Lay Summaries

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

 

Lay summaries for the current issue

 

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

 

Stress hormones regulate how the past can affect the future in wild banded mongooses.

Jennifer L. Sanderson, Andrew J. Young, Sarah J. Hodge, Solomon Kyabulima, Susan L. Walker & Michael A. Cant A banded mongoose (Mungos mungo) pup on the Mweya Peninsular, Western Uganda. Photo credit: Jennifer Sanderson.

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Virtually every decision that you make will affect your later life. For example, a decision to work hard can leave you tired and less likely to work hard the following day. In ecology this is called a ‘carry-over effect’. Such carry-over effects are widespread in animal populations and may explain why individuals with high parental investment in one breeding attempt often invest relatively little in a second breeding attempt.

Evidence suggests that carry-over effects arise when the energetic losses from previous parental investment persist into the next breeding attempt. However, little is known about the physiological mechanisms that regulate these effects. Here, we test the hypothesis that carry-over effects arise because working hard to raise offspring causes increased concentrations of stress hormones (glucocorticoids; GCs), which inhibit future parental investment. Our field study of wild banded mongooses provided strong support for this hypothesis, and suggests that factors known to influence an individual’s stress physiology can have lifelong impacts on reproductive behaviour and fitness.

The banded mongoose is a close relative of the meerkat and is found living in stable social groups across Central and Eastern Africa. Banded mongooses breed cooperatively; all individuals assist in offspring care even if they do not breed themselves. We collected faecal samples and behavioural observations from banded mongooses living on the Mweya Peninsular in Western Uganda to investigate if GCs mediate a carry-over effect whereby individuals that invest heavily in cooperative offspring care in one breeding attempt invest little in the next.

Banded mongooses that entered a breeding attempt with low GCs fed pups more often than individuals with high GCs, suggesting that elevated GCs inhibit offspring care. High investment in offspring care led to an increase in GCs during the breeding attempt, and this elevation persisted after the care period. Furthermore, supplementary feeding of carers led to a decrease in GCs, confirming that this GC increase is due to energetic losses. Our results provide new insight into the physiological regulatory mechanism behind carry-over effects and a better understanding of how stress associated with the past can affect behaviours in the present.

Image caption: A banded mongoose (Mungos mungo) pup on the Mweya Peninsular, Western Uganda. Photo credit: Jennifer Sanderson.
This article can be found here.

 

Nutritional geometry of the giant panda.

Yonggang Nie, Zejun Zhang, David Raubenheimer, James J. Elser, Wei Wei and Fuwen WeiPhotograph caption: Giant panda feeding on wood bamboo shoot. Photo credited to Fuwen Wei.

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Many studies have shown that herbivores face nutritional challenges, including plant-produced toxins and nutritionally imbalanced foods. These challenges, which can have significant influences on critical aspects of animals’ life cycles including longevity and reproduction, may become more acute under ongoing climate change. This is especially true for species that live in seasonal environments. In response to such challenges, animals have evolved behavioral, developmental, and physiological adaptations to meet their demands for various nutrients and maintain performance.

The giant panda (Ailuropoda melanoleuca) is a unique species in the order Carnivora that evolved to specialize on various species of bamboo, which are generally thought to be of poor nutritional quality due to low protein and high fiber and lignin contents. The giant panda may thus face particularly acute nutritional challenges. Previous studies have highlighted many ecological and life history characteristics that might be associated with the ability of panda populations to survive as bamboo specialists. For example, pandas have a seasonal reproductive pattern with mating in spring and birth in fall which is believed to be an ecological adaptation to different seasonal nutritional environments.

We combined behavioral observations of food selection with analysis of the calcium, phosphorus, and nitrogen (as a proxy for protein) composition of foods and matched feces, to determine how the panda's distinctive seasonal habitat choice and food selection relate to its nutritional balance. Our results showed that pandas displayed marked foraging changes, with four primary foraging periods corresponding to the annual life cycles of the two bamboo species that make up most of its diet. These foraging changes are also coupled to its seasonal migration between low and high elevations. Analysis suggests that the pattern of migration coupled with seasonal diet switches were necessary to obtain a diet balanced in calcium, phosphorus and protein, and likely play an important role in the life cycle and reproduction of giant pandas. These results have potentially important implications for habitat conservation for giant pandas, suggesting that the summer and winter habitats of giant pandas are not nutritionally interchangeable, but provide complementary nutrition required to complete the life cycle.

Image caption: Photograph caption: Giant panda feeding on wood bamboo shoot. Photo credited to Fuwen Wei.
You can find the article here.

 

Ageing gracefully: physiology but not behaviour changes with age in a diving bird.

Kyle H. Elliott, James F. Hare, Maryline Le Vaillant, Anthony J. Gaston, Yan Ropert-Coudert and W. Gary AndersonMurres in flight. Photo provided by authors.

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How can long-lived wild birds both work hard and live long? We examined this question by studying murres (also known as guillemots) aged 3-30 years. Murres have the highest flight costs, for their body size, of any flying animal. They dive exceptionally deep for their body size (over 150 m for five minutes). Yet they also have exceptionally long lives for their body size; they live decades longer than rabbits, which weigh roughly the same. To examine how metabolism changes with age in wild murres, and how that affects dive performance, we measured oxygen consumption, oxygen stores and dive behaviour. Both oxygen stores and oxygen consumption rate declined with age, which we suggest reduces the effect of high metabolism on ageing. In contrast, there was no change in dive performance with age; old murres dove as deep, for as long and spent as much time recovering at the surface as young murres. Thus, multiple physiological systems changed in tandem with advancing age in murres, and offset each other such that there was no detectable decline in behavioural performance. Murres were able to maintain their ‘healthspan’ into old age.

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

 

Pesticide chronically affects bee foraging.

Richard J. Gill & Nigel E. RaineBumblebee foraging on clover. Photo and permission provided by Steve Gill.

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Bees provide an essential environmental service by pollinating many wild flowers and key agricultural crops. The importance of these critical pollinators, both economically and for continued food security, make it particularly concerning that bees are suffering global declines. Pesticide exposure has been suggested as one of many possible factors driving bee declines. Although the levels of pesticide to which bees are exposed in the field are typically not lethal to bees, they may still produce sublethal effects, such as changes in behaviour leading to problems with colony function.

In this study we investigated how two commonly used pesticides affect the foraging behaviour of individual workers of bumblebees at approximately field relevant exposure levels. We examined the responses of bees and their colonies following short-term (acute) exposure, and (chronic) exposure over an extended period of time. Bumblebees are social insects, meaning the colony consists of a queen that lays almost all the eggs, accompanied by numerous workers that help to rear the brood, protect the colony and importantly go out to forage by collecting pollen and nectar from flowers. Therefore, understanding whether pesticides impair foraging behaviour is important because this can have detrimental consequences for colony growth and reproductive success. We attached Radio Frequency Identification Tags to automatically record all foraging trips made by each bee. Using this technology we recorded the natural activity patterns of 259 foraging workers from 40 bumblebee colonies over four weeks.

This is the first study to provide data on the impacts of pesticide exposure on the day-to-day dynamics of bee foraging behaviour in the field over a prolonged period of time. Our results showed that a neonicotinoid pesticide (imidacloprid) had both acute and chronic effects on overall foraging activity. Colonies exposed to the neonicotinoid recruited foragers at a higher rate over the four week period than control colonies, an effect that appeared to be a response to impaired individual foraging efficiency. While individual foragers from control colonies improved their pollen foraging performance as they gained experience, the pollen foraging performance of bees exposed to the neonicotinoid became worse. At the colony level, we observed that the proportion of neonicotinoid exposed foragers that successfully collected pollen decreased as the experiment progressed. There was also evidence to suggest forager preferences for particular flower types were affected by neonicotinoid exposure. Our findings highlight the importance of considering prolonged exposure when assessing the risk that pesticides pose to bees.

Image caption: Bumblebee foraging on clover. Photo and permission provided by Steve Gill.
This paper can be found free online here.

 

Maternal effects influence phenotypes and survival during early life stages in an aquatic turtle.

Timothy S. Mitchell, Jessica A. Maciel and Fredric J. JanzenA hatchling painted turtle emerges from the nest after winter.

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Many egg-laying animals do not care for their young, but this does not mean that good mothering is not important for offspring. For such animals, there are two maternal effects that are particularly important: nest-site choice and egg size.

We explored the importance of such maternal effects in the painted turtle (Chrysemys picta). By selecting particular microhabitats at the time of nesting, the mother turtle can partially influence the abiotic conditions her eggs will experience during incubation and the hatchlings will experience as they overwinter within the natal nest. This abiotic environment is very important for two reasons: it can shape phenotypes of developing offspring via phenotypic plasticity, and it can act as a selective force. In this field experiment, we compared offspring incubating and hibernating in maternally-selected nests to those in randomly-selected nests. Our results show that mothers selected nests that were relatively open (unshaded), and this resulted in maternal nests being significantly warmer than random nests during incubation. Hatchlings from these maternal nests were longer and developed faster than their counterparts in random nests. However, the ability to modify thermal environments of the nest faded during the overwinter stage. There was a weak correlation between vegetation cover and nest temperature, and maternal and random nests experienced similar thermal environments.

We also tracked individual eggs and hatchlings, and showed that larger eggs produce larger hatchlings. These larger hatchlings had a higher probability of surviving winter, where experiencing lethally cold temperatures was a substantial source of mortality. This novel result provides further support for the “bigger-is-better” hypothesis in early life stages of freshwater turtles.

In the turtle world, three clichés ring true: mother knows best, size matters and location is everything (or at least, it is very important).

Image caption: A hatchling painted turtle emerges from the nest after winter.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Do eggshells act like sunscreen?

Golo Maurer, Ivan Mikšík, Steven J Portugal, Mark E Hauber, Douglas Russell, Phillip CasseySong thrush eggs. Photo provided by authors..

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The eggs of birds have an amazing array of adaptations to ensure the safety of the embryo developing inside. Such adaptations can include camouflage of the shell to help protect against predation, special pores that allow the correct amount of air into the egg and infection-fighting pigments to help the embryo fight disease. One important aspect the shell of the egg must control is the amount of light that penetrates through to reach the embryo. Too much light penetrating the eggshell will result in lethal levels of radiation from the UV light, but too little light can cause embryo deformities and increase the likelihood of disease. Therefore, the eggshell has to ensure that just the right amount of light is allowed through the shell. Birds nest in a wide range of environments and habitats, including extreme temperatures, altitudes, in burrows, on cliffs; how does the egg of each species in differing environments make sure the right amount of light reaches the embryo? We examined how the eggshells of British breeding birds have adapted to different environments, and how different shells control the amount of light that reaches the embryo. We found that the eggs of species that nest in burrows, holes and other closed environments let more total light pass through the eggshell, compared with species that nest in the open. Specifically, we show that less light passes through thicker eggshells with greater total pigment concentrations. The pigment potentially acts like sun-block. It seems, therefore, that greater light transmission through the shell is required to assist embryonic development under low-light exposure. To make sure enough light gets through to the embryo in these dimly-lit conditions, eggs of birds that nest in burrows and holes are white, allowing more light in as there is less pigment to block the sun. For birds who have a long incubation period (exposing their eggs to the sun for longer), their eggs are often dark with pigment, letting significantly less of the potentially harmful, ultraviolet (UV) light pass through the eggshell.

Image caption: Song thrush eggs. Photo provided by authors..
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Daily energy expenditure during lactation is strongly selected in a free-living mammal.

Quinn E. Fletcher, John R. Speakman, Stan Boutin, Jeffrey E. Lane, Andrew G. McAdam, Jamieson C. Gorrell, David W. Coltman and Murray M. Humphries Female red squirrel with one of her pups outside of her grass nest. (Photo credit: Ryan W. Taylor).

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Energy is a currency of life because all animals must expend it to survive and reproduce. Despite the importance of energy as a currency, we know very little about the benefits and costs associated with the amount of energy that animals expend. Past research on mammals has demonstrated that lactation is an energetically costly time of the year because females must expend energy to forage for food, and synthesize milk to raise multiple offspring. We found that the female North American red squirrels that expended the most energy during lactation had the most offspring survive to the following year (i.e. they have greater reproductive fitness). At first glance, it makes intuitive sense that there would be reproductive fitness benefits associated with expending large amounts of energy during lactation. However, our results are interesting because they raise a series of mysteries. The first set of mysteries relates to the mechanism by which elevated energy expenditure during lactation is associated with greater reproductive fitness. The most obvious mechanism is that females that raise larger litter sizes or healthier offspring (i.e. faster growing) have more offspring survive to the following year, but also need to expend more energy to do so. However, this mechanism appears not to be true because there is no relationship between a female’s energy expenditure during lactation and either its litter size or the growth rate of its offspring. Moreover, in order for juveniles to survive until the following year, they must first obtain a territory, then hoard enough cones to survive the winter, and then evade a suite predators. Our results are definitely a mystery because they suggest that if pups are raised by females that expend elevated levels of energy, that this somehow helps them to survive these ecological challenges. The second mystery relates to our finding that females that expended the most energy during lactation experienced no negative consequences. Specifically, we found that females with high levels of energy expenditure during lactation had neither reduced survival to the following year, nor a decreased ability to invest in reproduction the following year. These results are interesting because if there are benefits associated with expending energy during lactation, but no costs, why do not all females expend energy at a high rate?

Image caption: Female red squirrel with one of her pups outside of her grass nest. (Photo credit: Ryan W. Taylor).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Subdigital adhesive pad morphology varies in relation to structural habitat use in the Namib Day Gecko.

Clint E. Collins, Anthony P. Russell, and Timothy E. Higham Rhoptropus afer pauses before ascending a granite outcrop.

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Locomotion is a quintessential aspect of animal life. Effective locomotor performance is crucial for many important tasks such as prey capture, mating, and predator evasion. Gecko locomotion is fascinating because of the specialized adhesive capability that allows them to live on vertical and inverted surfaces. Adhesion is finely controlled by the subdigital toe pad and the millions of microscopic, hair-like structures known as setae that are located on the bottom of each toe pad. However, this specialized behaviour and the adhesive system comes at a cost – running away from predators on level surfaces may be affected owing to the complexity and timing of adhering and detaching to surfaces during locomotion. Quantifying the interplay between escape behaviour and locomotor morphology across habitats that vary in structural composition could reveal how selection acts on locomotion at local levels.

Our study found that in habitats where escape behaviour relies on flatter surfaces, a species of gecko, Rhoptropus afer, the Namib Day Gecko, has exhibited a greatly reduced adhesive morphological system. We investigated the impact of habitat variation and escape behaviour on morphology, including the adhesive system, of Rhoptropus afer, a diurnal and cursorial (adapted to running) gecko from Namibia. Substrate incline and topographical variation are likely important for this pad-bearing gecko due to the trade-off between adhering and sprinting (i.e. using adhesion results in decreased sprint speed) that is triggered by certain inclines. We corroborate the hypothesis that the adhesive system exhibits the greatest degree of reduction in populations that utilize the flattest terrain during an escape. Our findings suggest that the adhesive apparatus is detrimental to rapid locomotion on relatively horizontal surfaces, and may thus be counterproductive to the evasion of predators in such situations.

Image caption: Rhoptropus afer pauses before ascending a granite outcrop.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

How to best assess the cold tolerance of Drosophila.

Jonas Lembcke Andersen, Tommaso Manenti, Jesper Givskov Sørensen, Heath Andrew MacMillan, Volker Loeschcke and Johannes OvergaardImage supplied by authors.

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Insects represent around three quarters of the world’s named species and they often play an important role in human society as pollinators, agricultural pests or carriers of disease. Insects’ distribution across the globe is partially limited by their ability to survive cold. In order to predict changes in the patterns of insect distribution across the world we need to understand how cold affects insects and how some insects survive for hours below 0°C while others die after only short exposures to low temperatures.

Many of the studies done on insect cold tolerance (temperatures that limits insects’ ability to survive, reproduce, or migrate) have been performed with fruit flies (Drosophila) utilizing several different methods to assess cold tolerance. In this study we evaluated the accuracy of cold tolerance estimates obtained using five commonly used methods. We assessed the cold tolerance of 14 Drosophila species using each of the 5 methods. An average natural latitudinal distribution and an expected minimum temperature exposure was determined for each of the species using databases with thousands of observations. These parameters were then correlated to each of the five cold tolerance measurements to investigate which method was best correlated to the actual distribution and minimum temperature exposures of the 14 species in the wild.

We found that the temperature where the flies lost their ability to move (chill coma onset), when ramping down the temperature, had a strong correlation to the environmental variables. So did measurements of survival after 2 hours of low temperature exposure (lethal temperature) as well as survival time at milder low temperatures (lethal time). However, the time it took the flies to recover from cold shock (chill coma recovery time) had a weaker correlation to the environmental variables and supercooling point, the temperature where the flies freezes over, had the weakest correlation to distribution and estimated temperature exposure.

Considering the amount of time involved and the difficulty of making the different measurements, we found that chill coma onset and lethal temperature are superior measurements when estimating cold tolerance in Drosophila.

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

 

Afforestation effects on understory shrubs in a semiarid Mediterranean ecosystem.

Cristina Moreno-Gutiérrez, Giovanna Battipaglia, Paolo Cherubini, Antonio Delgado Huertas and José Ignacio QuerejetaRhamnus lycioides radial growth rings. Photo courtesy of authors.

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Pinus halepensis (Aleppo pine) plantations cover extensive areas of the western Mediterranean Region, and are often characterized by a monospecific tree overstory with a sparse, depauperate and species-poor shrub understory. Rhamnus lycioides is one of the few woody shrub species capable of colonizing P. halepensis plantations in the drier parts of the region. Its presence in the understory enhances the structural complexity, functional diversity and resilience against disturbance of semiarid pine plantations. Understanding the processes that allow tree-shrub coexistence in these severely water limited environments is crucial to the design and adoption of forest management practices aimed at fostering colonization by late-successional plant species, and at buffering the negative impacts of climate change on these man-made plant communities.

We assessed the long-term net effects of P. halepensis plantations on the performance of the understory R. lycioides shrubs, and evaluated how the sign and strength of the interaction are modulated by the high inter-annual climate variability of this semiarid ecosystem. We compared the growth-rings widths and growth-ring oxygen and carbon isotopic composition of understory R. lycioides shrubs growing in a dense plantation of P. halepensis with those of shrubs growing in a nearby open woodland with widely scattered trees. We found that shrubs in pine plantations showed lower radial growth and greater water stress than those in open woodlands. The strong competitive effects of P. halepensis on understory R. lycioides were most evident in wet, productive years, whereas in very dry years there were indications of a facilitative effect of planted P. halepensis canopies on understory shrubs. Within pine plantations, understory shrubs growing at shorter distances from planted trees were forced to rely on more superficial and ephemeral soil water sources, which increased their drought stress and also interfered with nutrient uptake. Competition by P. halepensis on R. lycioides clearly outweighed facilitation in the long-term, especially during wet years, thus compromising the ability of understory shrubs in semiarid pine plantations to cope with climate change. In conclusion, pine afforestation strongly reduces water and nutrient availability for understory shrubs in drylands, with potential long-term consequences for ecosystem biodiversity, structure and functioning.

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

 

Tree phenology responses to winter chilling, spring warming, at north and south range limits.

James S. Clark, Carl Salk, Jerry Melillo, and Jacqueline MohanPhoto of tree at different stages. Image provided by authors.

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A warming climate may lengthen growing seasons in the future, increasing production of forests and favoring those species that best exploit the longer season. However, plants from temperate climates often require a cold period (‘vernalization’) before spring budbreak can begin. There has been debate concerning when and how much warming will benefit different types of plants, depending on species differences and at different locations within the species range. Within species, northern populations have been expected to respond most due to the fact that growing seasons are relatively short. It has also been argued that species most sensitive to spring temperature may show little overall response to warming, because the accelerating effect of warm springs will be offset by the delaying effect of warm winters—the ‘chilling requirement’ needed before budbreak can start in spring. These questions remain because models of spring development have been unable to use information on the continuous response to temperature variation through time.

We provide a new model for budbreak that makes use of continuous responses to warming throughout the growing season. Applied to a large experimental warming study near northern and southern boundaries of 15 tree species in the eastern deciduous forest of the US, in North Carolina and Massachusetts, we show a detailed time course for the onset of growth in spring, including vernalization during winter. Where traditional models find little evidence of a chilling effect (most are insignificant or have the wrong sign), the continuous development model finds evidence of chilling effects in most species. Contrary to the current views, we find southern populations are most responsive to warming. A stronger response in the southern range could allow residents to resist northward migration of immigrants as climate warms.

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

 

Long-lived mothers reduce the negative effect of old age on their sons' lifespan in a seed beetle.

Elena C. Berg, Martin I. Lind, Ghazal Alavioon and Alexei A. Maklakov Seed beetle. Photo by Markus Rehnberg.

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The offspring of older parents often have a reduced lifespan when compared to offspring of younger parents, a phenomenon that is widespread in the animal kingdom, including humans. Although the reasons for this effect may vary between species, it can generally be seen as a manifestation of ageing.

However, parents can also differ in lifespan, and two parents that have lived for the same time may differ in biological age, since physical decline may be delayed in a genetically long-lived parent. Therefore, we asked whether the negative effect of old parental age on offspring lifespan would be smaller when a genetically long-lived parent produced the offspring.

We tested this hypothesis using the seed beetle Callosobruchus maculatus, a common pest of grain stores that can easily be maintained in the laboratory. In a previous experiment, we created long and short-lived lines by experimental selection for male lifespan, where a 40% difference in male lifespan, and also a correlated response in female lifespan, evolved between the lines. Now, we let mothers from these lines lay eggs at different ages, and measured the development time and lifespan of their offspring.

We found that the lifespan of the offspring decreased, and their development time increased, with increased maternal age. This effect was partly caused by what we interpret as decreased maternal provisioning to the egg with increased age. Moreover, the negative effect of old mothers differed between the long- and short-lived lines, but this difference was found only in the lifespan of sons. While sons were severely affected by later maternal age in the short-lived lines, the effect of maternal age was much smaller in the long-lived lines. Thus, the negative effect of old mothers on offspring lifespan was smaller if the mother had a long genetic lifespan.

The reason why sons were more affected than daughters is not known, but since males of this beetle are known to be more sensitive to environmental stress, it is possible that they suffer more than daughters from poor maternal provisioning.

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

 

Wood varies dramatically during tropical forest succession.

Benjamin T. Plourde, Vanessa Boukili and Robin ChazdonPlourde processing wood cores in second-growth forests at La Selva Biological Station, Costa Rica. Photograph by Robin Chazdon.

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A central question in ecology asks how diverse communities assemble. This is especially profound in tropical rain forests, where more than one hundred species of trees can be found within two acres. A common approach to understanding how plant communities assemble is the measurement of traits related to how individuals occupy their niche. In our study, we sought to understand how the density of wood (e.g. softwood vs. hardwood) varies among the trees in forests regenerating from pastures in Costa Rica.

We measured the wood density of coexisting species across eight forests of different ages. We recorded variation in wood density at every level: within trees, among individuals of the same species, among the species of a forest, across forests and between second- and old-growth forests. The wood density of many species in all forest ages increased over time. For example, a tree that begins life with relatively soft wood similar to pines can produce a much harder wood akin to oaks after just 30 years.

For some time, researchers have supposed that this shift is an adaptation of species in young forests and less prevalent in the climax species of old-growth forests. We show that both second-growth specialist trees and second-growth forests have more dramatic changes in density while having lower density wood overall than their old-growth counterparts. Our approach is unique in that species specializations were determined statistically based on where they are found.

A current goal of many organizations is to reforest abandoned lands and reclaim lost ecosystem services. Forests sequester carbon from the atmosphere in plant tissues. To quantify this service, scientists estimate the plant biomass in an area using models that incorporate individual tree sizes and almost always their wood densities. To date, these estimates ignore within-tree density variation. We show the degree to which this omission affects biomass estimation. Forest stands dominated by species with large changes in wood density may have their tree biomass underestimated by more than 3.5%.

While variation in wood density at the forest level is mediated by species composition, variation among and within species is likely due to a number of drivers and is a subject of active research.

Image caption: Plourde processing wood cores in second-growth forests at La Selva Biological Station, Costa Rica. Photograph by Robin Chazdon.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Long-lasting effects of fire management on the population structure of different savanna tree species.

Shaun Levick, Claire Baldeck and Greg Asner Fire on the savanna. Photo provided by authors.

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Understanding how different fire regimes modify vegetation structure is important for sustaining ecosystem processes and conserving biodiversity in savanna landscapes. We know that fires markedly alter vegetation structure, by preventing small shrubs from growing into tall trees, but we lack understanding of how individual tree species respond to different fire frequencies. To advance current knowledge, we used airborne technology (Carnegie Airborne Observatory, http://cao.stanford.edu) to map individual trees across entire savanna hillslopes in 2008. Our airborne mapping system consisted of a LiDAR sensor (laser ranging) to measure the height of the individual trees, and a hyperspectral sensor to record how the tree canopies reflected and absorbed sunlight. We used the data from these two sensors to classify the species of trees that we had mapped. Knowing both the height and the species of a large numbers of individual trees is very powerful for ecological investigation, as it enables analysis of population structure – by exploring the height class distribution of thousands of individuals of different species. We used our unique dataset to contrast the height class distribution of three dominant savanna tree species (Acacia nigrescens – knobthorn, Sclerocarya birrea – marula, Combretum apiculatum – red-bushwillow) in two adjacent landscapes with fire histories that differed from 1970-1990 but have been similar for the last 20 years. We repeated our airborne survey in 2012 to track the fate of individual trees over the four-year period. We found that a history of higher fire frequency strongly reduced the recruitment of marula trees in the 5-8 m height ranges, but promoted growth of red-bushwillow shrubs. We also found higher rates of treefall in the landscape with a history of higher fire frequency. Knobthorn trees showed the highest rates of loss with over 40% of individuals in the 6-9 m height classes toppled (most likely due to utilization by elephant). These patterns suggest interactive effects of fire history and elephant on tree population structure. Fire management actions taken many decades ago are still influencing vegetation structure and dynamics today. We need greater consideration of time lags and historical context in understanding and conserving ecological systems.

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

 

Massive armature trumps running for stag beetles.

Jana Goyens, Joris Dirckx and Peter AertsPicture of a Cyclommatus metallifer male.

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Stag beetles are renowned for their spectacular male-male battles. In these scuffles, males fight each other with their long jaws over mates or desirable stumps of rotten wood. The jaw morphology is shaped by sexual selection and in some species, they can become as long as their own body. Intuitively, one would expect that such large structures may hamper their running, although some other insects are known to carry heavy loads remarkable efficiently (e.g. leaf-cutter ants or horned beetles).

We made high speed video recordings of male and female stag beetles running on a miniature running track. By tracing the 3D path of their body, we derived the energy cost for both sexes. Running a certain distance turned out to be an impressive 40% more costly for the males than for the females (who have normal, small-sized mandibles). This is a considerable ecological cost of the heavy jaws and their outsized musculature.

An increased energy cost is not the only nuisance of the heavy heads of male stag beetles. While the males were running on the running track, we saw them tumble over and bump onto the ground with their heads regularly. We quantified this instability by tracking the centre of mass of the beetle bodies. As long as this stays above the triangular base that is formed by the legs that stand on the ground, the beetle is statically stable. However, we saw that males go through an unstable period twice every running cycle, while females almost always stay within the safe leg base. Although the male legs are 27% longer than those of females, they do not sprawl out their legs to enlarge their leg base. Instead, their only stability enhancing strategy appears to be the timely planting of the next leg tripod.

Male stag beetles are very specialised for their aggressive encounters. The resulting heavy heads do however compromise their running capacity: it is energetically costly and they continuously risk falling over, which probably implies a fitness cost when they search for mates or try to escape from predators.

Image caption: Picture of a Cyclommatus metallifer male.
This article is available in Early View here.

 

Temperature sensitivity of seed germination shapes species distribution patterns.

Sergey Rosbakh & Peter PoschlodPrimula minima is a typical alpine species, those seeds germinate under relatively high temperature.

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Temperature has been long recognized as a major factor driving plant distribution along latitudinal or altitudinal gradients. Using this correlation, a large number of vegetation-climate models have been developed to explain plant distribution patterns at different scales. Although these models have a high informative value, they rarely provide information on the mechanisms by which temperature shapes species’ distributions.

Numerous experimental studies have previously shown that temperature has a strong influence on plant recruitment, but aspects of seed ecology are still rarely considered as explanations for the distribution patterns of plant species. Using data on seed germination along a temperature gradient for 49 species originating from contrasting climatic conditions, we tested whether minimum temperature of seed germination (Tmin) is a direct correlate of species distribution ranges along a temperature gradient. The results of our study indicate that Tmin is strongly negatively correlated with habitat temperatures. Seeds of species from habitats with higher mean annual temperatures have low Tmin values, suggesting that their germination may begin shortly after snowmelt. With decreasing habitat temperatures, which occur along altitudinal or latitudinal gradients, frequency of late frosts as well as duration of periods with temperatures negative for seedling establishment increase. Therefore, in order to reduce this risk, germination is triggered by relatively high ambient temperatures (high Tmin values) in late spring or early summer, which indicate the onset of favourable conditions for seedling survival.

We suggest that this finding will help to reach a better understanding of existing patterns of plant species distribution and will improve the accuracy and specificity of predictions of vegetation shifts under global change scenarios. In the last decade, a strong focus has been placed on the modelling of vegetation-climate interactions. However, these models still suffer from an essential lack of temperature-specific ecological data and a mechanistic understanding of how environmental factors shape current species distributions. The Tmin values could easily be integrated into models as they can quantitatively estimate the success of recruitment under certain climatic conditions and are technically easy to obtain (in contrast to other stages of the plant life cycle).

 

Image caption: Primula minima is a typical alpine species, those seeds germinate under relatively high temperature.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Divergent functioning of Proteaceae species: the South American Embothrium coccineum displays a combination of adaptive traits to survive in high-phosphorus soils.

Mabel Delgado, Lalith Suriyagoda, Alejandra Zúñiga-Feest, Fernando Borie & Hans LambersEmbothrium coccineum, like most Proteaceae, produces cluster roots when grown at a low phosphorus supply (left).  The specialised root structures are suppressed at a high phosphorus supply (right).

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Proteaceae in south-western Australia thrive on phosphorus-impoverished soils, employing a phosphorus-mining strategy involving cluster roots, which release citrate, malate or other organic acids that can release phosphorus from rocks. Some develop symptoms of phosphorus toxicity even at slightly elevated soil phosphorus concentrations, due to their low capacity to down-regulate phosphorus uptake. In contrast, Proteaceae species in Chile, e.g., Embothrium coccineum, occur on volcanic soils, which contain high levels of total phosphorus, but phosphorus availability is low. We hypothesised that the functioning of cluster roots of E. coccineum differs from that of south-western Australian Proteaceae, in accordance with the difference in soil phosphorus status. With more phosphorus to be gained from the soil with high levels of total phosphorus, we expected and found less investment in biomass of cluster roots, but more release of citrate by these structures. We also hypothesised and confirmed that E. coccineum regulates its phosphorus-uptake capacity, avoiding phosphorus toxicity when grown at elevated phosphorus levels. We show that E. coccineum allocates at least five times less biomass to cluster roots that release at least nine times more organic acids per unit cluster root weight compared with south-western Australian species. The highest phosphorus supply caused some growth inhibition and high leaf phosphorus concentration, but no visible signs of phosphorus toxicity in leaves, as expressed in many south-western Australian Proteaceae. This combination of traits indicates divergent functioning of Proteaceae species from southern South America, exposed to frequent phosphorus input due to volcanic activity, in contrast with the functioning of south-western Australian Proteaceae species that thrive on severely phosphorus-impoverished ancient soils. These traits could explain the functioning of E. coccineum on soils that are rich in total phosphorus, but with a low concentration of available phosphorus.

Image caption: Embothrium coccineum, like most Proteaceae, produces cluster roots when grown at a low phosphorus supply (left). The specialised root structures are suppressed at a high phosphorus supply (right).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

How is the UV-Visible colouration of crab spiders produced?

Felipe M. Gawryszewski, Debra Birch, Darrell J. Kemp and Marie E. HerbersteinSpider abdomen after the removal of the cuticle, showing the guanine crystals that reflect ultraviolet light. Photo taken under the dissecting microscope.

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The functions of colouration in animals, such as camouflage, warning colouration and mate attraction, have been extensively studied. However, for many organisms we do not know the components that form the observed colour and how these components interact. Crab spiders (family Thomisidae) are non-web building spiders that hunt prey with their long pair of forelegs. The most charismatic species ambush bees and other pollinators on flowers. Interestingly, these species often have a body colour that matches the colour of the flowers, and have the ability to change their body colouration over a few days. In addition, a few species are able to produce a colour that includes the ultraviolet (UV) range of the light spectrum. Although humans do not see at this range, most invertebrates do. Surprisingly, spiders seem to be luring their prey, because some bees are attracted to flowers that have a UV-reflecting crab spider on it. In this study we looked at three different crab spiders to try to understand the mechanism by which colour is formed and, especially, how the UV part of the colour is produced. We found that three components interact to form the observed colour: the cuticle (the external invertebrate skin), a middle layer (hypodermis) containing pigments/crystals and, below, guanine crystals. The cuticle, contrary to what has been previously argued, is not transparent, and therefore contributes to the colour formation. Changes in pigments and/or crystals generate the colour change we observe in these spiders. Guanine crystals, present in all spiders we analysed, function as a white background against which components in the hypodermis appear. Moreover, these crystals strongly reflect UV light and therefore are the source of UV in these spiders. In UV spiders the hypodermis lacked pigments/crystals, exposing the UV reflective guanine crystals. Non-UV spiders, on the contrary, had hypodermal pigments/crystals that filtered the UV light reflected by the underlying guanine crystals. Thus, relatively simple changes are necessary to produce the observed variation of crab spider colouration. Also, our findings suggest that the evolution of UV in crab spiders may have only involved the exposure of the underlying guanine crystals.

Image caption: Spider abdomen after the removal of the cuticle, showing the guanine crystals that reflect ultraviolet light. Photo taken under the dissecting microscope.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The interaction between genotype and juvenile and adult density environment in shaping multidimensional reaction norms of behaviour.

Chang S. Han and Robert C. BrooksTenagogerris euphrosyne, photo provided by authors.

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The effect of environments on behavioural expression has been shown to depend on when individuals experience the environments. Thus various environments at different life stages can interact with each other to affect the expression of behaviours and generate complex patterns of behavioural plasticity. The complexity gets more extreme when one considers that genetically different individuals may respond differently to the same environments. We housed full-sibling brother males of Australian water strider species (Tenagogerris Euphrosyne), semi-aquatic insects that live on the water surface, at a range of juvenile and adult densities. Then we tested how density environments at different life stages influence mating- and foraging-related behaviours and their genetic variation. We studied these effects on four different behaviours (exploration of a new environment, dispersal, same-sex sexual behaviour and attempts to remount a female after being dislodged) in order to test whether the environmental effect differed among behaviours. Our study showed that both juvenile and adult density interacted to affect expression of behaviour, but the magnitude of its genetic variation in plasticity depended on the specific traits. There was little genetic variation in the behavioural response to density at different life stages, other than same-sex sexual behaviour. Our study highlights that environments at different life stages can interact to affect the expression of behaviour, and do so in different ways for different behaviours.

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

 

Are leaf functional traits “invariant” with plant size, and what is “invariance” anyway?

Charles A. Price, Ian J. Wright, David D. Ackerly, Ülo Niinemets, Peter B. Reich, and Erik J. VeneklaasWillow leaves.

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Many studies have shown that as plant size increases, investment in different plant organs (leaves, stems), or in how plants fill space (height, canopy spread), differs considerably across plant species. Many studies have also shown that traits related to photosynthesis and growth vary systematically together. We explore the intersection of these two broad areas by exploring the idea that leaf traits related to growth and photosynthesis may not vary systematically as a function of increasing plant height across land plants. This lack of variability has been described by some as “invariance”. Unfortunately, leaf trait invariance as a concept is neither well defined nor understood, and has never been critically examined.

We used a global plant trait dataset to evaluate whether nine leaf traits can be considered as “invariant” as a function of the maximum height of different plant species. We examined this relationship within different plant growth forms, and across broad taxonomic groups. We also examine whether these relationships depended on the habitat or biome that the plant species were found in.

We suggest that invariance is an intuitive concept, but one for which a concrete statistical definition is difficult to define. To that end, we propose five simple criteria that researchers can use to help identify when traits can be considered to be invariant.

Using these five criteria, we show that eight of the nine leaf traits we examined can be considered invariant with respect to plant height. This basic relationship didn’t change when we looked within and between herbaceous and woody plant groups; flowering plants and conifers; and within most biome and habitat types. One trait however, did increase with plant height, that of individual leaf area.

These results demonstrate that generally, leaf traits related to photosynthesis and growth do not change systematically across species of increasing height. This finding is useful to theoreticians and modellers who want to invoke ideal plants with average leaf properties that don’t depend on plant size.

Image caption: Willow leaves.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Colour in a new light: a spectral perspective on the quantitative genetics of carotenoid coloration.

Simon R. Evans & Ben C. SheldonMale great tit (credit: Simon Evans).

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Animal coloration is a complex trait to measure and analyse because it is dependent on the relative amounts of light from across the visible spectrum. Reflectance spectra describe what proportion of light from across the spectrum an object reflects. However, because every reflectance spectrum represents a large amount of data, biologists typically summarise them based on the key features they are interested in. For example, we study the yellow feathers of great tits and have previously calculated a measure of 'yellowness'. Using this, we showed that 'yellowness' of the feathers is partly heritable, such that strongly yellow parents have offspring that also grow vividly coloured feathers, whilst dully-coloured parents have dull offspring. However, by condensing the reflectance spectrum into a single value, we have lost all other information, so this approach is highly subjective. In contrast, reflectance is a physical property of an object and therefore independent of lighting or the observer (e.g., human versus bird). Furthermore we know that this colour patch consists of a combination of carotenoid pigments and a highly reflective background and, because these two components have different effects on reflectance (carotenoids absorb only blue-to-violet light, whilst background reflectance has a more constant effect across the spectrum), a spectral perspective would allow us to diagnose which component is influenced by a given effect.

We partitioned the bird-visible spectrum (human-visible light, plus ultraviolet light) into a large number of very narrow segments ('wavebands'), and analysed each of these independently but in parallel. For each waveband, we estimated how much variation in reflectance could be attributed to genetic effects that individuals inherit from their parents, and how much could be explained by their environmental experiences. By arranging the results for each waveband in sequence, we could visualise how these effects change across the spectrum. This showed how the heritable effects on 'yellowness' we have described previously are achieved through the carotenoid content of feathers being heritable, whilst the background reflectance component is more sensitive to environmental effects. This heritability indicates that the carotenoid content of feathers – and thus their yellow coloration – will evolve in response to selection, and this could help explain the diversity of carotenoid-based colours we see amongst animal species.

Image caption: Male great tit (credit: Simon Evans).
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Aerobic scope predicts dominance during early life in a tropical damselfish.

Shaun S. Killen, Matthew D. Mitchell, Jodie L. Rummer, Douglas P. Chivers, Maud C. O. Ferrari, Mark G. Meekan & Mark I. McCormickPhoto provided by authors.

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Members of the same species often come into conflict over important resources, but knowledge of the physiological traits that make some individuals better competitors than others remains elusive. For example, individuals with an increased capacity to perform physically demanding behaviours during conflicts may be better fighters or be more likely to become dominant. A potential means to estimate this physical capacity is by measuring an animal’s aerobic scope, which is its ability to increase aerobic metabolism above its resting level to perform physiological tasks, including exercise.

We examined links between aerobic scope and aggression in juvenile Ambon damselfish. In many tropical damselfishes, competition for territory is intense after young fish migrate to the coral reefs where they settle. Predation can be so extreme during this time that individuals prioritise safety over food availability when selecting territories, with dominant fish claiming the best shelters from predators. Notably, adjacent territories can be close to each other and fish are likely to repeatedly encounter the same rival. Whether a challenger is a familiar neighbour or an unfamiliar stranger could affect the amount of aggression displayed toward them because each type of competitor could represent a different level of threat.

We found that fish with a higher aerobic scope were more likely to become dominant when competing in pairs for access to coral in the laboratory. However, the physical effort displayed during fights typically did not approach that displayed by fish during exhaustive exercise, suggesting individuals do not fully utilise their aerobic scope during aggressive encounters. A greater aerobic scope may, however, allow faster post-contest recovery.

Fish that lost fights showed a rise in metabolic rate that was likely due to the effects of social stress. Interestingly, dominant individuals also showed an increase in metabolic rate when later exposed to the same competitor after a period of separation, but displayed no metabolic response to a strange fish not previously encountered. This not only suggests that fish recognise previous competitors, but also indicates an energetic cost of stress associated with the maintenance of dominance status. An additional benefit of an increased aerobic scope may be an enhanced capacity to cope with socially-induced stress.

These results show that aerobic scope is associated with dominance during competitions for territory in young Ambon damselfish. Fish that have a higher aerobic scope could therefore obtain the best territories, and possibly be favoured by natural selection.

Image caption: Photo provided by authors.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Why do some plant species become so successful and wide-spread away from home?.

Yan Sun, Heinz Müller-Schärer and Urs SchaffnerSpotted knapweed in USDA Field Station in Missoula, USA (left) and a knapweed individual (right). Courtesy of Norman E. Rees & Ivan Bliek.

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Invasions by alien plants threaten the integrity of agricultural and natural systems, causing enormous economic and ecological cost. Throughout western North America, plant invasions have resulted in the replacement of vast areas of native perennial grasses with Eurasian and Mediterranean plants. Various factors have been shown to contribute to the negative impact of invasive alien plants, but their relative importance remains unclear. We assessed the relative effects of neighbouring plant community and soil biota in explaining the negative impact of spotted knapweed, Centaurea stoebe L., during the invasion of new sites in North America.

We conducted a greenhouse experiment with both European and North American spotted knapweed competing with/without European vs. North American neighbouring community and with the two neighbouring communities growing without knapweed. Plants were grown in sterilized commercial soil inoculated with soil originating either from the home or the introduced range, and half of which was sterilized to remove soil biota.

Our results suggest that during the colonization of new sites in North American grasslands, the impact of spotted knapweed is strongly driven by the lower competitive ability of new (North American) neighbours compared with old (European) neighbours, while altered biotic soil conditions in the introduced range are of less importance. Interestingly, this differential impact appears to be due to inherently different mechanisms, as biomass of knapweed explained a substantial amount of the variation in biomass of the coevolved European neighbours, but not of the new "naïve" North American neighbours. Thus, impact in the home range appears to be driven by simple competition for the same limiting resources, but by other factors in the introduced range, possibly by exploitation of resources that are not used by the new neighbours or by a direct chemical impact on those neighbours (e.g. allelopathy effects). These findings, if applicable to other species, have important implications for the management of alien invasive plants, in that ecosystem recovery is less likely after a simple removal of their biomass.

Image caption: Spotted knapweed in USDA Field Station in Missoula, USA (left) and a knapweed individual (right). Courtesy of Norman E. Rees & Ivan Bliek.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Site fidelity curbs sequential search and territory choice: A game theoretic approach.

Kenneth A. Schmidt Evolution of the acceptance threshold (μ) is influenced by ecological factors that directly or indirectly affect the intensity of competition for breeding sites. The factors examined include: adult survivorship (max ØA), site-fidelity (WSLS rule), predator danger, and density-dependence (β). The acceptance threshold, μ, has an eco-evolutionary feedback through the territory game (evolutionary dynamic).

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Choosing among options of different quality that are sampled one after another is a well-known phenomenon in ecology where it is fundamental to behaviours such as patch use and mate choice. It also occurs in human contexts where it is know as the ‘job-search problem’. In both cases an individual has to decide when to stop looking and choose from a set of available options. Territory choice in vertebrates likely includes sampling for prospective breeding sites combined with a decision rule for accepting a site. Repeated breeders can also use prior experience to determine whether to return to or abandon former territories. Here I consider a threshold rule: individuals choose the first option that equals or exceeds a preset level of quality. Because the benefit an individual derives from using a given threshold will depend on what the population does, I used a game-theoretical approach to examine the evolution of the threshold. I examined this with and without considering older individuals who simply returned to (or remained at) territories where they were successful, i.e., they are site-faithful.

Ecological factors that increase population size enhance competition for sites and this affects the acceptance threshold: individuals are less choosy with more competitors present. To understand why, consider that being choosier than the average individual requires more bouts of sampling, on average, to find a site that is acceptable. But this selectivity comes at a cost: with every unsuccessful sampling bout, the average quality of remaining sites you sample from in the next bout becomes progressively worse. This potentially favors a slightly less selective individual, especially at high population density, and the population evolves a lower selectivity. The impact of site-faithful individuals, when faithful only to previously successful sites, exacerbates this effect by preferentially pre-empting high quality sites. The effect of site-faithful behavior may lead to the evolution of a threshold rule that as a whole, may in fact be little better than choosing sites at random. However, site-faithfulness does provides a better safeguard against population extinction.

Image caption: Evolution of the acceptance threshold (μ) is influenced by ecological factors that directly or indirectly affect the intensity of competition for breeding sites. The factors examined include: adult survivorship (max ØA), site-fidelity (WSLS rule), predator danger, and density-dependence (β). The acceptance threshold, μ, has an eco-evolutionary feedback through the territory game (evolutionary dynamic).
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

A newly defined Leaf Relative Growth Rate predicts shade tolerance of trees in a cool–temperate forest.

Ayana Miyashita & Masaki TatenoA cool-temperate mixed forest of Abies firma and Fagus japonica.

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Some tree species have the ability to survive and grow in a low-light environment. Such “shade-tolerant” trees are considered to play an important role in forest dynamics as dominant species, but the plant traits responsible for shade-tolerance are still controversial.

An important feature of shade-tolerant trees is to keep a positive whole-plant carbon-balance (i.e., positive growth rate) in a shaded understorey. However, whole-plant carbon-balance does not always show a reasonable growth potential. To evaluate continuous growth potential, we should evaluate whether the leaf biomass of a plant increases with time. To do this, we have attempted to develop a new index focusing on “leaf carbon-balance” to evaluate growth potential in a shaded understorey. We named the new index “Leaf RGR”, expressed using important traits for plant growth: net assimilation rate (rate of dry matter production per unit of leaf area ), leaf life-span, leaf mass per area, and leaf partitioning rate (a measure of the extent of investment into leaves). A numerical value of Leaf RGR >0 shows a positive leaf carbon-balance leading to continuous growth. Leaf RGR allows a quantitative analysis of how traits affect leaf carbon balance.

We applied this new index to the cool–temperate forest trees Abies firma (an evergreen conifer) and Fagus crenata and F. japonica (both deciduous broad-leaf trees) to compare shade tolerance.

We planted seedlings of the species in different light environments (open, deciduous and evergreen canopy sites), and observed their traits. Overall Leaf RGR and whole-plant growth rates showed a good correlation, however whole-plant growth rate was positive even if Leaf RGR was negative (i.e., no potential for continuous growth). Negative values of Leaf RGR appeared to correspond to low survival rates.

We found that in the deciduous site A. firma showed higher Leaf RGR and survival rate than F. japonica and F. crenata. Analysis of Leaf RGR showed that A. firma’s relatively high net assimilation rate and long leaf life-span were important; especially in deep shade, long-lived leaves can be essential to keep leaf carbon-balance positive. These results suggest that in a cool–temperate forest, evergreen plants can be more shade tolerant compared with deciduous plants.

Image caption: A cool-temperate mixed forest of Abies firma and Fagus japonica.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

The regulation of leaf water conductance across tree species: An entire spectrum revealed.

Tamir KleinMeasuring contrasting stomatal responses to leaf water status in the field: the author measures stomatal conductance and leaf water potential in co-occurring pines and oaks in a forest site in Israel. Photograph by Idan Springer.

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Water transport in plants is regulated by the degree of aperture of small stomatal pores. Plant stomata form a major gateway between the biosphere and the atmosphere and hence directly affect the global carbon and water cycles. Among tree species, large variability exists in how stomatal conductance responds to leaf water status. This variability has given rise to the recognition of two behavior types: isohydric, i.e. operating only close to leaf water saturation, and anisohydric, i.e. extending gas exchange to partial leaf dehydration. To assess this variability, curves of stomatal sensitivity to leaf water status were collected for 70 woody plant species. The dataset is comprised of flowering plants and conifers from all major forest biomes. The hypothesis that curves from different tree species diverge between isohydric and anisohydric behaviors was tested.

Here, species-specific curves formed a continuum of leaf responses, rather than a dichotomy between isohydric and anisohydric, as confirmed by distribution models. The water status at 50% of the maximum stomatal conductance (Ψgs50) was used for quantitative comparison between species. A major difference emerged among wood anatomy classes, whereby ring-porous species (e.g. almond, Prunus dulcis; and various species of oak, Quercus) had higher stomatal conductance at low leaf water status than diffuse-porous (e.g. various species of Eucalyptus, Ficus, and Populus ) and coniferous species. On average, trees from Mediterranean forests and semi-arid woodlands had significantly lower Ψgs50 than trees from tropical and temperate forests. The results indicate a bias in the distinction between isohydric and anisohydric species and suggest that stomatal sensitivity to leaf water status depends strongly on wood anatomy. The analysis improves our understanding of tree function under water limitation, with implications for forest vulnerability to drought at present and in future.

Image caption: Measuring contrasting stomatal responses to leaf water status in the field: the author measures stomatal conductance and leaf water potential in co-occurring pines and oaks in a forest site in Israel. Photograph by Idan Springer.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Warming homogenizes leaf surface temperatures

Robin Caillon, Christelle Suppo, Jérôme Casas, H. Arthur Woods & Sylvain PincebourdePrimary organism, T. urticae (top, photo credit: Gilles San Martin) and infrared image of an apple leaf surface (bottom, photo credit: Amélie Ezanic)..

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Many ectotherms move rapidly over short distances to keep their body at, or close to, optimal temperatures. Such behavioural thermoregulation can improve performance and allow individuals to avoid temperature extremes. However, opportunities for behavioural thermoregulation depend on the local spatial heterogeneity of available microhabitats. Highly heterogeneous thermal environments provide ample opportunities for animals to adjust their temperature by making relatively small movements, whereas homogeneous ones may allow little or none.

Global warming is expected to alter the spatial heterogeneity of environmental conditions in many habitats. However, despite the great diversity of organisms living on plant leaves, little is known about the impact of global warming on the spatial heterogeneity of microclimatic conditions on individual leaf surfaces (scales finer than 10 cm). We examined this question by comparing the thermal heterogeneity of individual apple leaf surfaces under moderate and high air temperatures, and we explored the consequences of that heterogeneity for behavioural thermoregulation by the two-spotted spider mite Tetranychus urticae.

Our results showed that ambient warming both decreased the range of temperatures available at the leaf surface and increased their spatial aggregation. Hence, warming homogenized the leaf microclimate, which prevented mites from thermoregulating behaviourally. These results suggest that climate warming may not only shift mean temperature at leaf surfaces, but also depress their thermal heterogeneity, with potentially critical implications for leaf dwelling arthropods. In particular, small arthropods may have reduced opportunities for behavioural thermoregulation at fine spatial scales. Such an effect may depress the performance of relatively immobile individuals, and may force more mobile individuals to thermoregulate by moving among habitat patches that are farther apart.

Image caption: Primary organism, T. urticae (top, photo credit: Gilles San Martin) and infrared image of an apple leaf surface (bottom, photo credit: Amélie Ezanic)..
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Food-limited mothers favor offspring quality over offspring number: a principal components approach.

Zachary R. Stahlschmidt & Shelley A. Adamo Early development of the Texas field cricket (Gryllus texensis). From left: egg within 1 day of being laid, egg during late incubation, and a hatchling within 1 day of hatching.

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Mothers must typically balance a tradeoff between the number and quality of offspring, and the environment a mother experiences may influence this tradeoff. For example, according to life history theory, a good reproductive strategy for a mother in poor conditions is to have fewer (but higher quality) offspring.

However, the relationship between the number of offspring a mother produces (fecundity) and the quality of these offspring is often complex. Specifically, it can be difficult to accurately measure offspring quality and its implications. Thus, several measurements of offspring viability, size, and performance must often serve as proxies for investment per offspring and its fitness consequences. We demonstrate that applying multivariate analyses to these types of data might be a powerful way to examine patterns of reproductive strategy—that is, whether a mother chooses to have few, high-quality offspring or many, low-quality offspring.

In a factorial experiment, we manipulated the quality of maternal environment (food availability) throughout early and late adulthood in a field cricket. We then measured maternal fecundity and several metrics of offspring quality. An approach using principal components analysis (a type of multivariate analysis) indicated that females laid fewer eggs but increased offspring quality after prolonged exposure to a low-food environment. In contrast, traditional approaches that statistically analysed only one variable at a time yielded few significant effects of food limitation.

We show that multivariate analysis can increase our ability to assess the adaptive significance of reproductive strategies, particularly in situations when offspring size and fitness are difficult to measure with accuracy. Such an approach might ultimately help assess the adaptive significance of reproductive allocation across a wider range of animals, thereby providing broader insight into the evolution of reproductive strategies.

Image caption: Early development of the Texas field cricket (Gryllus texensis). From left: egg within 1 day of being laid, egg during late incubation, and a hatchling within 1 day of hatching.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Grazing mosaics: Seascape attributes drive differences in herbivory in seagrass meadows.

Jordi F. Pagès, Alessandro Gera, Javier Romero and Teresa AlcoverroA highly grazed Posidonia oceanica seagrass meadow (Jordi F. Pagès).

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Even the simplest ecosystems exist as a patchwork of connected habitats forming a complex matrix through which animals have to navigate. The configuration of this mosaic can seriously affect both the number of species that can use the landscape, as well as their abundances. Some of these species may themselves be important actors in ecosystem processes, performing critical roles as herbivores or predators. By modifying how these species use the ecosystem, these landscape characteristics could have important implications for ecosystem functioning.

In our study, we looked at how differences in seagrass meadow mosaics could influence the way herbivory (a key process in these systems) was distributed across the landscape. Our principal herbivores were a mobile fish and a much less-mobile sea urchin. If these species were being influenced by the configuration of the patchwork, we hypothesised that differences in their interaction with landscape attributes would significantly influence herbivory rates.

To do this we measured rates of herbivory in seagrass patches that were embedded either in rocky substrates or on sand (the matrix attribute), close or far from rocky reefs (the distance attribute), and in the interior of meadows or at their edges (the edge attribute). We found that herbivory was higher in patches set in a rocky matrix compared to those on sand, and that the centres of meadows received higher rates of herbivory than their edges. These patterns were not influenced by the distance of the patches to rocky reefs. In itself this shows that landscape configurations can play an important role in determining how vital functions are distributed across the ecosystem.

To understand if herbivore numbers or food quality could explain these patterns, we measured herbivore abundances, seagrass production and plant quality in all the studied patches. Interestingly, the patches did not show significant differences in these variables. This suggests that the most likely reason for the patterns we recorded in herbivory lie in behavioural differences between species in their evaluation of risk, movement and food preference in relation to landscape configuration. Our results indicate that species richness and abundance patterns may not be sufficient to predict the impact of key species on the functioning of ecosystems within a mosaic of habitats.

Image caption: A highly grazed Posidonia oceanica seagrass meadow (Jordi F. Pagès).
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Natural habitat loss and exotic plants reduce the functional diversity of flower visitors.

Ingo Grass, Dana G. Berens & Nina FarwigAn individual of the African honeybee (Apis mellifera scutellata) approaches a Yellow Everlasting (Helichrysum ruderale)..

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Pollinating insects are declining worldwide. This is worrying, as many of the world’s flowering plant species depend on insect pollinators for reproduction. Although the number of different pollinator species (pollinator richness) has been shown to be important for pollination, functional complementarity among different pollinators may play an even greater role. Functional complementarity means that flower visitors differ in certain characteristics that affect their pollination effectiveness. For example, a pollinator with a long tongue (proboscis) is a better match for plants with deep flowers than a pollinator with a short proboscis. Overall, the maintenance of plant diversity depends on pollinator species differing in morphological or behavioural traits, or, in other words, on the ‘functional diversity’ of pollinators.

Global change is a likely reason for the worldwide pollinator decline. Two strong drivers of global change are the loss of natural habitat and invasions of native communities by exotic (usually anthropogenically introduced) plant species. We know that these drivers often negatively affect pollinator richness; yet, we know virtually nothing about their effects on pollinator functional diversity. However, declines in pollinator functional diversity may be even more drastic than declines in pollinator richness.

We investigated the functional diversity of insect flower visitors in a subtropical South African landscape. Our study region is greatly affected by natural habitat loss and exotic plant invasions. We investigated functional diversity of three morphological traits that greatly influence flower handling and pollination efficiency: proboscis length, proboscis diameter and body length. We found that increasing habitat loss and abundance of exotic plants clearly reduced the functional diversity of flower visitors. In some cases, diversity of the three traits was negatively affected by both drivers and in other cases by only one of the two drivers. Contrastingly, we found no evidence for a decline in richness of flower visitors with either habitat loss or exotic plant invasions.

Our study shows that natural habitat loss and exotic plant invasions threaten the functional diversity of flower visitor communities, and that negative effects may not be evident if we only focus on species richness of flower visitors. Moreover, losses in functional diversity were partly driver-specific. This means that we need to consider multiple threats to flower visitors in order to gain insights into possible consequences of global change for pollination. Overall, our understanding of the effects of global change on pollinators and ultimate consequences for plant reproduction may greatly benefit from functional trait-based approaches.

Image caption: An individual of the African honeybee (Apis mellifera scutellata) approaches a Yellow Everlasting (Helichrysum ruderale).
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Pushing the limits to tree height: succulent treetop leaves of coast redwood store water.

H. Roaki Ishii, Wakana Azuma, Keiko Kuroda Stephen C. SillettPhotograph provided by authors..

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Coast redwood is the only tree species with living individuals exceeding 100 m in height. The tallest living individual stands 115.76 m as of 2013. The physiological mechanisms underlying its incredible stature have recently been documented, and water supply to treetop leaves is a key factor limiting physiological function and height growth of tall trees. However, mechanisms may exist that maintain water status of leaves and thus sustain physiological function near the treetop where light availability for photosynthesis is highest. Here we show evidence of foliar water storage as a mechanism for maintaining physiological function of treetop leaves in coast redwood. We measured water-use properties and morpho-anatomical characteristics of coast redwood foliage near the wet, northern and dry, southern limits of its geographic distribution in California, USA. We found that capacity to store water and the amount of water stored in foliage both increase with increasing height and light availability, maintaining tolerance of leaves to water stress constant with height. The morphology and anatomy of treetop leaves indicate increasing capacity for water storage and decreasing reliance on water transport from roots. Treetop leaves of coast redwood absorb moisture via leaf surfaces and have the potential to store more than five times the daily water demand. In coast redwood, water storage in foliage, near the site of photosynthesis, may be an important physiological adaptation that maintains water status and helps overcome constraints on water supply. This may explain how the world’s tallest species solves the dilemma that water stress is highest near the treetop, where light availability for photosynthesis is highest, and continues to push the limits of tree height.

Image caption: Photograph provided by authors..
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Chronic exposure to low-dose radiation at Chernobyl favours adaptation to oxidative stress in birds.

Ismael Galván, Andrea Bonisoli-Alquati, Shanna Jenkinson, Ghanem Ghanem, Kazumasa Wakamatsu, Timothy A. Mousseau and Anders P. Møller Caption: Mist nets in a field near the Chernobyl Nuclear Power Plant.  About 500 m of mist nets were used to catch birds from eight sites within and around the exclusion zone in 2010. Credit: T.A. Mousseau and A.P. Møller (c) 2010.

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Ionizing radiation creates chemicals that are potentially damaging to cells. Living organisms use a diversity of antioxidant compounds that can eliminate or reduce these damaging effects, but when antioxidant levels are low, it can lead to states of oxidative stress. Oxidative stress is often the ultimate cause of aging and the death of organisms. Most research on the biological effects of ionizing radiation have been conducted in cell cultures or with organisms under laboratory conditions which can be very unrealistic and limits the possibility for obtaining information on the consequences for the ecology and evolution of free-living organisms. Nuclear accidents like that at the nuclear power plant of Chernobyl in 1986 have had catastrophic environmental consequences, although the large amount of radioactivity released to the environment represents involuntary experiments and the opportunity to investigate the effects of radiation on wild populations of organisms. Here we present analyses of levels of the most important intracellular antioxidant (i.e., glutathione, GSH), its redox status, DNA damage and body condition in 16 species of birds exposed to radiation at Chernobyl. We used advanced statistical methods to permit unprecedented sensitivity in our analyses. Our study provides the first evidence for adaptation to radioactivity in wild animals when exposure is chronic and doses are low. These results suggest that chronic exposure to low-dose-rate radiation may stimulate antioxidant production that significantly reduces oxidative stress and DNA damage in some species of birds. In other words, these findings indicate that chronic exposure to radiation has favored adaptation of birds to the damaging effects of radiation.

Image caption: Caption: Mist nets in a field near the Chernobyl Nuclear Power Plant. About 500 m of mist nets were used to catch birds from eight sites within and around the exclusion zone in 2010. Credit: T.A. Mousseau and A.P. Møller (c) 2010..
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Nitrogen cycle response to precipitation change.

Melissa A. Cregger, Nate G. McDowell, Robert E. Pangle, William T. Pockman, and Aimée T. ClassenTree. Photograph courtesy of authors.

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Over the past century, human activities have caused unprecedented changes in the physical and chemical structure of the earth system. These changes include a 37% increase in atmospheric CO2 and a 0.7 °C increase in mean annual temperature, which together have altered the hydrologic cycle. Climate models predict that the frequency and severity of drought will increase globally. Increased drought will be especially important in the southwestern US where piñon-juniper (PJ) woodlands cover >36 million acres. In the last decade, areas encompassing PJ woodlands have experienced unprecedented levels of drought. These droughts have important consequences for PJ woodland composition and function, including changes in plant community composition, changes in the associated soil bacterial and fungal (collectively microbial) communities, and changes in ecosystem processes such as nitrogen cycling.

Using a large-scale precipitation manipulation in a PJ woodland, this study explored how changing precipitation regimes altered soil nitrogen cycling, a key ecosystem function. Additionally, we measured microbial biomass nitrogen and the abundance of bacteria involved in the rate-limiting step of nitrification (oxidation of ammonia to nitrate) to explore if microbial responses were driving these changes. We found that nitrogen availability decreased with increasing water availability, and nitrogen cycling differed between the two co-dominant trees, piñon and juniper. Surprisingly, we did not see differences in cycling rates across the precipitation treatments or differences in microbial biomass and abundance of microbes involved in nitrification. Our data suggest that changes in nitrogen cycling are driven by abiotic processes like leaching and by differences in plant and microbial nitrogen uptake. Given that piñon mortality under drought is higher than juniper mortality, we conclude that shifts in species composition may lead to landscape-level shifts in nitrogen cycling in this ecosystem.

Image caption: Tree. Photograph courtesy of authors.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

You are what you eat (and what your food has eaten).

Jennifer K. Rowntree, David Fisher Barham, Alan J. A. Stewart & Sue E. HartleyYellow rattle in its natural setting. Photo credited to Sue Hartley.

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Instead of getting nutrients from the soil, parasitic plants “steal” food from other plants. Around 1% of flowering plants are parasitic on other plants, including the well-known mistletoe. Yellow rattle feeds by attaching its roots to those of its host. It is commonly found in European grasslands, has yellow flowers that attract pollinators and seedpods that rattle when they are ripe. Yellow rattle does not specialise on one type of host plant, but will happily take nutrients from many different hosts. However, not all hosts are equal and the parasite can grow better on some compared to others. We grew yellow rattle on nine different host species, and showed that the yellow rattle grew larger when attached to some hosts than it did attached to others.

The grasslands where yellow rattle is found contain many species of plants and animals that interact with each other. While yellow rattle uses other plants for food, insects and other herbivores will feed on the yellow rattle. We found that the host species that the yellow rattle was growing on had an effect on aphids that were feeding on the yellow rattle. Some host plants were beneficial to the aphids, enabling them to produce lots of offspring. One host plant in particular (bird’s foot trefoil) was bad for the aphids and they were less able to reproduce when yellow rattle was attached to it. Bird’s foot trefoil provided the yellow rattle with protection from these herbivores.

In grassland, yellow rattle does not feed from a single host plant, but attaches to, and obtains nutrients from, many different host plants at once. This ensures that if one host dies, the parasitic plant can still survive. We found that if yellow rattle was growing on multiple host species, where one of the hosts was bird’s foot trefoil, the aphids reproduced more than when the yellow rattle was growing on bird’s foot trefoil alone. Therefore, we show that by attaching to multiple host species, yellow rattle is more susceptible to aphids than if it were to specialise on a single host such as bird’s foot trefoil.

Image caption: Yellow rattle in its natural setting. Photo credited to Sue Hartley.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

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