Lay Summaries Archive

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Early View Lay Summaries


The price of looking sexy: visual ecology of a three level predator-prey system

David Outomuro, Linus Söderquist, Frank Johansson, Anders Ödeen, and Karin NordströmPhoto provided by authors..

Many animals, such as parrots, tropical fish or butterflies, are very colourful. Such colourful displays are favoured in sexual selection as they make the animal stand out, and colour may therefore enhance mating success. However, colour can also be costly, as it makes the animal more conspicuous to both predators and prey. Colourful traits are therefore subject to opposing selection pressures: positive sexual selection by conspecifics (increased mating success) and negative natural selection by predators (higher predation risk) and prey (lowered hunting success). In this paper we studied the conspicuous wing coloration of two species of damselflies, which are predated by birds and prey on small flies. The conspicuous wing coloration is used in colour communication between the sexes and between different species of damselflies. Using electrophysiology, we first determined the colour vision of the damselflies and found that they see well in UV as well as in the human visible range. Second, we measured the wing coloration using spectrophotometry and confirmed that males are more colourful than females. Third, we estimated the predation risk in natural populations by quantifying the predated wings from bird feeding stations, and found that more males than females were consumed. We finally used our data together with previously known colour vision of the bird predator, and the fruit fly prey, to model how visible the wing coloration is in natural environments. We found that males are very conspicuous to bird predators, to other damselflies, and to prey, while females remain predominantly cryptic (i.e. hard to see against the background). This implies that males, but not females, pay a high cost when they use colour to communicate with other damselflies, both in terms of predation risk and visibility to prey. One of our most surprising findings was that male damselflies are unable to discriminate the wing coloration of perching females! We hypothesize that females use this to reduce male harassment, which is very intense in damselflies. Our study demonstrates that by including several levels of interactions in predator-prey systems, we get a more complete understanding of the costs and benefits of being colourful.

Image caption: Photo provided by authors..
Read the article in full here.


Competing for seed dispersal: evidence for the role of avian seed hoarders in mediating apparent predation among oaks

Mario Pesendorfer and Walter KoenigA western scrub-jay (Aphelocoma californica) searches the branches of a valley oak (Quercus lobata) for acorns at the Hastings Natural History Reservation in Carmel Valley, California. Photo credit: Jenna Kohles.

Species interactions come in many shapes and forms, from predation to mutualisms. Indirect interactions, mediated by a third party, often occur when two or more species share the same generalist predator. When the predators are also seed dispersers, as is the case for many large-seeded trees whose seeds are harvested by seed-hoarding animals, such indirect interactions can shift from seed dispersal mutualism to predation, depending on the relative seed production of the trees that co-occur in a community. Because the shift of mutualistic interactions from one tree species to another results in increased relative predation of the less-dispersed species’ seeds, this indirect effect is termed “apparent predation” – one tree species indirectly preys on the seeds of another.

To investigate the mechanisms underlying apparent predation, we studied the seed predation and dispersal dynamics of valley oaks (Quercus lobata) at Hastings Natural History Reservation in central coastal California, where they mainly co-occur with two other oak species, California blue oak (Q. douglasii) and coast live oak (Q. agrifolia). In the first year of the study, western scrub-jays (Aphelocoma californica), high-quality seed dispersers that scatter seeds across the landscape by hiding them in the ground, attended Q. lobata trees in large numbers to hoard acorns. However, when attending the trees, the jays encountered lots of aggression from another bird species, acorn woodpeckers (Melanerpes formicivorus) that mainly hoard acorns by storing them in so-called granary trees. These low-quality dispersers only help the oaks when they accidentally drop an acorn during transport and thus mainly function as seed predators.

In the second year of the study, Q. lobata and Q. agrifolia acorn crops were similar to the first year, but Q. douglasii crops increased tenfold. With acorns more widely available across the landscape, western scrub-jays only attended Q. lobata trees sparsely, likely to reduce the risk of injury during encounters with the woodpeckers which vigorously defend their preferred valley oaks in year-round territories. The jays have much larger home ranges in the fall and were able to optimise their foraging behaviour by shifting to less-preferred Q. douglasii acorns. As a result, Q. lobata trees experienced a proportional increase in seed predation and almost no seed dispersal from jays. Q. douglasii thus exerted apparent predation on Q. lobata acorns.

Indirect effects mediated by shared seed predators and dispersers may be one of the mechanisms that allows for the co-existence of multiple oak species in forest communities. The variable seed production of each tree species appears to drive seed predation and dispersal dynamics in ways previously not explored. Follow-up studies are necessary to investigate the details of the spatial and temporal variation of such species interactions in order to tease apart the fitness consequences for all the members of the community.

Image caption: A western scrub-jay (Aphelocoma californica) searches the branches of a valley oak (Quercus lobata) for acorns at the Hastings Natural History Reservation in Carmel Valley, California. Photo credit: Jenna Kohles.
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Sexual selection in hybridizing lizards

Hannah E A MacGregor, Geoffrey M While, Jade Barrett, Guillem Pérez i de Lanuza, Pau Carazo, Sozos Michaelides & Tobias Uller A typical Italian male from north-central Italy. Photo by Ben Halliwell.

Populations frequently undergo periods of relative isolation and differentiation that are followed by contact and hybridization (interbreeding). What makes hybridization so striking is the many different ways in which it can act as a catalyst for evolution, such as by accelerating the course of speciation or facilitating adaptation through the exchange of genes. But if members of each population look and behave differently then why does hybridization occur at all? Are some individuals more likely to hybridize than others?

Sexual selection has a reputation for preventing hybridization because females commonly prefer to mate with males of similar genes or traits. But in many animals, including many species of lizard, sexual selection via competition among males is the most important cause of mating patterns within populations. Intuitively, in these species male competition should also influence patterns of hybridization when populations come into contact.

Common wall lizards from north-central Italy have highly exaggerated male sexual traits compared to individuals from Western Europe, having diverged in isolation from one another during the last ice-age. Genetic data from a natural contact zone in northern Italy suggests that hybridization may occur asymmetrically, between Italian males and Western European females. In this study, we used experimental contact zones in outdoor enclosures to investigate the consequences of divergence in male sexual traits (such as body size, testes mass, and colour signals) for male-male competition and patterns of hybridization between Italian and Western European lizards.

During our experiment the Italian males completely dominated the Western European males in aggressive encounters, monopolised high quality territory and the courtship of females, and achieved greater reproductive success. Despite our data suggesting a competitive and reproductive advantage of the Italian males with the most exaggerated traits, these superior Italians were not more likely to hybridize. Instead, hybridization between Italian males and Western European females seems to arise because the Italian males with less exaggerated sexual traits are outcompeted for Italian females but remain competitive relative to the Western European males.

Image caption: A typical Italian male from north-central Italy. Photo by Ben Halliwell.
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The economics of sexual signalling

Thomas M. Houslay, Kirsty F. Houslay, James Rapkin, John Hunt and Luc F. BussièreCrickets.

Sexual selection theory explains the evolution of exaggerated and flamboyant ornaments, displays and mating behaviours in terms of male competition or mating preferences. Such characters are typically costly to produce, but can bring benefits to their bearers: greater mating success for those individuals with the biggest or brightest signals. If an individual produces such signals repeatedly over the course of their adult lifetime, they face ‘trade-offs’ between current and future investment. These trade-offs can create variation in the intensity of signalling at different ages, often interpreted as alternative strategies: ‘live fast, die young’ vs. ‘slow and steady’.

Another possible explanation for this age-related variation is that it is caused by differences in the ability to acquire resources that can be invested in signalling (meaning, for example, that ‘late bloomers’ do not have early investment options). Testing this hypothesis is challenging, not least because measuring both the acquisition and allocation of resources is a difficult task. As an additional complication, an individual’s energetic reserves both affect and are affected by their signalling investment.

Male crickets signal to females using an energetically expensive call, produced by rubbing together their hardened forewings: the more time a male spends calling, the higher his mating success. In this study, we simultaneously manipulated resource acquisition (through diet treatments) and access to females (as a proxy for manipulating sexual signalling) in male decorated crickets (Gryllodes sigillatus). We measured how much time they spent signalling, and how their energy budgets were affected.

Increased diet quality caused increased signalling effort and energy storage, while access to females increased both the likelihood of and time spent signalling. Males with lower resource budgets signalled less, but still suffered energetic losses and reduced lifespan. Our results suggest that energetic constraints, rather than strategic budgeting of resources, led to reduced signalling levels in males with lower acquisition ability. Our findings therefore imply that age-dependent variation in sexual signalling may not represent alternative adaptive strategies. In addition, energetic constraints can help maintain ‘honesty’ in sexual signalling, at least on average: after all, anything spent today cannot be spent tomorrow.

Image caption: Crickets.
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A fundamental problem in finding biomarkers confirmed using feather fault bars in nestling birds

Jelle J. Boonekamp, Rutger Dijkstra, Cor Dijkstra, and Simon VerhulstA female jackdaw (Coloeus monedula) approaching her nest box. Photo by Jelle Boonekamp.

Measuring fitness – essentially the product of survival and reproduction - is central to studies in evolutionary ecology that are aimed at gaining an understanding of natural and sexual selection. But measuring real fitness can be difficult and time-consuming, so fitness biomarkers – traits that predict survival and reproduction – are potentially powerful tools in evolutionary ecology when they can be used as surrogate study end points. For example, most vertebrate species have long reproductive lifespans and therefore valuable time and other resources could be saved by using fitness biomarkers.

Useful fitness biomarkers need to fulfil 2 criteria: (i) they need to be accurate predictors of fitness, and (ii) they need to be sensitive to environmental variation (or experimental manipulation), such that the biomarker successfully links environmental conditions to fitness. However, evolutionary theory predicts that traits that are important for fitness should be well protected (canalized) against the influences of environmental fluctuations, and hence biomarkers that are both accurate fitness predictors and sensitive to environmental conditions may be rare.

Here we tested for this canalization principle using free-living jackdaws. We manipulated the number of siblings in the developmental period to test how strongly developmental conditions affected the number of feather fault bars in tail and wing feathers. Fault bars are deformities on bird feathers associated with developmental stress and can cause feather breakage, thereby impairing flight and insulation. We show fault bars in the tail increased when there were more siblings in the nest, while the number of fault bars in wing feathers was not affected, suggesting tail but not wing fault bar number is sensitive to developmental conditions. In line with evolutionary theory, we found that fault bar number on wings, but not tails, predicted fitness prospects. These results confirm the theory that the development of traits that are important for fitness is strongly canalized.

The canalization phenomenon has implications for the utility of traits as fitness biomarkers, because when traits are good fitness proxies, they are also more likely to be strongly canalised, reducing sensitivity to environmental variation. Intriguingly, there are nevertheless traits that are both sensitive to environmental conditions and predict fitness prospects, and we discuss hypotheses that may explain this paradox.

Image caption: A female jackdaw (Coloeus monedula) approaching her nest box. Photo by Jelle Boonekamp.
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Telomere length and telomerase dynamics in frillneck lizard

Beata Ujvari, Peter A. Biro, Jordan E. Charters, Gregory Brown, Kim Heasman, Christa Beckmann and Thomas MadsenAdult frillneck lizard behind tree.

Much like the plastic tip of shoelaces, telomeres prevent the ends of DNA from fraying during cell divisions. Studies of human cells in culture have shown that telomeres become shorter at every cell division, and when telomeres reach a critically short length (after 50-70 divisions) the cells stop dividing and die. However, many vertebrates produce an enzyme, called telomerase, which replenishes the missing telomere copies. Telomerase not only prevents telomere shortening but is also able to increase the length of critically short telomeres.

In numerous vertebrates, including humans, telomere length (TL) has been shown to decrease with increasing age. Moreover, during recent decades numerous studies have observed an association between TL and organismal survival and/or fitness.

In the present study we therefore investigated how age affected TL and telomerase expression (TE) dynamics in frillneck lizards. We also examined whether TL and TE had any effects on lizard survival. We found that young lizards had short TL, and that TL increased in medium aged lizards but decreased in older cohorts, revealing a curvilinear relationship between TL and lizard age. Higher TE resulted in longer telomeres but in spite of this we did not observe any association between TL dynamics and lizard survival. Instead our results suggest that TL and TE dynamics in frillneck lizards reflect an adaptation to maintain TL above a critical minimum length in order to sustain cellular stability.

Our study has major implications for the role of telomeres in ageing by questioning the significance of TL dynamics as a significant underlying factor in vertebrate survival.

Image caption: Adult frillneck lizard behind tree.
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Plant–Pollinator Interactions from Flower to Landscape

Plant secondary metabolites in nectar: Impacts on pollinators and ecological functions

Philip Stevenson, Susan Nicolson and Geraldine WrightBombus terrestris on Rhododendron ponticum.

Flowers provide nectar as a reward for pollinators that transfer pollen, and allow otherwise stationary plants to reproduce. Nectar is sought after by pollinators because it contains high concentrations of sugars but also other important dietary components such as amino acids and minerals; almost all the dietary requirements of some animals. But the nectar of many flowers also contains toxic chemicals known as secondary metabolites which are produced naturally by the plant. These are often the same chemicals produced elsewhere in the plant for defence against herbivores such as leaf feeding insects. The ecological value of toxic secondary metabolites in plant defence is well established, but their role in plant-pollinator interactions is less obvious.

Increasing evidence supports potential benefits for both plant and pollinator from these nectar chemicals. For example, they can modify pollinator behaviour for the benefit of the plant. Coffee flower nectar contains caffeine, a distasteful defence chemical in the coffee beans protecting the plant’s offspring from weevils. In nectar it is too dilute for bees to taste but has a pharmacological effect on them; it enhances pollinator memory for cues associated with the nectar rewards, such as floral scent. Nectar containing caffeine is more likely to be revisited as bees remember it as a good reward, and the plant is therefore more likely to receive pollen from flowers of the same species through repeat visits by the pollinator.

Broadly speaking the other beneficial effects may include increasing specialization in plant-pollinator interactions, protecting nectar from robbery, and antimicrobial activity such as protecting nectar nutrients from degradation and reducing disease in flower visitors. This review synthesises evidence from recent literature that supports the suggestion that selection for secondary metabolites in floral nectar is an adaptation that drives the co-evolution between plants and their pollinators. However, in the absence of sufficient specific evidence of direct impacts on plant fitness it is still hard to argue with certainty that these compounds function for the benefit of the plant. Their presence in nectar could simply be a consequence of their occurrence elsewhere in the plant for defence.

Image caption: Bombus terrestris on Rhododendron ponticum.
Read the article in full here.


Endure and call for help: Strategies plants use to deal with a specialised caterpillar

Dani Lucas-Barbosa, Marcel Dicke, Twan Kranenburg, Yavanna Aartsma, Teris van Beek, Martinus Huigens and Joop van LoonCaterpillar of the Large Cabbage White butterfly feeding on flowers of a Black Mustard plant. Photograph credits: Dani Lucas-Barbosa.

Plants have evolved strategies to avoid, resist, and endure damage caused by insect herbivores. Plants may resist herbivore attack by, for instance, changing plant chemistry and producing compounds that are toxic or unpalatable to plant-feeding insects. However, this strategy will not be effective against herbivorous insects that are specialised to withstand the plant’s chemical defences, and will therefore not be deterred from attacking the plant. Thus, plants need to deal differently with specialist herbivores. Plants can, for instance, re-grow leaves to compensate for the tissues lost to plant feeders, invest in flower production and interaction with pollinators, or change odours in order to attract the natural enemies of the herbivores. We studied several strategies that plants can use to deal with herbivores to ensure that they will produce seeds. We investigated the extent to which plants can endure the damage caused by herbivores, and the role of carnivorous insects as a defensive strategy used by plants against their own enemies. In the laboratory, we measured changes in plant basic nutrients (carbon and nitrogen) that are triggered by herbivore attack. In the field, we quantified leaf biomass and seed production in the presence or absence of natural enemies of the herbivores. We also tested whether self-fertilisation increased in mustard plants when exposed to caterpillar damage, and investigated whether caterpillar attack rendered mustard plants more attractive to pollinators than control plants. We found that flowers of mustard plants are rarely visited by insects during the night, and exposure to caterpillars did not influence the rate of self-fertilisation. Mustard plants compensated for caterpillar damage in terms of leaf biomass. However, in the absence of natural enemies of the caterpillars, seed set of these plants was negatively affected by herbivore damage. Once attacked by caterpillars, plants allocated most basic nutrient content to flowers. The investment of plants in flower production or re-growth of leaf tissues per se was not sufficient to sustain seed set of these plants; interactions with the natural enemies of the caterpillars were really essential. We conclude that the natural enemies of the caterpillars play an important role in the plant’s defence strategy.

Image caption: Caterpillar of the Large Cabbage White butterfly feeding on flowers of a Black Mustard plant. Photograph credits: Dani Lucas-Barbosa.
Read the article in full here.


New insights into the origins of agriculture

Catherine Preece, Alexandra Livarda, Pascal-Antoine Christin, Michael Wallace, Gemma Martin, Michael Charles, Glynis Jones, Mark Rees and Colin P. OsborneThe lead author (C. Preece) working in the greenhouse growing crops and their wild ancestors. Photo credit – Catherine Preece.

Humans began farming the land 10,000 years ago, leading to an agricultural revolution, which had big impacts on human societies. The plants that we now use as crops have changed a lot since the first farmers started growing them. During the process of domestication, these plants changed in appearance and the amount of food that they produce increased. However, we do not fully understand how these changes happened. A deeper understanding of the origins of agriculture may prove useful for improving food production today.

We grew traditional versions of crops including wheat, barley, lentils and peas, and compared them with their wild ancestors, to see how they have changed through domestication, measuring a much wider range of characteristics than ever before. We found that crops are able to produce more food for us because of three important characteristics: they grow into bigger plants, they have larger seeds and they contain less non-edible material. Crops are also able to produce the same number of seeds as their wild ancestors, despite the seeds being bigger. This is important because normally plants must choose between producing a few big seeds or lots of small seeds, but this does not seem to apply so much to these plants.

Today we are seeing increasing pressure on global food production, and crop breeders are taking an increasing interest in traditional crops as a source of useful traits that may help to increase yields or increase resilience to climate change. Our work should help in this process by providing new insights into the process of crop domestication, which may lead to innovations in modern agriculture.

Image caption: The lead author (C. Preece) working in the greenhouse growing crops and their wild ancestors. Photo credit – Catherine Preece.
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Consequences of a nectar yeast for pollinator preference and performance

Robert N. Schaeffer, Yu Zhu Mei, Jonathan Andicoechea, Jessamyn S. Manson, and Rebecca E. IrwinBumblebees. Image provided by authors.

Pollinators provide essential services in natural and agricultural systems, driving global floral diversity and a significant percentage of food production. At the heart of interactions between plants and pollinators are key floral resources, such as nectar, produced by plants as a reward in exchange for pollination services provided. Comprised mostly of sugars and amino acids, this nectar reward can vary considerably in quality, and pollinator foraging decisions are frequently driven by nectar quality. Recently, considerable attention has been paid to the fact that microorganisms such as yeasts and bacteria often colonize nectar. These microorganisms consume nectar sugars and amino acids, altering the nutritional quality of this key resource. The consequences of these changes for pollinator foraging preferences and reproduction are poorly understood.

Here, we demonstrate that microorganisms in nectar, in particular the yeast Metschnikowia reukaufii, can significantly affect pollinator foraging decisions. Through a series of behavior experiments, we show that the yeast M. reukaufii may act as an honest signal, indicating the availability of nectar to common eastern bumble bee Bombus impatiens workers. Both naïve foragers, with no previous exposure to yeasts, as well as foragers trained to associate yeast with a flower color, used cues associated with yeast to make foraging decisions, actively seeking out yeast-inoculated flowers. However, miniature bumble bee colonies that consumed nectar containing active yeast or dead yeast did not differ in their reproductive performance, even when given a protein-limited diet, suggesting no apparent benefits or costs of yeast for bumble bee fitness.

Taken together, our results suggest that nectar yeasts can enhance floral signaling as well as alter foraging behavior at individual flowers, though these microorganisms may have no direct effect on pollinator performance. Thus, nectar yeasts may play a significant role in mediating pollinator foraging behavior, with consequences for plant fitness and evolution of floral traits.

Image caption: Bumblebees. Image provided by authors.
Read the article in full here.


It’s all about the pollinators in the Lapland marsh-orchid

Nina Sletvold, Matthew Tye and Jon ÅgrenImage provided by authors.

The amazing diversity of flowering plants is thought to be a result of interactions with pollinators, where flowers signal rewards to their visitors, who in turn transfer pollen from one plant to another, fertilizing the ovules and initiating seed development. Successful attraction of pollinators is required for offspring production, and pollinators thus have the potential to drive the evolution of floral traits. However, the production of flowers and seeds also demands resources in the form of essential mineral nutrients and water, and successful interaction with pollinators might not result in seed production if the plant has insufficient resources to respond to high pollen deposition. Changing the resource status of plants can thus be expected to change the selection pressure pollinators exert on floral traits. To test this, we experimentally increased both pollen and nutrient levels in a crossed design in the rare Lapland marsh-orchid Dactylorhiza lapponica. Plants that received supplemental hand-pollination on average produced 74% more seeds than plants that were naturally pollinated, whereas nutrient addition did not significantly increase seed production. Among plants receiving only natural pollination, those with more flowers and longer spurs produced most seeds, meaning that there was selection for more flowers and longer spurs. The selection on spur length disappeared when we hand-pollinated plants, demonstrating that the interaction with pollinators caused the positive relationship between spur length and seed number. In contrast, nutrient addition did not alter the strength or direction of selection on floral traits. Nutrient addition increased flower size the following year, but did not affect fruit production. This experiment demonstrates that D. lapponica does not increase flower production in response to nutrient addition, that the increase in seed production in response to hand-pollination is not limited by resource availability, and suggests that natural resource variation does not influence selection on floral traits in this system. This study is one of the first to disentangle the effects of pollinators and resource variation on patterns of selection on floral traits. This contributes to our understanding of how natural and human-induced changes in environmental conditions influence selection regimes and evolutionary dynamics.

Image caption: Image provided by authors.
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Herbivore-specific induction of defence metabolites in a grass-endophyte association

Benjamin Fuchs, Markus Krischke, Martin J. Mueller & Jochen KraussPhysical conditions of the plants four weeks after herbivore introduction. Weekly clipped plants show fresh green leaf material after cutting. Aphid treated plants turn towards a yellowish colour, while locust treated plants show reduced leaf material compared to control plants.

Plants have developed several strategies for defence against pathogens and herbivores. The production of chemical compounds is a successful defence strategy to minimise herbivory. Chemical defence can range from deterrence or intoxication of herbivores up to the attraction of natural enemies of herbivores. A key feature of many chemical defence strategies is the induced production of chemical defence compounds following herbivore attack.

Symbioses (mutually beneficial interactions) between plants and microorganisms can alter the defence strategies of plants, increasing their defence against herbivores. The symbiosis between cool season grasses and endophytic fungi of the genus Epichloё is an example where a plant symbiotic microorganism affects herbivory on its host plant. Epichloё endophytes infect the above ground parts of many cool season grass species and produce toxic, herbivore deterring alkaloids. However it is unclear whether these alkaloids can be induced by herbivory and whether herbivore specific plant damage affects the production of specific alkaloids.

Our study organism was the cool season grass Lolium perenne infected with the endophytic fungus Epichloё festucae var. lolii which produces three bioactive alkaloids: peramine, which deters invertebrate herbivores, and lolitrem B and ergovaline, which are both toxic to vertebrate herbivores.

In a controlled common garden experiment we tested the effects of three different herbivore treatments, and a control treatment, on the growth of the endophytic fungus and the production of alkaloids over 18 weeks. We showed that the concentration of the vertebrate toxic alkaloid lolitrem B increased following clipping (a simulation of grazing herbivores), while the insect deterring alkaloid peramine increased following locust herbivory (biting-chewing herbivores). Aphids (piercing-sucking herbivores) affected neither alkaloid production nor endophyte growth.

Our study provides evidence for an herbivore-specific induction of chemical defence compounds from a grass endophyte following herbivore attack on its host grass. Our results indicate a close chemical crosstalk between the interacting species of a grass-endophyte symbiosis.

Image caption: Physical conditions of the plants four weeks after herbivore introduction. Weekly clipped plants show fresh green leaf material after cutting. Aphid treated plants turn towards a yellowish colour, while locust treated plants show reduced leaf material compared to control plants.
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Cannibalism or burial: undertaking behaviour depends on the change of death cues in termites

Qian Sun, Kenneth F. Haynes, Xuguo ZhouA termite worker consuming a dead worker. Taken by Hu Li.

The ability to detect environmental cues is important for animals to exploit resources and defend themselves against predators and disease. Social insects frequently encounter the dead bodies of their nestmates, which may carry pathogens and could cause an outbreak in the colony. Many social insects dispose of the corpses with a stereotypic behaviour named undertaking behaviour. Ants and honeybees remove the corpses from the nest, but termites that feed on a nutritionally imbalanced woody diet could benefit from recycling rather than discarding nutrients from dead nestmates. Therefore, corpses represent both a food resource and a pathogen risk for termites. As corpses decay with time, the reward from feeding declines and the risk of disease increases. The central goal of our study is to determine how termites regulate this trade-off by detecting chemical cues from corpses. We combined behavioural and chemical analyses to address this question using the eastern subterranean termite, Reticulitermes flavipes.

We found that termites cannibalize the corpses if they are freshly killed, but resort to burying them when the corpses are highly decayed. Such a behavioural switch is mediated by the changes of death cues released by the corpses. Immediately after death, corpses release 3-octanol and 3-octanone. The early death volatile cue, consisting of this alcohol possibly in combination with the ketone, attracts workers to quickly retrieve and consume the bodies, but the two compounds decrease rapidly with time. Correspondingly, there was an accumulation of late death cues, including a blend of phenol and indole, which enable termites to locate the corpses, and a blend of six fatty acids that trigger burial behaviour. Cannibalism is more efficient than burial behaviour, because it requires fewer workers, and also allows termites to recycle nutrients. However, if corpses are not found within the recyclable time frame, burial behaviour could effectively prevent pathogenic propagation.

Our study indicates that the dynamic changes in death cues balance nutritional rewards and infection risks. This post-mortem communication highlights unique adaptations in termites to their feeding habit and social living.

Image caption: A termite worker consuming a dead worker. Taken by Hu Li.
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Bad boys bite, good girls eat their dinner

Alexis Y. Dollion, G. John Measey, Raphaël Cornette, Liza Carne, Krystal A. Tolley, Jessica M. da Silva, Renaud Boistel, Anne-Claire Fabre and Anthony Herrel Image provided by authors.

Cranial morphology is complex and how it evolves remains relatively poorly understood. One of the complicating issues is that the head serves many functions ranging from the protection of the brain and major sensory organs to the control of feeding and drinking, and display and communication. These different functions often impose different and conflicting pressures on the size and shape of the cranium in vertebrates. An additional complicating factor is that the selective factors driving the evolution of cranial shape may differ in males and females. Indeed, whereas in males of many vertebrates, and especially lizards, the head is used in territory defense and male-male combat, this is typically not the case in females. Here we explore these issues in a group of dwarf chameleons from South Africa. We quantify skull, mandible and quadrate shape in 3D using a cross-sectional imaging technique (computed tomography, or CT imaging) and test whether skull shape is related to diet as determined by stomach flushing and maximal bite force capacity. Our results do indeed show strong correlations both between shape and bite force, and between shape and diet. Bite force is also related to diet. However, the observed patterns differ between males and females and suggest that the role of the cranium is not identical in both sexes. Our results shed light on the relevance of sex when relating a lizard’s morphological adaptations to its ecological role, and show the importance of collecting comprehensive data on shape, bite force and diet to unravel the selective pressures that govern the evolution of complex integrated structures such as the skull.

Image caption: Image provided by authors.
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Plant-pollinator interactions: from flower to landscape

Novel interactions: invasive flowering plants and native pollinators

Jane C. Stout and Erin Jo TiedekenImage provided by authors.

Plant invasion and pollinator decline are two key issues of global concern. Invasive plants can affect the way ecosystems work by influencing native species and their interactions, and can cost a lot to control and manage. Pollinators are important for crops and wild plants, but many species of bee, fly, bird, and bat are in decline due to human activities. When animal-pollinated plants are introduced into novel environments, they can interact with the native pollinators, with knock-on implications for both parties. Non-native species can have direct influences on pollinators by affecting their diet and nutrition, behaviour, and the number of offspring they produce. This can affect the size of pollinator populations, and the relative abundance of different species in the invaded habitat. Furthermore, native pollinators may have a direct influence on the non-native plant, influencing its pollination and seed set, and potentially assisting its invasion. In this paper, we review studies that have examined these direct impacts. We found that characteristics of the plant, including what resources it offers to pollinators in terms of nectar and pollen, as well as where and when it flowers, influence the effects it has on pollinators. Some invasive plants may be beneficial to pollinators by providing a food resource, but others may not, or may even have negative impacts such as poisoning native pollinators. It is important to note that not all species of pollinator are affected in the same way. Similarly, native pollinators can play a role in plant invasion if they influence pollination and seed production: they may help the plant to produce the seeds that are required for further invasion. We identify key knowledge gaps and suggest future approaches for understanding the direct effects of invasive plants on native pollinators. Ultimately, we need to understand how native pollinators interact with invasive plants to determine how pollinators affect the invasion process, and how invasive species and their management may influence declining pollinator populations.

Image caption: Image provided by authors.
Read the article in full here.

Plant-pollinator interactions: from flower to landscape

A global perspective on hawkmoth pollination niches

Steven Johnson, Marcela Moré, Felipe Amorim, William Haber, Gordon Frankie, Dara Stanley, Andrea Coccuci, Robert A. RagusoFlowers of the African shrub Gardenia thunbergia are pollinated exclusively by the convolvulus hawkmoth Agrius convolvuli. The 10 cm floral tube of this shrub matches the length of proboscis of this hawkmoth species. Photograph by Steven Johnson.

Niches are ecological opportunities for organisms and determine where they can survive and reproduce. To occupy a particular niche, species must either evolve or already possess certain functional traits. Some of the major challenges in the field of ecology are to identify niches in nature, to uncover the various environmental variables that define niches, and to discover which traits are important for niche occupancy. Because pollination is usually required for seed production in plants, animal pollinators represent niches that plants adapt to in order to reproduce successfully. In this study we sought to determine whether proboscis length is a key dimension of the pollination niche. We used hawkmoths as a study system since these insects are important pollinators of night-flowering plants, particularly in the species-rich tropics, and vary greatly in the length of their proboscides. The analyses were based on studies conducted in nine regions spread across the Old and New Worlds. In many of these studies, relationships between plants and hawkmoths were inferred from analysis of the pollen loads carried by the hawkmoths.

The proboscis lengths of hawkmoths can vary between 2 cm and 25 cm, even within a single community, and tend to exhibit a frequency distributions characterized by several peaks (multimodality). These peaks can be considered to be pollination niches, and this proposition is supported by a good match between peaks in the frequencies of hawkmoth proboscis length and tube lengths of night-opening flowers.

Analysis of the networks of interactions between hawkmoths and flowers reveals that hawkmoths are even more generalist in their foraging habits than are bees and hummingbirds. Long-proboscid hawkmoths have a particularly wide niche breadth in terms of the diversity of flowers that they visit, although they tend to concentrate their foraging activity on longer-tubed flowers that have greater nectar rewards. By contrast, the hawkmoth pollination niche for plants becomes narrower and more specialized as their floral tube length increases.

This is the first study that has explored morphological niche axes for a pollination system at both regional and global scales. The approach could be extended to other pollination systems and could ultimately help to explain species distributions as well as co-diversification of insects and angiosperm flowers. By incorporating traits into analyses of species interaction networks, biologists may finally be able to identify some of the key principles underlying pollination niches.

Image caption: Flowers of the African shrub Gardenia thunbergia are pollinated exclusively by the convolvulus hawkmoth Agrius convolvuli. The 10 cm floral tube of this shrub matches the length of proboscis of this hawkmoth species. Photograph by Steven Johnson.
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How plant species colonize open spaces in meadows

Alena Vítová, Petr Macek and Jan LepšColonization of artificially created gap bounded by mesh after one year of monitoring. Photo provided by authors.

Most grasslands in Central Europe are dependent on human management. Their species composition and abundance have been shaped by centuries of regular mowing and pasturing. Small-scale local disturbances referred to as gaps are open to colonization and are often connected with management (a side-effect of machinery during mowing), or animals (burrowing animals, wild boar). Many meadow species efficiently colonize these gaps, some immediately after gap formation and some gradually over time. Meadow communities are thus dynamic systems containing gaps of various ages, each often differing in their species composition, forming a mosaic in space and time. Gap dynamics play an important role in the maintenance of meadow species diversity, which may be extremely high in some meadows. Nevertheless, species-specific information about dynamics of gap colonization is rather scarce. We aimed to disentangle the processes involved during gap colonization through a manipulative experimental approach in which we artificially created gaps.

Species can colonize gaps either vegetatively by rhizomes and other vegetative sprouts (from nearby in the neighbourhood), or by seeds which may be stored in the seed bank or that arrive via seed rain. We manipulated vegetative propagation into gaps by felting, and altered the seed bank using gamma radiation. We then followed the colonization of gaps by four main species groups with contrasting regeneration strategies (forbs [dicots, or broad-leaved plants], rushes [Juncaceae], grasses [Poaceae], and sedges [Cyperaceae]) over the following three years.

Initially, gaps were colonized mostly from seeds, with vegetative propagation dominating at later stages. There were also differences among species groups. Forbs regenerated mostly from the seed bank and were the first colonizing species. Later in the season, the seed rain also became important and resulted in a shift in species composition from forbs to grasses. The presence of a seed bank was essential for some species, and its presence in gaps had a consistent positive effect on species richness throughout the entire experiment. Gaps in meadow communities are very important for species regeneration via seed and the maintenance of species diversity, although species groups differ in their ability to colonize open spaces through time.

Image caption: Colonization of artificially created gap bounded by mesh after one year of monitoring. Photo provided by authors.
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Aphid toxicity to ladybeetles is not a function of host plant or facultative bacterial symbionts

Jennifer A. White, Joshua S. McCord, Kelly A. Jackson, Allison C. Dehnel, Paul A. LenhartSibling Harmonia axyridis larvae fed on toxic (top) or nontoxic (bottom) aphid lineages.  Larval age and image magnification are the same between panels.

For generalist predators that consume many types of prey, the world is complicated. Some prey species are reliably and consistently edible, but others are not. The multicolored Asian ladybeetle, Harmonia axyridis, is an invasive predator, but also an important biological control agent because it consumes a wide range of pest aphid species. One such pest, the cowpea aphid (Aphis craccivora), is extremely variable in its suitability as food for the ladybeetle. For decades, it has been known that cowpea aphids collected from locust trees (Robinia species) are toxic and can kill ladybeetles, whereas cowpea aphids from other host plants (such as vetch or alfalfa) can be perfectly good food. It is easy to assume that the toxicity of locust-feeding aphids is caused by locust; many other herbivorous insect species acquire chemical compounds from their host plants that they use in their own defense. Because different plant species vary greatly in their chemistry, it would make sense, then, that cowpea aphids from different plants would have different defensive properties. However, here we show that host plant doesn't affect the toxicity of cowpea aphid lineages. Toxic lineages that were originally collected from locust remain toxic even when the aphids had been feeding on vetch or alfalfa, and nontoxic lineages originally collected from alfalfa remain nontoxic even when feeding on locust. So, if current host plant has nothing to do with toxicity, why are toxic aphids consistently associated with locust trees in nature? We show that this is a correlative effect: the toxic aphid lineage is also infected with a heritable bacterial symbiont, Arsenophonus, which we've shown in previous studies to improve aphid performance on locust, but decrease performance on other plant species. Here we show that Arsenophonus doesn't cause aphid toxicity, because the toxic aphids retain their toxic properties even when cured of Arsenophonus. But because Arsenophonus happens to infect a toxic aphid lineage, aphids that do well on locust are also toxic. Our study therefore serves as a precaution that correlation does not necessarily mean causation, and establishes an interesting system to study how variation in prey defense affects predator populations.

Image caption: Sibling Harmonia axyridis larvae fed on toxic (top) or nontoxic (bottom) aphid lineages. Larval age and image magnification are the same between panels. .
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Diversity of ecological tasks in water fleas acts as a health insurance of lakes

Liisa Nevalainen and Tomi LuotoA fossil shell of a water flea (taxon Chydorus cf. sphaericus) extracted from lake sediment deposits. Photo credit: Liisa Nevalainen.

Human impact on lakes, most importantly agricultural land use and waste water draining, has continued for a long time, even for centuries in areas with prehistorical settlements, and has caused nutrient enrichment that may in severe cases lead to algae blooms and fish kills. Increase in nutrients, especially phosphorus, alters the structure of biological communities and how they function in lakes, for example what organisms eat and where they live. This may cause irreversible changes in how the lakes operate and act as resources for humans. Even though the state of lake pollution has improved during recent decades, the long lasting impact of agricultural land use close to lake margins has changed many lakes from their natural state. To understand how lakes operate and change during and after nutrient enrichment, we investigated 100-300 year old lake sediment deposits for water flea fossils for their occurrence and diversity of their specific tasks, such as feeding and habitats. Water fleas are microscopic crustacean animals that live in lake bottoms and open waters. Our study sites included two lakes with a similar history of nutrient enrichment caused by increased agricultural land use nearby. Our results suggested that water fleas occupying a range of different biological and chemical roles in lakes increase in the early stage of nutrient enrichment (~100-200 years ago) due to an increase in the variety of resources, such as different food items and habitats. When the lakes entered into even more nutrient rich conditions (mainly during the 20th century) as human impact continued, the interactions between nutrients and water flea functions varied between individual lakes, and were more related to the food web structure and presence of water flea consuming fish. Diversity of tasks in water fleas thus has a clear connection to lake productivity and food web structure in the historical period and recent decades. This makes the study of water fleas and their fossils in lake bottom sediments a promising tool to understand the long term health and recovery of lakes under human impacts.

Image caption: A fossil shell of a water flea (taxon Chydorus cf. sphaericus) extracted from lake sediment deposits. Photo credit: Liisa Nevalainen.
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Tree genetics strongly affect forest productivity, but intraspecific diversity-productivity relationships do not

Dylan G. Fischer, Carri J. LeRoy, Erika Hersch-Green, Clarissa Dirks, Randy K. Bangert, Gina M. Wimp, Joseph K. Bailey, Jennifer A. Schweitzer, Stephen C. Hartg, Gery Allan, Thomas G. WhithamTrees changing colour. Photo provided by authors.

Do more diverse mixtures of plants function more efficiently and take up more carbon? Previous studies have suggested this occurs frequently in grasslands when species are mixed. Other studies have now suggested that the same can be true of genetic mixtures within a species. When groups of plants are more genetically diverse, they might be more productive. Nevertheless, this idea requires that plants work together, and access resources differently, which may not always be true when looking at different genetic stock within a species. We conducted the first forest ecosystem-scale experiment designed to test if more diverse mixtures of genetic stock result in more productive forests. Our results suggest that they do not! We used a fast-growing cottonwood tree common to the Western USA, and found no effect of genetic stock diversity. We did, however, find enormous differences between different genetic monocultures. In fact, the differences between genetic stock of the same species were so big that they rivaled differences in productivity among forest biomes. In other words, one can go from the most productive forest in the world, to the least productive forest in the world, simply by changing the genetics of the tree. The accompanying photo by author Dylan Fischer shows trees in our experimental forest during fall when different genetic stock are clearly recognizable based on when the leaves change color. Gold-leaved trees represent one genotype of tree, and the larger green trees in the background are another genotype. Less productive trees drop their leaves earlier, even though all trees are the same species. The large observed differences in productivity demonstrate the importance of recognizing genetic variation within naturally occurring tree species, especially in novel climate environments.

Image caption: Trees changing colour. Photo provided by authors.
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Agricultural biodiversity enhances soil nutrient acquisition by crops

Wei-Ping Zhang, Guang-Cai Liu, Jian-Hao Sun, Dario Fornara, Fang-Fang Zhang, Li-Zhen Zhang and Long LiImage provided by authors.

Higher biodiversity is a key feature of intercropping systems, which involve the cultivation of two or more plant species at (about) the same time within the same agricultural field. Intercropping has been widely practiced in many parts of the world for thousands of years, especially in China, mainly because it promotes more efficient use of soil nutrients, water and light compared to monoculture crops, which is then associated with higher yields and a better use of agricultural land. Wheat/maize and barley/maize intercropping are long-established agricultural systems in arid northwest China, especially in areas where seasonal crop growth is significantly limited.

In this study, we addressed how rates of Nitrogen (N), Phosphorous (P) and Potassium (K) uptake might change through time between different agricultural systems. We compared temporal trajectories of N, P and K uptake by wheat, barley and maize in monocultures and intercropping. We asked how a high diversity of plant species might affect the acquisition of N, P and K uptake over time.

We found that maximum cumulative N, P and K uptake (kg ha-1) by wheat and barley were significantly greater in wheat/maize and barley/maize intercropping systems compared with wheat or barley monocultures. Similarly, maximum cumulative N and P (but not K) uptake by intercropped maize were significantly higher than in maize monocultures.

Wheat and barley plants reached their peak of daily N, P and K uptake rates at about 50 days after seedling emergence, whereas maize reached its peak of daily uptake rates at about 100 days after wheat emergence. This mismatch in nutrient uptake is evidence of an important temporal differentiation in nutrient use between these plants. Temporal differentiation in nutrient use between wheat or barley and maize was largely due to differences in the timing of sowing and harvesting of these species, which ultimately contributed to minimizing interspecific competition and the avoidance of negative effects of one crop on another. Our results suggest that ‘temporal complementarity’ in nutrient uptake by neighboring plant species is a key ecological mechanism, which contributes to overyielding (when a mixture of species yields more than you would expect from the yields of the individual species when grown in monoculture) and to higher plant nutrient uptake in intercropping systems.

Image caption: Image provided by authors.
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Accumulation of external nitrogen in decaying Norway spruce wood

Katja Rinne-Garmston, Tiina Rajala, Krista Peltoniemi, Janet Chen, Aino Smolander and Raisa MäkipääImage provided by authors.

Decomposition of dead wood, which is controlled primarily by fungi, contributes substantially to the long-lived forest carbon (C) pool and has a significant role in forest nitrogen (N) cycling. Because of the very high C:N ratios in decaying wood, the rates of N cycling processes and fungi-driven decomposition are tightly linked. External sources of N may be vital in establishing and maintaining high decomposition rates, due to the importance of N in the production of enzymes and fungal material. Wood N content has been found to increase during the decay process; however, the sources of this external N remain unclear.

To examine N dynamics of Norway spruce logs at various stages of decomposition, we combined a large variety of analytical methods: wood nitrogen isotope composition (δ15N), wood N content (N%), radiocarbon dating, fungal composition and fixation rate of atmospheric N2 into wood by bacteria. For N2 fixation rate we also determined its dependency on ambient temperature and decay class (i.e. extent of decay), when estimating annual N2 fixation rates for our study site.

N2 fixation was observed to have a major role in increasing wood N content during decay. For the most decayed wood it accounted for 60% of the total N accumulation. The calculated annual fixation rate was 85 g N/ha. Our δ15N model describing the sources of external N, statistical analysis and the fungal DNA composition of decayed wood suggest that other sources of external N accumulating in wood were soil foraging wood-decay fungi and mycorrhizal fungi.

Our study improves knowledge of the temporal dynamics of N accumulation in wood with advancing wood decay, the potential sources of external N and their relative significance. All of these factors are important for both nitrogen and carbon models that consider ecosystem responses to climate change.

Image caption: Image provided by authors.
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Healthy trees contain fungi that can recycle them back to soil

Zewei Song, Peter Kennedy, Feng Jin Liew and Jonathan SchillingDecay begins before life ends. Wood decomposer fungi Fomes fomentarius (white rot) and Piptoporus betulinus (brown rot) emerge from the same standing birch tree in Alaska. Jonathan Schilling.

Decomposition of wood is a process that recycles an immense global pool of aboveground carbon and that emits significant amounts of CO2 to the atmosphere. Predicting wood decomposition rates, however, is proving to be a challenge for modelers. Variability in these predictions is increasingly attributed to biotic variability (e.g. organism dynamics) rather than abiotic variability (e.g. climate) alone. Specifically, many studies show that altering the sequence of fungal inoculations in dead wood can steer decomposition in different directions, depending on which fungi arrive first. To a modeler, it might seem daunting that the fate of wood decay would rest, to a large extent, on timing. In nature, however, we know that certain fungi have rigid associations with certain trees (e.g. Piptoporus betulinus on Betula spp. trees) despite being flexible in laboratory trials. This indicates that wood decay may be more predictable than our dead wood inoculations might imply, and we hypothesize that this can be traced to fungi colonizing trees as endophytes (organisms living inside plants) prior to tree death.

To test the potential for these endophytic fungi to initiate and potentially dominate wood decay, we used laboratory microcosms to incubate stem sections cut from ten healthy birch trees. At time zero, there were 143 fungal taxa present in the wood, on average. After five months of incubation in isolation or in the presence of fungi inoculated to challenge the endophytes, the birch wood lost nearly two-thirds of its fungal endophyte taxa and became dominated by wood-degrading fungi. These endophytic wood-degrading fungi caused severe decay (30-40% wood mass loss) without any additional inoculum. Most surprising, however, was that although decomposition in the wood of all birch trees (ten replicates) was dominated by brown rot-type fungi, the dominant taxa did not include Piptoporus betulinus commonly found in decaying birch. Instead, wood decay was dominated (>90% relative abundance) by four taxa in the genera Coniophora and Postia – best known as pests in lumber. These results support our hypothesis that tree endophyte fungi can initiate and dominate wood decay with predictable outcomes, but it implies that these community-driven outcomes remain a function of environment.


Image caption: Decay begins before life ends. Wood decomposer fungi Fomes fomentarius (white rot) and Piptoporus betulinus (brown rot) emerge from the same standing birch tree in Alaska. Jonathan Schilling.
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Organic macromolecules and ultraviolet radiation combine in freshwater ecosystems to damage water flea DNA

Raoul Wolf, Tom Anderson, Dag Olav Hessen and Ketil HyllandImage provided by authors.

As a result of reduced acid rain, climate change, and increased vegetation cover, many lakes and rivers in boreal regions currently experience a phenomenon called “browning”. It describes an increasing transport of plant-derived material from terrestrial plants and soil into freshwater, which causes a distinct brown color. The substances responsible for this browning are usually organic macromolecules or humic substances, commonly referred to as dissolved organic carbon, or simply DOC.

Plants and animals living in lakes and rivers can benefit from increased browning, as it protects them from harmful ultraviolet radiation (abbreviated UVR). However, UVR photons can also react with these DOC substances and produce so-called reactive oxygen species (ROS). These are harmful for all organisms, as they can damage cell membranes, proteins and DNA.

The aim of our study was to find out if the interaction of DOC and UVR in freshwater could produce ROS, and if these harmful substances could then cause DNA damage in an aquatic animal. The animals of choice in our experiments were freshwater water fleas of the species Daphnia magna. Despite their name, water fleas are crustaceans and important members of freshwater food webs, and commonly used model organisms. In our experiments, the water fleas were put in artificially browned waters and put under artificial UVR sunlamps.

We found that by themselves, either DOC or UVR produced only modest amounts of harmful ROS, which caused only minor DNA damage in the animals. However, the combination of DOC and UVR resulted in substantial production of ROS, which caused high levels of DNA damage in Daphnia. This points out the importance of indirect and unsuspected effects, by which climate change may affect aquatic organisms.

Image caption: Image provided by authors.
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Accelerometers can measure total and activity-specific energy expenditure in free-ranging marine mammals only if linked to time-activity budgets

Tiphaine Jeanniard-du-Dot, Christophe Guinet, John PY Arnould, John R. Speakman, Andrew W. TritesAntarctic fur seals. Image provided by authors.

How much energy animals spend during their daily life and how they spend their time are two key factors in understanding their health and their ability to survive and produce viable young in the wild. However, this is really difficult to study in wild marine animals at sea. Recently, biologgers have allowed us to remotely track and record behaviours of these animals in their natural environment. Particularly, the use of accelerometers capable of recording 3D movements and posture of marine mammals at a sub-second resolution have opened a window onto the secret life of these animals over periods of weeks to months.

The theory that an animal’s movements, i.e. its body acceleration, are directly linked to the energy needed to perform them has found growing interest within the scientific community as it can provide a relatively easy and inexpensive way of measuring metabolic rates. This link has been tested and validated in various birds, sharks and mammals, mostly in controlled ‘laboratory’ settings. However, it is still uncertain whether the same relationships hold in wild conditions when animals perform a wide range of behaviours and activities (diving, traveling, grooming and sleeping). Consequently, we investigated whether animals’ dynamic body acceleration could accurately predict the energy expended by free-ranging marine predators during full trips at sea.

To do so, we equipped 25 lactating northern and Antarctic fur seals with accelerometers, GPS and time-depth recorders, and simultaneously obtained a reference measurement of total energy expenditure. We then compared measures of dynamic body acceleration of animals with their own energetic expenses. Our results show that acceleration was not a good predictor of fur seals’ energy expenditure over a full foraging trip at sea. However, accuracy of the link between acceleration and energetics increased greatly when analysed by type of activities separately at sea. Our study confirms that acceleration is a promising way to estimate energy expenditures of free-ranging marine mammals at a fine scale, but that it needs to be based on how animals partition their time between different activities rather than being derived as a single measure applied to entire foraging trips.

Image caption: Antarctic fur seals. Image provided by authors.
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The Ecology of De-Extinction

De-extinction and evolution

Alexandre Robert, Charles Thévenin, Karine Princé, François Sarrazin and Joanne ClavelPhoto credit: Alexandre Robert.

Some biologists suggest that they can recreate long lost creatures and bring revived lineages back into suitable habitats. However, the potential for this de-extinction process to contribute effectively to the conservation of biodiversity remains unexplored, especially from the perspective of evolution. We discuss the application of the existing evolutionary conservation framework to potential de-extinction projects. We aim to understand how evolutionary processes can influence the dynamics of resurrected populations, and what the potential evolutionary benefits of de-extinction are. In programs aiming to revive long-extinct species, the most important constraints to the short-term dynamics of any resurrected population are their intrinsically low potential to grow and persist, and their poor adaptation to biotic and abiotic changes in the recipient environment. Assuming that some populations of resurrected species can persist locally, they have the potential to bring substantial benefits to biodiversity if the time since initial extinction is short relative to the time scale of evolution. The restoration of lost genetic information could lead, along with the re-instatement of lost ecological functions, to the restoration of some evolutionary patrimony and processes, such as adaptation. However, substantial costs might occur, including unintended ecological and evolutionary changes in the local system, and unintended spread of the species. Further, evolutionary benefits are limited because extinct species that are original from an evolutionary point of view might be those for which de-extinction is the most difficult to achieve practically. Further, the resurrection of a few extinct species does not have the potential to conserve as much evolutionary history as traditional conservation strategies, such as the reduction of ongoing species declines. De-extinction is a stimulating idea, which is not intrinsically antagonistic to the conservation of evolutionary processes. However, poor choice of candidate species, and most importantly, lengthy time scales between a species’ extinction and its resurrection are associated with low expected evolutionary benefits and likely unacceptable ecological and evolutionary risks.

Photo credit: Alexandre Robert.
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The Ecology of De-Extinction

A mammoth undertaking: harnessing insight from functional ecology to shape de-extinction priority setting

Molly Hardesty-Moore, Douglas McCauley, Benjamin Halpern and Hillary YoungImage provided by authors.

De-extinction, or the process of resurrecting extinct species, is an idea that once only seemed possible in science fiction films. Rapidly advancing technologies, however, are bringing de-extinction within reach. Most of the scientific discussion of de-extinction has been focused on the methods that could be used to make it operable and the ethics surrounding whether it is right or wrong to bring back once-extinct species. If made successful, de-extinction could prove an interesting new tool for ecologists and conservation biologists. From an ecologist’s vantage point, the great risk in de-extinction is that it becomes overly focused on the fabrication of species that look like once-extinct species – but do not act like them. In this paper we critically evaluate how de-extinction as a science would have to evolve in order to become a tool of strategic value to ecological communities and ecosystems.

We suggest three ways that de-extinction can produce species that resurrect the ecological jobs of extinct species with high fidelity. First, select candidate species that played a unique role in ecosystems and their loss is more likely to have left gaps in the operation of living systems that have not yet been filled. Second, concentrate on species that went extinct recently, rather than older extinctions. Ecosystems change, and the more time that passes the harder it will be for once extinct species to step back into ecosystems and assume their former roles. Lastly, work only with species that de-extinction can bring back to historic abundance levels, because abundance and ecological performance are often tied together. Following this playbook can help ensure that de-extinction does more than produce ecological zombies.

Image caption: Image provided by authors.
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Stomatal regulation and efficient xylem water transport regulate diurnal water and carbon balances of tropical lianas

Ya-Jun Chen, Stefan A. Schnitzer, Yong-Jiang Zhang, Ze-Xin Fan, Guillermo Goldstein, Kyle W. Tomlinson, Hua Lin, Jiao-Lin Zhang and Kun-Fang CaoHuge lianas in tropical forest (photo by Chen YJ).

Lianas are a conspicuous component of tropical and subtropical forests, contributing up to 35% of woody plant diversity and 40% of stem density. Lianas are considered to be structural parasites because they use the stems of other plants (mostly trees) to ascend to the forest canopy, readily thrive and form a carpet-like leafy layer with little vertical structure, where they can get better position in terms of light. However, lianas have to cope with high light, high temperature, and high wind—all of which increase water stress, to which lianas are reported to be vulnerable due to their extremely wide and long water-conducting vessels. How lianas adapt to water stress and balance daily carbon fixation and water use have rarely been tested empirically to date.

Here we selected four liana and five tree species that co-occur in a tropical forest in southwest China. Specifically, we tested whether physiological regulation can help lianas mediate the diurnal water and carbon balances during the day. Lianas tend to run a more “risky” hydraulic strategy. They appear to have low water storage capacity and are vulnerable to daily water deficit due to their wide vessels and slim stems. However, physiological regulation and efficient water transport from the soil to terminal branches could help lianas maintain their stem water status within a safe range to avoid excessive water loss. Therefore, we provide experimental evidence for physiological adaptation of lianas to a hot/dry environment that may help explain how lianas operate efficiently in tropical seasonal forests.

Image caption: Huge lianas in tropical forest (photo by Chen YJ).
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Adaptation to heat stress reduces plasticity in a marine copepod

Morgan. W. Kelly, M. Sabrina Pankey, Melissa .B. DeBiasse and David.C. PlachetzkiTigriopus californicus (female).

Human-driven climate change is a major threat to global biodiversity. For species that are able to do so rapidly enough, evolutionary adaptation may provide some protection against changing environments. Organisms may also respond to changing environments via physiological acclimation, and this too may buffer some populations from extinction. However, while both are potentially beneficial, these two responses may either dampen or strengthen each other’s effects, and little is known about how they are likely to interact during periods of environmental change. We examined the effects of adaptation to heat stress on the ability to acclimate to this stressor in the crustacean Tigriopus californicus. We artificially selected populations for increased heat tolerance in the lab, then measured heat tolerance and the ability to acclimate to heat stress in both selected populations and controls. We also measured the gene expression response to heat stress in both populations. We observed increased heat tolerance in experimentally evolved animals, but also diminished ability to acclimate to heat, and a smaller gene expression response to this stressor. Our findings have important implications for biological responses to climate change: if adaptation to environmental stress reduces the ability to acclimate, then sensitive populations may not be able to count on the benefits of both adaptation and acclimation as buffers against climate change.

Image caption: Tigriopus californicus (female).
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A global method for calculating plant CSR ecological strategies applied across biomes worldwide

Simon Pierce, Daniel Negreiros, Bruno E.L. Cerabolini, Jens Kattge, Sandra Díaz, Michael Kleyer, Bill Shipley, S. Joseph Wright, Nadejda A. Soudzilovskaia, Vladimir G. Onipchenko, Peter M. van Bodegom, Cedric Frenette-Dussault, Evan Weiher, Bruno X. Pinho, Johannes H.C. Cornelissen, J. Philip Grime, Ken Thompson; Roderick Hunt, Peter J. Wilson; Gabriella Buffa, Oliver C. Nyakunga, Peter B. Reich Marco Caccianiga, Federico Mangili Roberta M. Ceriani, Alessandra Luzzaro, Guido Brusa, Andrew Siefert, Newton P.U. Barbosa, F. Stuart Chapin III, William K. Cornwell, Jingyun Fang, G. Wilson Fernandes, Eric Garnier, Soizig Le Stradic, Josep Peñuelas, Felipe P. L. Melo, Antonio Slaviero, Marcelo Tabarelli, Duccio TampucciImage provided by authors.

A vast range of plant biodiversity exists on Earth, with each species characterised by a particular suite of morphological traits. However, not all traits affect survival and many operate only during brief moments of the life-cycle. Plants exhibit a surprisingly limited number of basic ways in which they can use available resources to grow and persevere: differences in plant size affect the outcome of competition, and differences in the ‘economics’ of how plants invest resources – in individual robustness or in reproduction – determine how plant populations persist during environmental difficulties. Much of biodiversity represents variation around these general themes, or primary ‘strategies’.

Certain size and economics traits that can represent primary functioning, such as leaf size and aspects of photosynthetic tissue density, have now been measured around the world and can potentially provide a global framework within which strategies can be measured and compared. These absolute limits are used here to develop a tool for plant strategy classification, grounded in a theory of plant strategies (competitor, stress-tolerator, ruderal, or ‘CSR’, theory).

As plant adaptation within different geographic regions is intimately linked to climate (particularly temperature and seasonal water availability) there is reason to expect plant strategies to vary at the largest scales, between bioclimatic regions or biomes. The global CSR analysis method was used to analyse the range and character of plant strategies in all 14 major biome classes worldwide. The results did demonstrate differences in functional specialisation between biomes but also detailed a large amount of variability within biomes, probably due to the presence of contrasting habitats and plant communities within each one. However, it is clear that the global ‘CSR analysis’ tool presented here is valid for the functional description of plant species and communities worldwide, and can provide plant ecologists working in different habitats and biomes with a lingua franca equivalent to taxonomists’ use of Latin.

Image caption: Image provided by authors.
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Importance of deep water uptake in tropical eucalypt forest

Mathias Christina, Yann Nouvellon, Jean-Paul Laclau, Jose L. Stape, Jean-Pierre Bouillet, George R. Lambais , Guerric le MairePhotograph provided by authors.

Water uptake by deep roots is generally considered to be an efficient means of adapting to drought in tropical and subtropical forests. Although fine root biomass generally decreases exponentially with depth, with fewer than 10% below a depth of 1 m, many tree species can grow roots to depths of more than 10 m with maximum rooting depths reaching about 60 m for eucalyptus trees. Despite their low biomass, deep roots are likely to have a strong effect on the functional ecology of forest ecosystems.

There is a lack of in situ measurements investigating the multiple interactions between rainfall patterns, water fluxes in the soil, water table dynamics, root growth, and the dynamics of water uptake by tree roots down to the root front (maximum root depth) in tropical forests. Simple forest ecosystems such as Eucalyptus plantations may provide useful information on the belowground strategy of fast-growing trees, and more generally on the consequences of deep rooting patterns for tree water use in tropical forests.

The aim of this study was to explore the multiple functions of deep rooting profiles in terms of drought avoidance strategy and use of transient water resources, based on long term experimental and modelling analyses in a eucalypt plantation. Our study provides a quantification of water withdrawal throughout the whole rooting profile, including the interaction with the water table, in a planted tropical forest over an entire cultivation cycle of five years. We show that deep water uptake (3 to 16 m depth) is critical to explain the high transpiration rates throughout the year, with different mechanisms involved at different growth stages. Possible insights into the role of deep roots in tropical forests are discussed, as well as the impact of deep rooting on large scale ecosystem services.

Image caption: Photograph provided by authors.
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Conserving rare species when de-extinction is an option

Gwenllian Iacona, Richard F. Maloney, Iadine Chadès, Joseph R. Bennett, Philip J. Seddon, Hugh P. PossinghamThe Huia (Heteralocha acutirostris), is an extinct New Zealand bird species with an interesting dimorphism such that the female has a dramatically longer bill than the male. The last individuals may have survived until as recently as the 1960s. Species such as this are often suggested as candidates for de-extinction: they are recently lost species of significant conservation interest, and the threats that caused their extinction are known. This paper discusses how using a decision theory approach to conservation prioritization can help managers decide if de-extinction of such species is a good idea.   – photographer J.L . Kendrick. Photo courtesy of the New Zealand Department of Conservation.

The technology to revive extinct species (de-extinction) may soon no longer be simply in the realm of science fiction. In the exciting rush to bring back populations of wild mammoths, or moa, or passenger pigeons, we need to take a step back and make sure that the conservation benefits of such an action outweighs any potential perverse negative impacts. We suggest that the decision tools used in modern conservation prioritization approaches can quantitatively and transparently weigh the pros and cons of de-extinction. This is especially relevant to managing a de-extinct species in the wild in systems where there are extant species of conservation concern. While outlining the steps to the process, we discuss the new considerations that would be important if de-extinction was a possible conservation action. One particularly interesting implication of de-extinction would be its capacity to change the biodiversity conservation problem from the current one that is similar to managing non-renewable natural resources, to a version where the management is of a potentially renewable natural resource. This switch opens up a new suite of time preference and risk aspects to rare species management which could change the strategies employed by managers and the possible conservation outcomes. We are not arguing for or against de-extinction. Instead, we are proposing that the technological advances need to be considered within the context of the existing conservation landscape, and that such considerations may include unprecedented modifications to the current species prioritization problem.

Image caption: The Huia (Heteralocha acutirostris), is an extinct New Zealand bird species with an interesting dimorphism such that the female has a dramatically longer bill than the male. The last individuals may have survived until as recently as the 1960s. Species such as this are often suggested as candidates for de-extinction: they are recently lost species of significant conservation interest, and the threats that caused their extinction are known. This paper discusses how using a decision theory approach to conservation prioritization can help managers decide if de-extinction of such species is a good idea. – photographer J.L . Kendrick. Photo courtesy of the New Zealand Department of Conservation.
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Root heterogeneity along an arctic elevational gradient: the importance of resolution

Sabrina Träger & Scott D. WilsonRoots in arctic forest in a minirhizotron image (13.5 x 18 mm). Photo by S. Träger.

The majority of ecological studies focus on aboveground parts of plants and their interaction with the environment. However, plant roots often account for 80 – 90 % of plant biomass, especially in the Arctic. Roots are the key link providing plants with nutrients and water, and providing organic carbon to soils. Patchy distribution of resources can lead to and in turn be influenced by patchy root growth.

The magnitude and spatial scale of root patchiness varies with the dominant vegetation type (e.g. forest or grassland). However, studies are limited to temperate regions and deal with scales ranging between a few kilometers to a few centimeters. At the same time, the root diameter and thus the scale of interaction with the environment can be as small as fractions of a millimeter. Knowledge about root patchiness at those scales is still missing.

We analyzed the magnitude and scale of fine root patchiness in the Arctic at resolutions ranging from 1 to 300 mm² along an arctic alpine gradient (500 to 1100 m above sea level) to cover a variety of vegetation types (from forest to tundra). To study roots in their natural environment and in a non-invasive way we used a minirhizotron camera.

Roots in all vegetation types responded to or generated very fine scales of spatial patchiness of a few millimeters, which are scales about five times smaller than those that have previously been found. The patchiness of roots was greatest at the highest elevation, tundra, where the smallest plants dominated, which stands in contrast to studies from temperate regions where patchiness increases with plant size. Both the magnitude and scale of heterogeneity varied with sampling resolution, suggesting resolutions as small as a few millimeters are relevant to studies of spatial root interactions and belowground processes.

Image caption: Roots in arctic forest in a minirhizotron image (13.5 x 18 mm). Photo by S. Träger.
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Stress hormones may help handicapped moms produce young

James W. Rivers, Gretchen N. Newberry, Carl J. Schwarz and Daniel R. ArdiaPhoto provided by authors.

Stress hormones are typically thought of as being bad for one’s health, but they can be beneficial to individuals over short-term periods of high energetic demand. In this study, we evaluated whether female violet-green swallows, small insect-eating birds found throughout western North America, had altered stress hormone concentrations while undergoing unplanned energetic challenges when rearing young. To test this idea, we experimentally removed a small number of wing feathers at two different intensities (low and high) in some individuals, whereas other individuals were handled in the same manner but had no feathers removed. We measured stress hormone concentrations at two points during the breeding season when females were feeding their young: immediately prior to feather removal, and 10 days later. We also assessed whether females in the three groups varied in how often they fed their offspring, as well as the quality and quantity of young that were raised.

Females in the three groups were initially similar in their body size and in their baseline stress hormone concentrations. However, females experiencing feather removal were found to have much greater increases in baseline stress hormones, and the amount of stress hormones was positively linked to the degree of feather removal. Despite this, females in both feather-removal groups were able to maintain feeding rates at levels similar to control females, and they produced a similar number of young. Offspring from mothers in the different groups did, however, have different levels of stress hormones, the reason for which remains unclear. Overall, this study suggests that energetic challenges are associated with increases in stress hormones, and such increases appear to allow female swallows to maintain feeding rates at a level typical of control females and produce a similar number of offspring. Thus, stress hormones may provide individuals with a way of ramping up their parental effort when they encounter unexpected energetic challenges, so they can produce the same number of young they would have done during a normal breeding season.

Image caption: Photo provided by authors.
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Effects of flooding on relationships between plants and soil fauna

Corentin Abgrall, Matthieu Chauvat, Estelle Langlois, Mickaël Hedde, David Mouillot, Sandrine Salmon, Bruna Winck and Estelle ForeyView of the considered flooding gradient from the mudflats (photo credit: Estelle Langlois-Saliou).

Terrestrial ecosystems are composed of plants and soil animals (e.g. earthworms, small insects) with strong interactions between them that are central in ecosystem functioning. These interactions between plants, soil organisms and the soil itself regulate processes such as nutrient cycling or energy flow and control how plant and animal communities are structured. Simultaneous study of all these compartments can therefore provide additional information on how the ecosystem is structured and functions, more so than separate studies ever would. In this study we looked for links between plant and soil fauna characteristics (or traits) in relation to soil abiotic properties along a flooding gradient on the banks of the Seine River. Small and localized environmental gradients such as this one provide powerful tools to assess the effects of variations within a specific environmental variable (here flooding) on various processes. We sampled and identified soil fauna and plants in the field and used publically available databases to provide information on their traits. We observed a strong influence of flooding on the structuring of plant communities with particular traits, or adaptations, being selected by flooding intensity leading to the existence of functionally, and visually, different communities along the gradient. Springtails, small soil arthropods which we used as a proxy for the soil fauna, were not observed to be directly linked to variations in flooding intensity. Instead of being directly filtered by flooding, springtail traits were selected and filtered by variations within plant communities, especially their traits. We thus revealed an indirect influence of flooding intensity on soil fauna through its effects on plant communities. As this pattern has been previously observed for other gradients and species, our results enhance our understanding of how naturally-occurring communities can be influenced by other organisms as well as their physical and chemical environment.

Image caption: View of the considered flooding gradient from the mudflats (photo credit: Estelle Langlois-Saliou).
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Salivary cues: Simulated deer browsing induces changes in plant hormones and defense compounds in tree saplings

Bettina Ohse, Almuth Hammerbacher, Carolin Seele, Stefan Meldau, Michael Reichelt, Sylvia Ortmann and Christian Wirth Simulating deer browsing by clipping a tree sapling’s apical bud and applying deer saliva on the fresh cut (here on Acer pseudoplatanus). Photo by Bettina Ohse.

Young trees in temperate forests are often browsed by mammalian herbivores, such as deer. Studies on insect herbivory have shown that plants respond to herbivory by upregulating growth hormones and producing defense compounds. However, it remains unknown whether the same response mechanisms are induced when young trees are browsed by mammals. We also wanted to know if tree saplings can detect whether they are just injured mechanically, or whether they are browsed by deer. To answer these questions, we simulated deer browsing on field grown sycamore maple (Acer pseudoplatanus) and European beech (Fagus sylvatica) saplings by clipping their buds in winter and leaves in summer. For some of the saplings we additionally applied deer saliva with a pipette on the cut surface.

We found that two hours after clipping, wound hormones, called jasmonates, increased in the remaining maple buds and beech leaves. This is a well-known response to herbivory, but differed here between tree species and developmental stages. In maple buds, growth hormones (cytokinins) also increased after clipping, probably because if maple loses its one main apical bud through browsing, the upregulated growth hormones will help activate lateral buds for regrowth. Beech has more equal buds and may therefore not respond as strongly to clipping when losing one. Saliva application did not amplify wound hormone responses, but led to increased levels of the signaling hormone salicylic acid in beech leaves, suggesting that the trees were able to detect something in the deer saliva. Interestingly, changes in defense compounds were found only when deer saliva was also applied, which means that these compounds are only regulated specifically after deer browsing and not after any mechanical damage. Not all defense compounds changed in the same way. Mainly hydrolysable tannins increased, although they are not harmful to deer. Condensed tannins, which occurred only in beech and are known to be avoided by deer because they negatively impact digestion, did not change, and may rather act as a constitutive defense, i.e. one that is permanently present.

We conclude that tree saplings are able to detect and specifically respond to mammalian herbivory, although strategies to respond to mammalian browsing seem to be species-specific, probably based on distinct combinations of morphological and chemical characteristics.

Image caption: Simulating deer browsing by clipping a tree sapling’s apical bud and applying deer saliva on the fresh cut (here on Acer pseudoplatanus). Photo by Bettina Ohse.
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In, out or staying put? The landscape and the plant both have their say.

Alistair G. Auffret, Elsa Aggemyr, Jan Plue and Sara A.O. CousinsThe Stockholm archipelago from above (Photo: S. Cousins); Common Hepatica (Hepatica nobilis) responded well to grassland abandonment (Photo: A. Auffret);  However, Mountain Everlasting (Antennaria dioica) disappeared completely from the 27 islands  (Photo: A. Auffret); Harebell (Campanula rotundifolia) has characteristics of plants both able to persist and able to disperse (Photo: A. Auffret).

Every summer, Stockholm's idyllic archipelago is alive with tourists. People arrive at an island, stay for a while, and then leave. During the 20th century, the same has happened to the islands' plant species, albeit much more slowly. Up until the 1950s, the area was a busy farming landscape. Fodder was grown in the meadows and cattle were transported from island to island during the summer. Since then, agriculture has been almost totally abandoned and now most of the land area is covered in forest. This has had a huge impact on the area's plant life.

We compared species lists of plants from 27 small islands in 1908, when farming was still thriving, with our own survey from 2008. This meant that for each island, we were able to see which plant species had arrived, which had disappeared and which had stayed put during 100 years of landscape change. It was much easier for plants to survive on and arrive at larger islands and those close to the mainland, but it also depended on the plants themselves. Taller plants, which were able to compete for light in the overgrown pastures, could persist and spread to new islands, while plants with long life spans or long-lasting seeds were also more able to survive adverse conditions. Plant species that prefer to move (disperse) rather than stay put did not fare so well. Even if one would expect such species to move to more suitable areas following grazing abandonment, the magnitude of change meant that there was simply nowhere for them to go.

We also compared the species listed in the grid squares used for the historical and present-day plant atlases covering the same area. In this case it was only the plants, not the landscape, which explained change over time. Understanding how plants and animals are affected by human activity over time is interesting for ecologists, and historical species lists are therefore very useful. However, our results show that it is important to understand that different sources of species observations can affect the patterns we see and what drives them.

Image caption: The Stockholm archipelago from above (Photo: S. Cousins); Common Hepatica (Hepatica nobilis) responded well to grassland abandonment (Photo: A. Auffret); However, Mountain Everlasting (Antennaria dioica) disappeared completely from the 27 islands (Photo: A. Auffret); Harebell (Campanula rotundifolia) has characteristics of plants both able to persist and able to disperse (Photo: A. Auffret).
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Climate and atmospheric change impacts on sap-feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites

James M. W. Ryalls, Ben D. Moore, Markus Riegler, Lisa M. Bromfield, Aidan A. G. Hall and Scott N. Johnson Magnified pea aphids (Acyrthosiphon pisum) feeding on an experimental lucerne (Medicago sativa) leaf.

‘Little things that run the world’ is how E.O. Wilson described insects and other invertebrates, but which ‘little things’ will run a future world with higher atmospheric carbon dioxide concentrations and warmer temperatures? We set about answering this for aphids feeding on lucerne and aimed to get at the underlying plant-mediated mechanisms for changes in their performance. We chose aphids because these troublesome insects transmit at least 50% of insect-vectored plant viruses and therefore cause widespread damage to crops worldwide - a troubling prospect considering that we’ll need to feed another 3 billion people by 2050. In addition, they can have disproportionately large impacts on foodwebs and insect community structure simply because they can reproduce so rapidly in response to favourable environmental conditions. Aphids have been repeatedly identified in reviews and meta-analyses as being a net beneficiary of predicted increases in atmospheric carbon dioxide concentrations, yet the exact mechanisms for this aren’t always clear. Our study addresses a missing piece of this jigsaw by investigating the underlying chemical mechanisms for their success and how concurrent climatic factors (elevated air temperature) interact with elevated CO2. We demonstrated that it was a specific group of amino acids that increased and decreased, respectively, under elevated CO2 and temperature, which was directly correlated with aphid performance. This consistent pattern across five plant genotypes explained why aphids benefited from elevated CO2, yet performance declined when elevated temperature was included. Understanding the chemical mechanisms underpinning insect responses to climate and atmospheric change raises the possibility of building resistance into new crop cultivars and gives us some foresight for preventing pest outbreaks and preserving ecosystem functions.

Image caption: Magnified pea aphids (Acyrthosiphon pisum) feeding on an experimental lucerne (Medicago sativa) leaf.
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The honeybee leads the effect of an exotic plant on resident plant-pollinator communities

Ana Montero-Castaño and Montserrat VilàSubsample of the Mediterranean plant –pollinator community studied.

Exotic plants that depend on pollinators for their reproduction usually become well integrated into the diet of generalist pollinators. This integration can affect the entire recipient plant-pollinator community; for instance, by attracting pollinators, or on the contrary, by stealing pollinators from the recipient communities. Understanding the factors that govern such variable effects is among the fundamental goals in invasion ecology.

Because species traits determine the interaction between plants and pollinators (e.g. size, shape and colour of flowers and body size or tongue length in pollinators), trait similarity among plants or among pollinators might modulate how they affect each other.

We conducted a flower removal experiment to investigate the effects of the exotic legume Hedysarum coronarium on the pollination patterns of a Mediterranean shrubland community. We explored if the number, frequency or identity of interactions were affected by the exotic and whether the effects were influenced by trait similarity. Specifically, we explored the influence of similarity in flower morphology with Hedysarum (i.e., whether natives were also legumes or not). And in the case of pollinators, we explored the influence of belonging to the same functional group (i.e., whether they were also bees or not) as the main pollinator of Hedysarum, the highly competitive honeybee. Other pollinators were flies and beetles.

Hedysarum was well integrated into the diet of 15 generalist pollinators. Such integration did not affect the pollination of native plants (irrespective of their flower morphology) in terms of number and frequency of interactions, despite a reduction in proportion of honeybee visits. On the other hand, Hedysarum reduced the visitation frequency of bees to both natives and Hedysarum. In addition, pollinators switched the plants they visited (i.e., interaction rewiring) according to the changes in the proportion of honeybee visits. That is, the bigger the change in the proportion of honeybee visits to a given plant, the greater the interaction rewiring.

In conclusion, pollinators respond to plant invasions with a plastic use of floral resources. When the exotic attracts highly competitive pollinators such as the honeybee, plasticity is especially significant for pollinators functionally close to that pollinator, i.e. other bees. The result is an interaction rewiring due to pollinators avoiding competition with the honeybee.

Image caption: Subsample of the Mediterranean plant –pollinator community studied.
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Bridging frameworks to better understand the nutrition of animals in their environment

Erik Sperfeld, Nicole Wagner, Halvor Halvorson, Matthew Malishev, David RaubenheimerThe water flea Daphnia magna (photo: Silvia Heim), the grasshopper Locusta migratoria (adapted photo by Ferran Turmo Gort, CC BY 2.0), and the caddisfly larvae Pycnopsyche gentilis (courtesy of Bob Henricks)..

It is essential for ecologists to understand the interaction between animal nutrition and the environment to better predict how animals will respond to our changing world. The research field investigating this animal nutrition-environment interface, nutritional ecology, has developed tremendously within recent decades. Steering this field are two prominent research frameworks, offering a toolbox of concepts to address the challenges of nutritional ecology. One framework, ‘Ecological Stoichiometry’ (ES), uses elements (e.g. carbon, nitrogen, phosphorus) to explore how imbalanced diets alter animal physiology, population dynamics, and nutrient cycling in ecosystems. The second framework, ‘Nutritional Geometry’ (NG), uses geometry to study feeding decisions of animals to maximize their fitness. ES originates from studies on element cycling, often using aquatic invertebrates (e.g. water fleas) as focal organisms, whereas NG originates from animal behaviour research, particularly on terrestrial insects (e.g. grasshoppers and cockroaches). Both origins have influenced the types of questions investigated and the type of nutrient currency used, with NG focusing on macronutrients (proteins, carbohydrates, and fats) and ES on elements.

Despite their inherently different perspectives, NG and ES are unified by a shared concept that contributes to collectively achieving the common goal of understanding the animal nutrition-environment interface. This concept, called homeostasis, drives animal nutrition and is broadly defined as an animal’s ability to regulate its internal nutrient status under a varying diet. ES uses an “are you what you eat?” approach to homeostasis by measuring internal nutrient composition, while NG adds individual behaviour to diet choice and food intake. In this paper, we illustrate how the complementary homeostasis approaches of NG and ES can be integrated in a conceptual, mathematical model that a) describes animal metabolism and tracks the flow of multiple nutrients through the body, and b) describes individual animal feeding behaviour in its environment in time and space. Our described modelling approach aims to advance nutritional ecology by better connecting organisms with their environments across different scales by using a shared concept well established in the field.

Image caption: The water flea Daphnia magna (photo: Silvia Heim), the grasshopper Locusta migratoria (adapted photo by Ferran Turmo Gort, CC BY 2.0), and the caddisfly larvae Pycnopsyche gentilis (courtesy of Bob Henricks)
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Experimental warming in a dryland community reduced plant photosynthesis and soil CO2 efflux, but didn't change the relationship between the fluxes

Timothy M. Wertin, Jayne Belnap and Sasha C. ReedClimate manipulation experiment in a semiarid grassland, with Achnatherum hymenoides (Indian ricegrass) as the focal plant species; photo by TM Wertin.

As air temperatures warm and precipitation patterns shift, arid and semiarid grasslands, such as those typical of the southwestern US, are expected to expand throughout this century. At the global scale, drylands support up to 38% of the human population, a number that is expected to increase due to both population growth and climate change. Recent research also suggests dryland systems are a major factor dictating future carbon cycling and climate. From a regional perspective, arid and semiarid grasslands represent critical habitat for wildlife, agriculture, and livestock grazing. If climate change affects plant growth, it would have dramatic implications on the landscape’s ability to sustainably maintain food production and carbon stocks.

Nevertheless, our understanding of how dryland grasses will respond to climatic change remains notably poor. To test the effects of warming on arid grasslands we conducted a climate manipulation study where we artificially increased plant and soil temperature by ~2 oC, which is well within the expected range of temperature increase expected for the Southwest. Specific goals of this experiment were to determine how a change in temperature would affect photosynthesis (the process by which plants convert solar energy and CO2 into organic forms) and soil respiration (the conversion of plant carbon and soil organic matter into CO2 and energy). We conducted this experiment on Indian Rice Grass, a native plant that is heavily relied upon for native and domesticated animal grazing.

Our study showed that a relatively subtle increase in temperature reduced both photosynthesis and soil respiration. The close coupling between soil respiration and photosynthesis was surprising; although warmer temperature reduced both fluxes, it did not change the relationship between the fluxes. In our study site, soil organic matter is quite low, and our data suggest that soil CO2 efflux was strongly regulated by newly acquired photosynthetic products respired or exuded by roots. This finding may have dramatic implications for climate models, which are used to predict carbon cycling and climate, and also heralds concern for the important grasses of the Southwest.

Image caption: Climate manipulation experiment in a semiarid grassland, with Achnatherum hymenoides (Indian ricegrass) as the focal plant species; photo by TM Wertin.
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The Ecology of De-Extinction

How close can we get to bringing an extinct species back to life?

Beth Shapiro A researcher prepares a fragment of mammoth bone for DNA extraction in the Paleogenomics Lab at UC Santa Cruz. Credit: Beth Shapiro.

Over the last five years, de-extinction, which is the term used to describe the idea that extinct species may soon be brought back to life, has received increasing attention in both scientific and public arenas. Discussions about de-extinction tend to concentrate on the ethical and political implications of resurrecting extinct species and, increasingly, to focus on the ecological consequences of releasing resurrected species into the wild. Relatively less attention has been paid, however, to the process of de-extinction itself, specifically whether the technology is sufficiently advanced to bring an extinct animal species back to life.

I review the three main technologies that are being considered at present for de-extinction: back-breeding, cloning via somatic cell nuclear transfer, and genetic engineering. Back-breeding aims to concentrate ancestral traits that persist within a population into a single individual using selective breeding. Cloning aims to create genetically identical copies of an extinct species from preserved cells, which means that this approach may not be feasible for long-dead organisms whose cells, and the genetic material within them, have decayed. Genetic engineering draws on recent advances in both ancient DNA and genome editing technologies, and aims to edit the genome sequence within a living cell so that the sequence more closely resembles that of a closely related extinct species. This edited cell would then be cloned, creating a genetic hybrid between the living and extinct species.

Because the phenotype of an organism is the consequence of the interaction between its genotype and the environment in which it develops and lives, none of these processes will create exact copies of the extinct species that they are attempting to resurrect. Precise replication, however, is not necessary to achieve the conservation-oriented goals of de-extinction. In the majority of ongoing de-extinction projects, the goal is to create functional equivalents of species that once existed: ecological proxies that are capable of filling the extinct species’ ecological niches. It is this application of de-extinction technologies that is likely to have the most positive impact on conservation.

Image caption: A researcher prepares a fragment of mammoth bone for DNA extraction in the Paleogenomics Lab at UC Santa Cruz. Credit: Beth Shapiro.
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Assessing vulnerability of functional diversity to species loss: a case in Mediterranean agricultural systems

Carlos P. Carmona, Irene Guerrero, Manuel B. Morales, Juan J. Oñate & Begoña PecoDetail of one of the agricultural fields included in the study.

Increasing intensification of land use is leading to biodiversity losses worldwide, which in turn can alter the functioning of ecosystems. Agricultural intensification aims to increase yield through changes in management both at the local field and at the landscape level. Arable plants, which support services like biological pest control, as well as the presence of pollinators, birds and mammals, are one of the groups most notably affected by these practices. However, it is increasingly clear that not all species are equally important for ecosystem processes. Approaches based on the traits of plants (e.g. height or leaf area) have allowed ecologists to tackle questions regarding the effects of plants on ecosystem functioning, because these traits determine how species affect different ecosystem processes. Thus, whereas the loss of a species with unique functional traits from a community may result in a reduction in the capacity of the community to perform some function, the loss of a functionally redundant species should have a much smaller impact. Assessment of the changes in functional trait diversity –a proxy of the range of functions provided by a community– as species are lost appears as a promising tool to predict the impacts of land use intensification. Here, we modified a recently developed method that compares the changes in functional diversity caused by random losses of species with those expected under the most likely order of species losses. This approach allowed us to estimate the vulnerability of the functional diversity of biological communities. We applied this method to arable plant communities from 78 agricultural fields in the area of Madrid (Spain), across a gradient of agricultural intensification. We found that the vulnerability of functional diversity to species losses increased along with agricultural intensification. Importantly, vulnerability to intensification was markedly non-linear, with great increases in the first stages of intensification, and much smaller increases afterwards. Our results suggest that field-level agricultural intensification not only reduces the taxonomic and functional diversity of arable plant communities, but also eliminates functionally redundant species, thus increasing their vulnerability to further species losses.

Image caption: Detail of one of the agricultural fields included in the study.
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Long-lasting effects from previous winter warming events suggest that an important sub-Arctic moss will be disadvantaged in a future sub-Arctic climate

Jarle W. Bjerke, Stef Bokhorst, Terry V. Callaghan & Gareth K. PhoenixA shoot of splendid feathermoss with fertile organs (sporophytes) protruding from the green shoot segments, which are partly blurred. Photo credit: Jarle W. Bjerke.

Understanding the impacts of climate change on ecosystems is complex for many reasons. Firstly, there are many drivers of change and each driver has numerous interacting facets. Secondly, there are practical issues that hinder research, such as difficult species groups and winter research. Here we focus on a moss (an understudied plant group), the winter period (under-represented in field studies) and extreme warming events, that are both difficult to observe and even more difficult to predict. Winter is a period of dormancy for plants of cold environments. However, winter climate is changing, leading to an increasing frequency of warm weather events that temporarily reduce snow cover. These conditions can break dormancy for some plants and expose them to freeze-and-thaw stress. Mosses are a major component of northern lands, yet the longer-term impacts of such winter warming events on mosses remain unknown. Therefore, we undertook a field experiment to simulate these events over three consecutive winters in a sub-Arctic open woodland. The mat-forming splendid feathermoss (Hylocomium splendens), also known as the glittering woodmoss or stairstep moss, was the most abundant moss species at our site, and we studied it during both the experimental years and in the years following these events. This is probably one of the most abundant moss species in the World, and plays important roles such as insulating the ground. We found that the warming events reduced its vitality. Both photosynthesis and shoot growth rates declined considerably and were still much lower than in non-experimental plots even four years after the last warming event. These results suggest that this moss will be disadvantaged in a future sub-Arctic climate where a high frequency of winter warming events may become the norm. More broadly, this suggests the potential for large consequences for northern lands where mosses are often a major component of the vegetation and where the greatest increases in extreme winter events may be expected. This will again have a strong influence on ground temperature and moisture, cycling of nutrients and water, permafrost thaw and ecosystem carbon balance.

Image caption: A shoot of splendid feathermoss with fertile organs (sporophytes) protruding from the green shoot segments, which are partly blurred. Photo credit: Jarle W. Bjerke.
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The effect of egg size on hatch time and metabolic rate: theoretical and empirical insights on developing insect embryos

James L. Maino, Elia I. Pirtle, and Michael R. KearneyGumleaf Grasshopper from Australia’s Dry Eucalypt Forest. This grasshopper resembles a dry gum leaf and lays its eggs in the leaf litter. Photograph by James Maino.

As organisms change in size, they much also change in design to compensate for the mismatched scaling between surface-area and volume-based processes. Body size scaling relationships, combined with metabolic theory, allow biologists to study ecological phenomena in terms of processes at the organism level. By properly understanding biological processes at one level, higher level processes are able to be predicted and, in doing so, a mechanistic understanding is achieved. In this study we present a model based on simple energy and mass transfer processes during egg development that is able to explain how hatch time varies with species size and the time course of metabolic rate from egg lay to hatch. Our findings suggests that previous models made unrealistic assumptions regarding the metabolic activity of a freshly laid egg, leading to unreliable predictions. Metabolic theory is increasingly being applied in biology to understand a range of biological phenomena. Contributing to its success is its emphasis on the currencies of mass and energy, which are relevant at all scales of biology from the molecular to the ecosystem. Our presented model and supporting data on 98 species of insects advances our mechanistic understanding of egg development and highlights the usefulness of process-based models from which higher levels patterns can be derived.

Image caption: Gumleaf Grasshopper from Australia’s Dry Eucalypt Forest. This grasshopper resembles a dry gum leaf and lays its eggs in the leaf litter. Photograph by James Maino.
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Positive species diversity and above-ground biomass relationships are ubiquitous across forest strata despite interference from overstorey trees

Yu Zhang, Han Y.H. Chen, Anthony R. TaylorOld growth red spruce (Picea rubens) stand, typical of eastern Canadian temperate forest.  Photo Credit: Anthony Taylor.

There is growing concern over rates of global species diversity loss, given its important role in the healthy functioning of ecosystems and the many goods and services they provide. However, our knowledge of how diversity supports ecosystem function remains unclear. While positive relationships between tree species diversity and forest biomass production have been observed, forests are structurally complex, consisting of various understorey vegetation layers which also contribute to ecosystem functioning as they often account for the majority of species richness; however, the relationships between understorey vegetation diversity and function are largely unexplored. Further, few studies have simultaneously assessed how both overstorey and understorey vegetation interact and contribute to overall forest ecosystem function.

In our study, we used Canada’s National Forest Inventory data, covering many forest types across a wide spatial distribution, and a robust statistical modeling approach (structural equation modelling) to explore both overstorey and understorey relationships between species richness and forest biomass production while accounting for potentially confounding factors, including climate, physical site characteristics, and forest ageing. We found positive relationships between species richness and biomass production across all forest vegetation layers, but the relationship was strongest for the overstorey layer. Species richness of the understorey tree, shrub, and herb layers was positively related to overstorey species richness. However, overstorey biomass had a negative effect on the biomass production of all understorey layers. Our results suggest that resource filtering by overstorey trees might have reduced the strength of the positive diversity-productivity relationships in the forest understorey, supporting previous hypotheses that the magnitude and direction of diversity-productivity relationships is context specific and dependent on the conditions of the surrounding environment. Further, heterogeneity in understorey resources, as affected by overstorey trees, may promote niche complementarity (i.e. plants using different resources, or at different times or in different places) as the main mechanism driving diversity-productivity relationships in understorey vegetation.

Image caption: Old growth red spruce (Picea rubens) stand, typical of eastern Canadian temperate forest. Photo Credit: Anthony Taylor.
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Do thermoregulatory costs limit altitude distributions of Andean forest birds?

Gustavo A. Londoño, Mark A. Chappell, Jill E. Jankowski and Scott K. Robinson Andean cock-of-the-rock. Image provided by authors.

Tropical mountains contain the highest regional bird diversity in the world, largely because of high turnover of species with narrow altitudinal ranges. Understanding the mechanisms that limit so many species to narrow altitudinal distributions in the Andes is the central goal of our study. Our research is the first experimental approach to understanding the role of thermal physiology in limiting species’ altitudinal distributions. The biologist Daniel Janzen in 1967 hypothesized that tropical organisms should be specialized to a narrow range of temperatures because they experience little climatic variation in their ranges. As a result, they should be intolerant of temperatures outside of the optimal range, which would inhibit up- or downslope movements. Some tropical ectotherms (cold-blooded animals) fit Janzen’s predictions, but we do not know if endotherms, which maintain a constant internal temperature, are also excluded from environments outside their optimal temperature range. We measured several aspects of thermal physiology of 215 bird species across a 2.6-km altitude gradient in the Peruvian Andes. We predicted that highland species would show adaptation to the colder high-altitude climate, and that energy costs of thermoregulation might limit up-slope dispersal of lowland natives.

We found reductions in thermal conductance (amount of heat loss) and body temperature, and lower critical temperature (lowest temperature where metabolism increases) in highland birds compared to lowland species, all of which make birds of high elevations more resistant to heat loss. We did not, however, find convincing evidence that acute thermal limits or energy costs of thermoregulation constrained altitudinal distributions. However, to evaluate the amount of energy that low elevation birds would spend at high elevation, we built heat budget models that predicted low-to-moderate long-term costs at native altitudes. Costs increased for lowland natives modeled in the highland climate, but for all but a few species, these higher costs remained within putative expenditure limits as defined in the literature.

Although we did not test heat tolerances, we measured all species at temperatures similar to the hottest air temperatures at the lowland site. The lack of difference in basal metabolic rate at 30-34ºCdoes not suggest that high lowland temperatures preclude down-slope movements of highland birds. While thermal tolerances probably do not directly determine altitude occupancy by most species, there may be a tradeoff between the higher costs of thermoregulation experienced by lowland species moving up-slope and investment in important life history components such as breeding.

Image caption: Andean cock-of-the-rock. Image provided by authors.
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The plant you choose to make your home isn't always the one that protects you best

Jared G. Ali & Anurag A. Agrawal Image provided by authors.

A herbivore’s ability to feed, avoid predation, and succeed on specific host plants are some of the most important factors in its life. What we find, though, is that not all herbivores are able to perform equally well on every plant they encounter. Therefore, we assume most herbivores have specialized on plants that allow them to achieve optimal measures of performance. An important question that remains in ecology is whether herbivores select hosts more because of interactions with their host alone (nutrition, plant defenses, growth, etc.) or if predators and parasites play a major role in the selection of a plant host. A very interesting phenomenon occurs in many herbivores that specialize on particular hosts; they often gain the ability not only to cope with plant defenses (toxins produced to ward off herbivores), but to also steal them and keep them in their bodies to protect themselves from their own enemies. In this experiment we tested two specialized insect herbivores’ ability to perform on alternative plant hosts. We evaluated their performance while measuring toxins that these specialist herbivores steal from plants that might protect them from parasitic worms. We find specialization is driven primarily by plant-herbivore interactions, rather than by threat of predation/ parasitization, and that not all measures of performance are highest on the herbivores’ preferred host plants. This tells us that measures of performance are complex and that ecological interactions between a plant and host are not always those that result in optimal performance on every trait.


Image caption: Image provided by authors.
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Movement correlates of lizards' dorsal pigmentation patterns

Topaz Halperin, Liran Carmel and Dror HawlenaPhoto provided by authors.

The reasons why some animals have cryptic body patterns, such as spots, reticulations and blotches, while others have conspicuous stripes, has long intrigued scientists. We provide a simple explanation for this quandary that is based on the balance between the animal’s need to eat and the need to avoid being eaten. Species that remain still during much of their activity time, such as animals that hunt from ambush, may benefit from cryptic body patterns that help them blend in to the environment. However, cryptic patterns are less beneficial for species that actively search for food. This is because visual predators can easily detect a moving prey regardless of their coloration. Conversely, these highly detectable active species may benefit from conspicuous stripes that improve their chances to survive predator attacks. Stripes can dazzle the predator’s motion perception and hamper its ability to intercept escaping prey. Thus, we suggest that species that forage less actively should have cryptic patterns while species that actively search for food should have stripes. We tested this hypothesis by studying the association between lizard foraging behaviors and their pigmentation patterns. Using an extensive literature survey, we found that lizards with stripes were indeed substantially more active than lizards with cryptic patterns. Our findings provide the first quantitative support for the hypothesized relationships between pigmentation-patterns and foraging behavior. These findings might be relevant to other animals besides lizards. We hope that future studies will test our movement-patterns hypothesis, ultimately applying meticulous manipulations to tease apart and test its mechanistic details.

Image caption: Photo provided by authors.
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Testosterone and the cloacal microbiome in a free-living bird

Camilo Escallón, Matthew H. Becker, Jenifer B. Walke, Roderick V. Jensen, Guy Cormier, Lisa K. Belden, Ignacio T. Moore Image provided by authors.

Testosterone is a hormone that primarily functions to regulate reproduction in male vertebrates. It mediates processes such as sperm production, development of sexually-selected traits, and reproductive behaviors. There are many benefits for males maintaining high testosterone levels. However, it has been argued that maintaining high testosterone levels for prolonged periods also has costs, and could ultimately have negative consequences for long-term survival. One of the proposed pathways by which testosterone can affect survival is by increasing the risk of infection, including pathogenic bacteria.

We investigated testosterone and cloacal bacteria in free-living rufous-collared sparrows in the Ecuadorian Andes. Males of this species have high levels of testosterone during the breeding season, when they form socially monogamous unions with females. However, extra-pair paternity is common. We measured circulating testosterone concentrations, and assessed the diversity and types of bacteria living in their cloaca, which in birds functions as the opening from the gastrointestinal tract and is also the copulatory organ. Thus, it harbors bacteria that can be sexually transmitted.

We found that birds with higher levels of testosterone also had higher cloacal bacterial diversity, and had higher relative abundance of Chlamydiae, a group of bacteria that can be pathogenic. In addition, the cloacal microbes of low-testosterone birds were different from the rest of the males, seemingly because they were missing some bacteria that the other birds possessed. Two nonexclusive explanations for these results are that testosterone affects behaviors that lead to increased sexual contacts, and thus increased exposure to bacteria, or that testosterone is altering the bird’s immune system, thus making it easier for bacteria to colonize. Either way, these results suggests that increased exposure to sexually-transmitted pathogens in the form of cloacal bacteria could be a cost of maintaining high testosterone levels.

Image caption: Image provided by authors.
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Host phenology and potential saprotrophism of ectomycorrhizal fungi in the boreal forest

Stefan F. Hupperts, Justine Karst, Karin Pritsch, Simon LandhäusserMature aspen trees during late summer, when leaves are fully expanded and photosynthesizing at full capacity. Carbon allocation to ectomycorrhizal fungi is likely high during this phenological stage. Photo credit: Erin Wiley.

Ectomycorrhizal plants allocate some of their photosynthetically derived carbon to ectomycorrhizal fungi - organisms that colonize roots and provide mineral nutrients to their plant hosts in return for carbon compounds. With the onset of spring, trees will develop leaves for photosynthesis and then drop their leaves in autumn when temperatures decrease and daylight shortens. These seasonal changes in photosynthetic capacity induce fluctuations of carbon stored in tree roots, and may therefore influence the amount of carbon provided to ectomycorrhizal fungi.

Though traditionally considered dependent on living trees for carbon, recent work suggests that ectomycorrhizal fungi may be able to mobilize carbon from soil organic matter and plant litter (i.e. become saprotrophic). Two competing models exist to explain carbon mobilization by ectomycorrhizal fungi. Under the ‘saprotrophy model’, decreased allocation of carbon may induce saprotrophic behavior in ectomycorrhizal fungi, resulting in the decomposition of organic matter to provide the fungus with carbon if the supply from the host plant is inadequate. Alternatively, under the ‘nutrient acquisition model’, decomposition by ectomycorrhizal fungi may instead be driven by the acquisition of nutrients, such as nitrogen and phosphorus, locked within soil organic matter compounds, with carbon mobilization a secondary process.

We tested whether phenology-induced shifts in carbon reserves of fine roots of aspen affect potential activity of carbon-compound degrading extracellular enzymes by ectomycorrhizal fungi. Ectomycorrhizal roots from mature aspen were collected across eight sites in northeastern Alberta, Canada and analyzed during four distinct phenological stages: winter, spring, summer, and autumn. We predicted potential activity of carbon-compound degrading enzymes would be highest when root carbon reserves were lowest, should host phenology induce saprotrophism.

We found activity of EMF-derived carbon-compound degrading enzymes to be relatively constant across phenological stages. Furthermore, low-biomass ectomycorrhizal fungi appear to have a greater ability to degrade complex carbon compounds when compared to high-biomass ectomycorrhizal fungi. These findings support the nutrient acquisition model, and suggest that the degradation of soil organic matter and plant litter by ectomycorrhizal fungi is driven by nutrient foraging rather than saprotrophy.

Image caption: Mature aspen trees during late summer, when leaves are fully expanded and photosynthesizing at full capacity. Carbon allocation to ectomycorrhizal fungi is likely high during this phenological stage. Photo credit: Erin Wiley.
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New ranking algorithm can identify overall pattern from incomplete surveys, providing critical insight into complex problems

Timothy D. Swain, John Chandler, Vadim Backman, Luisa MarcelinoPhoto by Luisa A. Marcelino.

As the third global coral bleaching episode is currently ongoing and expected to kill thousands of square kilometers of coral reefs, our ability to understand why some corals are killed while others survive is hampered by our capacity to consolidate previous knowledge. Corals are a combination of simple animals and algae that work in highly efficient unison to collect sunlight to make food. This association is sensitive to changes in temperature; when stressed by heat, the combination unravels in the bleaching response, leaving corals weakened and starving. Rising ocean temperatures caused by global climate change have made bleaching more frequent and severe, and understanding the mechanisms underlying the bleaching response is an urgent ecological problem. It is known that the algae associated with coral are highly diverse, and that some types are better at helping corals resist thermal stress than others. This insight originates from many experiments and surveys that, for reasons necessitated by the biology of the organisms themselves, can only provide detailed information on small subsets of the algae types; meaning that we know a lot about the relative performance of short lists of algae types, but almost nothing about the relative performance of all types. It turns out that this problem, of having lots of information about the ranking of small partial lists and little information about the ranking of an entire population, is common in many fields including search engines, election schemes, ‘best of’ rankings, and theoretical and applied sciences and engineering. To overcome this problem we devised a new ranking algorithm that can accept these partial lists and return a consensus ranking of all the elements in the lists even when there are disagreements among lists. We also validated the performance and accuracy of the algorithm with known rankings; the algorithm is very robust at uncovering new comparisons absent from the initial lists and has a low misranking error. This novel tool has broad application potential to a variety of ranking problems and will provide critical insight into coral bleaching mechanisms.

Image caption: Photo by Luisa A. Marcelino.
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Fire impacts on soil organisms

Jennifer L. Soong, Marie Dam, Diana H. Wall, M. Francesca CotrufoImage provided by authors.

Fires occur in nearly all terrestrial ecosystems. The occurrence rate and severity of fires depends on many factors. One important impact of fires is the combustion of aboveground plant material. This plant material would typically die and be considered “litter” to be decomposed by soil microbes and other organisms, such as nematodes, who help to recycle the nutrients held in the litter for subsequent plant production. When plant litter is combusted during a fire, much of its biomass is volatilized and lost from the ecosystem but a small fraction remains as partially burned residues, or the black charred material remaining on the soil surface after a fire. Here we used pyrolized organic matter as a substance resembling the charred material left behind by fires.

We examined how soil microbes, nematodes and plant roots use organic matter from decomposing litter and pyrolized organic matter in order to understand how the alteration of decomposition inputs to the soil by burning affects soil biological processes. We found that while litter provides a carbon and nitrogen food source to soil microbes, nematodes and growing roots, pyrogenic organic matter remains in the soil mostly unused. We also saw that this litter food source shifts the structure of the belowground food web. These results help to explain the impact of fire on belowground biological processes. For example, if aboveground biomass is removed during fires there is less material remaining to fuel belowground organisms, and the partially combusted material remaining is not easily decomposed and recycled.

Image caption: Image provided by authors.
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Searching for prey in a three-dimensional environment: hierarchical movements enhance foraging success in northern elephant seals

Taiki Adachi, Daniel P. Costa, Patrick W. Robinson, Sarah H. Peterson, Masato Yamamichi, Yasuhiko Naito and Akinori TakahashiFemale northern elephant seals during moulting season at Año Nuevo State Reserve, CA, USA. Photo taken by T. Adachi in the morning on May 23, 2011.

In nature, prey is often patchily distributed. Therefore, to enhance foraging success, predators are expected to concentrate search paths in areas where prey is more abundant. This style of searching is generally called “area-restricted search (ARS)”, which is characterized by sinuous search paths of predators with increased turning frequency. ARS has been suggested as an optimal search strategy in a patchy environment for both terrestrial and marine predators. However, due to the technological challenge of coupling search paths of animals with records of feeding events (prey captures), it remains unclear if ARS actually enhances foraging success in free-ranging animals, especially in marine animals that forage in a three-dimensional (3D) underwater environment.

Here, we reconstructed fine-scale 3D dive paths of a deep-diving (occasionally over 1000 m) marine predator, the northern elephant seal, coupled with recording feeding events using accelerometers attached on their jaws. Then, we quantified the 3D foraging behavior to test if seals enhance foraging success by employing “volume-restricted search” (VRS, termed for ARS in three-dimensions) while exploring a 3D environment.

Our results showed that most feeding events occurred when seals employed VRS. Also, we found that there was a hierarchical structure to the VRS; most small-VRS (95%) were nested within large-VRS (nested VRS). Importantly, nested VRS had significantly higher feeding rates than non-nested VRS, because nested VRS contained small- and large-VRS with higher and lower feeding rates, respectively. These results provided the first empirical evidence that underwater sinuous search paths (VRS) are strongly linked to higher foraging success, especially when the search paths are hierarchically structured, suggesting that seals forage on prey in a hierarchical patch system where high-density patches at small scales are nested within low-density patches at larger scales.

For all animals that search for prey, it is a central question how to adjust search paths according to the spatial distribution of prey to enhance foraging success. Our results suggest that northern elephant seals enhance foraging success by employing hierarchical decision making to concentrate search paths in areas where prey appeared to be hierarchically structured in patches over a range of 3D spatial scales.

Image caption: Female northern elephant seals during moulting season at Año Nuevo State Reserve, CA, USA. Photo taken by T. Adachi in the morning on May 23, 2011.
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Litter microbial and soil faunal communities stimulated in the wake of a volcanic eruption in a semiarid woodland

Paula Berenstecher, Daniela Gangi, Adelia González-Arzac, M. Laura Martínez, Eliseo J. Chaves, Eduardo A. Mondino and Amy T. AustinMeliquina Valley, Argentina, several months after the massive eruption of the Puyehue volcano in December, 2011.  This site is approximately 70 km from the epicenter of the eruption.  The area is a mixture of natural woodland vegetation and exotic ponderosa pine (Pinus ponderosa) plantations.  Inset shows depth of ash deposition in the woodland ecosystem. Photo courtesy of P. Berenstecher.

Large-scale natural disturbances, such as hurricanes, fires, frosts and volcanic eruptions, are important factors that affect natural ecosystems, but generalities regarding their effects are difficult due to their infrequent and unpredictable nature. Volcanic eruptions figure as one of the most prominent of these natural disturbances, but the effects on microbes and soil fauna (ground-dwelling arthropods, such as ants, beetles or mites, and nematodes, microscopic round-worms) are relatively unknown. These organisms are important because they are key players in the formation of soil organic matter and turnover of nutrients which then become available for plants. We evaluated ecosystem changes induced by the dramatic Puyehue-Cordón Caulle eruption of June 2011 in Patagonia, Argentina. We were interested in how these microbes and soil animals responded to heavy ash deposition in both natural woodland vegetation and a pine plantation in the Meliquina Valley, located 70 km west of the epicenter of the eruption. As ash can be quite abrasive and is, in fact, used as an insecticide, we hypothesized that volcanic ash deposition would have marked negative effects on the soil biota and consequently on decomposition. We were extremely fortunate to have made pre-eruption measurements in the same sites in the year prior to the volcanic eruption, which provided a rare opportunity to make a real comparison before and after the ash deposition.

We measured environmental variables of soil and litter (moisture, pH, organic matter) and biotic variables (abundance of ground-dwelling arthropods, nematodes, microbial biomass and microbial activity in soil and litter) in both natural woodland and pine plantation sites. We were surprised to find that ground-dwelling arthropods actually dramatically increased in abundance after the eruption, while soil nematodes were negatively impacted. More surprising, however, was that evaluating the effects of ash on litter decomposition showed more than doubled rates of carbon turnover in litter from the native woodland. It seems that the effect of the ash deposition may be related to your habitat, with those who reside in the soil being negatively affected while the litter dwelling microbes and fauna were actually favoured by the conditions of the eruption. This study provides insight into the effects of large disturbances on the underappreciated soil biota, and highlights that these disturbances do not always result in the catastrophic effects that we might imagine.

Image caption: Meliquina Valley, Argentina, several months after the massive eruption of the Puyehue volcano in December, 2011. This site is approximately 70 km from the epicenter of the eruption. The area is a mixture of natural woodland vegetation and exotic ponderosa pine (Pinus ponderosa) plantations. Inset shows depth of ash deposition in the woodland ecosystem. Photo courtesy of P. Berenstecher.
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Author-suggested reviewers: Gender differences and influences on the peer review process at an ecology journal

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

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

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

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

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

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

Image caption: Image from “What is a journal and a peer reviewed article?” (Northeastern Illinois University Ronald Williams Library).
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Experimentally manipulating the harmful products of respiration

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

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

Image caption: The house finch (Haemorhous mexicanus) is one of the several species in which paraquat has been used as a physiological ROS generator within the field of oxidative stress ecology. Photo credit to co-author Geoff Hill.
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Joint effects of climate change and parasite infection on host in the wild

Matthieu Bruneaux, Marko Visse, Riho Gross, Lilian Pukk, Lauri Saks, Anti VasemägiEcologist at work. Photograph provided by authors.

Climate change can affect ecosystems in several ways, through direct temperature effects on organisms (e.g. limiting metabolic capacity at high temperatures) or through indirect effects, such as an increased parasite burden or the introduction of new parasites. These negative effects can interact with potentially dramatic consequences, when high temperatures disrupt the immune function of the host and make it unable to resist a parasite infection, or when the parasite infection compromises the ability of the host to cope with elevated temperatures.

The physiological effects of parasites have been traditionally evaluated under controlled laboratory conditions. However, much less is known about the effect of emerging parasitic diseases on host performance in nature. We studied wild-caught juveniles of brown trout (Salmo trutta) and measured several physiological and performance traits to evaluate the effect of proliferative kidney disease (PKD), which is caused by the myxozoan parasite Tetracapsuloides bryosalmonae This parasite can result in high mortalities in salmonid species, both in farms and in natural ecosystems, and its range has extended in recent years. To understand how parasite load, metabolic rate and thermal resistance are related to each other in the fish host, we brought our physiological laboratory into the field to measure oxygen consumption and thermal tolerance of wild brown trout.

We found that fish exhibited varying degrees of disease severity, with a wide range of parasite load, kidney swelling and associated anemia. Importantly, the aerobic scope, which is the maximum amount of usable energy a fish can produce using its aerobic metabolism, was negatively correlated with the severity of PKD. In addition, the thermal tolerance of the fish was also negatively correlated with disease symptoms. Our results demonstrate how a wild fish population can be at risk under the double threat of increased water temperature and expanding parasite range, and of their interaction. Understanding if and how local populations can adapt to these selective pressures will be critical to assess the long term evolution of this type of ecosystem.

Image caption: Ecologist at work. Photograph provided by authors.
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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.
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