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.

 

 

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

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

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

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

 

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

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

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

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

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

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

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

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

 

Socioecological predictors of immunity in wild spotted hyenas

Andrew S. Flies, Linda S. Mansfield, Emily J. Flies, Chris K. Grant, and Kay E. Holekamp Spotted hyena (Crocuta crocuta) feeding on the carcass of a giraffe that has been dead for three days. Photo by Andrew S. Flies.

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The immune system is critically important for survival and any breakdown of immune defenses could result in death. Most of what we know about the vertebrate immune system has been acquired by performing experiments on animals whose diet, pathogen exposure and social interactions are all tightly controlled. However, wild animals must compete for food and mates, produce offspring, avoid being killed by predators, and respond to a broad range of diseases over the course of their lifetime.

In this study we examine the effects of sex, social rank, and reproductive status on immune defenses in spotted hyenas (Crocuta crocuta) that can live for more than 20 years in the wild and are routinely exposed to a plethora of pathogens, including rabies and anthrax, yet rarely show signs of disease. Here we show that high-ranking spotted hyenas have stronger immune defenses than low-ranking hyenas. Additionally, females have stronger immune defenses than males, which is similar to the pattern observed in most other mammals. Interestingly, female hyenas are (unusually for mammals) larger and socially dominant to male hyenas, so we had suspected that the size and dominance reversals might also lead to a reversal of immune defense levels, but this was not the case.

We also found that immune defenses are lower in females when they are lactating than when they are pregnant. Producing milk for offspring actually uses more energy than producing the offspring in the first place, so this suggests that lactating females spend so much energy producing milk that they cannot spare extra energy for immune defenses. Our observations that high-ranking hyenas have stronger immune defenses than low-ranking hyenas also suggests that activating the immune system uses large amounts of energy, because high-ranking hyenas get more high-quality food than low-ranking hyenas and thus can devote more energy resources to immune function.

Altogether these studies shows that sex, social rank, and reproductive status are important for immune defenses. This information can help us predict how pathogens will impact wild animals at the individual and population levels and may lead to new insights into the relationship between socioeconomic status and disease in humans.

Image caption: Spotted hyena (Crocuta crocuta) feeding on the carcass of a giraffe that has been dead for three days. Photo by Andrew S. Flies.
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.

 

Ecological equivalence of species within phytoplankton functional groups

Crispin M Mutshinda, Zoe V Finkel, Claire E. Widdicombe, Andrew J IrwinDitylum brightwellii is one of many diatom species observed at Station L4 in the Western English Channel.

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Phytoplankton are a very diverse set of microscopic photosynthetic organisms that live in the upper sun-lit region of the water column. They account for about half of all photosynthesis on Earth. Anthropogenic climate change is expected to change phytoplankton biogeography and productivity through changes in temperature, resource availability, and ocean physics. Climate models that aim to predict changes in phytoplankton productivity usually approximate the tremendous diversity of phytoplankton by a very small number of functional groups, but the validity of this approximation is rarely tested. Two contrasting views of the dynamics of individual species’ biomass are that variability is driven primarily by changes in the environment and interactions among species (called niche selection) or alternatively that variability is largely random and all species are ecologically equivalent (called the neutral model).

Here we develop models to describe the variation in biomass of two major functional groups (diatoms, dinoflagellates) observed at a time-series station in the Western English Channel and show that the functional groups are strongly affected by niche selection. We then test if the biomass of individual species relative to the total biomass of the corresponding functional group varies neutrally or if there is evidence that individual species are further selected by environmental or other factors. We show that phytoplankton species vary neutrally within their functional group, which supports the approach of aggregating many species into broad functional groups for modeling purposes.

Image caption: Ditylum brightwellii is one of many diatom species observed at Station L4 in the Western English Channel.
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.

 

South for the winter? Foraging effort and divergent strategies in fur seals

Benjamin Arthur, Mark Hindell, Marthan N. Bester, W. Chris Oosthuizen, Mia Wege and Mary-Anne LeaFemale Antarctic fur seal with geo-location tag (flipper) and time-depth recorder (back). Credit Chris Oosthuizen.

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Obtaining food is a problem that is faced by all animals. As a result, a diverse array of foraging strategies has evolved to acquire food resources. Understanding these strategies, and the choices made by foraging animals, is a fundamental aim in animal ecology. Air-breathing divers, such as seals, are a unique case when examining foraging choices, as individuals must forage throughout both horizontal and vertical space within the limits of oxygen availability. Being able to measure foraging effort within dives can reveal not only how animals use their environment, but the energetic trade-offs associated with different foraging strategies, particularly when combined with additional information on location, dive depth and dive duration.

Using a novel within-dive approach, we quantified the foraging effort of 12 female Antarctic fur seals across a wide geographic area in the Southern Ocean during their post-breeding winter migrations. We identified two main contrasting foraging strategies. Seals that stayed closer to the colony and remained North of the Polar Front (a prominent oceanographic feature) had relatively long and deep dives and an increased foraging effort. On the other hand, seals that travelled South of the Polar Front had relatively short and shallow dives with a reduced foraging effort. As the prey of fur seals is closer to the surface at night and therefore more easily accessed, the longer night duration further south at this time of year also meant that these seals had more available foraging time each day. However, seals foraging in this region also have to balance the energetic cost of travelling to such remote areas.

The fact that these two contrasting foraging strategies seemingly co-exist within the population indicates that neither currently offers a significant long-term energetic advantage over the other. However, our results raise questions about the viability of these strategies over the long term, particularly with potential future changes to population size and environmental conditions.

Image caption: Female Antarctic fur seal with geo-location tag (flipper) and time-depth recorder (back). Credit Chris Oosthuizen.
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.

 

Direct and indirect effects of shrub encroachment on alpine grasslands mediated by plant-flower-visitor interactions

Carlos Lara-Romero, Cristina García, Javier Morente-López and José M. IriondoImage provided by authors.

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Rural abandonment is widespread across anthropic landscapes and, in combination with global warming, has elicited profound shifts in the composition of plant communities. These changes in vegetation have cascading effects on many organisms that interact with plants, such as microorganisms or pollinators. As a result, ecosystem services provided by these ecosystems, such as pollination services, may be extensively altered.

Alpine grasslands have been reported to undergo rapid shrub encroachment in recent decades mainly as a result of rapid land-use changes. This is expected to impact the population dynamics of native herbs by modifying the type and strength of their mutualistic interactions, such as the pollinator services that are crucial to seed production. Yet we lack a robust quantification of the effect of shrub encroachment in modifying plant-pollinator interaction networks between native alpine herbs and their floral visitors (as a proxy for pollinators).

The Functional Biodiversity Hypothesis (FBH) states that higher diversity of functionally complementary plants (the producer trophic level) contributes to better meeting of pollinator requirements (the consumer trophic level). This in turn results in increased diversity of specialist pollinators and improved plant performance (via increased pollinator services provided by specialist pollinators). In order to evaluate the effect of shrub encroachment in alpine grasslands we tested the FBH by applying network theory that accounts for both trophic levels simultaneously. We compared several structural metrics of two plant-floral visitor networks collected in two alpine grasslands, one of them undergoing a moderate level of shrub encroachment.

Encroached grasslands harboured a more diverse community of both herbaceous flowering plants and floral visitors than non-encroached ones, thus supporting the FBH. Moderate levels of shrub encroachment increased the number of pollen visitors per plant, but it also intensified indirect plant-plant competition for shared pollinators, which can result in reduced reproductive success of key native wildflowers. From an applied perspective, our results show how changes in community function can be efficiently tracked using metrics of plant- and flower-visitor networks.

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.

 

Genes that influence salmon growth in wild don’t matter in captivity

Anti Vasemägi, Siim Kahar and Mikhail Yu. OzerovPhoto provided by authors.

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Understanding how and what genes affect ecologically important traits provides the important first step towards understanding the targets of natural selection and adaptation processes in the wild. Typically, identification of the genomic regions influencing various traits, such as growth, coloration or behaviour has been performed in controlled laboratory conditions, and it is often assumed that genes have similar effects both in the laboratory and in nature. However, the environment may strongly influence the impact of genes.

Atlantic salmon is one of the major aquaculture species and a popular target for various restoration and supplementary stocking programs, in which the species is bred and reared in a hatchery for subsequent release into the natural environment. Both selective breeding and inadvertent selection have increased farmed salmon growth rate, and earlier studies have identified a large number of genomic regions that influence growth of salmon in fish farms. However, no studies exist that have compared if the genes that affect growth in farmed conditions have similar effects in the wild.

In this study, we identified several genomic regions that influence the size of juvenile salmon only in either hatchery or natural conditions. Our results indicate that the growth of juvenile salmon is controlled by different genetic mechanisms in the two environments. We suggest that genes affecting growth of juvenile fish in fish farms are more likely driven by competition for food, aggression and energy balance; whereas genes that affect growth in the wild may be linked to other factors such as individual movement and anti-predator behavior. Our findings also imply that a substantial proportion of the genomic regions associated with growth in salmon may be specific to farmed conditions and hence, have no effect on fish growth in the wild. Our work demonstrates the benefits of studying the effects of genes in multiple environments and in a realistic ecological context.

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.

 

How do metabolic rate and food-deprivation affect sociability in fish?

Shaun S. Killen, Cheng Fu, Qingyi Wu, Yu-Xiang Wang and Shi-Jian FuImage provided by authors.

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Many animal species spend at least part of their time living in groups. With many eyes searching, group membership can allow animals to consistently find food. A potential drawback is that some group members can take more than their fair share of found food. Animals must weigh these benefits and costs when determining how closely they will associate with groups.

A number of factors might affect an animal’s level of sociability. Previous studies in fish have shown that a few days of fasting can cause individuals to stray from groups to decrease competition for food. In the same way, individuals with a higher metabolic rate could be less social to maximise food intake to satisfy their heightened energy demand. Unknown is how prolonged food-deprivation affects sociability. It is very common for wild fishes to experience weeks of food-deprivation during seasonal changes in food availability. The effects of longer-term food deprivation on sociability could differ drastically from the effects of shorter-term hunger.

We examined these issues in juvenile qingbo carp Spinibarbus sinensis. In the laboratory, individuals were either food-deprived for 21 days (to simulate a bout of seasonal food-deprivation), or fed a maintenance ration. Fish from each diet treatment were measured for metabolic rate and tested for sociability twice: once in the presence of a well-fed control shoal of fish and once with a food-deprived shoal.

Over the course of a 30 minute trial, fish that had been on a maintenance ration ventured further away from shoals, while food-deprived fish remained close to the shoal. This is unlike fish that have been fasted for a few days, which tend to decrease association with shoals. Prolonged food-deprivation may cause individuals to put such a high priority on food-acquisition that they need to remain with their group to help alert them to predators while they continuously forage.

Among well-fed fish, those with a higher metabolic rate were least sociable, especially when exposed to food-deprived shoals. This probably minimises competition, allowing them to satisfy an increased energetic demand while foraging. Overall, these results suggest that energy demand and food-deprivation – a challenge common for many ectothermic species – can affect individual sociability as well as the attractiveness of groups to members of their 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.

 

Both spreading and non-spreading exotic plants receive sufficient pollination

Mialy Razanajatovo and Mark van Kleunen Pimpinella peregrina, a non-spreading exotic plant, visited by a syrphid fly in our research garden. Photo credit: Samuel Carleial.

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As a result of introduction by humans, many plant species manage to maintain reproducing populations without further human intervention in regions where they did not naturally occur. Some of these exotic species spread in the new regions, and can cause serious environmental and economic damage. Therefore, what drives species invasions is a major question in ecology.

The ability to reproduce in the new regions determines, at least partly, whether or not exotic species can found and maintain populations. As exotic plants are decoupled from their usual pollinators, not all of them might find suitable pollinators. Exotic plants that can reproduce in the absence of pollinators and those capable of attracting suitable pollinators should therefore have an advantage over the ones that lack these capacities, as the latter might not receive sufficient pollination.

Using a common garden experiment, we compared pollination characteristics of eight native and 16 exotic plant species in Germany. We included eight widespread exotic species and eight rare ones. For each species, we assessed the degree to which fruit and seed production deviate from that expected under sufficient pollination. We also assessed fruit and seed production capacities when pollinators are excluded.

In all three plant groups (native, widespread exotic and rare exotic species), fruit and seed production did not significantly deviate from that expected under sufficient pollination, and this did not significantly differ among groups. Species in all three plant groups were, to some extent, capable of fruit and seed production when pollinators were excluded, and this also did not differ among groups. Our results thus suggest that all three plant groups receive sufficient pollination, at least in our common garden.

Plant species that do not receive sufficient pollination might not be able to found populations. Later in the invasion process, however, when the exotic species spread in the landscape, other factors that we did not investigate in our study might play a more important role.

Image caption: Pimpinella peregrina, a non-spreading exotic plant, visited by a syrphid fly in our research garden. Photo credit: Samuel Carleial.
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.

 

Wildlife mobility and extinction risk in human-altered landscapes

Amanda E. Martin and Lenore FahrigAn aerial view of New York City, New York, USA, as an example of a human-altered landscape. Photo courtesy of Jason C. Newland.

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It is widely thought that a species’ mobility affects its extinction risk in a human-altered landscape; however, some studies suggest that mobile species are less at-risk than sedentary species, while others suggest the opposite. In this study we asked: Why do studies find different effects of species mobility on extinction risk? We used a computer model to address this question, so that we could investigate a number of possible explanations, and identify which explanations are most likely and should therefore be investigated empirically.

Our results supported two explanations for the contradictory findings on the role of mobility in extinction risk. First, that the mobility-risk relationship depends on how you measure mobility: extinction risk increased with mobility when mobility was measured as emigration, i.e. the tendency of individuals to leave their home range or territory, but decreased when mobility was measured as immigration, i.e. successful movement between populations. This is likely because emigration reflects the cost of dispersal, i.e. risk of mortality when moving through human-dominated areas, while immigration reflects the benefits of dispersal, i.e. ability to recolonize unused habitat and rescue small populations that might otherwise go extinct. Second, our results suggest that the mobility-risk relationship depends on the attributes of the landscapes in which the studied species evolved. Species in landscapes with historically abundant, un-fragmented habitat and frequent disturbance had greater risk and mobility than species in landscapes with historically rare, fragmented habitat and infrequent disturbance: for these species, risk was higher for more mobile species. However, species in landscapes with high-risk matrix (i.e. non-habitat areas in the landscape) had greater risk but lower mobility than species with low-risk matrix; for these species, risk was lower for more mobile species.

To our knowledge, this is the first study to investigate why some studies find that more mobile species are less at-risk, while others find the opposite. Understanding what influences extinction risk can help us identify species of conservation concern. Our results suggest that we should focus on species with high emigration rates but low immigration rates, and those that evolved in landscapes with non-fragmented habitat and high-risk matrix.

Image caption: An aerial view of New York City, New York, USA, as an example of a human-altered landscape. Photo courtesy of Jason C. Newland.
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.

 

Parental age influences offspring telomere loss

Britt J. Heidinger, Katherine A. Herborn, Hanna M.V. Granroth-Wilding, Winnie Boner, Sarah Burthe, Mark Newell, Sarah Wanless, Francis Daunt and Pat MonaghanIncubating shag. Photo provided by Mark Newell.

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Older parents are known to produce offspring that tend to show reduced longevity. However, currently we do not know much about the processes responsible for this effect. One contributory factor might be offspring telomere length. Telomeres are protective caps at the ends of chromosomes; they function a bit like the plastic caps at ends of shoelaces and protect the coding DNA from loss during cell division. Telomere loss reduces the lifespan of cells and is thought to be involved in the ageing process. Individuals with longer telomeres or slower rates of telomere loss have been shown to live longer in a wide range of species. There is evidence that the offspring of older parents have shorter telomeres, but it is not clear whether this is due to the offspring inheriting shorter telomeres, or if their telomere loss during pre or postnatal growth is higher. We examined the relationship between the age of the parents and the telomere length of their offspring in a long-lived seabird, the European shag. We found that when the chicks first hatched, there was no effect of parental age on offspring telomere length, suggesting that there were no pre-natal effects of parental age. However, chicks produced by older parents had greater telomere loss during nestling growth than chicks produced by younger parents. These results are consistent with the hypothesis that the age of the parents influences offspring longevity in part through its effects on offspring telomere loss during post-natal growth. This could be due to a link between the quality of care that offspring receive and their telomere loss. Poorer quality care provided by older parents during post-natal growth could increase offspring stress and telomere loss. Such poorer quality care might occur because older parents are senescent, or perhaps because those parents that put less effort into rearing their offspring are more likely to live to be old.

Image caption: Incubating shag. Photo provided by Mark Newell.
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.

 

Ecological relevance of cellular energy metabolism in intertidal species

Yun-wei Dong & Shu Zhang After a summer thundershower, a limpet, Cellana toreuma, habitat on a rocky shore in Dongshan, Fujian, PR. China.

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Rocky intertidal ecosystems face some of the harshest environmental stresses on earth and are also one of the ecosystems most vulnerable to climate change. At low tide, animals living on the rocky shore frequently face high temperature, episodic heavy rainfall and other physical conditions. These stressors can at times be lethal, but, even if sublethal, they can reduce or eliminate growth and reproduction. To cope with sublethal stress, more energy has to be produced to repair stressor-induced damage.

A group of proteins called metabolic sensors are gauges of cellular energy status and can effectively regulate cellular energy production. When cellular energy level is low, the levels of genes encoding such energy sensors as AMP-activated protein kinase (AMPK) and histone/protein deacetylase sirtuin (SIRT) can be elevated. The increased levels of these genes can lead to more energy generation from improved breakdown of glucose and lipids.

In order to study cellular energy responses to high temperature, desiccation and freshwater spray (simulated rainfall), we measured the expression of genes involved in energy sensing, energy production, and energy expenditure in an intertidal limpet Cellana toreuma. During a three-day period, animals were maintained at different temperatures (18 or 30°C). Every day at 16:00-18:00, they were either aerially exposed or freshwater sprayed. Based on the gene expression patterns, all individuals could be divided into three groups. The different gene expression patterns in the three groups indicated a sequence in which individuals from group 1, group 2 and group 3 were faced with increasing shortage of energy. The frequency distributions of individuals in the three groups were different among treatments, indicating that high temperature, desiccation, and rainfall, singly or in combination, could all cause energy stress The genes examined in this study provide a validated set of indices (biomarkers) for quantifying environmental stress, including future stress from climate change, in this and, likely, other animals exposed to harsh conditions in the rocky intertidal zone.

Image caption: After a summer thundershower, a limpet, Cellana toreuma, habitat on a rocky shore in Dongshan, Fujian, PR. 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.

 

Top-down becomes bottom-up: consequences of nutrient cycling for trophic cascades between green and brown webs

Kejun Zou, Elisa Thébault, Gérard Lacroix and Sébastien Barot An oxbow lake of Bandama River, Côte d’Ivoire. Photo by Gérard Lacroix.

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Food webs represent trophic (feeding) interactions among species in ecosystems. Top-down trophic cascades in food webs are key to understanding population dynamics and ecosystem functioning. For example, because fish consume zooplankton that feed on algae, the removal of fish can increase the abundance of herbivorous zooplankton and strongly decrease the abundance of algae. Such trophic cascades are widely studied in classical food web theory, where the green (based on primary producers such as plants on land and algae in water that produce organic matter through photosynthesis) and brown food webs (based on decomposers such as bacteria and fungi that break down detrital organic substances) are usually studied separately.

Studies on trophic cascades have so far ignored that nutrient cycling connects green and brown food webs. Nutrients that cannot be assimilated or are lost from organisms can either be returned directly to the nutrient pool (direct cycling), or indirectly through decomposition processes performed by decomposers of the brown food web (indirect cycling). The recycled nutrients support primary producers in the green food web but also decomposers when their growth is limited by mineral nutrients and not by carbon.

We developed a simple food web model to explore the consequences of nutrient cycling for cascading effects between green and brown webs. We found that top-down effects propagate from one web to the other in a bottom-up way to affect ecosystem production. We show that on the one hand, since direct recycling immediately supports the growth of primary producers, predators of decomposers in the brown food web can increase or decrease primary production depending on whether they release more or less nutrients directly than decomposers. On the other hand, top predators of the green food web decrease or increase decomposer production depending on whether decomposers are carbon or nutrient limited. These results could be useful to ecosystem management where human activities strongly impact nutrient fluxes worldwide. For example, they could allow the improvement of agricultural practices through the management of belowground-aboveground interactions, or taking better account of the effects of recycling processes when using biomanipulation techniques for improving water quality.

Image caption: An oxbow lake of Bandama River, Côte d’Ivoire. Photo by Gérard Lacroix.
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.

 

Reseeders benefit from arid climates and infertile soils

Rafael O. Wüest, Glenn Litsios, Félix Forest, Christian Lexer, H. Peter Linder, Nicolas Salamin, Niklaus E. Zimmermann, Peter B. Pearman Restioid fynbos at the Roikloof dam near Ceres, South Africa. Photograph: R. O. Wüest.

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Fire is a key factor that impacts vegetation structure, composition and biodiversity both globally and locally. There is growing evidence that the effects of fire could be mediated by a basic life history trait: the ability of species to resprout after fire (resprouters) or the need to germinate from seeds (reseeders). Theory predicts that the relative proportion of resprouters in the vegetation should increase with increasing soil fertility and decreasing aridity, but little is known about how reseeders and resprouters are distributed in local plant communities with respect to environmental conditions.

The Cape Floristic Region, one of the Earth’s richest biodiversity hotspots, is to a large degree covered by fynbos vegetation. The evergreen rush-like Restionaceae family of the grass-order Poales dominate many fynbos vegetation types. These vegetation types burn frequently, grow on diverse soils with distinct levels of fertility and are exposed to various climatic conditions. This makes the Restionaceae of the Cape Floristic Region an ideal study system to investigate how aridity and soil fertility relate to the relative proportion of resprouters and reseeders in the vegetation.

Our results show that the relative proportion of resprouters is lowest in arid and unproductive conditions that do not allow for fast accumulation of biomass, i.e. fuel for fires. The resulting low fire frequency allows reseeders to complete their regeneration cycle between fires and occur at relatively high frequencies. On infertile soils, a decrease in aridity leads to faster biomass (fuel) accumulation and more frequent burning. This results in higher fire frequencies, which prohibits reseeder regeneration and favors resprouters because they can rapidly recover fire-induced vegetation gaps by resprouting from roots that survive fires below ground.

While decreasing aridity on infertile soils leads to increased fire frequency, the contrary relationship is expected on fertile soils. A decrease in aridity on fertile soils slows down drying of available fuel, leading to lower fire frequencies, which potentially eliminates the advantage of resprouters over reseeders. Indeed, our results suggest that aridity and soil fertility interact in complex ways to determine the relative proportion of resprouters in the Cape Floristic Region.

Image caption: Restioid fynbos at the Roikloof dam near Ceres, South Africa. Photograph: R. O. Wüest.
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 soil respiration components and their specific respiration change with forest succession?

Wenjuan Huang, Tianfeng Han, Juxiu Liu, Gangsheng Wang and Guoyi ZhouForest succession in subtropical China. Photo credited to Xuli Tang, Qianmei Zhang and Yunting Fang.

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Soil respiration usually includes two parts: heterotrophic respiration (RH) and autotrophic respiration (RA). The former refers to CO2 (or C) release through microbial decomposition of soil organic matter, while the latter primarily denotes respiration by roots themselves and microbial decomposition of carbohydrates derived from live roots. It is still unclear how soil respiration components change during forest development from its early to later stages (‘succession’). Based on Odum’s theory of ecosystem development, it has been hypothesized that the ratio of respiration to biomass (specific respiration) is likely to decrease with forest succession because forests tend to evolve towards less energy-wasting (i.e. a reduced ratio of maintenance to structure). However, this hypothesis has seldom been tested on the specific soil respiration components.

In this study, we practically separated total soil respiration into RH and RA using a trenching method in three successional forests in subtropical China. This method can effectively prevent tree roots from entering a dedicated volume of soil so that RH can be measured. The results showed that RH in the growing season was significantly greater in the old-growth forest than in two early-stage forests. RA in the old-growth forest also tended to be the highest among the three forests, but specific RH and specific RA showed a declining trend with forest succession. Our results highlighted the importance of forest succession in determining the variation of RH and RA. The relatively high efficiency of the old-growth forest may suggest an important mechanism for increasing C storage in subtropical soils.

Image caption: Forest succession in subtropical China. Photo credited to Xuli Tang, Qianmei Zhang and Yunting Fang.
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.

 

To sprout, or not to sprout: freezing temperature drives spring flushing

Armando Lenz, Günter Hoch, Christian Körner and Yann VitasseA mixed forest in the French Pyrenees on May 1 2007. Beech trees already started to sprout, when temperatures suddenly dropped and it began to snow, while less freezing resistant tree species have their leaves still in the protection of the buds. Photo credit: Y. Vitasse.

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For trees, as for any other organism, frost is a major determinant of the annual life cycle in the temperate and boreal zones. Deciduous trees shed their leaves in autumn and form winter-hardy buds that contain the new leaves for next spring. In the buds, young leaves are well protected from freezing temperatures in winter. The time when trees sprout differs remarkably among species growing at the very same site within a forest. For instance, rowan or wild cherry sprout more than a month earlier than maple or European beech, even if they grow side by side and experience the very same climate. But why do different tree species sprout at different times within the same climatic conditions? Since leaves are safe from freezing damage as long as they are packed into a bud, but become very vulnerable as soon as the bud opens, the timing of bud-break should reflect the species-specific ability to tolerate freezing temperatures in the newly emerging leaves in spring. We compared long-term records of low temperature extremes in spring with long-term observations of sprouting from low and high elevations in Switzerland, as well as the species-specific resistance of emerging leaves to freezing temperatures. Our study revealed that across all species studied, sprouting occurs exactly at the time when the risk of frost damage approaches zero. The variation in sprouting among temperate tree species can thus be explained by the species-specific freezing resistance of newly emerging leaves. Spring phenology ensures tree survival in an ever more variable climate.

Image caption: A mixed forest in the French Pyrenees on May 1 2007. Beech trees already started to sprout, when temperatures suddenly dropped and it began to snow, while less freezing resistant tree species have their leaves still in the protection of the buds. Photo credit: Y. Vitasse.
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.

 

Survival benefits of winter dormancy: warmer climates are associated with shorter hibernation seasons and reduced survival in rodents

Christopher Turbill and Samantha PriorCommon dormouse (Muscardinus avellanarius). Image provided by authors.

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Doing nothing can have important benefits. Many animals spend the temperate winter season in a state of dormancy. In mammals, seasonal dormancy (hibernation) is facilitated by employing periods of deep torpor, when metabolic energy expenditure is reduced to a trickle. Torpor, in combination with pre-winter fattening or food storage, permits even mouse-sized hibernators to forego all external foraging activity for a large proportion of the year.

The principal cost of activity is an increase in risk of mortality, especially from predation. Hibernation may appear to make mammals vulnerable to predation but in fact mortality rates while hibernating are five times lower compared to the active season. Enhanced survival over winter allows hibernating mammals to exhibit relatively slow life-histories (slow rates of growth and reproduction) compared to their non-hibernating counterparts.

To understand the ecological function of seasonal dormancy in mammals, we analysed published data to test for associations among local thermal climate, duration of hibernation and annual survival rate in hibernating rodents. Annual temperature is known to be linked to a negative relationship between activity and survival among lizard populations. We hypothesised that local thermal conditions might underlie an analogous pattern in annual survival rates of hibernating rodents.

We found that mean annual temperature is negatively associated with hibernation duration and annual survival rate in hibernating rodents (but not in a representative sample of non-hibernating rodents). A straight-forward explanation is the known positive effect of dormancy on survival (i.e. in colder climates, a greater proportion of the year is spent in the relative safety of hibernation). Thus seasonal dormancy has a positive effect on annual survival even in mammals. Our results suggest that shortening of winter hibernation owing to global warming will reduce annual survival rates (by 5% per 1 °C warming). Reproductive output might increase under longer growing seasons, but this compensatory effect is likely to be constrained. Our study highlights an important yet unappreciated mechanism leading to impacts of global climate change on animal populations in temperate climates.

Image caption: Common dormouse (Muscardinus avellanarius). 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.

 

Which is more important: direct environmental effects, or local adaptation, in determining how many times animals reproduce?

Lin Schwarzkopf, M. Julian Caley and Michael R. KearneyImage provided by authors.

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When should organisms be born? How big should they grow? When should they have have babies? How often, and how many? The answers to these questions for most organisms, including humans, depends on environmental conditions, but this is especially true for ‘cold-blooded’ ectotherms. In warm conditions, ectotherms should reproduce more, and more quickly, and grow more quickly than in cooler conditions. There are, however, many other factors that influence growth and reproduction, and so determining the relative influence of environmental temperatures can be difficult. We examined the number of reproductive events in populations of a geographically widespread, viviparous lizard, with an unusual life history, as a model system to examine the influence of environmental temperature on life history. Most viviparous lizards reproduce only once per annum, or even less frequently, but the lizard we examined reproduced twice per year in the tropical parts of its range. We modelled the entire life history of these lizards using a Dynamic Energy Budget model parameterised using data for this species, and predicted reproductive output assuming unrestricted food intake, and thermoregulation based on predictions from environmental models of available temperatures. Although we had to make a range of simplifying assumptions, the model was remarkably good at predicting the observed levels of reproductive frequency for these lizards, strongly suggesting that environmental temperature, rather than local adaptation, was the critical determinant of reproductive frequency. The model also suggested, however, that in locations where second reproductive events were possible, but likely to be risky, real lizards produced only one litter, as we might expect from natural selection to avoid costly mistakes, evidence for some local adaptation. Overall, our paper suggests that environmental temperature, and its direct effects on physiological rates, was critically important to the life history of this organism.

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.

 

Temperature-dependence of fish performance in the wild: links with species biogeography and physiological thermal tolerance

Nicholas L. Payne, James A. Smith, Dylan E. van der Meulen, Matthew D. Taylor, Yuuki Y. Watanabe, Akinori Takahashi, Teagan A. Marzullo, Charles A. Gray, Gwenael Cadiou & Iain M. SuthersSand whiting Sillago ciliata. Image Credit: Nick Dawkins.

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It is well known that temperature has a strong influence on the performance, growth, and fitness of ectothermic (“cold-blooded”) animals. However most of our understanding comes from studies of animals in captive laboratory settings. Unlike in the laboratory, ectotherms in the wild need to balance the influence of temperature on their physiology (e.g. rates of metabolism or enzyme reactions) with a need to eat, avoid predation, compete and also reproduce, but we have little understanding of how temperature influences performance of ectotherms in their natural habitats.

We measured body activity and growth rates in the wild for fishes from nine species, and across a broad range of temperatures. Temperature had a strong influence on fish performance in the wild, and in terms of both body activity and growth rates, the more-tropical species performed best in the wild at higher temperatures than did species with more-temperate distributions (tropical species had higher “optimum temperatures”). The tropical species also tended to have optimal temperatures that were closer to the highest temperatures they experience throughout their geographical distributions than did temperate species; temperate species generally maintained a larger “buffer” between their optimum temperatures and the warmest temperatures encountered in their natural range.

We were also interested to know whether the trends seen in our wild data reflect trends seen in earlier physiological studies of how temperature influences performance in captive fishes. We compiled published, laboratory-derived data on fish aerobic scope – the difference between minimum and maximum metabolic rates – and found that the buffer which wild fish maintain (between their optimum performance temperatures in the wild and the highest temperatures in their range) is very similar to the difference between the optimum temperature for aerobic scope and the critically high temperature where aerobic scope plummets to zero in the laboratory.

The combination of data from the field and laboratory highlights the major influence of temperature on ectotherm performance, and shows how closely the influence of temperature on physiology (in this case aerobic scope) seems to translate into patterns of performance in the wild. Interestingly, these data also suggest that fish species tend to perform best in the wild near the highest temperatures they encounter in their range, while maintaining a “safety margin” from the negative effects of critically high temperatures.

Image caption: Sand whiting Sillago ciliata. Image Credit: Nick Dawkins.
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.

 

Decoupled root and leaf decomposition in trees

Chengen Ma, Yanmei Xiong, Le Li, Dali GuoRoots and leaf litter in the monoculture plantation of Acacia crassicarpa. Photo credit: Chengen Ma.

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Conceptual frameworks describing how measurable plant characteristics (plant functional traits) influence ecosystem processes have been based largely on observations of aboveground traits. Recently, belowground traits and processes are receiving more attention. Several studies have proposed the “whole-plant economics spectrum framework” in which species with “fast” leaves (high nutrient concentrations, short lifespan, fast physiological rates and fast decomposition rates) also have “fast” roots, leading to fast ecosystem processes, whereas species with “slow” leaves have “slow” roots, and therefore “slow” ecosystem processes. Under this whole-plant economics framework, root traits and root decomposition mirror leaf traits and leaf decomposition, thus one can be predicted from the other.

In this study, we showed that plant chemical traits were highly correlated between root and leaf litter across 18 tree species. However, root and leaf litter decomposition rates were significantly correlated only when the most easily-decomposed carbon is available, but it took only three months in our lab incubation to consume this labile carbon fraction. For the remaining 12 months of our 15-month long incubation, root decomposition rates were very low and no longer correlated with leaf litter decomposition rates.

Decoupled root and leaf litter decomposition has several implications for better understanding plant-soil feedbacks. First, root and leaf litter need to be considered separately when evaluating their role in plant-soil feedbacks. Second, roots of woody plants seem to have tissue chemistry highly resistant to decomposition. This high tissue recalcitrance should be better understood in the future. Finally, due to the recalcitrant nature and slow decomposition of roots, roots may contribute disproportionately more to stable soil organic matter than leaf litter. In conclusion, our results clearly showed that decomposition of roots and leaves in woody plants are decoupled for the majority of litter mass, thus whole-plant “fast-slow” economics theory cannot be used as a predictive tool for ecosystem processes such as decomposition, at least in woody plants.

Image caption: Roots and leaf litter in the monoculture plantation of Acacia crassicarpa. Photo credit: Chengen 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.

 

Functional strategy composition is a good indicator of species dynamics

Péter Török, Enikő T-Krasznai, Viktória B-Béres, István Bácsi, Gábor Borics and Béla TóthmérészThe Szűcs-Holt-Tisza oxbow sampling site in summer.

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The humpback model of Grime is a popular model of the species richness versus biomass relationship. This model predicts that species richness displays a unimodal curve along a wide gradient of biomass with a peak at an intermediate level of biomass. Originally, the humped-back model was about terrestrial vegetation, and most papers presenting the model report studies of terrestrial plant communities. To provide new insights, the study of the relationships within phytoplankton assemblages is essential to help explain the coexistence of species. The analogues and other similarities between phytoplankton and terrestrial vegetation will help elucidate the dynamics and mechanisms that support diversity. Groups of functionally similar species are essential to understanding the dynamic processes in phytoplankton assemblages because of the extremely high number of species.

We hypothesized that changes in the taxonomic diversity of phytoplankton along a biomass gradient are associated with altered functional diversity. For the analyses, 768 samples were collected from 30 oxbows, reservoirs and lakes in the Hungarian Lowland Region and analysed between 1992 and 2002.

We found that the diversity and also the number of functional species groups showed a humped-back curve similar to the species richness curve, which indicates that the changes in functional group composition is a good proxy for phytoplankton species responses. The peak of species richness tended to occur towards the high biomass scores (>60% of the biomass range) compared to terrestrial plant communities (typically 20-60%). We found that the peaks of the number of strategy groups and of a diversity index (which accounts for how evenly individuals are distributed within species) were at a much lower biomass than that of species richness.

The Cyanoprokaryota (‘blue-green algae’) were positively correlated with increasing biomass and negatively with the increase in species richness; thus, the high increase in their abundance and/or biomass can be responsible for the abruptly decreasing part of the humped-back curve. Our findings revealed fine-scale effects of increasing dominance of this species group with increasing biomass. This increase was clearly indicated by changes in the functional characteristics: first, the species evenness; then, the diversity index; and finally, the species richness started to decrease with increasing biomass.

Image caption: The Szűcs-Holt-Tisza oxbow sampling site in summer.
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 decision-making by prey may affect the strength of food chains

Sarah A. Gravem and Steven G. MorganLeptasterias and Tegula. Photo provided by authors.

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It is common for the state of an individual prey to influence its response to predators. For example, satiated or vulnerable individuals may be more inclined to cease foraging and flee from predators than hungrier or less vulnerable individuals. It is also well known that predators can benefit primary producers (e.g. plants and algae) by causing prey to graze less. However, these two concepts are rarely considered together; behavioral studies seldom test whether state-dependent prey behavior affects organisms lower on the food chain, and studies of food chains usually assume all individuals behave similarly. However, predators may strongly benefit primary producers when satiated or more vulnerable prey flee, but predators may exert no benefit on primary producers when hungry or less vulnerable prey ignore the predator and continue to graze.

We strengthened the link between individual behavior and community outcomes by testing whether the effect of predators on primary producers hinged on the hunger level or size of the prey. In rocky intertidal tidepools in California, the small predatory seastar Leptasterias spp. can cause its abundant herbivorous snail prey Tegula funebralis to flee tidepools, which benefits tidepool algae. Using short experiments during low tide in the field, we showed that this benefit was strong when snails were well fed or medium-sized because these snails fled tidepools and grazed less. However, the benefit to algae by seastars disappeared when snails were hungry or small because the snails continued grazing or ate very little algae, respectively. Though our experiments suggest that large snails were nearly invulnerable to seastar predation, many fled from seastars. However, those large snails remaining actually grazed faster when seastars were present, so in this circumstance seastars had unexpected negative effects on algae.

Because hunger level and size may vary predictably over time and space in nature, the cascading benefits to algae by predators may be patchy. We demonstrate that the common assumption that individuals in a food web are the same may not accurately predict outcomes. Further, state-dependent individual behavior of prey can cause domino effects on lower trophic levels. This approach strengthens our knowledge of the links between individual processes and community outcomes.

Image caption: Leptasterias and Tegula. 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.

 

When does clumping help insects escape parasitism?

Richard M. Gunton and Juha PöyryNatural History Museum.

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Insects often find themselves hosts to parasitoids: other insects that lay eggs inside or close by them, so that the host is attacked and killed by the larva of the parasitoid. Although repulsive to humans, parasitism can provide useful biological control of certain crop pests. For this to be realistic, the attacks must follow certain kinds of patterns in space, so that the pest cannot simply escape by living in clumps, for example. A primary question is whether the per-capita risk of a host being attacked is higher or lower for denser clumps of hosts: do parasitoids target denser clumps enough to limit their role as refuges?

We combined data from 61 studies of parasitism rates to expore factors relating to whether the risk of parasitism goes up or down when a host lives at higher densities. We found that it normally goes up, but species characteristics can make a difference: exotic hosts are much more likely to reduce their risk by living at higher densities than are native hosts, and exotic parasitoids, and also smaller ones, produce the same phenomenon. At the same time, the taxonomic group that a host insect comes from seems to make a difference. For example, an exotic moth or beetle is likely to suffer more for living at lower densities, especially if a larger exotic parasitoid is hunting it.

But we also have to consider the way a study is performed. Parasitism risks have to be calculated by counting up the proportions of hosts attacked within patches of a certain area, and we found that studies using larger areas (e.g. 1-ha plots in a field) tended to find risks increasing with density more than those that used smaller areas (e.g. single leaves). But here lies a mystery: individual studies comparing different areas don’t seem to find any consistent effect.

We conclude that ecological context is very important, and more work is needed. We hope that our findings will help improve the design and interpretation of studies on parasitism as well as how they get applied to population dynamics models and biological control on the farm.

Image caption: Natural History Museum.
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.

 

Do invaders most strongly impact similar species?

Erica. J. Case, Susan Harrison, Howard V. Cornell Image provided by authors.

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Although invasive plants may eliminate some resident species at local scales, they seldom cause region-wide extinctions. One possible explanation is that highly successful invaders tend to be functionally similar to, and therefore compete most strongly with, resident species that are also relatively successful and widespread. High abundance may then buffer these functionally similar residents from complete extinction over large areas despite their stronger competition with the invader.

We examined whether greater declines among abundant species could be explained by greater resemblance to the invader in a diverse, species-rich Californian serpentine grassland invaded by Aegilops triuncialis (barb goatgrass). We calculated the relative change of each resident species’ abundance in invaded plots compared to paired uninvaded plots, and explored whether this change correlated with abundance and/or functional resemblance to Aegilops.

We found Aegilops most strongly impacted other annual grasses, which are more abundant than other functional groups. However, we did not find a relationship between regional declines, functional resemblance to the invader, or abundance in general. Additional factors, such as varying environmental conditions, must contribute to the relative scarcity of large-scale extinctions under invasion.

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.

 

Tree resprouting and carbohydrate allocation

Rei Shibata, Hiroko Kurokawa, Mitsue Shibata, Hiroshi Tanaka, Shigeo Iida, Takashi Masaki and Tohru Nakashizuka The Ogawa Forest Reserve (upper) and the surrounding secondary-growth stand (lower), Japan. Photo by Toru Nakashizuka.

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Many woody plants possess the ability to resprout and restore the aboveground biomass lost during a disturbance. Resprouting is an important trait of woody plants that increases their survival in forest environments, even if major disturbances are rare. Resprouting requires the storage of photosynthates at the expense of other investments such as growth and reproduction. This resource allocation trade-off may affect species co-existence, but the general relationship between resprouting ability, carbohydrate storage, and other traits remains unclear.

In this study, we investigated the relationships among root and shoot contents of total nonstructural (i.e. storage) carbohydrates (TNC), root mass ratio (root dry mass/total dry mass), resprouting ability, and species’ traits for 24 co-occurring deciduous broadleaved woody species in a cool-temperate forest in Japan. We defined two resprouting groups: single-stemmed species that resprout only after aboveground damage, and multi-stemmed species that resprout without requiring aboveground damage.

Single-stemmed species with greater resprouting ability in the juvenile and mature stages had larger roots and higher root TNC content, suggesting that they store large belowground carbohydrate reserves to support resprouting. On the other hand, multi-stemmed species with greater resprouting ability did not have larger belowground carbohydrate reserves.

Traits associated with light-demanding species (high foliar nitrogen and low wood density) were related to large root TNC reserves for single-stemmed species. This may represent a resource allocation trade-off between physical defences (e.g., tough wood) and large belowground reserves, and having a high photosynthetic rate (high foliar nitrogen) could allow greater allocation to belowground reserves in addition to fast growth of aboveground parts for these species. On the other hand, we found no trade-offs between belowground reserves and other traits for the multi-stemmed species. We hypothesized that the smaller species would allocate more photosynthate to belowground reserves, but found no such relationships for the single- and multi-stemmed species.

This is the first demonstration that contrasting carbohydrate allocation and resprouting patterns among single-stemmed and multi-stemmed species, and variations in the underlying resource allocation trade-offs, affect species co-existence in a cool-temperate forest.

Image caption: The Ogawa Forest Reserve (upper) and the surrounding secondary-growth stand (lower), Japan. Photo by Toru Nakashizuka.
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 functional role of silicon in plant biology

Silicon in aquatic vegetation

Jonas Schoelynck & Eric Struyf Researchers from Antwerp, Lund and Maun on their 2012 expedition to study the silicon cycle in the Okavango Delta, the largest inland delta in the World. Courtesy of D.J. Conley.

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Most people think about sand, computers or glass when they hear about silicon (Si). However, silicon intrudes much more deeply into our daily lives. It is found in drinks (e.g. beer), in crops (e.g. rice), in cosmetics (e.g. shampoo)… it is basically everywhere. This is not surprising since silicon is the second most abundant element on the planet. It is a major constituent of rocks and soils and it only slowly dissolves from this massive Si pool. This dissolved silicon is transported through rivers to the coasts, where single-celled organisms feed on it, and take large amounts of CO2 from the atmosphere during their growth. This intimate link with carbon strongly influences the climate on Earth. We now know that most of the dissolved silicon is taken up by plants during this transport from land to water. Plants store it as ‘phytoliths’, tiny silica ‘plant stones’. The painful cuts when pulling sharp grass are often caused by tiny silicified ‘razor blades’ on the grass leaf surface. In contrast to the physical and chemical dissolution from rocks, this biological control on the silicon cycle has only recently been acknowledged by science. Improving our understanding of this bio-control is important: Si is an essential nutrient that influences the health of many ecosystems. Up to now, only a few researchers have studied the effects of aquatic vegetation on the silicon cycle. Still, the knowledge available shows that aquatic vegetation can store significant amounts of the element. It alleviates stress by fast current velocities, nutrient limitation and herbivory, and potentially aids in the photosynthetic process. Si also determines decomposition processes of decaying water plants. This is especially important in large rivers and wetlands (such as the Okavango Delta in Botswana, see picture) where the majority of the silica is stored in the organic matter of the sediments. This review provides an overview of the state-of-the-art of knowledge on silicon in aquatic vegetation.

Image caption: Researchers from Antwerp, Lund and Maun on their 2012 expedition to study the silicon cycle in the Okavango Delta, the largest inland delta in the World. Courtesy of D.J. Conley.
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.

 

City slickers: poor performance does not deter Anolis lizards from using artificial substrates in human-modified habitats

Jason J. Kolbe, Andrew C. Battles, and Kevin J. Avilés-RodríguezA male Anolis cristatellus feeding while perched at the top of a brick wall.  Photo by Jason J. Kolbe.

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How do lizards adjust to life in the city? Urbanization transforms natural environments into a mix of buildings, roads, parks and natural habitats. Through this process, humans are creating novel environments for other organisms. For example, we add artificial substrates, such as buildings, fences, posts, and walls, which become part of the structural habitat of a city. Lizards may use these novel substrates as they do trees in natural forests, but their performance ability on these substrates may be altered.

In this study, we tested how lizards run on substrates that differ in inclination and roughness. We compared rough surfaces like the trunks and branches of trees in the forest to the smooth and vertical surfaces typical of posts and walls in the city. Then we investigated whether lizards use artificial substrates when they are available in human-modified areas. Lizards living in natural environments tend to use habitats in which they perform better. In contrast, lizards in human-modified areas do not avoid the artificial substrates on which they perform poorly. Lizards run slow as well as slip and fall on smooth, vertical surfaces, yet they often use posts and walls when available in human-modified areas. Despite their poor performance, lizards with longer limbs run faster and fall less when moving on smooth, vertical surfaces. From this relationship we predict that natural selection will favor lizards with longer limbs when they use artificial substrates in cities.

Human-induced global change such as biological invasions and urbanization may fundamentally alter the ecological relationships found for organisms living in natural environments. This makes predicting the consequences of global change extremely difficult. Moreover, human-altered environments are likely to be strong sources on natural selection for the organisms that can persist there.

Image caption: A male Anolis cristatellus feeding while perched at the top of a brick wall. Photo by Jason J. Kolbe.
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.

 

Coexistence resulting from being more different or more similar?

Lin Zhao, Quan-Guo Zhang and Da-Yong ZhangBacterial colonies growing on nutrient agar plates.  Competing strains are distinguishable by their colony colors. Picture by Lin Zhao.

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The conventional wisdom of the ‘competitive exclusion principle’ in ecology stresses the importance of being different for stable species coexistence. It states that two species competing for the same niche (say, using the same resources and the same habitats) cannot coexist; and evolutionary thinking suggests that related species, when competing with each other in their overlapping ranges, will evolve toward greater differences in their niches, which in turn alleviates competition and promotes stable coexistence. The recently emerging neutral theory in ecology, however, highlights the importance of being similar for species coexistence, that is, species that use the same niche but also have the same competitive ability can co-occur for a very long time. However, how neutrality among species could emerge in the first place remains unclear. One possibility is that populations of related species that evolve in isolation show convergence in both niche use and competitive ability, and thus become ecologically equivalent competitors. Such species may form a ‘neutral community’ when they have a chance to colonize the same habitat (secondary contacts).

We carried out an experimental evolution study with laboratory bacterial populations. Bacteria can grow fast and thus their evolutionary changes can be observed in real time. Several pairs of Escherichia coli strains that showed niche differences were used to examine how evolution alters coexistence mechanisms. When bacterial strains were allowed to evolve under competition for over one thousand generations, niche differences among them were maintained. Strains that evolved in isolation showed convergence in niche use, but not in competitive ability. Therefore, our work fails to provide support for the possibility that convergent evolution creates equivalent competitors and leads to the emergence of neutral communities. The origin of neutral communities remains an open question.

Image caption: Bacterial colonies growing on nutrient agar plates. Competing strains are distinguishable by their colony colors. Picture by Lin Zhao.
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.

 

Evolution in space: metapopulation structure and life history evolution

Annelies De Roissart, Nicky Wybouw, David Renault, Thomas Van Leeuwen & Dries Bonte Spider mites as a model for experimental evolution (mature female, on bean). Photo credit by Gilles San Martin.

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Organisms live usually –not to say always- in heterogeneous environments. Habitat patches vary typically in size and connectivity, and this variation determines the local population dynamics, the exchange of individual among patches and the resulting synchronization of changes in population size. While there is a large body of theory on how changes in this ‘metapopulation’ structure affect demography and evolutionary dynamics, empirical evidence remains extremely scarce. Experimental metapopulations and experimental evolution are a strong tool to study these dynamics in a controlled manner.

We installed replicated experimental sets of patches connected by dispersal (metapopulations) that vary in the spatial and spatiotemporal availability of habitat. The metapopulations were inhabited by spider mites living on bean leaf patches. Spider mites are arthropod herbivores with short generation times that are known to evolve fast in response to, for instance, host plant and pesticides. They are a serious pest in greenhouses. Our experimental metapopulations reflect the dominant metapopulation types in nature: a classical metapopulation consisting of equally sized patches where resources are randomly fluctuating, a patchy metapopulation with stable patches of similar size, and mainland-island metapopulations that are characterized by stable patches that differ in size.

We earlier reported that this variation in metapopulation structure affects the local and metapopulation-level demography (< a href="http://onlinelibrary.wiley.com/doi/10.1111/1365-2656.12400/abstract">De Roissart et al. 2015 in Journal of Animal Ecology) and anticipated additional evolutionary changes in life history, physiology and gene-expression. By following a common garden approach to exclude environmental effects, we demonstrate strong evolutionary divergence in relation to metapopulation structure. Contrary to expectation from metapopulation ecology, no evolution in dispersal was found. Instead, the evolutionary changes could be attributed to local demographic variation, especially the degree of local competition and resource shortage. Patterns of life history evolution and especially changes in the expression of genes associated with several important metabolic pathways suggested that the evolutionary changes could be attributed to a general stress response. Such responses are known to allow organisms to cope with other unfamiliar stressors, and we indeed found that those mites that evolved in the stressed metapopulations performed better on this challenging host. Changes in habitat configuration and the emerging local dynamics thus induce the evolution of general stress responses that may reverse demographic threats due to other non-related environmental changes, a phenomenon known as evolutionary rescue.

Habitat fragmentation and habitat loss are a major component of global change. Our experimental work demonstrates that changes in spatial configuration of the habitat alone can induce evolutionary dynamics of the inhabiting species, which eventually affect responses towards other environmental disturbances.

Image caption: Spider mites as a model for experimental evolution (mature female, on bean). Photo credit by Gilles San 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.

 

Soil microbial communities matter for carbon cycling during drought

Kate H. Orwin, Ian A. Dickie, Jamie R. Wood, Karen I. Bonner, Robert J. HoldawayDifferent land uses in the Wairau Valley, taken by Robbie Holdaway.

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Land use intensification results in changes in soil conditions (e.g. pH, total soil carbon and nutrient contents), the microbes that inhabit the soil, and the way in which soil carbon and nutrients are cycled between the soil, the atmosphere and plants. Soil microbes are the organisms that are primarily responsible for recycling the carbon and nutrients found in dead matter (leaves, roots animals). They are therefore fundamentally important for determining how much carbon is stored in the soil, and how fertile it is. However, because land use, soil conditions and soil microbial communities all change simultaneously across land use gradients, it is unclear whether the types, biomass, and diversity of soil microbes drive variation in carbon and nutrient cycling independently of land use and underlying soil resources. Further, we have a poor understanding of whether the main drivers of carbon and nutrient cycling are the same under both stable and disturbed conditions. Understanding this is particularly relevant given the projected increase in disturbance frequency (e.g. drought) under climate change. Here, we examined whether the types, biomass, and diversity of soil microbes were able to predict various measures of carbon and nutrient cycling under stable and disturbed (a simulated drought) conditions, after effects of land use and underlying soil conditions were taken into account. The land use gradient consisted of natural forest, planted forest, high- and low-producing grassland, and vineyards. Results showed that although measures of the soil microbial community were frequently correlated with carbon and nutrient cycling under stable conditions, they did not add any further predictive power once land use and soil conditions were accounted for. However, knowledge of the microbial community was essential to explain the response of carbon cycling to drought. This suggests that carbon cycling in the future may be strongly dependent on the characteristics of the microbial community.

Image caption: Different land uses in the Wairau Valley, taken by Robbie Holdaway.
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.

 

Heat hardening in a tropical lizard: geographic variation explained by the predictability and variance in environmental temperatures

Ben L. Phillips, Martha M. Muñoz, Amberlee Hatcher, Stewart L. Macdonald, John Llewelyn, Vanessa Lucy and Craig MoritzCogger's sunskink, from Australia's Wet Tropics Rainforest.  Populations of this species show strong, predictable geographic variation in heat-hardening; a physiological trait of importance under climate change.  Photograph by Ben Phillips.

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Climate change will place considerable stress on populations over the coming decades. Whether populations can adapt to these changes will depend on the levels of variation that are present in key traits, such as heat tolerance. In this paper, we show that a rainforest lizard (Lampropholis coggeri) has a strong heat-hardening response: a rapid increase in its capacity to withstand high temperatures following a brief exposure to high temperature. We then measure this trait in 13 populations spanning a range of climatic conditions. Our results reveal considerable variation in this important trait and show that this variation is stored across space, in locally adapted populations. By looking at underlying climatic variables (the seasonality and predictability of environmental temperatures), we also show that we can predict which populations will have the greatest heat-hardening capacity. Thus, our work demonstrates adaptive variation in an important trait, and also that we can predict which populations contain individuals with the greatest heat-hardening capacity. This ability to predict the location of important trait variation will prove invaluable to future efforts to use assisted gene flow (the assisted movement of individuals between populations to provide recipient populations with important genetic variation) to mitigate the impacts of climate change.

Image caption: Cogger's sunskink, from Australia's Wet Tropics Rainforest. Populations of this species show strong, predictable geographic variation in heat-hardening; a physiological trait of importance under climate change. Photograph by Ben Phillips.
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 changes how birds make decisions

David Costantini, Giulia Casasole, Hamada AbdElgawad, Han Asard and Marcel Eens Canary, Serinus canaria. ©David Costantini.

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Resources are finite; therefore allocation of a resource to one function, such as reproduction, means that less can be allocated to others, such as body maintenance. This simple concept, referred to as a trade-off, helps us understand the diversity among organisms in their rate of growth, reproductive rate, and longevity. A classic trade-off is that between reproduction and body maintenance because reproduction is generally held to be a demanding phase of animals’ lives, since they must produce, and in some cases protect and provision, their young. Hence, high investment of resources into reproduction means that less is available to protect the body against any processes that might damage it. One reason why individuals deteriorate is thought to be through accumulation of oxidative damage to tissues. 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. Such body deterioration may also in turn influence future investment in reproduction if it results in reduced fertility or changes in hormonal status. We examined whether a state of oxidative stress influences reproductive decisions (when and how many eggs to lay) and reproductive success (hatching and fledging success, number of hatchlings and fledglings produced) in females of a songbird (canary, Serinus canaria). Prior to the reproductive season, females were injected a substance that increases oxidative stress. Then females were mated with a non-relative male and their reproductive activity was followed. Those females whose oxidative stress level was increased delayed the start of egg laying and laid significantly smaller clutches than those females whose oxidative stress level was not increased. However, reproductive success was similar between control and stressed females. Our study provides a rare insight into the cellular mechanisms that constrain reproductive decisions under female control in a vertebrate.

Image caption: Canary, Serinus canaria. ©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.

 

Air humidity thresholds trigger active moss spore release to extend dispersal in space and time

Victor Johansson, Niklas Lönnell, Üllar Rannik, Sebastian Sundberg and Kristoffer HylanderThe peristome movements of Brachythecium rutabulum in response to relative air humidity (RH), when (a) open (RH; 40%), (b) closing (RH; 75%) and (c) closed (RH; 90%).

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Plants that can disperse their seeds or spores over long distances can decrease competition with relatives, and can better sample their surrounding environment to ensure colonization of new suitable habitats. For species living in variable environments it may also be beneficial to spread dispersal over time. However, the dispersal processes, and especially what triggers the release of spores, is poorly understood for many species groups. One example is mosses – a group with approximately 12 000 species. Mosses disperse their spores from one or several capsules that are often elevated a bit above the shoot. Many species have a structure called a peristome in the capsule opening that closes in response to increasing air humidity and opens when dried, but the significance of this is unclear.

Using the moss Brachythecium rutabulum, we investigate the importance of peristome movements for spore release, when the peristome movements occur in nature, and how this may affect dispersal distances. We did this based on spore release measurements in a humidity chamber in the lab, micrometeorological measurements close to the ground in nature, and spore dispersal simulations using a mechanistic dispersal model.

We show that spores are released only when the peristome teeth open in response to decreasing humidity, which usually occurs in the morning. During spore release wind speeds are comparatively low, which contrasts with several studies of seed release. Nevertheless, the release mechanism seems to enhance dispersal distances, compared to mechanisms that release spores in higher wind speeds later in the day. The reason is that release in the morning results in more vertical dispersal of the light spores. The mechanism may also spread dispersal in time more than other known release mechanisms for moss spores.

Image caption: The peristome movements of Brachythecium rutabulum in response to relative air humidity (RH), when (a) open (RH; 40%), (b) closing (RH; 75%) and (c) closed (RH; 90%).
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.

 

Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?

Annie S. Guillaume, Keyne Monro and Dustin J. MarshallImage provided by authors.

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In most organisms, the early life-history stages are the most sensitive to environmental stress. Parents sometimes use cues from their environment to tailor their offspring to local conditions. This process, known as transgenerational plasticity, is thought to be critical for organisms that release tiny, vulnerable gametes, and may be important for buffering populations from the impacts of global change. Most studies of transgenerational plasticity have either focused only on the effect of mothers on offspring phenotype (maternal effects), or on the combined effect of parents on offspring phenotype – few have disentangled the relative effects of mothers and fathers (paternal effects) on offspring phenotype.

We manipulated the water temperature that parents experienced prior to reproduction and measured the performance of offspring across temperatures. We used the marine tubeworm Galeolaria caespitosa, a broadcast spawning marine invertebrate that is an important habitat forming species in southern Australia.

We found that the experiences of both parents affected gametes and larvae: fertilisation success and larval survival depended on the acclimation temperature of the parents. Surprisingly, paternal effects mattered more than maternal effects. We also found that the paternal effects often decreased offspring performance, especially when the temperature experienced varied compared to when the temperature was kept the same.

Our results suggest that, while transgenerational plasticity may play an important role in modifying the impacts of global change, these effects are not always positive. Importantly, paternal effects can be as strong, or stronger, than maternal effects and environmental variability strongly alters the impacts of paternal effects.

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.

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