Lay Summaries

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

Lay summaries for the current issue.

 

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

 

Slow development as a cost of long life

Martin I. Lind, Hwei-yen Chen, Sara Meurling, Ana Cristina Guevara Gil, Hanne Carlsson, Martyna K. Zwoinska, Johan Andersson, Tuuli Larva and Alexei A. MaklakovPhotograph provided by authors.

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Long life is not for free; instead evolutionary theory predicts that investment in early life reduces lifespan, since resources are taken away from maintenance of the body, resulting in short life and reduced resistance to stressful conditions. Commonly, high reproduction is associated with short life, but in many cases animals can have high reproduction and still have a long life. Can long life then be for free after all?

Reproduction is not the only costly trait; animals also have to develop from an egg cell to a fully developed sexually mature animal, and they also have to grow larger. Previous studies have shown that rapid growth is also associated with short lifespan. But what about development? To develop new cells and tissues is fundamentally different from growing in size, but these processes are hard to separate. The millimeter-long soil nematode worm Caenorhabditis remanei offers an opportunity to differentiate between development and growth, since cell division and therefore development stops at sexual maturation, while most of the growth remains.

We studied this using evolution in the lab. First we selected worms in environments with different stress levels. Worms from stressful environments evolved a longer lifespan, at the cost of slow development. We then performed another evolution experiment, where we selected worms with either short or long development time. We found that worms that had evolved long development were also long-lived and stress resistant, while they still had the same reproduction as the fast developing worms, and no consistent pattern was found for growth. Thus, our results suggest that fast development is costly in terms of lifespan and stress resistance.

Why do animals then develop fast? Many animals live in temporary environments, for example a seasonal environment where development has to be finished before winter comes or the pond dries out. The nematode in this research naturally lives on decomposing fruit, an environment that is short-lived and where fast development would be advantageous. Our results therefore suggest that organisms living in temporary environments, which have repeatedly been shown to evolve fast development, may pay the price of a short lifespan.

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

 

Resistance of plant–plant networks to biodiversity loss and secondary extinctions following simulated environmental changes

Gianalberto Losapio & Christian SchöbSampling plot of plant species in the Sierra Nevada Mountains (Spain) at 2725 m a.s.l. The grass Festuca indigesta Boiss. (Poaceae) is supporting other plant species to survival in this stressful environment. © Christian Schöb.

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In Mediterranean alpine ecosystems, harsh conditions make plants’ lives difficult: drought, low temperature, poor soil and strong winds are some of the problems plants have to cope with to survive and reproduce. Two decades ago, ecologists started to report that plants can cooperate with neighbouring plants to survive in such a harsh environment. Since then, hundreds of studies were subsequently conducted, but few of these described the network of interacting plant species, despite our knowledge that natural plant communities are organized in such interaction networks. Thus, it remains unclear whether such plant interaction networks differ in their resistance against different environmental changes. Here we assessed the susceptibility of a network of interacting plants to simulated increases in drought, temperature and drought, and nitrogen deposition.

We combined observational data from an alpine vegetation in the Sierra Nevada Mountains (Spain) with computer simulations to explore the probabilities of these environmental changes causing species extinctions, either due to environmental conditions becoming unsuitable or due to the loss of their microhabitat. We found that plant interaction networks’ responses, and the extinctions of species, depended on the type of environmental change. In particular, the studied plant community was most resistant against species losses when drought increased. However, it was least resistant, and experienced early and heavy species losses, when nutrient pollution increased. We further showed that the higher network resistance against increasing drought was due to drought-tolerant species that facilitated the survival of many other plant species.

This study suggests that the fate of species and communities with the on-going global environmental changes will depend on the main driver of environmental change and how this might affect the network of interacting species. Consequently, knowledge about species interaction networks in natural communities could improve our understanding of how ecosystems will respond to global changes, which in turn may help to improve current conservation and restoration practices.

Image caption: Sampling plot of plant species in the Sierra Nevada Mountains (Spain) at 2725 m a.s.l. The grass Festuca indigesta Boiss. (Poaceae) is supporting other plant species to survival in this stressful environment. © Christian Schöb.
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 diverse fish species coexist in the Amazon Basin

Daniel B. Fitzgerald, Kirk O. Winemiller, Mark H. Sabaj Pérez, Leandro M. SousaHypancistrus zebra, known commonly as the zebra pleco, is one of numerous species that are found only in the Xingu River. Photo by: Mark H. Sabaj Pérez.

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In the Xingu River, a major tributary of the Amazon River, over one hundred fish species adapted to life in swift flowing water coexist in a series of rapids a few hundred kilometers long. How do tropical regions maintain such high levels of diversity? Part of the answer to this question lies in understanding why certain species occur together while others do not, a process known as community assembly. Recently, ecologists have studied community assembly using species’ traits, or characteristics such as the size and shape of different body parts that influence how species interact with their environment and other species. Shared habitat and resource requirements may cause species with similar traits to occur together, while competition for limiting resources may lead to co-occurring species having divergent trait values to minimize competition.

Different traits may be involved in separate aspects of species’ ecology, causing species occurring together to be similar in some traits and divergent in others. Species found in rapids worldwide tend to have similar body shapes designed to cope with high water velocities, but high diversity in the tropics increases potential competition for food resources. Therefore, we expected that species occurring together in rapids of the Xingu River would be more divergent in traits associated with feeding compared to traits related to swimming performance. To test this, we measured 45 traits related to swimming performance and feeding behavior for 37 species, and correlated each trait with species’ trophic position to estimate how strongly a trait is associated with feeding. Then, we tested if traits with stronger correlations with trophic position are more divergent among co-occurring species relative to weakly correlated traits.

We found traits with stronger associations to trophic position were more divergent among species occurring together compared to traits with weaker associations. This result demonstrates that multiple factors can influence community assembly simultaneously and that our understanding of this process may vary depending on the traits we analyze. It also suggests that traits involved in feeding behavior may play an important role in promoting the ecological differences that help maintain high levels of diversity in tropical rivers.

Image caption: Hypancistrus zebra, known commonly as the zebra pleco, is one of numerous species that are found only in the Xingu River. Photo by: Mark H. Sabaj Pérez.
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 nitrogen and plant diversity interact in decomposition of leaf litter in streams

Alan M. Tonin, Luz Boyero, Silvia Monroy, Ana Basaguren, Javier Pérez, Richard G. Pearson, Bradley J. Cardinale, José Francisco Gonçalves Jr., Jesús PozoImage provided by authors.

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Biodiversity is currently being lost at an alarming rate, and understanding the effects of such loss on how ecosystems function is a major scientific challenge. One key ecosystem process potentially affected by the loss of plant species is decomposition of leaf litter, which is crucial to carbon and nutrient cycling in terrestrial and aquatic ecosystems. Whether or not the number of plant species affects the rate at which litter is decomposed is still under debate, partly because of the complex role of different plant characteristics, and because of the influence of environmental variables. We explored the influence of two factors on the relationship between the number of plant species and decomposition rate in streams: the plants’ ability to harness bacteria that fix atmospheric nitrogen, making it available to the plant; and the concentration of dissolved inorganic nitrogen in the water, which is a key environmental factor, often enhanced by human activity. We conducted a laboratory experiment that mimicked stream conditions, in which we exposed different combinations of plant species, with or without nitrogen-fixing capacity, to organisms that decompose litter (microbes such as fungi and selected invertebrates) at natural and elevated nitrogen concentrations. We found that increasing the number of plant species increased decomposition rate, subject to the influence of microorganisms and invertebrates (the latter having stronger effects). However, the ability of plants to fix nitrogen was not important, as this ability was not related to the nitrogen concentration of litter, and probably because other litter characteristics played a role. In contrast, nitrogen concentration of the water modulated the effect of larger numbers of plant species on decomposition because it enhanced the decomposition of nitrogen-poor litter by microbes. Our findings suggest that the consequences of loss of terrestrial plant species for decomposition in streams will depend on the identity of the species that are lost or remain and on levels of nitrogenous pollution, typically associated with fertiliser run-off and animal and human waste.

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.

 

Differential responses of ecosystem carbon and water processes to increased and decreased precipitation

Bingwei Zhang, Xingru Tan, Shanshan Wang, Minling Chen, Shiping Chen, Tingting Ren, Jianyang Xia, Yongfei Bai, Jianhui Huang, Xingguo Han  View of the precipitation manipulation experiment in a semiarid grassland, Inner Mongolia, China. Photo by Bingwei Zhang.

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Precipitation is one of the key determinants of productivity in almost all terrestrial ecosystems, through its effects on plant photosynthesis and respiration. Global climate change is predicted to alter precipitation with greater inter-annual fluctuation, with consequent effects on plant photosynthesis and respiration, and thus on ecosystem productivity.

Arid and semiarid ecosystems, like deserts and grasslands in rainless regions, represent the largest terrestrial biome, and are extremely sensitive to changing precipitation. Therefore, arid and semiarid ecosystems play an important role in global carbon cycling. Many manipulation experiments in these regions have found increased precipitation promoted ecosystem photosynthesis and respiration, and ultimately productivity; decreased precipitation reduced them. However, it is still inconclusive whether the influence intensities are equal between decreased and increased precipitation, for the lack of experiments combining decreased and increased precipitation treatments together. To answer this question, we conducted a 5-level precipitation manipulation experiment with both decreased and increased precipitation treatments in semiarid grasslands of Northern China during 2012-2014. Specific goals were to examine the influences of changing precipitation on gross ecosystem photosynthesis (rate of total CO2 uptake by plants), ecosystem respiration (rate of CO2 release by plants and soil microbes), net ecosystem photosynthesis (difference between gross ecosystem photosynthesis and respiration, representing net ecosystem productivity), ecosystem evapotranspiration (rate of water release from soil evaporation and plant transpiration), carbon use efficiency (ratio of net to gross ecosystem photosynthesis) and water use efficiency (ratio of gross ecosystem photosynthesis to evapotranspiration).

Our study showed that decreased precipitation reduced photosynthesis, respiration and evapotranspiration; in contrast, increased precipitation did not significantly increase those processes. That is, the effects of decreased precipitation were greater than those of increased precipitation. Soil water content was the most important factor determining changes in gross ecosystem photosynthesis, ecosystem respiration and evapotranspiration. Soil temperature caused by changing precipitation, meanwhile, explained most of the variation in net ecosystem photosynthesis and carbon and water use efficiency. The asymmetric response to changing precipitation tells us that the relative effects of decreased and increased precipitation on ecosystem processes cannot be assumed to be similar. Taking this into consideration will inevitably reduce uncertainties in simulating global carbon cycling.

Image caption: View of the precipitation manipulation experiment in a semiarid grassland, Inner Mongolia, China. Photo by Bingwei Zhang.
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.

 

Temperate and tropical snails share an appetite for native and non-native temperate aquatic plants

Bart M.C. Grutters, Yvonne O.A. Roijendijk, Wilco C.E.P. Verberk, Elisabeth S. BakkerSnail eating freshwater plants. Photos provided by authors.

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The plants and animals found in our ecosystems are rapidly changing because of a warming planet and the global transport of people and goods. As a consequence, Himalayan balsam colors our river banks pink, Japanese knotweed is the bane of house owners and floating pennywort transforms waterways into buoyant lawns. Ultimately, the success of such non-native plants depends strongly on whether native herbivores feed on them. Native herbivores and non-native plants are evolutionarily novel to each other (i.e. they have not evolved adaptations to one another), which can benefit either plant or herbivore. If herbivores are maladapted to consume exotic plants, the non-native plants will grow vigorously. Alternatively, if novel plants are maladapted to native herbivores, there will be strong biotic resistance against plant invaders because herbivores will prefer them to natives. Because novelty can work both ways, it does not consistently predict the palatability of plant invaders.

We tested whether plant palatability traits (plant traits that were expected to be indicative of their palatability to snails) and the latitudinal origin of plant species would help explain the palatability of non-native plants. We fed twenty native and twenty non-native aquatic plants (some of temperate origin, others of tropical origin) to two freshwater snails, one from Eurasia, the other from South America.

Our results show that both the temperate and tropical snail herbivores preferred to eat plants with a high ratio of specific plant traits, namely the ratio of a feeding stimulant (nitrogen content, often related to protein) to a feeding deterrent (total phenolics content; phenols are defense compounds that contribute to the bitter or astringent flavor of tea). The preference of snails for novel or non-novel plants was inconsistent as both preferred temperate plant species, i.e. the tropical snail preferred novel plants and the temperate snail preferred non-novel plants. The difference in consumption rates of temperate and tropical plants was reflected in the nitrogen-to-phenolics content, which was higher in temperate than tropical plant species. These findings indicate that herbivore preference for plants depends on plant traits and the latitudinal origin of plants, not simply on the novelty of plants to herbivores. Overall, exotic plants from the tropics are less edible to temperate and tropical animals than plant invaders from temperate regions.

Image caption: Snail eating freshwater plants. Photos 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.

 

Climatic effects on population declines of a rare wetland species and the role of spatial and temporal isolation as barriers to hybridization

Katja Rohde, Yvonne Hau, Nicole. Kranz, Jasmin Weinberger, Ortwin Elle & Axel HochkirchImage provided by authors.

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Climate change and habitat fragmentation are known to have detrimental effects on the habitats of many wetland species and lead to new species compositions in these ecosystems. The impact of climate change on the interactions among species, particularly on interbreeding (hybridization) is, however, poorly understood. Hybridization can have severe consequences for the fitness of the species involved, as it might lead to genetic displacement of a species. Therefore, it is of particular interest for conservation practice to understand the effects of climate change and extreme weather events on population dynamics, population structure and hybridization.

We investigated the population dynamics of Ch. montanus (a rare, flightless grasshopper species which is strongly specialized on wetland habitats) and its sibling species Ch. parallelus, which is very widespread and common in many habitats. We hypothesized that climatic fluctuations have negative effects on the population trend of Ch. montanus. By studying the population dynamics over seven years and applying genetic methods, we further tested the hypothesis that Ch. montanus is more likely to hybridize with decreasing population size and that reproductive barriers (i.e. differences in the timing of the mating period, differences in mating behaviour or habitat affilitation) are altered by environmental changes.

We found that droughts and heavy rainfall are strongly correlated with population declines in Ch. montanus. Based on genetic and spatial analyses, we show that spatio-temporal segregation of both species provide an effective barrier to hybridization. However, this barrier can weaken if the Ch. montanus population decreases as the probability to encounter mates of the other species increases. This indicates that climatic extremes threaten rare species directly by reducing reproductive success and also indirectly by increasing hybridization risk.

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.

 

Causal relationships in food-web theory

Angelo B. Monteiro and Lucas Del Bianco FariaPhoto provided by authors.

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Ecological studies usually stress that natural communities are extremely diverse and possess a high degree of complexity. An early assumption was that this complexity promotes stability: damping the propagation of perturbations and regulating population outbreaks, while optimizing energy transfer between resources, consumers and predators. Later, however, a seminal paper used theoretical tools to assemble randomly constructed communities, and demonstrated that complexity was inherently unstable. In view of this paradox, food-web studies evaluate species trophic interactions (i.e. what eats what) to discover the mechanisms by which natural communities maintain stability despite the observed complexity. Historically, the two main research programs in food-web theory either emphasize the topological patterns in natural communities (i.e. how species are connected by feeding relationships), or the mechanisms regulating population dynamics. In this contribution, we explored the causal relationship between these two perspectives. We addressed two hypotheses: do particular topological patterns maintain population stability, or, alternatively, does population stability promote certain food-web topologies? Given that the process of collecting a large number of high-quality food-web data involves many practical problems, we simulated natural communities, but contrasted three different biological assumptions about trophic interactions. For each community, within each assumption, we measured three population-stability variables and two topological variables. Analyzing how these variables correlate, we could assemble path diagrams to infer causal relationships between them. Path diagrams measure the likelihood of each hypothesis generating the observed correlation, while evaluating if a given hypothesis is more likely than a random process. Our results demonstrated that population stability promoted food-web topology whatever the underlying assumptions about the trophic interactions. Thus, we demonstrated that only because population dynamics are stable (i.e. perturbations are damped and return to an equilibrium) are natural communities able to manifest certain topologies. These topologies are, for example, the presence of subgroups of taxa that interact more within that subgroup than with other subgroups; or the frequency of omnivorous behavior, in which, for example, a predator feeds on both the consumer and the basal resource. In addition, our results strongly support a recently proposed theory, which suggest that selection of stable topologies acts to shape natural communities into a single and consistent pattern.

Image caption: 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.

 

An experimental test of state-behaviour feedbacks: gizzard mass and foraging behaviour in red knots

Kimberley J. Mathot, Anne Dekinga, and Theunis PiersmaRed knots. Image provided by authors.

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Red knots (Calidris canutus islandica) are shorebirds that feed on hard-shelled molluscs. They swallow these prey whole and crush them in their muscular gizzards (stomachs). Gizzard mass is remarkably flexible; knots increase gizzard mass in response to seasonal increases in energy demands, and in response to decreases in the digestive quality of their diets (i.e. ratio of digestible to indigestible components). Intriguingly, free-living knots exhibit consistent among-individual differences in gizzard mass. Given that gizzard mass is so flexible, what causes some individuals to maintain relatively large gizzards and others to maintain relatively small gizzards? One possible explanation is that there are positive feedbacks between gizzard mass and diet choice. It has previously been shown that a low digestive quality diet induces increases in gizzard mass. If larger gizzards in turn increase the probability of feeding on low quality diets, then even small, chance differences in gizzard mass and/or diet choice among-individuals could be maintained over time because the feedback between gizzard mass and diet choice would act to reinforce differences between individuals. We tested this idea experimentally using wild-caught red knots. Although experimentally determined diet quality had large effects on gizzard mass, the effect of experimentally manipulated gizzard mass on diet choice was weak at best. Furthermore, we observed consistent among-individual differences in gizzard mass even when animals did not have the opportunity to choose between items of different digestive quality. We conclude that positive feedbacks between diet choice and gizzard mass play at best a limited role in maintaining among-individual variation in gizzard mass in red knots. We suggest instead that social foraging interactions may play an important role determining the expression of behaviours (e.g. intake rate) that themselves influence gizzard mass. The possibility that group composition influences individual behaviour and organ mass is a new perspective, warranting further study.

Image caption: Red knots. 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.

 

‘Reproductive effort and oxidative stress: effects of offspring sex and number on the physiological state of a long-lived bird

Thomas Merkling, Pierrick Blanchard, Olivier Chastel, Gaëtan Glauser, Armelle Vallat-Michel, Scott A. Hatch, Etienne Danchin & Fabrice HelfensteinKittwakes. Photo provided by authors.

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In an ideal world, individuals should maximize the transmission of their genes to the next generation by maximally investing in all activities related to reproduction and survival. However, such a ‘Darwinian demon’ does not exist because these activities draw on a common pool of limited resources. Consequently, individuals need to make allocation trade-offs between competing life-history traits, the physiological nature of which is largely unknown. Oxidative stress is defined as a deleterious accumulation of oxidative damage resulting from an imbalance between free radical production and antioxidant defences and/or repair mechanisms. Oxidative stress is hypothesised to underlie life-history trade-offs, because greater investment in reproduction may result in increased oxidative damage leading to faster bodily deterioration and reduced lifespan.

Despite a growing body of research, it is still unclear whether and how oxidative stress is involved in such trade-offs. Most studies to date have investigated the oxidative cost of natural or manipulated variation in offspring number. However, although the energetic requirements to producing sons or daughters can differ, the impact of variation in offspring sex-ratio on parental oxidative balance remains unexplored. Here, we studied how variation in offspring sex and number influenced several markers of oxidative stress and corticosterone levels in the black-legged kittiwake (Rissa tridactyla), a long-lived bird where sons are energetically costlier than daughters.

First, only individuals that could afford to invest heavily in reproduction did so. Those with higher pre-laying baseline corticosterone - known to facilitate higher parental workload - and lower antioxidant activity invested more in subsequent reproduction. Second, individuals rearing more sons had higher baseline corticosterone - both parents - as well as oxidative stress - mothers only - than those rearing daughters, and those rearing chicks for longer accumulated more oxidative damage to their lipids.

Our study provides the first evidence that brood sex-ratio can affect oxidative balance, potentially in a sex-specific manner, and highlights the need to consider offspring sex-ratio in future studies investigating the role of oxidative stress in life-history trade-offs.

Image caption: Kittwakes. 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.

 

Contrasting effects of climate and population density over time and life-stages in a long-lived seabird

Rémi Fay, Christophe Barbraud, Karine Delord and Henri WeimerskirchSPhotographic credit: Aurélien Prudor.

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Demographic processes of wild populations are affected by environmental variability. Such functional relationships have been extensively studied for many organisms but mainly through adult vital rates (e.g. adult survival and fertility). So far, early-life stages have strikingly been less studied because of the inherent difficulties in tracking the fate of young individuals. Yet, young organisms are expected to be more sensitive to environmental stochasticity owing to their inexperience and lower competitive abilities. Hence, this lack of information on the juvenile compartment of populations currently constrains our ability to fully understand population dynamics.

In this study, we investigated the effect of climate and population density on early-life demographic parameters of a long-lived seabird, the wandering albatross. We provided evidence that climate and population size affected both survival and age at first reproduction of young individuals, but in different ways according to the trait. In particular, although both early-life demographic parameters are affected by population density, we found that survival was more strongly impacted by density than age at first reproduction, showing different sensitivities to changes in population density. We also found a shift in the effect of population density on age at first reproduction, suggesting that density dependence mechanisms can temporarily disappear. In the context of globally decreasing seabird abundance, density dependent processes could be less evident but still essential to consider for long term population size projections.

With regard to environmental conditions, we showed that increasing sea surface temperature had a positive effect on young individuals becoming reproductive at a younger age, while at the same time, it had a negative impact on juvenile survival. We suggest that age-specific demographic responses to sea surface temperature observed in wandering albatrosses may be caused by the age-specific at sea distribution and thus local oceanic responses to climatic variation. Such results show that it is essential to consider age effects to understand population responses to climate change, since similar climatic conditions may have opposite effects on individual performances according to the life stage considered.

Such results are critical for our ability to make robust predictions on the impact of climate change on marine predators such as albatrosses.

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

 

Leaf Dry Matter Content is better at predicting above-ground Net Primary Production than Specific Leaf Area

Simon Mark Smart, Helen Catherine Glanville, Maria del Carmen Blanes, Lina Maria Mercado, Bridget Anne Emmett, David Leonard Jones, Bernard Jackson Cosby, Robert Hunter Marrs, Adam Butler, Miles Ramsvik Marshall, Sabine Reinsch, Cristina Herrero-Jáuregui and John Gavin HodgsonExclosure. Photo provided by authors.

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We depend on plants to do something truly amazing: that is turning carbon dioxide and minerals into food using nothing more than water and sunlight. Because plants are so important it is no surprise that we have spent millennia moving them from place to place, cultivating them and feeding them to domesticated animals. Yet as well as providing food and timber they also do other amazing things for us for free like contributing to soil formation, providing nectar, helping stabilise the climate and even reminding us of the places where we have lived and worked. However we also know that the environment is changing in ways that are hard to predict. If changes in water supply, soil moisture, nutrient levels and climate alter the conditions for plant growth then, because we depend on plants so much, the free services that plants provide could also change in any one place. If that happens we need to know about it and plan for it. This means developing models that can estimate what a future environment might mean for plant growth. Getting these models right means basing them on good scientific understanding about which plant properties are the best indicators of the effect of environmental change and which are most closely linked to the things we need from plants. In our research we studied two properties of plant leaves that were known to be correlated with the production of vegetable matter. If an easy to measure property can predict plant production then this relationship could be used to help develop more accurate models and maps. In fact we found that the easiest property to measure, called Leaf Dry Matter Content, had the strongest correlation with plant production. It tends to be low for plants that grow quickly and produce more vegetable matter per year – think green grasses in the lowlands that cows like – versus plants that have a greater proportion of dry matter and grow more slowly – think Heather or Oak trees. The unique thing about our study was that we successfully measured productivity across an unusually large range; from high mountains through to lowland pastures.

Image caption: Exclosure. 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.

 

The shape of fish success beneath the ocean waves

Sonia Bejarano, Jean-Baptiste Jouffray, Iliana Chollett, Robert Allen, George Roff, Alyssa Marshell, Robert Steneck, Sebastian Ferse, Peter J Mumby Fish in a reef. Photo credit: Dr. Mark Priest.

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Coral reefs dissipate large amounts of energy carried by ocean waves, and offer a broad spectrum of sheltered to powerfully turbulent habitats. Underwater, wave energy shapes the landscape of the seafloor, and affects the distribution of the associated fauna and flora. Coral reef fishes, essential for ecosystem services and ecological functions, are no exception. Herbivorous fishes in particular, play crucial roles in maintaining productive and healthy coral-dominated systems. Certain species are however considered slow swimmers, based on the shape of their fins, and tend to be excluded from turbulent habitats. The way herbivorous fishes and their feeding rates are further affected by wave exposure, based on their overall swimming performance, remains poorly understood.

In this study, we assess the swimming performance of 37 fish species using ten morphological traits related to swimming mode, speed, and manoeuvrability. We record their feeding frequency using video cameras on 12 sites distributed across sheltered, moderate, and turbulent reefs. We find that some species minimise drag through a hydrodynamic shape while others rely on tail propulsion. Feeding frequency is limited for certain species on turbulent reefs, while it is unaffected or increased for others.

There are important implications of these findings. Herbivorous fishes have been classified in four subgroups capable of feeding on different types of algae. Subgroups are usually considered complementary to each other, and species within subgroups are often viewed as functionally redundant, meaning that they can replace each other. However, we find that two important subgroups (grazers and scrapers) and the species within them respond differently to wave exposure. The fact that grazers responded differently to wave exposure compared to scrapers emphasises their distinctness and complementarity. Because certain grazers and scrapers responded differently to wave exposure compared to their counterparts, we highlight the risk in regarding species within subgroups as redundant. We therefore challenge the way biodiversity is often perceived and confirm that species presence does not imply their complete functionality, especially under harsh environmental conditions. We demonstrate that neither redundancy nor complementarity, which are desirable attributes of communities and prerequisites for resilient systems, should be assumed to be homogeneous throughout heterogeneous systems.

Image caption: Fish in a reef. Photo credit: Dr. Mark Priest.
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.

 

Goldenrod “eavesdrops” on the communication of its specialist herbivore and defends itself in proportion to its proximity to the communication source

Eric C. Yip, Consuelo M. De Moraes, Mark C. Mescher and John F. TookerPhotograph by E.C. Yip.

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Plants often employ chemicals that deter feeding to defend themselves from herbivores; however, if plants allocate resources to defensive chemicals, they may have fewer resources left for growth and reproduction, thereby making these defences costly. To mitigate the cost, defensive chemicals are often not continuously produced, but rather deployed only after herbivore attack. Plants can further anticipate attack and accelerate defence deployment by “priming” defences in response to cues that indicate future herbivory. We recently discovered that goldenrod (Solidago altissima) primes itself for defence by “eavesdropping” on the chemical communication of its specialist herbivore, the gall fly Eurosta solidaginis. Male flies perch on the tips of goldenrod and release an airborne chemical blend that attracts females. When exposed to this chemical emission, goldenrod increases its defensive chemistry and suffers less damage from herbivores. In this experiment, we examined the distance the priming signal extends from the fly by monitoring stems at varying distances from a central stem caged with a male fly. Leaf damage increased with distance from the fly, suggesting that, as the chemical signal dissipates, plants prime themselves to lesser degrees. Contrary to the predicted trade-off between plant defence and growth, stems caged with flies grew faster than stems without flies; however, increased growth and defence early in the season did not result in greater flower production, as stems caged with flies produced a similar number of flowers as those stems farthest from the fly. Instead, stems that were a mid-distance from the fly experienced decreased growth and flower production. The gradation of plant defence surrounding each fly is likely important in goldenrod fields, where individual stems are often only a few centimetres away. As herbivores move from more to less defended plants, they might alter their distributions, with possible ramifications for the entire goldenrod community. Our finding that stems a mid-distance from the fly were shorter with fewer flowers suggests that the ultimate consequences of priming on the reproductive success of plants may be complex and require further investigation.

Image caption: Photograph by E.C. Yip.
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.

 

Oxidative stress reduces song rate in subordinate individuals

Simone Messina, Marcel Eens, Giulia Casasole, Hamada AbdElgawad, Han Asard, Rianne Pinxten and David CostantiniEuropean starling, Sturnus vulgaris. ©David Costantini.

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Work on ‘honest signalling’ has been a major area of research in animal behaviour and evolutionary ecology in recent decades. Honest signals accurately reflect individual quality, which depends on various interacting factors, such as foraging capability and also functionality of the hormonal and immune systems. In recent times, it has been suggested that dysfunctional regulation of the oxidative balance (resulting in oxidative stress) might be a significant handicap for the expression of sexual signals in low quality individuals. The term ‘oxidative stress’ describes a state where oxidative damage to body tissues increases because oxidising molecules, which are mostly a by-product of metabolism, exceed the body’s level of antioxidant defences, and thus are free to react with molecules like lipids, proteins and nucleic acids.

We examined experimentally for the first time whether a state of oxidative stress influences song behaviour in male starlings (Sturnus vulgaris). Males were injected with a substance that reduces specifically the synthesis of a key cellular antioxidant called glutathione. Treated subordinate males suffered increased oxidative damage, while treated dominant males did not. Treated subordinate males also reduced their song rate. On the other hand, treated dominant males did not suffer any reduction in song rate. Our study therefore provides experimental support for the hypothesis that acoustic signals may honestly convey information about the individual’s oxidative status and capacity to regulate its oxidative balance, raising the possibility of hitherto unexplored impacts of oxidative stress on fitness traits in social species.

Image caption: European starling, Sturnus vulgaris. ©David Costantini.
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.

 

Robustness of insect-flower networks to disturbance

A.J.Vanbergen, B.A.Woodcock, M.S. Heard and D. S. ChapmanInsect-flower network.

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The connections formed between species by their feeding interactions can lend stability to the structure of ecological networks. Environmental change can re-organise species interactions and affect the capacity of a network to absorb or resist shocks. Using community networks comprising flowering plants and insects seeking pollen and nectar, we investigated if habitat disturbance by cattle affected network robustness to species extinctions.

With these field data, we simulated extinction cascades, the number of secondary extinctions following a plant species extinction, which we correlated with variation in network structure between disturbed and undisturbed habitat. We also tested whether species’ differences in their level of dependence on mutualism (where species mutually benefit in terms of food and/or reproduction) affected the propensity for extinction cascades. For example, bees depend wholly on pollen and nectar for nutrition, whereas many other insects like flies and butterflies do not, at least as larvae. Similarly, certain plants need insect pollinators for reproduction, while others do not. Species less reliant on mutualism should thus have lower risk of extinction, so we expected the balance of mutualism-dependency in the network would also affect its robustness.

Habitat disturbance produced larger, species-rich networks that were less connected. Disturbed networks were also wholly re-organised, with fewer, more specialised interactions and reduced nestedness (specialist species interacting with generalists). Changes to network structure from habitat disturbance and the level of mutualism dependence affected different aspects of community robustness to simulated plant extinction. Disturbance increased network robustness by reducing connectance, thereby lowering the chance that a plant species extinction could propagate through the network to eliminate an insect species. Although, when an initial insect extinction occurred then the larger size of disturbed networks increased the probability of another extinction, and so they were more prone to large extinction cascades. However, once we accounted for variation in species’ dependence on mutualism, the disturbed networks were disproportionately more robust to very large extinction cascades.

Our study reveals multiple mechanisms (network size, connectance, mutualism dependence of species) that affect the robustness of plant-pollinator networks to extinctions and hence community cohesiveness under environmental pressure.

Image caption: Insect-flower network.
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.

 

Does water shortage generate water stress?

Karim Barkaoui, Marie-Laure Navas, Catherine Roumet, Pablo Cruz and Florence Volaire Experimental plot in the Mediterranean rangeland of study (Larzac Causse, South of France).

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In the Mediterranean, increasing aridity has major impacts on species composition and functioning of plant ecosystems, especially of grasslands. Under increasing aridity, less drought-adapted plant species may disappear from local vegetation, while plant biomass, productivity and water exchange with the atmosphere may be strongly reduced. Consequently, the regional biodiversity dynamics as well as the carbon and water cycles could be modified. 

Water stress occurs when water availability is too low to fulfill plants’ requirements. Physiological responses such as stomata closure help plants to save water by controlling transpiration flows, but in return they have negative effects on plant health. Beyond a certain threshold of water stress intensity and duration, plant survival is threatened. In drought-prone areas, perennial vegetation was therefore hypothesized to have ‘optimally’ adjusted water requirements, buffering water stress to low levels over time. However, the mechanisms underlying such possible adjustments are not clear. 

In this study, we focused on local soil conditions and tested whether water stress may be buffered along a gradient of soil water availability in a Mediterranean rangeland. During five successive years, we assessed soil water use dynamics and plant biomass productivity, and determined water stress in twelve contrasting plant communities along the soil gradient. Our observations revealed that water stress remained quite similar in intensity and duration along the soil gradient, suggesting the existence of local buffering mechanisms as predicted by theory. In addition, plant biomass productivity and water consumption were together proportionally related to local soil water availability. We hypothesized that the abundance of slow-growing species with lower water requirements increased with decreasing soil water availability while plant density decreased, explaining how full soil depletion is avoided and water stress buffered. Despite many expectations, vegetation water-use efficiency did not change along the soil gradient. 

Predicting how plant ecosystems will be altered by increasing aridity remains an important challenge. Considering the relative invariance of water stress, we concluded that ‘stressful’ habitats may not exist for well-established vegetation. Species replacement ensures proportionality relationships between plant productivity, water consumption and soil water availability. Such mechanism could underpin how plant ecosystems may ‘optimally’ adjust to aridity.

Image caption: Experimental plot in the Mediterranean rangeland of study (Larzac Causse, South of France).
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.

 

Tree species functional group is more important for soil carbon stock and soil nutrient status than tree species diversity across six major European forest types

Seid Muhie Dawud, Karsten Raulund-Rasmussen, Sophia Ratcliffe, Timo Domisch, Leena Finér, François-Xavier Joly, Stephan Hättenschwiler, Lars Vesterdal1-species (Norway spruce) and 5-species forest plot (Norway spruce, Scots pine, hornbeam, oak, birch) in the exploratory platform site of the FunDivEUROPE project in Białowieża, Poland. Photo Credit: Dawid Zieliński.

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Forests deliver a range of ecosystem services to society, such as climate regulation, by storing carbon (C) in biomass and in soil, while other services such as maintaining soil nutrient status support the provision of sustained wood production. Selection of tree species can influence soil properties, but it remains unclear whether conversion to more species-diverse forests can increase soil C stock or influence soil nutrients. Mixed forests composed of tree species with complementary traits and growth habits could possibly exploit resources more efficiently than single-species forests, thereby improving forest ecosystem functioning. Studies of wood production and aboveground C stocks have supported this idea, but the influence of tree species diversity on soil C stock and soil nutrients remains unexplored for common forest types at the European scale.

We used 209 plots from the FunDivEUROPE project covering six major, widely-distributed European forest types to explore the effects of tree species diversity (1 to 5 tree species) and tree species type (conifers vs. broadleaves) on soil C stock and soil nutrient status, as indicated by C/N ratio and pH. We found a modest, but consistent positive effect of tree species diversity on soil C stocks across the six forest types, whereas effects on soil nutrient status were region-dependent. Tree species type was more important than tree species diversity; soil C stocks increased and soil nutrient status decreased with an increasing share of conifers in the forests, but the impacts differed between forest types. The results imply that targeted selection of tree species with desired characteristics (e.g. complementary traits for effective resource use) is a preferred management approach for influencing soil C stock, C/N ratio and pH in mixed forests, rather than increasing the number of tree species per se. Such information is needed to evaluate consequences of ongoing species loss, but also to develop sound management approaches for the selection of tree species mixtures to support soil nutrient status and increasing C stocks in forest ecosystems adapted to climate change.

Image caption: 1-species (Norway spruce) and 5-species forest plot (Norway spruce, Scots pine, hornbeam, oak, birch) in the exploratory platform site of the FunDivEUROPE project in Białowieża, Poland. Photo Credit: Dawid Zieliński.
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.

Commentary

Relationships grow with time – watch out when estimating diving energetics!

Lewis G. Halsey Photograph provided by authors.

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We are rightly fascinated by the underwater exploits of diving animals, which hold their breath for unconscionable durations while diving into the great depths of our oceans in search of prey. Our own bodily limitations make it very difficult to observe them in this realm. Instead, since the 1960s scientists have been developing ever more cunning, miniature devices to attach to diving animals, that record enlightening data on their exploits, such as the animals’ body temperature, the light levels around them, their heart rate, and their levels of activity. Because breath-hold diving animals have to return to the surface eventually, to breathe, they are presumably very energetically efficient while underwater, to make the oxygen stores they take down with them last a long time. So it is important to understand how efficient they really are. Measures of heart rate or activity levels can potentially provide good estimates of oxygen consumption during diving. Unfortunately, while investigating whether activity levels in diving animals, which are measured using accelerometers, correlate with their energy expenditure, some scientists have been introducing an error to their analyses. I have coined this 'the time trap’: the process of correlating summed values of energy expenditure with summed value of activity levels. These two variables are likely to show a strong relationship simply because both of them include the duration of the experiment. I demonstrate with modelled simulations how data for energy expenditure and activity levels that are completely unrelated can nonetheless appear related once each of them are summed. When investigating the efficacy of variables as a measure of energy expenditure in diving animals, scientists need to be careful to compare rates of energy expenditure with rates of activity level (or heart rate, or any other potential proxy of energy expenditure), rather than summed values.

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

 

Treadmill endurance predicts how far salamanders move in the wild

Robert D. Denton, Katherine R. Greenwald, and H. Lisle Gibbs A mole salamander (genus Ambystoma) is measured for walking endurance on a custom treadmill (left) and a breeding Small-mouthed Salamander (A. texanum) is observed at a vernal wetland field site (right). While only active for a small portion of the spring, these small salamanders can travel long distances to new breeding wetlands, a result supported in this study by both genetic data and physiological performance trials.

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The movement of animals between breeding populations is one of the foundational mechanisms by which these populations persist. This dispersal process is complex and includes several stages: the decision to move, the act of movement, and the resulting breeding event in a new population. Combining data that represents these stages of dispersal is important for furthering our understanding of animal movement and persistence, but few studies have provided such a link.

We combined measurements of dispersal ability (walking endurance) with the end product of dispersal (immigrant animals in new population) to understand if walking endurance is related to actual animal movement. We collected this data among two groups of mole salamanders (genus Ambystoma): Small-mouthed Salamanders (A. texanum) and an all-female group of clones that “steals” sperm from males of other Ambystoma species. Because of the genetic complexity of these all-female Ambystoma salamanders, we predicted that they would exhibit physiological limitations and reduced dispersal distances.

As predicted, Small-mouthed Salamanders walked four times longer on treadmills before fatiguing, and dispersed animals were identified approximately twice as far from their place of birth compared to individuals from the all-female lineage. This result is the first to link a potential physiological limitation for dispersal to the resulting pattern of animal movement in the landscape. This example, where greater walking endurance is associated with greater dispersal distance, also informs our spatial understanding of how sexual and all-female salamanders coexist while directly competing with one another. Impressively, our genetic data reveals that these small amphibians travel an average of 10 kilometers to new breeding sites across a rugged and challenging agricultural landscape.

Image caption: A mole salamander (genus Ambystoma) is measured for walking endurance on a custom treadmill (left) and a breeding Small-mouthed Salamander (A. texanum) is observed at a vernal wetland field site (right). While only active for a small portion of the spring, these small salamanders can travel long distances to new breeding wetlands, a result supported in this study by both genetic data and physiological performance trials.
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Juvenile concentrations of IGF-1 predict life-history trade-offs in a wild mammal

Nora Lewin, Eli M. Swanson, Barry L. Williams and Kay E. HolekampHyena mother with cubs.

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In fluctuating or competitive environments, various trade-off patterns may arise and persist within populations. For example, a life history characterized by ‘live fast, die young’ may be optimal for some individuals, while a ‘slow and steady’ life history may be more advantageous for others. However, it remains largely unclear what determines whether organisms will adopt one life history over another. Here we investigated the hypothesis that circulating concentrations of the growth hormone insulin-like growth factor-1 (IGF-1) in early life (between 5.5 and 12.1 months of age) mediate life history trade-offs later in life. To accomplish this, we used detailed hormone and life-history data collected over the past 26 years from a wild population of spotted hyenas (Crocuta crocuta) in Kenya. Hyenas were followed from birth to death to capture the entire lifespan and a full reproductive history.

Consistent with our hypothesis, we found that a hyena’s IGF-1 concentration as a youngster predicted various life-history trade-offs later in life. Specifically, we found that females with higher IGF-1 concentrations lived a faster pace of life: they were heavier than normal as juveniles, more likely to survive to reproductive maturity, gave birth to their first litters at earlier ages, and had shorter adult lifespans. Females with lower IGF-1 concentrations exhibited a slower pace of life: they were smaller than normal as juveniles, were less likely to survive to reproductive maturity, gave birth to their first litters at older ages, and had longer adult lifespans. We investigated the reproductive consequences of these life histories and saw that a shorter lifespan correlated with higher annual reproduction, but a longer lifespan positively correlated with the number of offspring.

Our study highlights the importance of early postnatal development as a determination point in mammals, and suggests that circulating hormone concentrations measured during the first year of life can be used to predict reproduction and lifespan in animals that live up to 23 years in the wild.

Image caption: Hyena mother with cubs.
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Compounded perturbations in coastal areas: contrasting responses to nutrient enrichment and the regime of storm-related disturbance depend on life-history traits

Iacopo Bertocci, Jorge A. Domínguez Godino, Cristiano Freitas, Monica Incera, Ana Maria Ferreira Bio, Rula DomínguezImage provided by authors.

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Natural systems are exposed to simultaneous perturbations, including climate-related physical disturbances (e.g. wave impact during storms) and nutrient inputs. There is increasing evidence that temporal variation in disturbance can be as important as average disturbance intensity in shaping the structure of animal and plant communities. Nevertheless, most previous studies have focused on a single disturbance, while experimental tests of the combined effects of multiple perturbations are generally lacking. Filling this gap is key to understanding, and possibly anticipating, ecological responses of natural assemblages to climate change, combined with other globally relevant stressors. For example, marine coastal systems are exposed to the physical impact of waves during storms. Climate change implies not only an increase in the intensity of events (more severe storms), but also modifications to their temporal distribution (e.g. several severe storms in a short period of time, separated by calm periods). Intense precipitation is a common component of storms, and is responsible, through erosion and terrestrial runoff, for the delivery to coastal areas of nutrient-rich water from inland agricultural fields, industrial plants and urban areas.

In this study, we examined the effects of manipulations of nutrient enrichment and mean intensity and temporal variability of storm-like mechanical disturbance on benthic assemblages of tide-pools along an Atlantic rocky coast in Portugal.

We observed consistent negative effects of disturbance intensity on the mean cover of long-living taxa (algal canopies and the polychaete worm Sabellaria alveolata), whose temporal fluctuations were also reduced by more severe mechanical stress. More resilient taxa (ephemeral green algae) increased under enriched conditions, particularly when low intensity events happened irregularly in time. The effect of physical disturbance intensity on filamentous algae depended on the availability of nutrients; cover was reduced by the high, compared to the low, intensity treatment combined with the natural nutrient, but was increased by high intensity disturbance combined with nutrient enrichment. Grazers (such as limpets and sea urchins) were also more abundant under nutrient enrichment, likely responding to the increase in algal food caused by this treatment.

Our study provides one of the first experimental tests of responses to realistic changes in the regime of multiple anthropogenic perturbations. However, all examined organisms persisted throughout the study, even under the most stressful experimental conditions. Therefore, in systems like this one, where most organisms have great tolerance to disturbance (through high resistance and/or quick recovery), the separate or interactive effects of the various components of the disturbance/nutrient enrichment regime may cause population fluctuations via changes in relative species abundance, rather than by elimination and substitution of species. Our results contrast with the theory that large fluctuations in abundance, by temporarily reducing species to near-zero levels, are directly related to the risk of local extinction of species. Consequently, our findings may help to predict the combined impact of direct and indirect human-induced perturbations on the biodiversity of marine and terrestrial systems, e.g. grasslands and some coral reefs, in which the dominant organisms share similar recovery abilities. Moreover, they call for analogous experiments to test whether similar responses occur in other systems.

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.

 

Heating the superorganism: Comprehensive metrics of thermal performance

Clint A. Penick Sarah E. Diamond, Nathan J. Sanders and Robert R. DunnImage provided by authors.

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For millions of years, species have faced changes in climate that have shaped their evolution and their biology. The result is that species display differences in key traits that can be used to predict their responses to climate change in the future. For the most part, these traits capture responses of individuals, but what about species that live in groups? Can we also predict how colonies of ants or bees will respond to climate warming based on traits of individuals?

To find out how individual traits correlate with performance of an entire colony, we compared the thermal limits of ant foragers with optimal temperatures required for colony survival and growth. Ant species whose foragers could tolerate hotter temperatures—and could forage under hotter conditions—also had higher survival at warm temperatures. In contrast, less heat-tolerant species were able to maintain growth at cooler temperatures and stay active over a longer portion of the year.

The relationship between forager thermal limits and thermal requirements for colony growth suggest two strategies ants adopt when dealing with their thermal environment: species can either forage in the heat and restrict growth to a short season, or they avoid the heat and extend growth over a longer portion of the year. With future climate warming, we predict that heat-tolerant species will be able to expand their growing seasons and, ultimately, increase competition with less heat-tolerant species.

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.

 

Parents protect offspring from negative effects of UV-B radiation

Ensiyeh Ghanizadeh Kazerouni, Craig E. Franklin and Frank SeebacherGuppies. Image provided by authors..

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Parents go to great lengths to make sure that their offspring fare well in the real world. Caring for offspring such as providing food and shelter is common among many vertebrates. However, there is also a different form of parental influence over their offspring, which is mediated by biochemical signals in response to changes in the environment such as diet or temperature. In this case, the environment induces particular enzymes in parents that change the way genes are expressed. As a result, offspring may do better, because their characteristics are matched to the environment they experience later in life. The downside of such "epigenetic modifications" is that there is a chance that parents get it wrong and offspring are actually mismatched to their environment.

We show here that UV-B radiation, which is the harmful radiation contained in sunlight, can act as a trigger for epigenetic modifications. We used guppies, a tropical fish that is popular with aquarium keepers, to show that exposure of parents to UV-B radiation renders their offspring more resilient to its harmful effects. These interactions are of course beneficial when animals live in areas that experience a lot of sunshine. However, there is a drawback. Offspring whose parents were exposed to UV-B, but who themselves are not exposed, become more susceptible to infection. Exposure of parents to UV-B can thereby be damaging to their offspring. Whether or not epigenetic modifications are beneficial therefore really depends on the environmental conditions experienced by both parents and offspring. These dynamics are quite complex. However, it is really important to understand them both for the sake of understanding how animals evolved in different environments, and to predict the consequences of environmental degradation by humans. Ozone layer depletion and deforestation, for example, have an enormous impact on the levels of UV-B animals are exposed to. Knowing the biological responses to UV-B will be instrumental for effective management and remedial action.

Image caption: Guppies. 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.

 

Seasonal transitions and aggressive phenotypes

Nikki M Rendon, Andrea C Amez, Melissa R Proffitt, Elizabeth R Bauserman and Gregory E Demas Siberian hamsters in long “summer-like” days (left) exhibit thin, brown/grey coats and display low levels of aggression despite have high levels of oestradiol. In contrast, hamsters in short “winter-like” (right) days exhibit thick white coats and are highly aggressive despite having low levels of oestradiol. Short-day hamsters compensate for low hormone sources during the winter by increasing sensitivity in areas of the brain associated with aggression, but not reproduction. Photo credit: JM Ho.

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In many animals, appropriately expressed aggression functions to allow the successful acquisition of limited resources such as territory and mates, which increases the chances of surviving and reproducing. Non-breeding aggression may aid in the acquisition of food, a limited resource during winter, thereby functioning much like aggression observed during breeding conditions. The mechanisms of seasonal aggression, however, remain largely an enigma. One leading theory suggests that breeding aggression is regulated by gonadal steroids such as testosterone and oestrogen; however, these hormones are low during the non-breeding season. How, then, is non-breeding aggression fuelled when sources of hormones are not available?

In order to answer this question, we looked for evidence of increased sensitivity to oestradiol during non-breeding conditions in year-round highly territorial female Siberian hamsters (Phodopus sungorus). Within a seasonal context, we manipulated day length (photoperiod), the primary cue used by most animals to detect seasonal transitions, and mimicked winter, early spring and summer conditions. Females were much more aggressive but had lower levels of oestradiol during winter-like conditions when compared with summer/spring-like hamsters. These results reveal that across seasonal transitions the paradox of high levels of aggression despite low levels of gonadal steroids is specific to winter-like periods. Since oestradiol acts on oestrogen receptors resulting in robust biological and behavioural action, we quantified oestrogen receptors in the brain, predicting that winter-hamsters would have more receptors in areas associated with aggression. Our results supported this hypothesis.

We propose a compensatory mechanism involving increased oestradiol sensitivity specific to regions associated with aggression underlying winter-like aggression. The lack of changes in areas associated with reproduction facilitates the decoupling of these two behaviours, likely manifesting as mating being prevented from occurring during the winter but allowing aggression to persist. Such insights help us get closer to explaining the mechanistic paradox of robust aggressive behaviour that occurs outside of mating contexts and reveals potential candidates that could explain changes in aggression and other social behaviours on seasonal and evolutionary timeframes.

Image caption: Siberian hamsters in long “summer-like” days (left) exhibit thin, brown/grey coats and display low levels of aggression despite have high levels of oestradiol. In contrast, hamsters in short “winter-like” (right) days exhibit thick white coats and are highly aggressive despite having low levels of oestradiol. Short-day hamsters compensate for low hormone sources during the winter by increasing sensitivity in areas of the brain associated with aggression, but not reproduction. Photo credit: JM Ho.
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.

 

New analysis shows that the body feathers of birds evolved in response to lifestyle

Péter L. Pap, Orsolya Vincze, Beatrix Wekerle, Timea Daubner, Csongor I. Vágási, Robert L. Nudds, Gareth J. Dyke, Gergely OsváthPelican. Image provided by authors.

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Bird feathers are amongst the best known biological structures; having feathers is what makes ‘a bird a bird’. However, what is much less well-known and understood is just how the huge range of different feather types that are seen within birds are influenced by the functions they perform. Birds don't just have feathers on their wings that are used for flight, they also have ‘body feathers’ that cover their bodies and that are used for insulation and water-proofing, amongst other functions. Although it seems obvious that birds that dive underwater need their body feathers to work in different ways to those that live in cold environments, the reasons underlying how these differences evolved have never been tested.

Our new study shows that there is a clear relationship between a bird’s habitat, the temperature at which it lives, and body feather structure. To further investigate this relationship, we measured five key parameters of bird body feathers and related them to lifestyle and temperature. Taking evolutionary history into account, we show that mode-of-life is the key factor controlling the evolution of body feather structural parameters in birds. Thus, the morphology of body feathers is the result of selection pressures from the environment.

Our research builds on earlier work hypothesizing that both habitat and temperature regulation control the morphology of these feathers. We were able to confirm several predictions in this research; living in water means that a bird’s body feathers are more likely to be shorter and fluffier, reflecting a need to perform better in water by being more buoyant (trapping air close to the body) and water resistant. In contrast, life in low temperatures means that a bird’s body feather are likely to be longer and less fluffy.

Although our earlier results are tantalizing, much more work remains to be done to understand the factors underlying the evolution of the diverse range of feathers seen in living birds.

Image caption: Pelican. 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.

 

Thermal over predation benefits of enclosed vs open nests

Thomas E. Martin, Andy J. Boyce, Karolina Fierro-Calderón, Adam E. Mitchell, Connor E. Armstad, James Mouton and Evertius Enroe Bin Soudi Blue-naped Chlorophonia (Chlorophonia cyanea) sitting on its nest in Venezuela.  It builds a nest of moss and rootlets that is enclosed on all sides except the opening (photo by T. E. Martin).

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Many species of animals construct nests to raise offspring, but nests can differ in their structure. More complex nests that are enclosed on all sides except the opening (see image) are usually thought to provide greater protection from predators than simpler open cup nests that are exposed on all sides. Enclosed nests might also help keep eggs, nestlings, and their parents warm or shaded, but historically this potential benefit has been considered of secondary and minor importance. Yet, broad tests are lacking.

Using data from the literature and our own field studies at five sites on four continents, we show that a higher proportion of songbird species build enclosed nests in the tropics and southern hemisphere compared to the northern hemisphere. Predation is commonly thought to be greater in southern regions, so this pattern may reflect protection from predators, as historically thought. However, based on data from 319 species, we show that nest predation risk is not actually greater in southern regions compared with northern regions, nor is it consistently lower in enclosed compared to open nests. Both results challenge widely accepted perspectives and raise questions about the benefits of building enclosed nests.

Enclosed nests may improve thermal conditions, which can benefit growth, development, and survival of adults and offspring. We provide three pieces of evidence that suggest thermal benefits are important: 1) Species that built enclosed nests were smaller than species using open nests, and since smaller species lose heat fastest, they benefit most from thermal protection. This directly contrasts with the predation hypothesis, where larger species often have higher predation rates, and should tend to build more enclosed nests. 2) Parents of species with enclosed nests incubated eggs for less time than open nests, as can be expected if eggs cool slower in enclosed nests due to thermally favorable conditions. 3) Offspring of species using enclosed nests exhibited faster growth of mass and wings compared with open nests, suggesting that when less energy is spent on staying warm, more energy is available for growth. Enclosed nests may therefore provide more consistent thermal than nest predation benefits, counter to long-standing perspectives.

Image caption: Blue-naped Chlorophonia (Chlorophonia cyanea) sitting on its nest in Venezuela. It builds a nest of moss and rootlets that is enclosed on all sides except the opening (photo by T. E. Martin).
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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