Lay Summaries

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

Lay summaries for the current issue, including our new Special Feature: Advances and challenges in the study of ecological networks.

 

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.

 

Oxidative stress reduces song rate in subordinate individuals

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

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

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

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

 

Robustness of insect-flower networks to disturbance

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

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

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

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

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

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

 

Does water shortage generate water stress?

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

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

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

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

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

Image caption: Experimental plot in the Mediterranean rangeland of study (Larzac Causse, South of France).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

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

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

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

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

Image caption: 1-species (Norway spruce) and 5-species forest plot (Norway spruce, Scots pine, hornbeam, oak, birch) in the exploratory platform site of the FunDivEUROPE project in Białowieża, Poland. Photo Credit: Dawid Zieliński.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Commentary

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

Lewis G. Halsey Photograph provided by authors.

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

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

 

Treadmill endurance predicts how far salamanders move in the wild

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

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

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

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

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

 

Juvenile concentrations of IGF-1 predict life-history trade-offs in a wild mammal

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

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

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

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

Image caption: Hyena mother with cubs.
Read the article in full here.

 

Compounded perturbations in coastal areas: contrasting responses to nutrient enrichment and the regime of storm-related disturbance depend on life-history traits

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

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

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

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

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

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

 

Heating the superorganism: Comprehensive metrics of thermal performance

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

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

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

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

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

 

Parents protect offspring from negative effects of UV-B radiation

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

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

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

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

 

Seasonal transitions and aggressive phenotypes

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

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

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

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

Image caption: Siberian hamsters in long “summer-like” days (left) exhibit thin, brown/grey coats and display low levels of aggression despite have high levels of oestradiol. In contrast, hamsters in short “winter-like” (right) days exhibit thick white coats and are highly aggressive despite having low levels of oestradiol. Short-day hamsters compensate for low hormone sources during the winter by increasing sensitivity in areas of the brain associated with aggression, but not reproduction. Photo credit: JM Ho.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

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

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

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

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

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

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

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

 

Thermal over predation benefits of enclosed vs open nests

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

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

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

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

Image caption: Blue-naped Chlorophonia (Chlorophonia cyanea) sitting on its nest in Venezuela. It builds a nest of moss and rootlets that is enclosed on all sides except the opening (photo by T. E. Martin).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Mothers increase yolk oestrogen levels and the production of female offspring across the nesting season

Amanda W. Carter, Rachel M. Bowden, Ryan T. Paitz Mothers increase yolk oestrogen levels and the production of female offspring across the nesting season .

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Moms can permanently affect the phenotype of their offspring through a variety of causes termed “maternal effects,” (e.g., health during gestation affecting offspring growth rates, or the amount of care provided to young after birth impacting offspring stress). Maternal effects can help match the phenotype of the offspring to the offspring’s environment to enhance fitness, but sometimes the phenotype that is most advantageous differs between sons and daughters. Therefore, conditions that enable females to either directly manipulate the sex of their offspring or match maternal effects to a predictable pattern of sex ratio variation would be advantageous.

We investigated the ability of red-eared slider turtles to match maternal effects to offspring sex. Turtles are a great system for investigating sex-specific maternal effects because females transfer steroids to the eggs which may affect hatchling phenotype, including sex. In our species, females deposit higher concentrations of oestrogens in late season eggs, compared to early season eggs, which could result in a seasonal sex ratio shift. Also, in many turtles, incubation temperatures determine whether offspring develop as male or female. Turtle nest temperatures fluctuate daily, however, and we don’t know how even slight increases in fluctuating temperatures, as would occur across the nesting season, affect sex determination.

We collected turtle eggs early and late in the nesting season and incubated them under fluctuating incubation temperatures. We found that late season eggs, which contain higher concentrations of maternally derived oestrogens, are more likely to produce female hatchlings than early season eggs. Combined with even a slight increase in incubation temperature (0.5°C), late season eggs produce up to 49% more female hatchlings than early season eggs.

These findings demonstrate a seasonal shift in sex ratios driven by maternal effects and subtle increases in incubation temperatures. This predictable pattern of sex ratio variation creates the potential for sex-specific maternal effects mediated by oestrogens, and furthers our understanding of how moms may influence offspring.

Image caption: Mothers increase yolk oestrogen levels and the production of female offspring across the nesting season .
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 wind, the wind, the heaven-born wind! Forest windthrow effects on soil carbon dynamics

Mathias Mayer, Hans Sandén, Boris Rewald, Douglas L. Godbold, Klaus KatzensteinerImage provided by authors.

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Forests are the predominant terrestrial sinks for atmospheric carbon dioxide (CO2). However, forest disturbances, such as insect attacks or windthrows (from storm events) can negatively affect the carbon (C) balance of a forest ecosystem. Climate change is likely to intensify these disturbance regimes in the future. A precise quantification of disturbance effects on the C dynamics of forests is key to lower uncertainties of their C sink capacities.

Soils are the largest C pool in forests and the CO2 efflux from soils represents the largest C flux to the atmosphere. Our understanding of how forest disturbance affects the sources of soil CO2 efflux, namely autotrophic (from roots and associated microorganisms) and heterotrophic soil respiration (from decomposition of dead organic matter), is however poor.

In this study we investigated the impact of forest windthrow on the sources of soil CO2 efflux, underlying biotic and abiotic drivers (i.e. plant community composition, soil organic matter properties and soil temperature and moisture), and consequences for soil organic C stocks in a temperate forest ecosystem in the European Alps.

We found that windthrow had no obvious effect on soil CO2 efflux in the first years after disturbance, because a reduction in autotrophic soil respiration was offset by a ~60% increase in heterotrophic soil respiration. Since all trees were blown over at the research site, an increase in heterotrophic soil respiration was principally related to higher soil temperatures. Autotrophic soil respiration was mainly driven by grasses and herbs rather than young trees in the first six years after disturbance. However, abundant symbiotic soil fungi (ectomycorrhiza) suggests an important indirect tree contribution to autotrophic soil respiration after windthrow. Soil C stocks significantly declined over the post-windthrow period.

Our results show that heterotrophic soil respiration was by far the dominant source of soil CO2 efflux after forest windthrow. Since C losses from heterotrophic soil respiration and soil organic C stocks were of the same order of magnitude, this study demonstrates that a decline in soil C stocks after windthrow was mainly driven by a temperature-related increase in heterotrophic soil respiration and thus decomposition.

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

 

Shade tolerance and the functional trait – demography relationship in temperate and boreal forests

Aitor Ameztegui, Alain Paquette, Bill Shipley, Michael Heym, Christian Messier and Dominique GravelImage provided by authors.

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Although shade tolerance is a fundamental concept in forest ecology, its definition is complex, and there is still open debate about what confers the ability of species to withstand shade conditions, and how shade tolerance is related to growth and mortality. Here, we hypothesize that shade tolerance can be achieved by alternative combinations of traits depending on the type of tree (deciduous vs. evergreen), and that its relationship with growth and mortality will also vary across these groups. We collected data on 48 tree species (23 evergreen and 25 deciduous species) from 10 sites in temperate or boreal forests across 4 continents. We identified the main traits (leaf characteristics, seed mass, wood density, etc.) that helped predict species growth and mortality, and whether these traits were related to shade tolerance. To test different hypotheses about the relationship between traits, shade tolerance, growth and mortality we used a technique called “structural equation modelling”. This technique allowed us to confirm that the traits involved in shade tolerance are different for evergreen than for deciduous trees, making an interesting contribution to the debate on the nature of shade tolerance. For instance, according to our results shade tolerance may be a good example of convergent evolution, that is, the parallel adaptation of evolutionarily distant species to the same condition (shade) but possibly using different strategies. Moreover, if researchers want to use shade tolerance as a predictor of forest dynamics and species coexistence, they should first be sure about the role it plays in the demography of the species under study.

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

 

Honest floral colour change to maintain a long-lasting relationship with pollinators

Takashi T. Makino and Kazuharu Ohashi A bumblebee collecting nectar from an artificial flower. (photo by Takashi T. Makino).

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Floral colour change, reported in hundreds of plant species, is a well-known example of ‘honest signalling’ in plant–pollinator interactions. It occurs in fully turgid flowers, and usually correlates with a cessation of reward production (such as nectar) in individual flowers. The question is “Why do these plants honestly tell pollinators which flowers are rewarding?” In previous studies, the trait has been considered a plant strategy that enhances distant pollinator attraction, while minimizing visits to non-reproductive flowers at close range.

Here, we propose an additional benefit of floral colour change, which emerges when we consider the spatial learning ability of pollinators to avoid unprofitable plants. If a plant retains rewardless flowers without colour change, it is difficult for pollinators to visually locate the rewarding flowers. Although the enhanced display initially attracts more pollinators, its low profitability for foraging may discourage them from returning to the plant. This plant-level avoidance resulting from rewardless flowers may be prevented by floral colour change because it helps pollinators to find rewarding flowers. To test this possibility, we observed the behavioural changes of bumblebees foraging in an array of artificial plants.

We found that the retention of rewardless flowers without colour change could initially attract bees by increasing the plant’s display size, but their lack of reward resulted in plant-level avoidance by those bees that used spatial memories when choosing plants. The colour change in rewardless flowers, in contrast, encouraged bees to return by helping them to find rewards on plants. Consequently, honest plants with floral colour change received more visits by bees than those dishonest plants that did not display colour change. Floral colour change thus can prevent plant-level avoidance, and thereby enable plants to maintain a long-lasting relationship with experienced pollinators. For employing learning pollinators such as bumblebees, honesty may be the best policy.

Image caption: A bumblebee collecting nectar from an artificial flower. (photo by Takashi T. Makino).
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 structure of flower-visitor networks in relation to pollination across an agricultural to urban gradient

Panagiotis Theodorou, Karoline Albig, Rita Radzevičiūtė, Josef Settele, Oliver Schweiger, Tomás E. Murray and Robert J. PaxtonImage provided by authors.

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Pollination is a major ecosystem service in which insects play an important role for the reproduction of most flowering plants, including crops. Among the major threats to insect pollinators, and consequently pollination services, is land use change. However, few studies have addressed the relative effects of (i) local habitat and (ii) anthropogenic land use on local plant-flower visitor community structure, the architecture of flower-visitor mutualistic networks and potential knock-on effects for the ecosystem service of pollination.

In our study, we performed a landscape-scale experiment using insect pollinator-dependent plant communities as ‘pollinometers’ and empirically examined the relative effects of local and landscape drivers on pollination. Using a statistical technique termed Structural Equation Modelling to analyse our empirical data, we found that plant-flower-visitor communities and their mutualistic networks were largely influenced by local factors. In addition, there were positive and correlated effects on the ecosystem service of pollination of (i) increasing urbanization in the surrounding landscape, (ii) flying insect abundance and (iii) bee richness. Yet, we surprisingly found that mutualistic network metrics were themselves largely independent of pollination service provision.

Our findings show that, in moderately urbanized areas providing rich floral resources, positive effects on both bee richness and plant reproduction can be observed. From a theoretical perspective, it is noteworthy that we did not find a relationship between flower-visitor network metrics and pollination of four experimental plant species, challenging the notion that flower-visitor networks can be used as surrogates for the ecosystem service of pollination. From an applied perspective, and as cities expand worldwide, the strong effects of local habitat on pollinator communities further emphasize the potential for local management as a tool for biodiversity conservation in urbanized areas.

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

 

To bask or not to bask? Lizards do not follow current theory

Christine H. Basson, Ofir Levy, Michael J. Angilletta Jr., Susana Clusella¬TrullasBasking lizard. Image provided by authors.

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One means by which lizards can maintain favourable body temperatures is by thermoregulating. For example, they can shuttle back and forth between sites with sun and shade. However, depending on the availability and distribution of favourable sites, basking may become a costly activity. Longer distances or more time spent moving and searching for optimal sites should involve higher energetic costs. According to theory, lizards should abandon searching for favourable sites when the costs of doing so surpass the benefits and when this net difference is higher than when lizards passively track their surrounding temperatures. In this study, we compared data from a virtual (computer-simulated) lizard that either used an optimal behaviour by maximizing the net benefit of shuttling between available basking sites or used a passive behaviour. We simulated two environments: a ‘poor’ environment which only had one suitable basking site versus a ‘good’ environment which had multiple basking opportunities shifting throughout the day. We then compared the results of these simulations to the results for real lizards placed in experimental arenas with a single or multiple basking sites in the laboratory. Surprisingly, we found that our real lizards do not follow the predictions of the theoretical model. In both environments, lizards searched for basking sites despite the high costs of doing so in the ‘poor’ environment. We revealed that costs were associated with missed opportunities, such as less time available to explore the arena, rather than costs associated with energy spent moving between basking sites. These results highlight that the prediction of thermoregulatory behaviour, to bask or not to bask, depends on the complexity of the habitat mosaic formed by sun and shade sites in the landscape. Flat arid areas, deserts or dense tropical forests are likely to impose high energetic costs if optimal sites are scarce, while temperate and more variable environments may impose non-energetic costs, such as missed opportunities.

Image caption: Basking lizard. 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.

 

Stay cool or warm up? Individual differences in energy-saving have consequences for survival and reproduction

Melanie Dammhahn, Manuelle Landry-Cuerrier, Denis Réale, Dany Garant and Murray M. HumphriesEastern Chipmunk (Tamias striatus).

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Energy is in short supply for most animals. Therefore, individuals have to find a balance between investing energy into growth, body maintenance and reproduction. During times of food scarcity and unfavorable temperatures many mammals go “on stand-by” and reduce their energy and water requirements by entering into torpor, a reversible state of reduced body temperature, metabolism and activity. Here, we asked whether individual variation in torpor use has consequences for survival and reproduction. We recorded body temperature of individuals of free-ranging eastern chipmunk (Tamias striatus), a small squirrel species that hoards food in a burrow and hibernates during winter. Using small temperature loggers, placed around the neck of animals, we continuously recorded skin temperature over the whole winter. We found that individuals of the same population differ from each other in how much torpor they use on average over the winter, even though they are exposed to similar environmental conditions. This among-individual variation had consequences for winter survival and reproductive success in the following breeding season. Individuals using less torpor at the beginning of the winter had decreased survival in resource-rich but not in resource-poor years, and higher reproductive success in the subsequent breeding season. Thus, whether it is beneficial for an individual chipmunk to stay cool and save energy, or to warm up and reduce the costs of torpor and prepare for reproduction, depends on local environmental conditions. Since individuals are the target of selection, we think that considering individual variation in eco-physiology can contribute to a more thorough understanding of the evolution of energy-saving strategies in mammals.

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

 

Functional traits of marine macrophytes predict primary production

Holger Jänes, Jonne Kotta, Merli Pärnoja, Tasman P. Crowe, Fabio Rindi and Helen Orav-KottaImage provided by authors.

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Large seaweeds and higher plants (macrophytes) are commonly found in coastal marine habitats where they photosynthesise i.e. they build up their own organic compounds by using the sun’s energy. Primary production underpins aquatic food webs, plays an important role in the global carbon cycle and connects the life from surface ocean layers with the species at the seabed. However, the rate of primary production can greatly vary between species, communities, ecosystems, seas and oceans, simply because species differ in terms of their functional setup and oceans in their environmental settings. Here we investigated the possibility to link functional traits (i.e. biological characteristics) of macrophytes from the major European seas to primary production and we asked if there were specific functional traits that could be effectively used to predict primary production of macrophyte communities.

We first measured primary production of macrophyte communities and then quantified how large fractions of the total community biomass different traits compose. By linking community production and trait information we found out that primary production mostly depended on the amount of large epilithic seaweeds of marine origin in the community. Interestingly, we also found that several traits were clustered together meaning that the occurrence of one trait increased the likelihood of another. Our findings suggest that functional traits of macrophytes can be effectively used to monitor primary production. Furthermore, taxonomically distinct species might possess similar traits meaning that functional aspects of ecosystems can be analysed without extensive taxonomic knowledge. This could result in simplification of the general procedure of production estimations and establish transparent framework how to link community structure with functioning.

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

 

Are certain types of plumage colours more likely to differ between males and females?

Kaspar Delhey & Anne PetersImage provided by authors.

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In many birds males and females show different colours and often males are more colourful than females, a phenomenon called sexual dichromatism. More colourful males are generally favoured by females. But why would females choose males based on their colours? One hypothesis states that females choosing colourful males are selecting mates of higher quality. Consequently, sexual selection should lead to the elaboration of colours that honestly signal quality and these should be more sexually dichromatic.

Certain types of plumage colours, for physiological reasons, may constitute better signals of male quality. Among these are carotenoid-based colours. Carotenoids are yellow to red plant pigments that animals need to ingest in their food and which also play important roles in immune function and health maintenance. These links with food and health, which are particularly strong for red carotenoids, make them good candidates to be sexually selected and dichromatic. Other pigments, such as melanins, are produced within the body and are considered cheaper to produce. Colours can also be produced by the interaction between light and feather microstructure, known as structural colours, which often have blue, violet or ultraviolet hues.

Here we quantify sexual dichromatism for colours produced by different mechanisms (including carotenoids) in a large sample of Australian birds. By measuring plumage colours on museum specimens and using models of bird colour vision we could estimate how different male and female plumage colours look to birds.

In general, sexual dichromatism was highest when males and females had plumage coloured by different mechanisms of colour production (e.g. males by carotenoids and females by melanins). This is not surprising, since colours caused by different mechanisms are usually quite different. We also found that, as predicted, red carotenoid plumage had higher sexual dichromatism and that species with a higher proportion of their plumage coloured with red carotenoids showed higher levels of sexual dichromatism. However, these correlations did not explain a large amount of variation in sexual dichromatism. We conclude that knowing the mechanisms behind the different types of colours has only limited utility in predicting which colours should be sexually selected in birds.

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

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