Lay Summaries Archive

Read Lay Summaries from previous volumes of Functional Ecology here:

Early View Lay Summaries

 

Basal Metabolic Rate in Tropical Birds: The Influence of Latitude and Altitude on the "Pace of Life".

Gustavo A. Londoño, Mark A. Chappell, María del Rosario Castañed, Jill E. Jankowski, and Scott K. Robinson Overview of the Manu Gradient, photo taken from the field site at 3000 m elevation with the lowland site in the background.

For decades scientists have acknowledged latitudinal and altitudinal differences in bird life history (number and size of eggs laid, nesting behaviors, and lifespan). For example, tropical birds are thought to have a slower ‘pace of life’ – they lay fewer eggs (usually two) and generally live longer than temperate birds. These differences could result from the large variation observed among latitudes and altitudes in abiotic (e.g., temperature, rainfall) and biotic (e.g., nest predation, competition) conditions. Higher latitudes and altitudes tend to be colder with more variable temperatures, whereas low latitudes and altitudes have warmer and more stable temperatures. Biotic pressures, such as nest predation, competition and parasites, tend to be higher at low latitudes and altitudes.

Our study provides data on a basic life history trait, Basal Metabolic Rate (BMR), loosely defined as the energy expended by an animal at rest, for ~250 Peruvian bird species along a 2600-m tropical altitude gradient. We also compare our BMR data from birds in Peru with BMR data collected from > 500 bird species from other studies across temperate and tropical latitudes. We use this dataset to ask the following questions. Do substantial differences in native altitude—and hence environmental temperature—influence the BMR of tropical forest birds? Is the low BMR found in other lowland tropical birds also characteristic of the geographically distant tropical birds in Peru? Do tropical birds have lower BMR than those of temperate birds? Does BMR differ among different groups of bird species (songbirds and others)?

We found that BMR does not vary among tropical altitudes or regions, but does vary among tropical and temperate latitudes and avian orders, such that birds breeding in temperate regions and songbirds have higher BMR. Our study confirms previous reports of differences in BMR between temperate and tropical bird species, consistent with the concept of tropical birds having a slower ‘pace of life’. We found no effect of environmental temperature on BMR in Peruvian forest birds across a 2600-m altitude transect (a 12 °C temperature change), reinforcing the view that low BMR in tropical birds is mainly driven by slow life history.

Image caption: Overview of the Manu Gradient, photo taken from the field site at 3000 m elevation with the lowland site in the background.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

When it comes to water, snake foetuses have priority over mom.

Andréaz Dupoué, François Brischoux, Frédéric Angelier, Dale F. DeNardo, Christian D. Wright and Olivier LourdaisUltrasonographic picture of a developing embryo (Vipera aspis).

Conflicts between a parent and offspring are not unique to humans and may occur in nature whenever there is a limited resource that the two must share. Typically, energy has been the focus of such conflicts, but water is another vital resource that has yet to be considered in the framework of parent-offspring trade-offs or conflicts. In many dry environments, water can be quite limited during certain seasons and such times often coincide with pregnancy. However, physiological demands of pregnancy mean females require a greater amount of water during this period compared to times when the female is not pregnant. Since female snakes supply energy to their developing offspring in the form of yolk that is allocated prior to fertilization, using snakes as study organisms enabled us to examine possible intergenerational water conflicts independent of energy conflicts.

We explored the trade-off over water resources between a mother and her developing embryos in a live-bearing snake, the aspic viper. We manipulated water availability (control vs. water-deprived for 20 days) to pregnant and non-reproductive female snakes. Snakes can tolerate considerable levels of dehydration and thus our treatment was ecologically relevant and non-threatening to the general health of the snakes. We examined the effects of water deprivation on female water balance, water transfer to the embryos, and reproductive performance.

Water deprivation resulted in significant female dehydration, with more pronounced effects in pregnant compared to non-reproductive females. The impacts of water deprivation on water balance were correlated with the number of offspring, with the most fecund females being more dehydrated. In contrast, water deprivation had no effect on water transfer to the offspring or on reproductive performance. Our results demonstrate that, when water is unavailable, female water balance is compromised in favour of the developing embryos, highlighting a significant trade-off over water resource between a mother and her offspring. Whether the prioritization of the offspring is a result of a “generous” mother preferentially allocating resources to her offspring or the offspring “selfishly” taking the water from the mother remains unknown. Regardless, this work demonstrates that parent-offspring conflict over water may be a substantial hurdle during the evolution of the live-bearing reproductive mode.

Image caption: Ultrasonographic picture of a developing embryo (Vipera aspis).
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.

 

Silicon concentration and population dynamics of voles.

Monika Wieczorek, Karol Zub, Paulina A. Szafrańsk, Aneta Książe and Marek KonarzewskiRoot vole, Microtus oeconomus. Photo courtesy of  K. Zub.

Population cycles of small rodents have puzzled researchers since the advent of ecological studies. One of the hypotheses is that time-delayed plant-herbivore interactions could be responsible for generating population fluctuations. Under this scenario, past overgrazing induces plants to accumulate toxic, or hard to digest, components that negatively affect growth and survival of herbivores, and thus induces cycling of their populations. Induced mechanical defences that reduce plant digestibility could be essential in deterring herbivory in grasses, which are the primary diet component of numerous herbivores that show population cycles.

Most tests of the plant-herbivore hypothesis have focused on broad categories of chemical defences, with much less attention given to mechanical defences, such as abrasive silicon (Si), which reduce palatability and digestibility of plant tissues. In contrast, many studies considered accumulation of Si by plants as a process primarily controlled by geo-hydrological factors. Therefore, we investigated the relationship between concentration of Si in fibrous tussock sedge and the population density of a major sedge consumer, the root vole, in field enclosures located in the Biebrza river valley (NE Poland) under a variety of natural water regimes and weather conditions.

We found that a high density of voles resulted in the immediate accumulation of Si by rhizomes, followed by accumulation of Si in leaves with a one-year lag time. The level of river flooding had an additional impact on Si concentration in rhizomes but did not affect silicification of leaves. Overwinter changes in concentration of Si in sedges were also influenced by fluctuations in ambient temperature and the depth of snow cover, thus affecting the quality of winter food available for voles. Smaller voles had lower mortality during early winter than large voles, which suggests that small individuals better coped with the need to extract adequate nutrients and energy from a highly silicated diet. Our results showed that changes in Si concentration in sedges can be induced by changes in vole population density and are also additionally affected by flooding and weather conditions.

Image caption: Root vole, Microtus oeconomus. Photo courtesy of K. Zub.
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.

 

Implications of lifespan variation within a leaf cohort for evaluation of the optimal timing of leaf shedding.

Noriyuki Osada, Shimpei Oikawa, and Kaoru Kitajima Photo provided by authors.

When should a piece of equipment that is increasingly worn out and less efficient be replaced? The answer should depend on how quickly it is aging. Plants face a similar question with their leaves. Plants invest resources to produce leaves in order to obtain benefits in terms of photosynthetic production. The newest fully-expanded leaf is the most productive, with minimum wear and tear and usually created at the sunniest part of the plant crown. However, as leaves get older, they become shaded more and become less efficient in their photosynthetic productivity. When should an aging leaf be replaced? For such optimization of leaf life span (LLS), how photosynthesis declines as leaves age is a critical parameter. Many researchers have attempted to quantify this parameter, often using a method of space-for-time substitution, comparing young and old leaves at a given time. Unfortunately, this approach results in a significant underestimation of the age-related decline rate of photosynthesis, as we demonstrate with a simple simulation in our paper. Our simulation also predicts that the degree of such underestimation is greater for species that have leaf cohorts that vary a lot in LLS. This prediction is supported by an analysis of published data demonstrating that the photosynthetic capacity at the cohort mean LLS was positively correlated with the variation in LLS. This strongly suggests that the age-related decline of carbon gain may be underestimated in many previous studies that neglect within-cohort variation in LLS.

Image caption: Implications of lifespan variation within a leaf cohort for evaluation of the optimal timing of leaf shedding.
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.

 

Impacts of repeated stress events on an overwintering insect.

Katie E. Marshall and Brent J. SinclairLate-instar Choristoneura fumiferana caterpillar.  Photo courtesy of Jerald E. Dewey, USDA Forest Service, United States, downloaded from Wikimedia Commons.

Organisms live in complex worlds where environmental stresses can be more or less intense, occur for longer or shorter periods, and repeat more or less frequently. And although we know a lot about the effects of a single stress event, the effects of these more complex patterns of stress are not well understood.

We tested the impacts of each of these different aspects of stress simultaneously in the eastern spruce budworm Choristoneura fumiferana to attempt to identify which types of stress cause the largest impact on physiology and long-term fitness. We subjected overwintering spruce budworm larvae to four different low temperatures either once or multiple times, with three different periods of time between each exposure. We then measured short-term effects on physiology by looking at changes in freezing point and stores of carbohydrate and cryoprotectants (chemicals that protect the larva’s tissue from freezing damage). We also allowed a subset to leave diapause (winter dormancy) and feed, then recorded survival, development time, and adult body size.

We found that in all cases the greatest impacts were due to the number of exposures and the time of year the cold exposure occurred. While there were long-term effects of cold exposure during overwintering on survival, there was no impact on adult body size or development time. This suggests that current understanding of the way stress impacts individual organisms may be missing the effects of stress variability.

Image caption: Late-instar Choristoneura fumiferana caterpillar. Photo courtesy of Jerald E. Dewey, USDA Forest Service, United States, downloaded from Wikimedia Commons.
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.

 

Variability in potential to exploit different soil organic phosphorus compounds among tropical montane tree species.

Brian S. Steidinger, Benjamin L. Turner, Adrianna Corrales, and James W. DallingGrow house at the Fortuna Forest Reserve.

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The mineral nutrients that plants need to grow and reproduce occur in the soil in a variety of chemical forms. This diversity of form makes it possible for plants to specialize in the acquisition of specific forms, which can reduce competition over growth-limiting nutrients and promote species coexistence. A key nutrient is phosphorus (P), which most plants are helped to acquire by a fungal partner, known as a mycorrhiza. Of the two commonest types of mycorrhiza, one actually penetrates plant roots, while the other forms a sheath around the root.

Previous work suggests plants that associate with these two different functional groups of mycorrhizas differ in their ability to acquire P from organic vs. inorganic sources. We tested this hypothesis at the Fortuna Forest Reserve, a tropical montane forest along Panama’s Central Cordillera, where representative species from both mycorrhizal groups and non-mycorrhizal tree species coexist. First, we collected seedlings of tree species with different mycorrhizal associations from the field, sampled their root systems, and measured the activity of enzymes that allow plants to exploit organic P. Next, we took the same tree species, exposed them to P exclusively in one of four different chemical forms (three organic + one inorganic), and gauged their performance.

Our results confirm that specialized plants that lack mycorrhizal fungi are better able to exploit a specific form of organic P that is unavailable to the mycorrhizal plant species. This difference appears to be related to a markedly higher activity of enzymes that attack organic P. In contrast, we found no evidence that plants associating with different types of mycorrhiza differ in their ability to exploit organic and inorganic forms of P. Overall, our results support the potential for P partitioning to occur in a tropical montane forest, but suggest that it occurs more coarsely among functional groups than previously imagined.

Image caption: Grow house at the Fortuna Forest Reserve.
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.

 

Bolder lizards discard their tails to compensate for risky behavior when food is abundant.

Chi-Yun Kuo, Duncan J. Irschick and Simon P. LailvauxA male brown anole lizard displaying its colorful dewlap. Photograph by Duncan J. Irschick.

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Traits that confer benefits often have costs. A fascinating phenomenon in evolutionary ecology is that individuals can offset the costs of a beneficial trait with the function of another trait (trait compensation). The most common examples of trait compensation are those between behavioral and morphological defense mechanisms, in which individuals that are morphologically more vulnerable tend to show a higher degree of predator avoidance, and vice versa. Despite numerous reports of compensation between defensive traits, two fundamental questions have still not been fully addressed. First, whether trait compensation exists among similarly-aged individuals; and second, whether and how the relationship between compensatory traits would be influenced by the amount of food resource in the environment. Using juvenile brown anole lizards, we examined the relationship between boldness, or a willingness to take risks, and the propensity for employing tail autotomy, a costly defense trait in which a lizard voluntarily discards its tail (which gradually regrows over time), under low and high food availability. We expected bolder lizards to compensate for their higher risk-taking tendency by discarding their tails more readily. We also expected the relationship between the two traits to differ under different food availability, although the exact effect might be complex and difficult to predict a priori. Although lizards raised under low and high food availability on average did not differ in boldness or the propensity for tail autotomy, bolder lizards overall did discard their tails more readily. However, this compensatory effect was present only among individuals raised with abundant food, which suggested that trait compensation was a viable strategy only when lizards can obtain enough food to quickly regrow the lost tails. Our results showed trait compensation existed among similarly-aged individuals and served as a basis for compensatory effects observed at the population, species or higher levels. In addition, we demonstrated that food availability can influence the dynamics between compensatory traits without significantly changing the mean values of the traits per se.

Image caption: A male brown anole lizard displaying its colorful dewlap. Photograph by Duncan J. Irschick.
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.

 

Changes in resource availability have profound consequences for the microbial communities of tropical forest soils.

Nicolas Fanin, Stephan Hättenschwiler, Heidy Schimann & Nathalie Fromin Fungi are main actors of leaf litter decomposition in the tropical forest.

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Tropical forest ecosystems play a key role in the global carbon (C) cycle. In these forests that grow on highly weathered and nutrient-impoverished soils, a mechanistic understanding of how resource availability controls soil C dynamics is urgently needed for accurate predictions of global change effects on the C cycle.

Because soil microorganisms (i.e. bacteria and fungi) have different nutrient requirements, we expected the soil microbial community and the processes it drives to strongly respond to fertilization with different major nutrient elements. We report the results of the first combined fertilization experiment with cellulose (C), urea (nitrogen) and phosphate (phosphorus) in a nutrient-poor tropical rainforest of French Guiana.

After two years of fertilization, we showed that changes in resource availability had profound consequences for soil microorganisms, with clear shifts in the structure and function of the soil microbial community and its ability to process various C substrates. In particular, phosphorus addition enhanced both bacterial and fungal biomasses and overall microbial activity, as well as the ability of the soil microbial community to use a wide range of C substrates. However, the strongest effects of phosphorus fertilization were observed with the simultaneous addition of nitrogen and or C, showing limitation of soil microorganisms by multiple, interacting nutrient elements.

The reported multiple element control of soil microbial biomass, community structure and activity may contribute to a better understanding of spatial and temporal heterogeneity in microbial community structure, their associated functions and the dynamics of C and nutrients in tropical ecosystems.

Image caption: Fungi are main actors of leaf litter decomposition in the tropical forest.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Oxidative stress in breeding northern elephant seals.

Jeffrey Sharick, Jose Vazquez-Medina, Rudy Ortiz and Daniel Crocker Photo provided by authors.

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Life history theory suggests that the timing and amount of effort devoted to reproduction over an animal’s lifespan is shaped by natural selection to maximize lifetime reproduction. Central to this theory is the assumption that current reproduction reduces the ability of an organism to reproduce in the future, including negative impacts on survival. This cost may involve allocation of resources to reproduction that reduce energy available for maintenance and health. In some species, called ‘capital breeders’ these trade-offs are distinct as all of the energy used for breeding comes from body reserves stored prior to reproducing. Metabolism produces a variety of reactive oxygen species that can cause damage to biomolecules, and this ‘oxidative stress’ has been theorized to be a potential source of the survival costs associated with reproduction.. Since both high rates of metabolism and fasting are associated with oxidative stress, capital breeders might be especially subject to these costs.

We examined the potential for oxidative stress in breeding northern elephant seals. Since elephant seals forage in the ocean and breed on land, they are capital breeders. Males fast from food for over 100 days while maintaining high rates of metabolism for fighting and mating. Females fast for a month while making one of the most nutrient rich milks found in nature. We compared markers for oxidative stress in males and females at the beginning and end of breeding. We measured a pro-oxidant enzyme that makes reactive oxygen species, three important anti-oxidant enzymes, markers for oxidative damage to fats, protein and DNA, and a marker for inflammation in blood samples. We found that the pro-oxidant enzyme increased across breeding and the seals responded by increasing the levels of anti-oxidant enzymes. Despite this protective response, males showed evidence of oxidative damage to fats and DNA and showed increased levels of inflammation. Females showed evidence of oxidative damage to proteins. Our results provide evidence for oxidative stress as a cost of breeding in polygynous male elephant seals and weaker evidence in females. These data support the idea that oxidative stress may underlie survival impacts of reproduction in some species.

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

 

Swimming loss and recovery in the Atlantic silverside.

Kestrel Perez & Stephan MunchAdult Atlantic silversides collected in little neck bay, Long Island, NY USA. Photo credited to Kestrel O. Perez..

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For many animal species, large body size leads to higher survival and reproductive success. Because fast growth rates enable an individual to obtain a large body size sooner, it stands to reason that fast growth should be similarly beneficial. Why then, do growth rates commonly still vary in many species? In fact, most species do not grow as fast as possible, suggesting that there must be some down-sides to rapid growth. Across a wide range of animal species, there have been many documented cases of the negative effects of fast growth. One such example is the Atlantic silverside, a common marine fish, where individuals that grow rapidly have poorer swimming ability compared to slow-growing individuals of the same size. But, how long this effect lasts is currently unknown. In this study, we determined how long it takes for a fish to recover its ability to swim following a period of fast growth. We manipulated growth rate in Atlantic silversides by providing variable amounts of food, either unlimited food for the fast growth treatment or limited food for the slow growth treatment. After two weeks of these feed rations we then fed both treatments limited rations to maintain slow growth rates. We monitored swimming ability over this period. Full recovery from the effects of earlier fast growth would be indicated if swimming ability of the fish that had previously been growing fast, but were currently growing slowly, improved and became comparable to swimming ability of the fish that had always been growing slowly. Interestingly, we found that fish that had grown rapidly early in life not only had significantly poorer swimming ability, but continued to show the effects of this early period of rapid growth. We found that fish fully recovered normal swimming ability only after 1 month of growing slowly. Most surprisingly, swimming ability actually decreased before it improved.

Image caption: Adult Atlantic silversides collected in little neck bay, Long Island, NY USA. Photo credited to Kestrel O. Perez..
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.

 

Community phylogenetics and ecosystem functioning

Clarifying the discussion of how environmental variation shapes community diversity.

Nathan J. B. Kraft, Peter B. Adler, Oscar Godoy, Emily James, Steve Fuller & Jonathan M. LevineIn the Central Valley of California, USA, small depressions in the ground can fill with rainwater in the winter, creating a vernal pool habitat. The dominant plant species (shown here in bloom) that are found in these pools can tolerate immersion in the rainwaters, while the flooded conditions exclude many of the surrounding grassland species. This process of environmental filtering, seen here at a small scale, shapes patterns of biodiversity across the planet. Credit: Nathan Kraft.

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Variation in environmental factors such as temperature, rainfall and soil chemistry have profound effects on the distribution of biodiversity across the planet. Community ecologists often use the concept of "environmental filtering" to describe situations when a species is unable to survive at a site because of the environmental conditions. However, the evidence that ecologists have used to test for environmental filtering in the past is often indirect, as it is not always sufficient to rule out other potential causes, such as competition with other species. This uncertainty is particularly problematic if we try to use results from these studies to make predictions about how global change will impact species and communities.

In this study we describe a conceptual framework to help distinguish environmental filtering from other sources of variation in community structure. Strong evidence for environmental filtering comes from showing that species have the potential to arrive at a site (as a dispersed seed or as a migrant from a nearby area, for example) but are unable to survive in the environmental conditions found there. We reviewed the ecological literature to assess how environmental filtering is typically assessed, and despite the widespread use of the concept, only 15% of published studies included this direct evidence. Most studies instead rely on patterns such as species changes in abundance or changes in physiological characteristics across an environmental gradient, patterns that can be driven by other factors.

We discuss a number of ways in which both experimental and observational studies can be improved to give a more precise accounting of the role of abiotic variation in shaping community structure. By addressing these issues, ecologists can come to a clearer understanding of the multitude of ways in which environmental variation shapes patterns of diversity across communities.

Image caption: In the Central Valley of California, USA, small depressions in the ground can fill with rainwater in the winter, creating a vernal pool habitat. The dominant plant species (shown here in bloom) that are found in these pools can tolerate immersion in the rainwaters, while the flooded conditions exclude many of the surrounding grassland species. This process of environmental filtering, seen here at a small scale, shapes patterns of biodiversity across the planet. Photo credited to Nathan Kraft.
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.

 

Plant uptake elements as influenced by phylogeny, soil and climate.

Zhuan Hao, Yuanwen Kuang & Ming KangPrimulina bullata growing calcareous soils (Photo credit: Ming Kang).

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Plants require a large number of chemical elements to sustain their life. Understanding factors that influence elemental composition of plants is important because it provides insight into a wide range of ecological and environmental processes. Numerous experimental studies have previously documented the influence of soil and climate on elemental composition of plants, but phylogeny is still rarely considered as a factor in determining plant elemental contents (i.e. whether closely related species have similar elemental composition, even in different environments). In this study, we measured leaf concentrations of seven elements and evaluated soil properties for 177 species of the African violet subfamily Didymocarpoideae from subtropical China, a global biodiversity hotspot. We partitioned the variation in leaf element contents into the effects of soil, climate and phylogeny. Then we tested whether closely related species tend to have similar ecological characteristics (i.e. phylogenetic signal) at two different phylogenetic scales (subfamily vs genus). We also used phylogenetic comparative methods to assess the impacts of soil and climatic conditions on leaf element concentrations.

We detected a strong phylogenetic signal in leaf elements as well as for soil and climate variables at the subfamily level, whereas the large genus Primulina exhibits no significant phylogenetic signal in leaf elements or in most soil variables. We found an influence of both soil and climatic conditions on leaf element concentrations. However, the patterns of the relationships between leaf elements and soil and climate variables vary at the subfamily and genus levels. Phylogeny has a stronger effect than soil and climatic factors on leaf element contents at the subfamily level, while leaf elements within the genus Primulina are mostly influenced by environmental conditions. We conclude that the influences of taxonomy, soil and climate on leaf element concentrations are dependent on the phylogenetic scale of analysis, highlighting the need to integrate phylogenetic scales to explore the influence of soil and climatic conditions on leaf element concentrations.

Image caption: Primulina bullata growing calcareous soils (Photo credit: Ming Kang).
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.

 

Hard work, dominance and health in a Kalahari bird.

Dominic L. Cram, Jonathan D. Blount & Andrew J. YoungFemale white-browed sparrow weaver in an Acacia tree. Credit Dominic Cram.

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When groups of animals live together (including humans), they often divide workloads, and some individuals work harder than others. Are the hardest-working individuals the healthiest, and does this allow them to work harder than everyone else? Does their work-rate impact their health, leaving the hard-workers in poor condition?

We investigated these questions in groups of white-browed sparrow weavers, in the Kalahari Desert. Although they share workloads as ‘cooperative breeders,’ within each group the dominant male and female work much harder than the subordinates. Dominants are the only birds that breed, with dominant males singing to attract their mate and dominant females producing all eggs and providing most of the care for nestlings. Both dominants also work hardest to defend the group’s territory. How do the unequal workloads of dominants and subordinates relate to their health?

We focussed on one aspect of the birds’ health: oxidative status. Previous studies have shown that hard work can increase the generation of harmful free radicals. Antioxidant defences help animals protect themselves, but if this protection is overwhelmed, oxidative stress can result. Oxidative stress is thought to be involved in many diseases and ageing.

First, we blood-sampled 93 birds before the breeding season began, to look at whether dominants (the hard-workers) had better oxidative states than subordinates, with stronger antioxidant protection and lower oxidative damage. We found that, in fact, there were no differences between dominants and subordinates in oxidative states before breeding.

Next, we sampled the same 93 birds after their long breeding season, to examine whether the dominants’ hard work during the intensive six months of breeding left them exposed to oxidative stress. After the breeding season, we found that dominant females (the hardest workers) were suffering from weakened antioxidant protection, compared to their subordinates.

Our study suggests that differences in oxidative status may not lead to differences in work-rates, but that unequal sharing of workloads in animal societies can leave the hardest-workers with poor antioxidant protection. This could leave those working hardest at higher risk of poor health, and could lead to accelerated ageing.

Image caption: Female white-browed sparrow weaver in an Acacia tree. Credit Dominic Cram.
This article can be found here.

 

Is the energy expenditure of free-living animals linked to their metabolic costs at rest?

Jorg Welcker, John R. Speakman, Kyle H. Elliott, Scott A. Hatch and Alexander S. KitayskyKittiwakes breeding at the study site on Middleton Island, Alaska, USA. Photo  by Jorg Welcker.

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Reproduction is energetically costly and the overall rate at which animals expend energy is usually highest when they rear their young. The overall rate of energy expenditure integrates the energy an animal spends to raise its offspring and to keep its own body up and running. The resting metabolic rate, on the other hand, measures the minimal energetic cost to an animal at rest to maintain its body tissues.

A widespread assumption is that an increase in parental energy expenditure requires a concurrent increase of the resting metabolic rate as higher energy intake and expenditure would need to be facilitated by larger or metabolically more active internal organs such as the heart, liver or alimentary tract. Larger or costlier metabolic machinery would, in turn, result in higher resting energetic costs. However, if changes in resting and overall energy expenditures were not inherently linked, it could be beneficial for animals to reduce their resting energetic costs as they could thus increase the amount of energy spent on raising young.

We examined whether this might be the case in free-living kittiwakes. We manipulated the energy demands of parents by increasing the number of chicks in their nests or by removing entire broods. We also manipulated energy supplies by providing some nests with supplemental food.

We found that overall and resting metabolic rates were not inherently linked: birds that raised chicks had higher overall energy expenditure yet lower resting metabolic costs compared to birds that had their broods removed. Overall energy expenditure was constrained as neither parents of enlarged broods nor those provided with unlimited food spent more energy than controls. Thus, our results suggest that reducing resting energetic costs is a strategy to increase the amount of energy allocated to raising young when overall energy expenditure is constrained. The increase in energy allocated to chick rearing caused higher levels of stress incurred by parents, suggesting that such a strategy might be costly to the parental birds.

Image caption: Kittiwakes breeding at the study site on Middleton Island, Alaska, USA. Photo by Jorg Welcker.
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.

 

Less is more: choosy wasps used in biological control show why a diverse diet is not always an asset.

Silvia Rossinelli and Sven Bacher Parasitic wasp searching for its leafminer host.

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The question of why species should specialize, i.e. use only a fraction of all resources available to them, has puzzled scientists and non-scientists alike. The proverbial saying "the Jack of all trades is master of none" provides an intuitive explanation. It implies that there should be a trade-off between the ability to use many different resources and the efficiency of using each single one. Thus, specialists should gain advantages on their resource compared to generalists. However, empirical tests so far have had problems showing such trade-offs and their importance for the evolution of specialization is still debated.

Parasitic wasps are one of the largest insect groups with maybe more than 1 million species. They parasitize other insect species by laying their eggs upon or inside the host’s body, where hatching larvae develop and eventually kill the host. For about 100 years, parasitic wasps have been widely used for the biological control of insect pests worldwide. Within this insect group all degrees of diet breadth are found, however, narrow host ranges prevail.

We analysed the history of parasitic wasps that were released to control pest insects and found that specialised wasps, i.e. those that can only parasitize a few pest species, establish better than generalist species with a wide host range. Thus, this is the most comprehensive test for the hypothesis that specialists are generally better able to use their hosts than generalists. The results provide the first robust support for the general importance of trade-offs in the evolution of specialization in the mega-diverse group of parasitic wasps. However, specialization is not always more advantageous; in environments where the preferred host is not always available, generalists will profit from being able to utilise a variety of different hosts.

Image caption: Parasitic wasp searching for its leafminer host.
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.

 

Food jumpstarts feather moult.

Raymond M. Danner, Russell S. Greenberg, Julie E. Danner and Jeffrey R. WaltersA swamp sparrow moulting throat, face, and crown feathers in eastern North Carolina.  Photo by Jeff Lewis, used with permission.

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Moulting (periodic loss of old feathers and growth of new ones) is critical for many bird species, but it costs both time and energy. Moulting may interfere with other important activities, such as breeding, migration, and maintaining body heat. Therefore, the timing of moult is essential for ensuring a successful year. In birds, the prebreeding moult is especially important because it may delay breeding. The prebreeding moult is also when males of many species acquire colourful plumage that is important for attracting mates and competing with other males.

The end of the winter is a lean time for many birds because food resources have been depleted since the previous fall. We hypothesized that the scarcity of food in late winter inhibits the initiation of prebreeding moult. We experimentally tested, for the first time, if food abundance influences the timing of moult in the wild. We conducted a controlled food supplementation experiment on free-living swamp sparrows (Melospiza georgiana) preceding and during the time of natural prebreeding moult (January–March 2009, 2010).

Supplemented birds began moulting the body, face, and crown earlier than control birds (11, 14, and 8 days earlier, respectively) indicating that food abundance limits the initiation of moult. Along with interannual variation in moult timing, these results indicate that day length is not the sole cue for moult initiation. Both control and supplemented birds moulted in sequence, starting with the body, followed by the crown 9 days later, and the face 11 days later. The presence of a sequence further suggests energetic limitation of moult or possibly a strategy to moult specific regions first to ensure completion at an optimal time.

This study provides novel experimental evidence that food abundance can limit moult timing in the wild. Food limitation of moult timing could affect the timing of breeding or feather quality, and thus cascade through other life history stages in the annual cycle and ultimately affect reproductive success. These results indicate that food availability is a cue for moult initiation, possibly acting secondarily to photostimulation.

Image caption: A swamp sparrow moulting throat, face, and crown feathers in eastern North Carolina. Photo by Jeff Lewis, used with permission.
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.

 

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.

 

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.

 

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.

 

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.

 

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.

 

Changing drivers of species dominance during tropical forest succession.

Madelon Lohbeck, Lourens Poorter, Miguel Martínez-Ramos, Jorge Rodriguez-Velázquez, Michiel van Breugel & Frans BongersThe study area in Chiapas, Mexico, where the landscape consists of a mosaic of agricultural fields, young secondary forest and old secondary forest.

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Tropical forests are celebrated for their high aboveground biomass and high tree diversity. Here we study secondary succession: the process of forest recovery after complete clearance of the vegetation for agriculture. This represents a natural gradient of biomass and diversity build-up. As the forest grows back over time, some of the species that are present in the forest manage to attain high biomass and become dominant, whereas other tree species remain rare. We ask whether such dominance is related to the characteristics of the species (functional traits) and what mechanisms drive species dominance. Is it environmental filtering, i.e. does the environment select for specific types of trees? Or is it limiting similarity, i.e. successful species tend to be specialists that differ from other dominants?. We answer these questions by studying tropical secondary forest in Chiapas, Mexico.

We found that in young forests with low overall biomass the trees that are dominant, even if they are from different species, all have similar light capture strategies. Thus at this stage the main mechanism explaining dominance is environmental filtering: only species with a specific strategy are best adapted to the prevailing (high light) conditions and will dominate the young forest. As the forest gets older, biomass increases and a dense canopy prevents sunlight from entering the understory. The fierce competition for light means that trees need to specialize to make optimal use of different light-niches to be able to thrive here. Now dominant species need to be different from each other in terms of their light-capture traits, a mechanism known as competitively-driven limiting similarity. By exhibiting different strategies many species are able to co-exist in an environment that is increasingly packed by trees and limited in resources such as light.

During the first 25 years after agricultural abandonment the importance of environmental filtering as a driving force fades away rapidly and the importance of light gradient partitioning for species dominance starts to emerge. Understanding what factors shape species dominance is relevant as mainly the large dominating trees in an ecosystem determine how the forest functions.


The article is available here.

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