greatly in their diet breadths, while milkweed plants produce variable amounts of toxic cardenolides. Populations of the two more generalist species grew the fastest overall, and both species grew best on plants growing at a high rate, thus these species were likely limited by low resources on slower-growing plants. Food consumption of aphids increased with decreasing population growth, indicating decreasing resource-use efficiency with increasing specialization.

All four aphid species contained cardenolides in their bodies, but the amount of sequestered toxin increased with degree of diet specialization. Contrary to our predictions, the only species that was negatively affected by increasing levels of cardenolides in the host plant was the most specialized aphid, perhaps due to the very high levels of cardenolides accumulating in its body. The type of cardenolides accumulated in aphid bodies indicates a mostly passive mode of sequestration, with body cardenolide content being directly related to the rate of food consumption.

Generalist aphids performed best overall and were limited only by low plant growth but not by plant toxins. Specialist aphids were not affected by variation in plant growth but appeared to use resources less efficiently. Their increased food consumption resulted in higher cardenolide sequestration to the point of causing negative effects on population growth at the very highest levels. Variation in both growth rate and cardenolide levels of milkweed plants is thus likely to determine the relative distribution of generalist and specialist herbivores in the field.

Image caption: The milkweed aphids Aphis nerii and Aphis asclepiadis sharing their host plant, the common milkweed Asclepias syriaca. T. Züst.
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.

 

What features do plants use to survive drought?

Alexandria L. Pivovaroff, Sarah C. Pasquini, Mark E. De Guzman, Karrin P. Alstad, Jenessa S. Stemke, and Louis S. Santiago Photo by Louis Santiago.

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Tree mortality during drought has been documented in forests worldwide. It is thought that with global change, the frequency and intensity of extreme climatic events, such as drought, will increase. Although we have some information about the relative drought resistance of plant species, in many ecosystems, we still do not have a good physiological understanding of which species are most likely to die first. Physiologists are also currently trying to determine which mechanisms cause plants to die during drought. When water is limiting, plants can either close their stomata to conserve water at the risk of restricting photosynthetic carbon uptake, or they can open stomata to continue photosynthetic carbon uptake at the risk of losing too much water. Plants could therefore die of carbon starvation or hydraulic failure during drought, but which mechanism is more prevalent under what kind of conditions? And, what are the other traits that are important for maintaining internal carbon and water supplies during drought?

In this study, we measured seven drought survival traits to characterize how these traits combine in species and whether there were obvious drought survival strategies. We found that hydraulic architecture, the relative amount of water transport tissue and evaporative leaf surface area, was related to resistance of the stem tissue to water deficit. Yet, we also found that many traits occurred with no apparent pattern with regard to other traits, leading to a vegetation community with a large diversity of strategies for dealing with drought. This is likely because the study was conducted along a transition between two major vegetation types: California chaparral shrublands and the Mojave Desert. At the continental meeting of these two vegetation types, many species are on the edge of their range, so it is thought that areas such as the study site of this paper have a high chance of mortality during climate change. California is currently in a major drought, so if mortality begins to strengthen, the drought resistance characteristics studied in this paper should help us understand why certain species are dying and allow predictions for other sites.

Image caption: Photo by Louis Santiago.
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.

 

Butterfly males can smell the mating status of females and use this information to design their ejaculate

Helena Larsdotter-Mellström, Kerstin Eriksson, Niklas Janz, Sören Nylin and Mikael A. CarlssonImage of a female Pieris napi. Photo by Mikael A Carlsson

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One of the most fascinating aspects of sexual selection is sperm competition. In many species, females mate with several partners, causing competition among sperm from the different males. One option for the males to maximise the number of fertilizations is to increase the size of the ejaculate. A large ejaculate would however be a more important investment when mating with an already mated female than with a virgin. Therefore, it would be beneficial for males to be able to assess the female mating history and accordingly adjust the size of the ejaculate.

So how can the male assess the mating status of a female? There is evidence that many animals can use odour cues, pheromones, for this purpose. A previous study showed that males of the Green Veined White butterfly, Pieris napi, transfer an anti-aphrodisiac signal, methylsalicylate, to females together with sperm at ejaculation. This compound signals to other males that the female is already mated, making her less attractive as a partner. Here, we asked if males may also use this signal to tailor the ejaculate accordingly, i.e. transfer more sperm to an already mated female than to a virgin.

We could show that males have a sense of smell that can distinguish between different concentrations of methylsalicylate. Females also have this ability but are less sensitive to it.

Next we found that males transferred a larger ejaculate to mated females than to virgins. But most interestingly, males also transferred a larger ejaculate to virgin females with artificially added anti-aphrodisiac.

Thus, we have shown a mechanism for how males can assess the mating status of females and we have furthermore shown that they can use this signal to tailor their ejaculates.

Image caption: Image of a female Pieris napi. Photo by Mikael A Carlsson
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.

 

Breath of death: how a parasite favours its transmission through hijacking its host’s hypoxia-acclimation processes

Marie-Jeanne Perrot-Minnot, Matthieu Maddaleno, Frank Cezilly The thorny-headed worm Polymorphus minutus : larvae dissected from the crustacean host, and infective to the definitive host, a waterbird.

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Parasites with complex life cycles, involving more than one host, often alter the behaviour of their intermediate hosts in ways that increase their chances of getting transmitted to final hosts. For instance, the thorny-headed worm Polymorphus minutus is known to induce ‘reversed geotaxis’ in its amphipod host Gammarus roeseli, such that infected hosts swim closer to the water surface and presumably become more vulnerable to predation by aquatic birds (in which the parasite will complete its life cycle).

So far, the mechanisms underlying host manipulation by parasites remain poorly known. As hypoxia (shortage of oxygen) in aquatic invertebrates is known to induce complex physiological responses and reversed geotaxis, we conjectured that the reversal of geotaxis induced by P. minutus in amphipod hosts could result from a hypoxia-like state through two potential mechanisms. First a decrease in the metabolic rate of amphipods could be directly caused by infection with P. minutus. Second, the parasite could mimic a state of hypoxia in its host, as P. minutus has been previously shown to excrete both lactate and succinate (two end-products of its own anaerobic metabolism).

Under hypoxia, uninfected G. roeseli showed negative geotaxis and lower metabolic rate, two traits altered by infection with P. minutus, albeit with different intensities. The injection of a mixture of lactate and succinate in uninfected amphipods also mimicked the parasite-induced reversion of geotaxis, without affecting metabolic rate. In addition, both P. minutus-infected gammarids and uninfected ones conditioned to hypoxia for two days showed elevated levels of lactate in the brain, but not in the haemolymph (the fluid analogous to blood in vertebrates). Overall, our results strongly suggest that the pathways involved in anaerobic metabolism and hypoxia-signalling might be responsible for the changes in geotaxis and metabolic rate induced by P. minutus infection.

This study emphasizes the need to consider the tight and complex connections between physiological processes and behavioural adjustments, in particular at the brain level, in the understanding of parasitic manipulation, and more broadly of behavioural changes in infected hosts.

Image caption: The thorny-headed worm Polymorphus minutus : larvae dissected from the crustacean host, and infective to the definitive host, a waterbird.
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 elephant seals optimal divers?

Joffrey Jouma’a, Yves Le Bras, Gaëtan Richard, Jade Vacquié-Garcia, Baptiste Picard, Nory El Ksabi and Christophe GuinetFemale elephant seal and her pup on Kerguelen Island. Photograph by Joffrey Jouma’a.

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Optimal foraging theory offers a conceptual framework to describe and understand behavioural strategies adopted by an animal to maximise its fitness. Based on the optimisation principle, this theory aims to predict the best strategy for maximising efficient foraging under energetic and temporal constraints, e.g. where is the best place to feed on, what is the best type of prey to catch, and when to switch from one patch to another? Because marine predators must find prey in three dimensions and air-breathing divers are forced to come up to the surface to renew their oxygen store, several adaptations need to be considered to study foragers in a marine context. Things are twice as difficult, because only a few studies deal with the optimal theory applied to diving predators, and even fewer have tested in situ the associated assumptions. Here, we focus on the Southern Elephant Seal, a nearly continuous diver that can however be easily equipped with Time-Depth-Recorders (TDR) due to its annual presence on land for reproduction. Using TDR associated with accelerometers provides information on diving behaviour, such as the time spent in the foraging zone, the swimming effort or even the number of prey catch attempts. Accelerometers are a powerful tool that can also tell us about the animal’s buoyancy. We showed that elephant seals adjust precisely their time spent in the foraging zone with the depth targeted, their body condition, but also with prey encounter rate. For instance, an animal with a high body density will usually tend to stay less time in the foraging zone due to the energy required to come up to the surface. This study also highlights that using only the time spent in the foraging zone to estimate foraging success can be seriously misleading in the Southern Elephant Seal. Indeed, a long time spent in the foraging zone suggests a strong foraging success for shallow depths (>300 m), whereas at greater depths foraging success is lower.

Image caption: Female elephant seal and her pup on Kerguelen Island. Photograph by Joffrey Jouma’a.
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.

 

Nonlinear responses of ecosystem carbon fluxes and water use efficiency to nitrogen addition

Dashuan Tian, Shuli Niu, Qingmin Pan, Tingting Ren, Shiping Chen, Yongfei Bai and Xingguo HanView of typical steppe, Inner Mongolia, China (left) and experimental site of nitrogen addition (right). Photo by Qingmin Pan.

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Human activities (e.g. fertilization and fossil fuel combustion) have greatly altered the global nitrogen cycle, leading to widespread reactive nitrogen inputs (nitrogen deposition), which may have profound impacts on ecosystem processes (e.g. biomass production, carbon and water cycles) and services. Therefore, it is an urgent task for scientists to explore how such elevated nitrogen inputs affect ecosystem processes. However, most previous simulation experiments dealing with the influences of nitrogen deposition on ecosystem carbon and water cycles used only two discrete levels of nitrogen treatment (i.e. with and without addition of nitrogen), which cannot reveal the likely nonlinear response of these processes to continuous nitrogen deposition in terrestrial ecosystems.

The Eurasian steppe is the largest remaining natural grassland in the world, and is subjected to increasing levels of nitrogen deposition. To evaluate the impacts of nitrogen enrichment on ecosystem functioning in this grassland ecosystem, we have started a long-term nitrogen addition experiment with multiple nitrogen input levels in a typical steppe ecosystem in Inner Mongolia of China, a representative area of Eurasian steppe, since 2000. In the current study, we focused on the responses of carbon and water processes to a gradient of nitrogen addition. We showed that both ecosystem carbon uptake and ecosystem respiration followed nonlinear patterns with increasing levels of nitrogen addition, and specifically that the magnitude of nitrogen-induced increases in these processes declined at high nitrogen levels relative to those at low nitrogen levels. In contrast, ecosystem-level water flux was not greatly affected by nitrogen addition. Therefore, the response patterns of ecosystem water use efficiency, the ratio of carbon uptake to water loss, were mainly determined by carbon rather than water processes. These findings have important implications for predicting the changes in ecosystem carbon and water balance under future nitrogen-enriched scenarios and for the management of the world’s largest natural grassland.

Image caption: View of typical steppe, Inner Mongolia, China (left) and experimental site of nitrogen addition (right). Photo by Qingmin Pan.
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.

 

Small but active – pool size does not matter for carbon incorporation in belowground food webs

Johanna Pausch, Susanne Kramer, Anika Scharroba, Nicole Scheunemann, Olaf Butenschoen, Ellen Kandeler, Sven Marhan, Michael Riederer, Stefan Scheu, Yakov Kuzyakov and Liliane RuessConnectedness food web visualizing qualitative feeding relationships in the investigated arable soil (Photo credit: B. Lang).

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Soils store approximately 80% of global terrestrial carbon (C) and small changes of fluxes into and out of this pool may influence the atmospheric CO2 concentration and interact with climate change. Soil food webs are important drivers of major ecosystem functions such as C and nutrient cycling, and hence they play a central role in soil fertility as well as in C stocks. Despite this importance, the cryptic soil habitat and the complex interplay between multitudes of organisms hamper the understanding of C and energy fluxes through the soil food web.

Carbon resources enter the soil as shoot- and root-litter after plant death and as organic compounds released by living roots (rhizodeposits). In particular in agroecosystems, where aboveground plant biomass is harvested, C dynamics are largely controlled by the input of rhizodeposits. Rhizodeposits contain various substances that can easily be utilized as C and energy source by bacteria and fungi and are passed on to higher trophic levels.

To follow the flux of rhizodeposits into the food web of an arable system, maize plants were exposed to 13C-enriched CO2. 13C is a natural isotope of carbon, usually occurring in low amounts in the environment. After 13CO2 assimilation by plants, we followed the release of C from living roots into the soil and into various food web members. These were microorganisms (bacteria and fungi), microfauna (nematodes – small roundworms), mesofauna (mites and springtails) and macrofauna (spiders, beetles).

In contrast to general views we showed that the flux of root-derived C in soils is not necessarily driven by pool size, i.e., by food web members with large C stocks. Instead, members with small pool size but with high turnover rates (growth and death) dominate the C flux through the food web. This becomes evident at our arable site where easily available rhizodeposits are predominantly utilized by fungi and channelled through the fungal energy pathway to higher trophic levels. Our findings disprove the widely held idea of the dominance of the bacterial-energy channel and showed the importance of the fungal-energy channel for belowground utilization of root-derived C in arable soil.

Image caption: Connectedness food web visualizing qualitative feeding relationships in the investigated arable soil (Photo credit: B. Lang).
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 foraging behaviour of four co-occuring perennial grassland plant species alone does not predict behaviour with neighbours

Gordon G. McNickle, Michael K. Deyholos, and James F. Cahill Jr.A pot with one individual of each of the four species competing in soil.

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To the untrained eye plants might appear to be more like inanimate objects than organisms that exhibit complex behavioural responses or engage in competitive games with neighbour plants. However, like any living organism, plants must solve problems in a world full of complex and ever changing stimuli. A plant that does respond adaptively to these changing stimuli should outperform a plant that does not. Indeed, if you know where to look, you will find that plants are remarkably good at assessing and responding to a variety of stimuli in ways that are often best described using behavioural models.

Here, we explored what has become known as the nutrient foraging behaviour of plants either growing alone or with neighbours. When plants are alone, it is well established that their foraging behaviour is to place more roots into nutrient rich patches than they do in nutrient poor patches. However, it is less well understood how plants forage in the presence of other plants that are competing for those nutrients in soil. We showed that the behaviour of plants grown alone does not predict the behaviour of plants grown with neighbours. Instead, plants grown with competitors engage in a sort of arms race for nutrients under competition: they produce more total roots in the presence of competitors than they do when grown alone. Broadly speaking this is a result that is predicted from game theory. Plants are playing games with each other!

Image caption: A pot with one individual of each of the four species competing in soil.
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.

 

Visual and odour cues: how plants change after herbivore damage and pollination

Dani Lucas-Barbosa, Pulu Sun, Anouk Hakman, Teris A. van Beek, Joop J.A. van Loon and Marcel DickeA Hoverfly visiting a Black Mustard flower. Photograph credits: Dani Lucas-Barbosa.

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Plants in nature interact with many antagonistic organisms, such as insects that feed on them, and beneficial organisms, such as carnivorous and pollinating insects. To defend themselves against plant-feeding insects, plants can, for instance, produce odours that can be used by carnivores to find their herbivorous prey. However, odours that plants produce upon herbivore attack may repel pollinators that help the plant to reproduce, by carrying pollen from one flower to another. Thus, the attraction of pollinators may conflict with attraction of carnivorous insects. In this study, we investigated the role of plant chemistry in such a conflict. We assessed how plant chemistry changes after pollination or to damage by herbivores, and how this affects the behaviour of flower visitors. In terms of plant chemistry, we investigated how the production of odours and visual cues changes after the plant has been pollinated, and exposed to herbivore damage. Both herbivores and pollinators elicit important changes in the chemistry of flowers. Black mustard plants indeed change their odour production as well as the production of compounds that can confer colour to flowers, after having been pollinated or exposed to insect damage, or even to both. Our results show that butterflies use different cues when searching for a plant to deposit their eggs, or for a flower to feed from. Changes in chemistry, following pollination, influenced the behaviour of butterflies that feed on nectar, but not that of hoverflies that collect pollen from the flowers. We discuss the results in the context of the trade-off between plant defence and pollinator attraction, and suggest that changes after herbivory can interfere with changes after pollination. Therefore, these responses must be addressed in an integrated way because, in nature, plants are exposed to herbivores and pollinators at the same time.

Image caption: A Hoverfly visiting a Black Mustard flower. Photograph credits: Dani Lucas-Barbosa.
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.

Mechanisms and consequences of facilitation in plant communities

The dark side of facilitating grasses

Richard Michalet, Christian Schöb, Sa Xiao, Liang Zhao, Tuo Chen, Li-zhe An and Ragan M. Callaway Cushion of Thylacospermum caespitosum facilitating beneficiary species in the Qilian Shan range (China).

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In stressful environments, such as the high alpine, plants often benefit from each other’s presence. For example, shrubs or plants with so-called cushion morphologies ameliorate the most stressful conditions in the high alpine by providing substrate for other plants to root and providing access to water and nutrients. Such positive effects of cushion plants for other plant species are very widespread in the alpine and an important process to sustain alpine biodiversity. However, the close co-occurrence of these other, so-called beneficiary species with the cushion plant may feed back to the benefactor cushion and influence their fitness. This feedback effect of the beneficiary species on the benefactors is still poorly understood. In this study we show that grasses associated with benefactor cushions have a negative feedback effect on cushions, whereas other associated species, such as other herbaceous species and shrubs don’t. Some of our results even demonstrated positive feedback effects of herbaceous plants on the cushion, indicating some sort of symbiosis. In contrast, the grasses acted more like parasites of the cushions. In addition, since we replicated this study at over 30 sites across the globe, we could also demonstrate that this negative effect of grasses on the benefactor cushions was strongest under dry environmental conditions. This suggests that the co-occurrence of grasses and the cushion plant increased competition for water among them, thereby reducing the fitness of the cushion. As a consequence, while earlier studies showed that beneficiary species have mostly a negative feedback effect on their cushion benefactors, with this study we could show that it is in particular the grasses that are responsible for this ‘cost’ of facilitation by the cushion plants.

Image caption: Cushion of Thylacospermum caespitosum facilitating beneficiary species in the Qilian Shan range (China).
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

Macrophysiology – a decade of novel insights

Steven L. Chown and Kevin J. GastonTiliqua rugosa (sleepy lizard) in a South Australian agricultural landscape. Macrophysiology provides a means to understand life’s responses to such impacts at broad scales.

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The investigation of variation in physiological characteristics over large geographic and temporal scales, and the ecological and evolutionary implications of this variation, has now been undertaken, as a defined field, for a decade. Known as ‘macrophysiology’ the field has contributed substantially to our understanding of the world. A notable example is the demonstration that geographic variation in the ability of animals to tolerate high temperature is much less pronounced than geographic variation in responses to low temperature. Moreover, it appears that environmental temperatures are close to tolerances in tropical and subtropical areas. In consequence, climate change may be especially problematic for species from the tropical and mid-latitudes. These concerns have now made their way into conservation policy.

This review provides a range of other examples of progress realized by the field, and then shows how macrophysiology can further help to address some of the most pressing modern challenges of environmental change. It also shows just how similar evolved responses to the environment are in plants and animals, though the benefits of comparing these groups have yet to be fully realized. We identify 10 key challenges for macrophysiology. These include better understanding of geographic variation in organismal characteristics, understanding how small scale climate variation affects plants and animals, working out how multiple interacting factors might influence populations, and exploring how modification of landscapes by urban areas and agriculture has affected plant and animal environmental responses.

We provide a comprehensive overview of the current standing of the field and its future prospects, giving any newcomer immediate access to its conceptual and methodological foundations. Easy access to the full range of work in the field is also provided along with rich graphic illustrations of its relationships to other areas of biology and the insights it has delivered.

Image caption: Tiliqua rugosa (sleepy lizard) in a South Australian agricultural landscape. Macrophysiology provides a means to understand life’s responses to such impacts at broad scales.
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.

 

Experimental reduction of hematocrit affects reproductive performance in European starlings

Raime B. Fronstin, Julian K. Christians and Tony D. WilliamsEuropean starling. Image provided by authors.

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Hemoglobin plays a critical role in the transport of oxygen from the lungs to the tissues. It is therefore widely assumed that hemoglobin levels and hematocrit (the proportion of blood volume occupied by red blood cells) are positively related to aerobic performance. Indeed, in birds, hemoglobin and hematocrit increase during aerobically demanding periods such as migration. However, hematocrit and hemoglobin levels generally go down during egg production in female birds, and this decrease can be similar in magnitude to the increases associated with activities such as migration. Furthermore, these decreases can persist beyond egg production, into incubation and chick-rearing. Why would females decrease their aerobic capacity just before they have to gather food for their offspring? One hypothesis is that the decrease in hematocrit is caused by the increased estrogen levels needed to produce eggs. This could potentially mean that estrogen creates a non-resource based trade-off (i.e. one that does not depend on competition for a limiting resource) between egg production and chick-rearing. Such a trade-off would be novel and intriguing, but its existence hinges on the assumption that decreased hematocrit will adversely affect reproductive performance. To address this question, we treated free-living female European starlings (Sturnus vulgaris) with phenylhydrazine (PHZ), which destroys red blood cells. Females treated with PHZ after the removal of their first clutch took longer than controls to produce a replacement clutch, but there were no other effects on measures of reproductive performance. Females treated with PHZ during incubation had chicks that were lighter at hatch. Furthermore, in one of two years, females treated with PHZ during incubation produced fewer and smaller fledglings. The year in which PHZ affected fledgling size and number was a particularly difficult year (low annual productivity) based on other data. Our results suggest that the decrease in hematocrit that routinely occurs during egg production may exert costs on subsequent stages of reproduction, but that these costs may be exacerbated when ecological conditions are poor.

Image caption: European starling. 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.

 

Climate-induced collapse of a tropical predator-prey community

Beata Ujvari, Gregory Brown, Richard Shine and Thomas MadsenBeata Ujvari and Thomas Madsen catching water pythons in the “good old days” when the snakes were common.

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If climate change threatens wildlife populations, will that be by gradual shifts in mean condition such as rainfall and/or temperature, or by increased frequency of extreme weather events? Based on long-term data (from 1991 to 2014), the aim of the present study was to analyze and compare the responses of predator (water pythons, Liasis fuscus ) and prey (dusky rats, Rattus colletti ) to extreme climatic events versus normal, albeit highly variable, climatic conditions in the Australian wet-dry tropics. From 1991 to 2005, water pythons and dusky rats showed significant climate-driven fluctuations in numbers, and annual fluctuations in rat numbers generated a corresponding variation in female python reproductive output (recruitment). Our analyses showed that annual variation in recruitment was the main factor in driving the annual variation in water python numbers. The fluctuations in rat and python numbers recorded from1991 to 2005 were, however, trivial compared to the impact of two massive but brief (24 h) deluges in 2007 and 2011. The two extreme weather events resulted in massive and rapid flooding of the dusky rat’s habitat which drowned virtually the whole rat population. As dusky rats constitute the water python’s main prey, the two floods have resulted in the pythons experiencing an unprecedented famine in 7 out of the last 8 years. The virtual lack of prey has resulted in a significant reduction in python feeding rates, reproductive output, growth rates, condition, survival, body length and importantly in python numbers, from a high of 3173 snakes recorded in 1992 to 96 in 2013. Our results demonstrate that attempts to predict animal responses to climate change, even if based on long-term studies, may be doomed to failure. Consequently, biologists may need to confront the uncomfortable truth that increased frequency of brief unpredictable bouts of extreme weather can influence populations far more than gradual deviations in mean climatic conditions.

Image caption: Beata Ujvari and Thomas Madsen catching water pythons in the “good old days” when the snakes were common.
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.

 

How tadpole competition affects frog guts and feeding

Sarah S. Bouchard, Chelsea R. Jenney O’Leary, Lindsay J. Wargelin, Julie F. Charbonnier, and Karen M. WarkentinRed-eyed treefrog, Agalychnis callidryas, metamorph.  Photo credited to Karen M. Warkentin.

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The transformation of an aquatic, herbivorous tadpole into a terrestrial, carnivorous frog is a striking example of metamorphosis, involving coordinated changes in many body parts. Legs grow, the tail is absorbed, and the tiny tadpole mouth becomes the broad mouth of a frog. The digestive system, particularly the intestine, is also dramatically remodeled for the frog’s new diet, shrinking in length by about 80%. During the aquatic tadpole stage, digestive systems also vary. In ponds teeming with tadpoles, where individual tadpoles compete for food, they develop very long guts that help them extract more nutrients from their food. Despite this, they grow slowly and emerge from the water as small frogs. In contrast, when tadpoles are few and far between and food is abundant, they invest less in intestines, but are still able to grow fast and leave the water as large juvenile frogs. In the red-eyed treefrogs of Central American rainforests, small frogs that emerge from competitive pond environments grow quickly after metamorphosis, whereas large ones from resource-rich ponds grow slowly once on land. In this research we asked why, specifically testing the hypothesis that initial differences in tadpole guts, despite their radical shortening during metamorphosis, might partially persist to affect frog feeding and growth on land. We raised tadpoles in large outdoor tanks with either high or low levels of competition. Low tadpole competition resulted in big, fat frogs that took nearly two weeks after metamorphosis to begin feeding regularly. High tadpole competition produced very small, skinny frogs that were one third the size of the larger frogs. These small frogs began feeding at a high level even before they finished absorbing their tadpole tails. Despite large differences in body size, small frogs had the same length guts as large frogs. This means that differences in tadpole guts do persist after metamorphosis, despite the extensive remodeling that takes place.

Their relatively large guts allow very small frogs to eat the same amount of food as large frogs without sacrificing digestibility. Together, long guts and high feeding rates help explain why small juvenile frogs grow faster than large ones.

Image caption: Red-eyed treefrog, Agalychnis callidryas, metamorph. Photo credited to Karen M. Warkentin.
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.

 

Immune response in breeding elephant seals

Hannah E. Peck, Daniel P. Costa and Daniel E. CrockerFemale northern elephant seal with suckling pup. Photo provided by authors.

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Mounting an immune response to infection requires substantial energy. During reproduction, animals must balance the energy requirements of investing in their offspring with the energy required for immune responses that will insure their health and survival. Some animals, known as capital breeders, leave their food resources during reproduction and used stored body reserves to supply these energy costs. Little is known about the impact of capital breeding strategies on the ability to resist infections in mammals. Northern elephant seals forage in the marine environment, breed in dense terrestrial colonies, and exhibit high rates of milk production while fasting completely from food. Their body reserves strongly influence how much milk they give their pups. Mobilizing fat for milk production requires elevation of cortisol, a stress hormone that frequently suppresses the immune system in other animals. We characterized their ability to resist infection by measuring a suite of immune markers in 197 blood samples from elephant seals at the beginning and end of their breeding and moult haul-outs on land. We explored impacts of breeding, body condition, and plasma cortisol on the ability to fight infections while on shore.

Immune system responses were greater and more varied among individuals during breeding. Body mass and fat reserves had positive associations with the ability to fight infections. A marker for the ability to resist infection by parasites was lower in animals with higher cortisol. These data show that coming together in dense breeding colonies increases the risk of infection and that committing energy to milk production while fasting reduces the ability of mothers to fight these infections. Elephant seal mothers need to balance the energy required to stay healthy and survive with the energy needed to make milk and produce healthy pups.

Image caption: Female northern elephant seal with suckling pup. 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.

 

Structure and functioning of intertidal food webs along a shorebird flyway

Teresa Catry, Pedro M. Lourenço, Ricardo J. Lopes, Camilo Carneiro, José A. Alves, Joana Costa, Hamid Rguibi-Idrissi, Stuart Bearhop, Theunis Piersma and José P. GranadeiroShorebirds gather in large numbers at tidal flats of Bijagós archipelago, Guinea-Bissau.

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Shorebirds are long distance migrants which during the non-breeding season depend on an intercontinental network of extremely diverse coastal wetlands at temperate, sub-tropical and tropical latitudes. In these wetlands, shorebirds gather in huge numbers and mostly feed on macroinvertebrates (e.g. worms, crustaceans and molluscs), playing a key role as predators in local food webs. These food webs include the whole network of trophic interactions among all co-existing organisms, as well as the transfer of nutrients and energy (trophic pathways) from its basal sources (e.g. plants) to primary consumers (e.g. macroinvertebrates) and their predators (e.g. shorebirds). Structure and dynamics of food webs depend on an extensive range of biotic and abiotic conditions which might vary considerably among areas.

In our study we characterized food webs using a set of community metrics based on stable isotopes. Stable isotopes (such as carbon δ13C and nitrogen δ15N) can inform the trophic ecology of consumers (i.e. what eats what), given that isotopic composition in tissues of consumers is directly linked with their diet. We compared the structure and functioning of food webs in four tidal ecosystems along a shorebird flyway: Tejo estuary (Portugal), Sidi Moussa (Morocco), Banc d’Arguin (Mauritania) and Bijagós archipelago (Guinea-Bissau). Our results suggest that food web structure is shaped by the number of trophic pathways of organic matter transfer. Indeed, the food web of Banc d’Arguin was characterized by lower trophic diversity and higher functional redundancy (higher number of community members with similar trophic roles) than the other sites, which might be related to the lack of inputs from both freshwater and nutrient-rich offshore oceanic waters.

There were also differences in the organization of shorebird communities among the study areas, which were largely coincident with the patterns found for the whole food webs. Shorebird communities of Banc d’Arguin and Bijagós archipelago showed comparatively low inter-specific niche overlap, which might result from species differently exploiting available resources. As tropical systems typically offer comparatively lower harvestable prey biomass for shorebirds, niche partitioning can be a strategy to reduce inter-specific competition. While our results highlight the trophic plasticity of species inhabiting areas with distinct environmental conditions, they also suggest that shorebirds’ community structure might serve as a proxy to describe the overall structure of tidal food webs.

Image caption: Shorebirds gather in large numbers at tidal flats of Bijagós archipelago, Guinea-Bissau.
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.

 

Assessing the ability of flies to adapt to heat

Sandra Hangartner and Ary A. HoffmannDrosophila melanogaster. Photo provided by authors.

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Average temperatures are now predicted to increase by 2-4°C by the end of the century and extreme temperatures are expected to increase even further. This can threaten the survival of species if their upper thermal limits are repeatedly exceeded. Whether animals have the capacity to evolve to adapt to increasing temperatures is widely debated but still poorly understood. One of the limitations of work carried out to date is that resistance to extreme temperatures has been measured in different ways, but the relationships between components of resistance measured by these different methods is unclear.

The fruit fly, Drosophila melanogaster, has been extensively used to study thermal resistance. Previous studies have produced inconsistent results on its evolutionary capacity to increase upper thermal tolerances. We have therefore re-examined this issue using the powerful approach of selection experiments. These experiments also allow us to test the extent to which resistance can be altered and whether different components of resistance are connected or independent.

To undertake selection, we exposed the flies to high temperatures in each generation and then selected the most heat resistant flies. We also kept flies as control populations which were not exposed to any heat stress. After more than ten generations of strong selection, we tested for differences between the selected and control populations. We found that the selected flies had evolved higher heat resistance in all components measured, but the increase in resistance amounted to no more than 0.5°C. We also showed that these changes did not depend on the way in which resistance was measured.

These results suggest that while D. melanogaster flies have some evolutionary potential to become more resistant to heat, there are limits to this potential. The level of evolution detected here may be insufficient to keep up with temperature increases predicted under climate change. If evolution of upper thermal tolerance is also similarly constrained in other species, then those species that live at temperatures near their upper tolerance limit may be at a particularly high risk of extinction following climate change.

Image caption: Drosophila melanogaster. 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.

 

Individual plasticity of fish metabolic rate

Tommy Norin, Hans Malte and Timothy D. ClarkJuvenile barramundi. Photo by Timothy Clark.

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Metabolic rate can vary substantially between individual fish of the same species, size, and sex, with some individuals metabolising energy 2-3 times faster than others. This between-individual variation can have considerable ecological and evolutionary consequences as it is associated with variations in growth and other important life history traits. However, almost nothing is known of how this diversity in metabolism is impacted by the dynamically changing conditions of the natural environment. We first measured how individual barramundi, a tropical fish inhabiting estuaries and tidal creeks in Australia, differed in their resting and maximum metabolic rates, as well as in their metabolic scope for various energy-demanding tasks (termed aerobic scope) under acclimation conditions (35 ppt salinity, 29oC, 100% air saturation). Subsequently, we determined how differences in these metabolic attributes were related to the individual fish’s metabolic response (i.e. their change in metabolic rate) when faced with environmental changes in salinity, temperature, and oxygen availability. We found a close relationship between the metabolic attributes of the individual fish at their acclimation conditions and how much the fish changed their metabolic rates when environmental conditions were altered. Individuals that had elevated metabolic attributes under acclimation conditions showed little change in resting or maximum metabolic rate and aerobic scope in response to low salinity (10 ppt) and high temperature (35oC), but maximum metabolic rate and aerobic scope were greatly depressed by low oxygen availability (hypoxia; 45% air saturation). In contrast, individual barramundi with low metabolism under acclimation conditions displayed a substantial increase in resting and maximum metabolic rates, as well as in aerobic scope, in response to high temperature and (to a lesser extent) low salinity, but hypoxia had very little effect. These findings highlight the diversity of physiological responses to environmental change within a population by showing how individual fish can remain metabolically insensitive to one environmental stressor at the cost of being highly sensitive to another. This suggests that possession of certain physiological traits may be advantageous in dynamically changing habitats, depending on the combination of environmental challenges being faced.

Image caption: Juvenile barramundi. Photo by Timothy Clark.
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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