Lay Summaries

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

 

Lay summaries for the current issue, including our new Extended Spotlight: Community Phylogenetics and Ecosystem Functioning

 

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.

 

Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context, and reproductive state

Glenn T. Crossin, Oliver P. Love, Steven J. Cooke, & Tony D. WilliamsResearchers prepare an adult Atlantic salmon (Salmo salar) for physiological manipulation in order to test predictions regarding individual variation in overwinter migration strategy. Photo by Xavier Bordeleau.

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Attempts to identify the physiological basis of life-history variation in wild animals often use an experimental increase or blocking of a particular hormone combined with observations of subsequent behaviour, breeding investment (e.g. fecundity, parental care), and survival. Experimental manipulations of ‘stress’ hormones (glucocorticoids - GC) can be very useful, but predicting their effects is often difficult. Much uncertainty can emerge given that GCs possess a dichotomous physiological role: baseline levels regulate daily energy use while higher levels mediate responses to stress. As such, the relative levels that are expressed and their interaction with life stage, ecological variation, age, and sex can differentially impact fitness.

In this Perspectives piece, we review the literature surrounding GC manipulations, discuss the potential pitfalls when designing GC studies, and make recommendations for how future studies can benefit by considering broader sets of overarching hypotheses. Ultimately, we urge researchers to consider three key points when designing experiments: the life-history context of the species under study (e.g. long- vs. short-lived, reproducing only once or repeatedly, etc.), the ecological context that it is studied in, and the choice of the most appropriate GC dose that will best test the predictions posed by the hypotheses.

Image caption: Researchers prepare an adult Atlantic salmon (Salmo salar) for physiological manipulation in order to test predictions regarding individual variation in overwinter migration strategy. Photo by Xavier Bordeleau.
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.

 

Evidence of trophic specialization in cave species challenges the usual prediction of generalist feeding in food-limited environments

Clémentine Francois, Florian Mermillod-Blondin, Florian Malard, Francois Fourel, Christophe Lécuyer, Christophe J. Douady and Laurent SimonSampling of groundwater organisms at Borne aux Cassots cave (France). Photo: Robert Le Pennec.

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The identification of feeding strategies along a specialist-generalist continuum is fundamental to the understanding of many ecological processes associated with food web structures and ecosystem functioning. Theory states that the amount of food available in a given environment influences these feeding strategies. In food-limited environments, generalist species are expected to occur because species may not be able to subsist when feeding only on a reduced set of food sources. However, species living in these poor environments often exhibit peculiar biological traits, such as improved food-finding abilities or low metabolic rates, which may release the constraints due to low food availability, and allow for specialist species even in these harsh habitats.

This paper tested this hypothesis of specialist species in food-limited habitats by focusing on two aquatic cave-dwelling water slaters (isopods within the Proasellus genus), as they live in one of the most food-limited environments on Earth. We used carbon and nitrogen stable isotopes (13C and 15N) to quantify the transfers of carbon and nitrogen from each food source to the organism.

The degree of specialization of these two isopod species was determined in the laboratory by measuring the rate at which they assimilated C and N when being fed separately with one of the 3 food sources available in caves: fine and coarse particulate organic matter (corresponding to fragments of leaves and wood of different sizes) and sedimentary biofilm (corresponding to the conglomeration of microorganisms developed on the surface of sediments). We demonstrated that both species assimilated far more (up to 10 times) C and N from the sedimentary biofilm than from both kinds of particulate organic matter, indicating a high degree of specialization on biofilm.

In parallel, the actual diets of these isopods were estimated for five populations (= five distinct caves) per species. All isopods fed predominantly on the sedimentary biofilm (representing in average 83 % of the diet), regardless of the population or species considered.

Our results showed for the first time in cave species a strong trophic specialization on the sedimentary biofilm. This evidence of specialist species in groundwater challenges the traditional view of the selection of generalist species in food-limited environments.

Image caption: Sampling of groundwater organisms at Borne aux Cassots cave (France). Photo: Robert Le Pennec.
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 does temperature affect colonies of a pollinating bumble bee?

Jacob G. Holland and Andrew F. G. BourkeInside a nest of the buff-tailed bumble bee (Bombus terrestris), complete with marked bees. Photo credit: Andrew Bourke, 2013.

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Many plants are entirely dependent on pollination by insects, but this interaction may be disrupted by predicted future climate change. Since this has the potential to create costly environmental and economic problems, it is vital that we understand how these insect pollinators respond to changes in temperature. A number of important insect pollinators live in complex social colonies, which are fundamental to almost every aspect of their biology, and yet we understand little about how these colonies are affected by temperature. We investigated this relationship using colonies of buff-tailed bumble bees, which are common in the British Isles and the rest of Europe. Bumble bee colonies develop from a single queen, but can reach several hundred individuals before producing new queens and males, which are needed to produce daughter colonies in the following year. When exposing laboratory colonies to two different temperatures (20oC or 25oC), we found that the lifespans (longevities) of individual bees were surprisingly resilient to temperature differences. However, we also found that colonies, when taken as a whole, responded in more complex ways to temperature. For example, higher-temperature colonies produced more queens and lived slightly longer, but did not differ in the timing of their growth. These findings show that it is important to consider the effects on whole colonies when predicting the responses of social bees and other social animals to environmental changes.

Image caption: Inside a nest of the buff-tailed bumble bee (Bombus terrestris), complete with marked bees. Photo credit: Andrew Bourke, 2013.
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.

 

Seed transport by physically active animals: farther than we think?

Casper H.A. van Leeuwen, Rosanne Beukeboom, Bart A. Nolet, Elisabeth S. Bakker, Bart J.A. PolluxCarp in tank. Photo provided by authors.

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Seeds enable plants to spread within and between patches of suitable habitat. Wind and water often transport ripe seeds to new places. However, also animals can be vectors for seeds: many animals feed on nutritious seeds or fruits, but do not completely digest all the ingested food. Numerous plants produce seeds that can still germinate after multiple hours of retention in the digestive system of animals. In case animals defecate these seeds after they have moved to a new location, plants may spread into new suitable habitat.

To estimate the impact of this dispersal mechanism on ecosystems, we need to estimate how far animals might be able to transport seeds. This largely depends on how long it takes before an ingested seed is defecated again. This is often determined experimentally by feeding animals with a known quantity of seeds, followed by monitoring seed retrieval over time. However, up until now, almost all these experiments have been performed with animals resting in cages, while animals dispersing seeds in the wild will be actively moving elsewhere by either swimming, walking or flying. We hypothesized that seed digestion in resting animals would be different than in animals engaged in the physical activity involved in moving to new habitat.

In our study we therefore compared seed retrieval patterns between animals that were resting in a cage, and actively swimming animals. We used common carp as a model species, as fish are increasingly recognized as important seed dispersers in rivers, particularly for plants colonizing upstream habitat. Physically active fish were found to retain ingested seeds for up to two hours longer than resting fish. This implies fish may transport seeds many kilometres further upstream in river systems than previously estimated. We expect that also in other seed dispersing animals physical activity will influence their seed digestion, and emphasize that this should be taken into account when making predictions of the impact of seed dispersal by animals on ecosystems.

Image caption: Carp in tank. 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.

 

What can we predict about a forest based on the sizes of its trees?

Kristina J. Anderson-Teixeira, Jennifer C. McGarvey, Helene C. Muller-Landau, Janice Y. Park, Erika B. Gonzalez-Akre, Amy C. Bennett, Christopher V. So, Norman A. Bourg, Jonathan R. Thompson, Sean M. McMahon & William J. McSheaImage provided by authors.

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Numerous characteristics of trees vary predictably with trunk diameter. These include height and other dimensions, water use, growth rate, mortality rate, and abundance. The mathematical descriptions of these relationships, known as “scaling relationships”, are broadly useful for understanding forests globally and their role in Earth’s changing climate system. Characterizing scaling relationships and understanding the underlying mechanisms are therefore of great value.

This study, which was conducted in a forest at the Smithsonian Conservation Biology Institute, Virginia, characterized scaling relationships for a broad suite of tree characteristics. Field measurements were used to quantify how tree height, crown dimensions, water use, growth rate, mortality rate, and abundance related to trunk diameter. To put results from this forest in a global context, corresponding scaling relationships observed in forests throughout the world were reviewed. All of these results were used to evaluate the consistency of observed scaling patterns in forests with the predictions of ecological theory.

Results show that existing ecological theory had mixed success at predicting scaling patterns in forests. Some tree characteristics, such as height, were relatively well explained by theoretically predicted scaling relationships. However, scaling relationships for some other characteristics, such as growth rate, deviated meaningfully from theoretical predictions, pointing to mechanisms that have not yet been accounted for. Scaling patterns also varied among tree species and were affected by environmental variation. These findings reveal that while existing ecological theory can often provide reasonable approximations of scaling patterns, a more nuanced understanding of scaling in forests will be important to characterize forest structure and function with sufficient precision to address some of the most pressing questions in forest ecology. In particular, a more refined understanding of scaling in forests will be invaluable in the current era of global change, when understanding how forests are changing and interacting with Earth’s climate is important for both forest conservation and climate change mitigation.

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.

 

Big, warm woodlice “chill out”, rather than cross a habitat corridor

Andrew D. Barnes, Ina-Kathrin Spey, Lena Rohde, Ulrich Bros, and Anthony I. Dell Camera system (left) within the environmental chamber used to film woodlice as they move around an experimental fragmented landscape (right, blue line indicates woodlice trajectories), also seen at the bottom of the filming chamber. Woodlice movement patterns can then be automatically tracked and analysed using automated image-based tracking software.

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With increasing global temperatures and habitat fragmentation, the question of whether animals will be able to cope with these environmental changes becomes increasingly important. Species are already tracking rising temperatures by moving to cooler latitudes or elevations in order to remain in their preferred temperature ranges. However, the ability of species to do this is hindered by habitat fragmentation. One possible solution is to create dispersal corridors that link habitat fragments, thus allowing animals to move more easily across the landscape. This gives rise to another important question: will changes in temperature alter the way animals use corridors?

Theory and data suggest that larger and warmer animals should be more active, thus suggesting that larger, warmer animals should encounter habitat corridors more often. To test this, we used novel automated methods to track the movement of different sized woodlice around a fragmented experimental landscape at temperatures ranging from 15 to 25 ºC. By quantifying the movement and behavior of individuals (e.g., mean and maximum body velocity, the proportion of time spent moving, corridor encounter rate), together with overall corridor crossing rates, we were able to isolate the biological mechanisms driving the relationship between body size, temperature, and corridor use.

Surprisingly, our results showed that warmer and larger woodlice moved more slowly and crossed corridors less often than colder and smaller woodlice. We also found that the woodlice which moved more often crossed habitat corridors less than the less active woodlice. We explain these counterintuitive findings by individual variability in behavioural responses to warming. Our results suggest that individual behaviour plays a key role in determining how animals use habitat corridors, making the story more complicated than might be expected from general theory, such as a general metabolic response to rising temperature. Understanding this story becomes more critical as global temperatures continue to rise and landscapes become ever more fragmented.

Image caption: Camera system (left) within the environmental chamber used to film woodlice as they move around an experimental fragmented landscape (right, blue line indicates woodlice trajectories), also seen at the bottom of the filming chamber. Woodlice movement patterns can then be automatically tracked and analysed using automated image-based tracking software.
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.

 

Nitrogen saturation in humid tropical forests after 6 years of nitrogen and phosphorus addition: hypothesis testing

Hao Chen, Geshere A. Gurmesa, Wei Zhang, Xiaomin Zhu, Mianhai Zheng, Qinggong Mao, Tao Zhang, Jiangming MoAn old-growth tropical forest. Photo credit: Yunting Fang.

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Nitrogen (N) deposition is increasing globally causing N-saturation, where N input to forests exceeds plant and microbial demand. It has been hypothesized that this N saturation will cause increasing N leaching, nitrous oxide (N2O) emission and N transformation rates and cause limitation of other elements. However, this hypothesis has commonly been tested in temperate forests, but it is not well tested in N-saturated tropical forests.

To test this hypothesis, we measured soil inorganic N, soil N mineralization and nitrification rate, soil N2O emission rate, and nitrate (NO3-) leaching rate in an N-saturated old-growth tropical forest in south China after 6-years of N and phosphorus (P) addition.

The results showed that N addition indeed caused further N saturation, as indicated by a significant increase in soil inorganic N, N2O emission and nitrate leaching after N addition, however, N addition significantly decreased in situ rates of net N mineralization and nitrification. On the other hand, P addition significantly decreased soil inorganic N concentration, N2O emission and NO3- leaching, but it significantly increased the net rates of N mineralization and nitrification.

Our study showed that long-term N deposition in tropical forest may not induce N-saturation symptoms as observed for temperate forest, and that P addition can alleviate N-saturation in such tropical systems; hence it provides new insight into the N-saturation hypothesis.

Image caption: An old-growth tropical forest. Photo credit: Yunting Fang.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Arboreality and associated gravitational stress on blood circulation have influenced the evolution of tail length in snakes

Coleman M. Sheehy III, James S. Albert and Harvey B. LillywhiteAn arboreal eyelash viper (Bothriechis schlegelii) resting on a branch in Costa Rica.  Photograph by Coleman M. Sheehy III.

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Gravity is a pervasive force that can severely affect blood circulation in terrestrial animals, and these effects can be particularly pronounced in tall or long organisms such as giraffes and snakes. Upright postures create vertical gradients of gravitational pressures within circulatory vessels that increase with depth. In terrestrial animals, this pressure potentially induces blood pooling and edema in the lower-most tissues and decreases blood volume reaching the head and vital organs.

Since their evolutionary origins about 100 million years ago, snakes have diversified into a wide variety of aquatic, burrowing, terrestrial, and arboreal habitats where they experience various levels of gravitational stress on blood circulation. At the extremes, these stresses range from low to none in fully aquatic species living in essentially “weightless” environments, to relatively high in climbing species, especially arboreal forms specialized for climbing trees. As a result, arboreal snakes exhibit many adaptations for countering the effects of gravity on blood circulation, including relatively tight tissue compartments in the tail. However, patterns of tail length in relation to arboreal habitats and gravity have not been previously studied.

We obtained length data for 226 snake species representing almost all snake families to test the hypothesis that arboreal snakes have longer tails than do non-climbing species. We found that average tail length increased and average body length decreased with increasing use of arboreal habitats and that arboreal snake species had average tail lengths 3–4 times longer than those of non-climbing species. Snakes with longer tails have a higher percentage of elongate blood vessels contained within the relatively tight skin of the tail, which counters blood pooling experienced during climbing. Total body length appears to be constrained in arboreal species, and total body length in adult female arboreal snakes appears to be an evolutionary tradeoff that favors longer tail lengths over maximum production of offspring as arboreal habitat-use increases. Our findings provide evidence that long tails of arboreal snakes function, at least in part, as an adaptation to counter cardiovascular stresses on blood circulation imposed by gravity.

Image caption: An arboreal eyelash viper (Bothriechis schlegelii) resting on a branch in Costa Rica. Photograph by Coleman M. Sheehy III.
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 wood decomposition affected by nutrients in a tropical forest?

Yao Chen, Emma J. Sayer, Zhian Li, Qifeng Mo, Bi Zou, Yingwen Li, Yongzhen Ding, Xiankai Lu, Jun Wang, Jianwu Tang and Faming WangWood decomposition patterns over time. Photo from Yao Chen.

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Tropical forests represent a major store of carbon, a large proportion of which is contained in woody plant parts. The decomposition of woody debris plays an important role in the forest carbon cycle, so understanding what controls wood decay will help us determine how much carbon may be released from wood decay in future. Previous research suggests that wood decomposition is regulated in part by the availability of nutrients. This topic has recently received much attention because nitrogen inputs from the atmosphere are increasing dramatically in tropical regions as a result of human activities. To investigate how changes in nutrient inputs will affect the decomposition of woody debris in tropical forests, we conducted a fertilization experiment using branch segments from four common tree species in a lowland tropical forest in China .

Fertilization with phosphorus increased decomposition rates whereas fertilization with nitrogen had no significant effect. We observed changes in the patterns of nutrient release from the decaying branches that highlight the importance of the balance of nutrients for decomposer organisms. Our results indicate that the decomposition of wood is primarily constrained by phosphorus availability in this tropical forest. Our study suggests that it may be possible to predict decay rates using the ratio of carbon to phosphorus in tropical woody debris. Additional work with more tree species is needed to determine whether the patterns we observed are more generally applicable.

Image caption: Wood decomposition patterns over time. Photo from Yao Chen.
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.

 

Xylem vessel traits tell the timing of leaf emergence and senescence in native and non-native understory species of temperate deciduous forests

Jingjing Yin, Jason D. Fridley, Maria S. Smith and Taryn L. BauerlePhoto of the common garden at Syracuse University, Photo by Jason D. Fridley.

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Non-native understory deciduous woody species tend to advance spring leaf emergence and delay autumn leaf fall compared to native species when growing among natives in temperate forests, whereby they can exploit temporally available resources, such as water, nutrients, sunlight and pollinators. This strategy can potentially enhance growth in non-native species, affect their distribution and abundance, and ultimately cause significant changes to native ecosystems. However, prolonged leaf display also subjects non-native species to possible disruptions in their water conducting cells, due to freezing during the periods of increased frost probability in early spring and late autumn, blocking the water-conducting pathway and disrupting normal water transport capacity. Little is known about how non-native understory species are able to maintain normal water transport for leaf display within this context.

Xylem vessels are long hollow chains of dead cells, and can carry water from roots to leaves in a plant. Earlier spring leaf emergence in temperate deciduous trees has been shown to be related to narrower xylem vessels because narrower vessels are more resistant to freezing-induced disruptions. We examined the xylem vessel traits in different developmental stages of xylem formation, i.e. metaxylem (formed before true wood), earlywood and latewood, across 82 native and non-native understory deciduous woody species common to Eastern U.S. deciduous forests, and monitored their timing of leaf emergence and senescence during 2008-2010 in a common garden.

We found that compared to the natives, non-native species possessed specific xylem vessel traits that facilitated their tolerance to frost and allowed them to extend leaf display in late autumn, such as larger metaxylem vessels, smaller latewood vessel diameter and a higher proportion of solitary vessels within early- and latewood. In the spring, native and non-native species exhibited similar dates of spring budbreak and leaf emergence, linked to their similar xylem vessel size and vessel area percentage (the proportion of xylem cross section occupied by vessels) within metaxylem and earlywood. Within both groups, species with earlier bud and leaf emergence had a higher vessel area percentage within metaxylem and earlywood, suggesting understory species need sufficient water to support their early spring growth, even at the risk of freezing-induced cavitation.

Image caption: Photo of the common garden at Syracuse University, Photo by Jason D. Fridley.
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.

 

Agriculture increases temporal variability of stream ecosystem functioning

Mikko Tolkkinen, Heikki Mykrä, Annamari Markkola and Timo MuotkaImage provided by authors.

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All biological communities exhibit variability over time but increased variability may indicate a disturbed ecosystem, even if species richness and mean rates of ecosystem functions remain unaltered. Most previous studies on temporal variability of biological communities have focused on biomass production, while variability in the rates of other ecosystem functions has gained much less attention. We measured leaf decomposition during three consecutive years in three types of headwater streams: naturally acidic streams, agricultural streams with moderate nutrient enrichment and non-impacted reference streams. Leaf decomposition is frequently used as an indicator of stream ecosystem functioning, based on the rationale that food webs of most headwater streams are fuelled by the autumnal input of leaves from riparian trees. Once in the stream, leaf litter is processed by invertebrates and microbes, particularly freshwater fungi. We surveyed the species composition of fungal decomposer assemblages on submerged alder leaves in all three stream types in each study year to test whether fungal community composition and leaf decomposition rates are more variable over time in human disturbed than in reference streams. Temporal variability of leaf decomposition was indeed higher in nutrient-enriched than in non-modified reference streams whereas human impacted and naturally acidic streams did not differ. Fungal assemblages in both agricultural and naturally acidic streams were strongly dominated by a few key species whereas non-modified reference streams supported communities with more even abundance distributions. Inter-annual variability of leaf decomposition rate was positively related to dominance, with more variability in streams where fungal assemblages were dominated by a few prominent species. Our results show that although the process rates and diversity of fungal communities are regulated partly by the same environmental factors (for example, stream water pH and agricultural nutrient enrichment), processes are more sensitive to human disturbances. We emphasize the importance of measuring not only the mean rates, but also, and perhaps even more importantly, temporal variability of ecosystem process rates in any attempt to assess the influence of human disturbance on ecosystem 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.

 

Plasticity in sexual size dimorphism

Camille Bonneaud, Erin Marnocha, Anthony Herrel, Bieke Vanhooydonck, Duncan J. Irschick and Thomas B. SmithA sagrei Bimini. Image provided by authors..

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Why do male and female animals differ in body size? Differences between males and females in body size, known as sexual size dimorphism (SSD), is one of the most fascinating and mysterious features of animals. Both different species, and different populations within a species, often vary notably in this feature, but the reasons have remained obscure. Many studies have focused on sexual selection being the primary factor driving variation in SSD. Sexual selection involves the selection of features that help to maximize reproductive success, either by attracting mates, or by outcompeting rivals of the same sex. But another possibility is that variation in resource availability, such as food, could explain much of the variation in SSD. For example, consider two populations that vary in food availability – if males and females differ in how rapidly they grow in response to increased food, then variation in food availability could explain among-population variation in SSD. We tested this hypothesis by integrating laboratory and field studies for different populations of the common Bahamian lizard Anolis sagrei. In this species, males are typically larger than females, but how much they differ varies among different populations. The Bahamas offers a wonderful test case because islands vary in size, which usually correlates with variation in food availability. We first performed laboratory studies which showed that the amount of food had a significant impact on male, but not female, growth. Then, in the field, we showed that the total amount of food biomass within an island explained variation in male, but not female, body size. Our data therefore offer a fairly simple explanation for variation within some species in SSD – namely, the amount of food available to them. This is an alternative view to the common explanation of sexual selection driving variation in SSD. Further, these findings provide support for the condition-dependence hypothesis, according to which the larger sex should display greater plasticity in growth in response to environmental conditions.

Image caption: A sagrei Bimini. 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.

 

Subordinate plants and fungi: what happens when these minorities join the effort?

Pierre Mariotte, Bjorn J.M. Robroek, Vincent E.J. Jassey, Alexandre ButtlerImage provided by authors.

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Drought events are recurrent phenomena, which are predicted to increase over the next few decades. The response of grasslands to drought seems to be determined by both species diversity and community composition. According to the diversity-insurance hypothesis, diverse plant communities have a higher chance of containing species well adapted to drought. Indeed, many experiments have confirmed a positive effect of plant species diversity on community resistance to drought, but the underlying mechanisms remain unknown.

In parallel, the subordinate insurance hypothesis suggests that highly diverse communities contain higher number of subordinate species, which are more resistant than dominant species to climate change conditions and can compensate for less resistant species. Earlier, it has been reported that subordinate species can improve grassland productivity during drought but, surprisingly, these species seemed not to possess a better physiological ability for water use efficiency. Therefore, we hypothesized that their role might be better found belowground.

Using a combination of subordinate species removal and summer drought in grassland, we show that soil processes play a critical role in the community resistance to drought. Our results highlight that subordinate species shift the balance within the soil microbial community towards more fungal dominance. Fungal communities, promoted by subordinate species, were more resistant to drought and maintained higher rates of litter decomposition and soil respiration. These results emphasize that subordinate species play an important role in mitigating drought effects on soil ecosystem functions. Reciprocal effects between fungi and subordinate species explain also how subordinate species better resisted drought conditions.

Our findings highlight interesting plant-soil feedback effects between subordinate species and fungi, which seem delayed in time following a perturbation. Indeed, we showed plant effects on soil under ambient precipitation, with subordinate plant species favoring fungal communities, followed by soil effects on plants under drought conditions, with more resistant fungal communities being able to improve the resistance and growth of subordinate species. Additionally our results extend the diversity-insurance hypothesis by showing that more diverse communities not only contain species well adapted to perturbations, but also species with higher impact on soil microbial communities and related ecosystem functions.

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.

 

Birth date predicts alternative life history pathways in a fish with sequential reproductive tactics

Teresa Fagundes, Mariana G. Simões, João L. Saraiva, Albert F. H. Ros, David Gonçalves and Rui F. OliveiraThe two alternative male morphotypes of the peacock blenny: bourgeois nest-holders (front) and parasitic female mimics (back).

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In some species individuals of the same sex, usually males, can reproduce by adopting different behaviours, depending on factors such as body size. In this paper we studied the factors that determine the alternative mating tactics that males can adopt in a littoral fish, the peacock blenny (Salaria pavo). In this species two mating tactics occur: (1) larger males defend nests in crevices to which they attract gravid females to mate with; after spawning nest-holder males provide parental care to eggs until they hatch; (2) smaller males do not express the ornaments of males and instead mimic females, both morphologically and behaviourally, in order to get access to the nests defended by nest holders, and to sneak fertilizations. Here we report a long term (6 years) mark–recapture study, which demonstrated that these alternative reproductive tactics are sequential, that is younger and smaller males may act as sneakers but as they grow older and larger all behave as nest-holders. We also found that males may follow different developmental trajectories depending on their date of birth. Males born earlier in the breeding season get to their first breeding season with a larger size than males that born later in the season. Accordingly, the former express the nest-holder tactic from their first breeding season onwards, whereas the later reproduce in their first breeding season as sneaker males and subsequently switch to nest-holders. The occurrence of a birth date effect on the expression of alternative reproductive tactics leaves room for important parental effects that should be investigated in future studies.

Image caption: The two alternative male morphotypes of the peacock blenny: bourgeois nest-holders (front) and parasitic female mimics (back).
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.

 

An invasive plant evolves rapidly in response to changes in climate

Ferran Colomer-Ventura, Jordi Martínez-Vilalta, Paolo Zuccarini, Anna Escolà, Laura Armengot and Eva Castells Plants at their native area in South Africa (left) grow under wetter and hotter conditions than those introduced into novel regions, for example Australia (right). Differences in climate are driving a rapid evolution of this invasive species. Pictures: Eva Castells.

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Biological invasions are one of the largest problems affecting biodiversity at a global scale. The study of invasive species, however, can also provide us with information on the response of organisms to a changing environment. Current hypotheses predict that invasive plants can rapidly evolve when they encounter new environmental conditions. Contemporary adaptation, which is revealed by different plant characteristics in the native and invasive plants, could facilitate the invasion process. Here we have evaluated how invasive plants respond to simultaneous changes in climate and herbivory.

Senecio pterophorus is a shrub from the daisy family native to the Eastern Cape in South Africa. This species was accidentally introduced into the Western Cape in South Africa, Australia and Europe 40-100 years ago. In their native habitats plants are subject to wetter and hotter summers than those in the introduced areas. Additionally, native plants are more attacked by herbivores than their invasive counterparts. All these differences could lead to changes in plant morphology after invasion.

Seeds collected from the native and the three non-native regions were grown in an experimental field under similar environmental conditions. We had two objectives. First, we aimed to determine whether plants from different origins were genetically distinct for some traits related to plant performance, such as growth, leaf area or reproductive capacity. Second, we aimed to determine whether climate and herbivory measured at the collection sites played a role in this genetic differentiation.

Plants from the non-native regions were smaller and had a lower reproductive output than plants from the indigenous area. Herbivory was not related to these changes in plant traits. In contrast, our results are consistent with the role of climate driving rapid evolution of the non-native plants. Understanding the mechanisms for rapid differentiation in response to novel climatic conditions improves our ability to explain the dynamics of biological invasions and also to predict the response of native populations under a climate change scenario.

Image caption: Plants at their native area in South Africa (left) grow under wetter and hotter conditions than those introduced into novel regions, for example Australia (right). Differences in climate are driving a rapid evolution of this invasive species. Pictures: Eva Castells.
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 mice select foraging site according to the extent of within-plant variability in seed characteristics

Takuya Shimada, Akiko Takahashi, Mitsue Shibata, and Tsutomu YagihashiThe Japanese wood mouse, endemic to Japan, is a major consumer of acorns. When they found acorns, they carry and hide them mostly in the ground or under fallen leaves for future use. Photograph credit: Y. Suzuki.

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In general, foods are not uniformly distributed for animals, but distributed patchily in their home range. In this situation, animals have to evaluate the quality of foraging patches and select one for foraging. An oak tree, for instance, forms a foraging patch for seed-eating rodents, where acorns (seeds of oaks) are the food resource. Characteristics of these resources often vary largely even within a foraging patch (an individual plant), which is known as within-plant variation. In such a case, how does the animal evaluate the quality of patches? One of the simple and widespread ideas is using the mean as a representative. Namely, the quality of a patch is defined as the mean of the quality of each resource (acorn), such as acorn weight or nutritional value. However, patches with the same mean but different variation may not be equal for animals. To best describe the quality of a patch, within-plant variation must be considered in addition to the mean values.

In this study, we examined which trees the Japanese wood mouse (Apodemus speciosus) would select as a foraging patch for acorns of konara oak (Quercus serrata). Here, the mean, variance (spread of values), and skewness (tendency to extreme values) of within-plant distributions of two acorn characteristics (weight and tannin content) were used as indicators of the quality of patches, and we examined the relationships between these indicators and patch selection by the wood mouse. Tannins are a bitter tasting chemical, and most animals tend to avoid tannin-rich food.

There was notable within-plant variation in acorn weight and tannin content, and significant among-individual variation was also observed. We found that wood mice preferred to forage beneath trees with a large mean and variance of seed weight and a small variance and skewness of tannin content. These findings highlight that, in order to understand ecological and evolutionary processes at work in plant-animal interactions, within-plant variation in seed characteristics must be considered as well as mean value.

Image caption: The Japanese wood mouse, endemic to Japan, is a major consumer of acorns. When they found acorns, they carry and hide them mostly in the ground or under fallen leaves for future use. Photograph credit: Y. Suzuki.
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.

 

Mechanisms and consequences of facilitation in plant communities

A portfolio effect of shrub canopy height on species richness along a competitive stress gradient

Kari Anne Bråthen and Christopher LortieImage provided by authors.

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Biodiversity is a critical resource in ecosystems both ecologically and economically for humans. It is thus a pivotal challenge for ecologists to explain and predict the biodiversity of any given ecosystem. In this study we focus on how the biodiversity of plants in tundra ecosystems can be facilitated. In tundra ecosystems plants are exposed to low temperatures and strong winds and on top of this the plants are grazed by herbivores. Consequently, the presence of dominant tundra shrubs with woody canopies can facilitate other plant species to cope with both stressful environments and presence of herbivores. These shrub canopies protect against grazing and wind abrasion, provide a protective snow layer in winter, trap particles and seeds for soil formation and new species establishment in summer, and buffer against temperature extremes. We propose that this range of positive mechanisms be termed “a portfolio effect of shrub canopy height”, and thus that the presence of higher shrub canopies increases biodiversity. We find support for our prediction. Along the entire gradient from low productivity, stressed plant communities to higher productivity, more competitive communities, we find that greater shrub canopy height promotes biodiversity. More particularly we find shrub canopy height to promote biodiversity on top of a humped-back relationship between biodiversity and plant productivity (i.e. at low and high productivity levels biodiversity is low and at intermediate productivity levels biodiversity is high), and as such we also find support for a general theory explaining biodiversity, i.e. the humped-back relationship. Climate change is currently causing encroachment of shrub species into tundra ecosystems. This study suggests that a universal theory of biodiversity is at play also in tundra plant communities, and that shrub dynamics are a crucial additional element in understanding changes in tundra plant biodiversity. It is thus likely that including the presence and height of shrub dominants will improve predictive models of biodiversity.

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.

 

Stress, immunity, and energy use in snakes

Lorin A. Neuman-Lee, H. Bobby Fokidis, Austin Spence, Marilize Van der Walt, Geoffrey D. Smith, Susan Durham, and Susannah S. FrenchA male Terrestrial Gartersnake (Thamnophis elegans).

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Wild animals undergo resource limitations throughout their lives, and must allocate this limited energy to a variety of physiological functions, such as growth, response to stress, and immune functions. In infrequent feeders, such as many snakes, shorter term limitations may not be as critical. Stressors, commonly experienced by wild animals, can also affect resource allocation “decisions” when energy is limiting. When an animal experiences stress, adrenal steroid hormones (such as cortisol in humans) are released into the bloodstream. These hormones have many functions, but chiefly mobilize energy for use in the body. When an animal is chronically stressed, it may be continuously secreting these hormones and therefore mobilizing energy. This energy usage may become detrimental, especially if no new sources of energy are available.

The objective of this study was to determine how infrequent feeders, such as gartersnakes, are affected by chronic stress and food restriction. We restricted food for six weeks in half of the animals in the study and chronically stressed half of the animals (half food restricted and half not) using restraint stress. At the end of the experiment, we measured energy metabolites (triglycerides, glycerol, protein, and ketone) and compared the metabolite levels to two physiological measurements (immune and stress response). Food restricted animals did not lose significant amounts of body weight over the six week period, but did have altered levels of the energy metabolites triglyceride and glycerol. Also, chronically stressed animals responded by releasing significantly greater amounts of adrenal steroid hormones during acute stress than animals not chronically stressed. Finally, chronically stressed snakes had a reduced ability to heal wounds and a combination of both food restriction and chronic stress resulted in suppressed innate immune function. This study provides evidence that energetic limitation and stress can result in interactive and dramatic changes in energy usage and storage as well as in physiological functions that are critical to maintain life.

Image caption: A male Terrestrial Gartersnake (Thamnophis elegans).
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.

 

Preferred nest-sites help female song sparrows successfully raise chicks in early spring conditions

Ryan R. Germain, Richard Schuster, Kira E. Delmore, and Peter ArceseFemale song sparrow searching for nesting material. Photo credit: Sylvain Losdat.

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Choosing the right location to raise offspring can have important consequences for an individual animal’s overall reproductive success. For North American songbirds that build open-cup nests in the potentially harsh conditions of early spring, breeding in higher quality habitat can reduce some of the costs associated with producing and caring for their young. With the potential hazards of early spring breeding like cold temperatures and heavy rainfall, come the rewards of greater offspring survival and more future nesting opportunities for the parent. Thus, any advantages available to breeding birds during this crucial reproductive stage could lead to important benefits over both the entire year, and their lifetimes.

We used 38 years of nesting records from an island song sparrow (Melospiza melodia) population to determine the relative influences of preferred, high-quality nest-sites on early spring reproductive success. We found that females that used these preferred sites tended to lay their eggs earlier in the season, incubated their eggs more efficiently, and produced chicks that were more likely to survive and become breeders in the population the following year. We also investigated potential cues (relative warmth and food availability) by which female sparrows may select early season nest-sites. Preferred nest-sites were relatively cooler overall, likely due to greater vegetation cover than less-preferred sites, but also had indicators of greater caterpillar abundance, a key food source during the early spring. Our findings show that breeding in preferred, high-quality habitat may offer female sparrows a reproductive advantage by allowing them to produce and care for their young at a lower energetic cost to themselves. These results provide clear evidence of the importance of habitat quality on the success of animals living in seasonal environments.

Image caption: Female song sparrow searching for nesting material. Photo credit: Sylvain Losdat.
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.

 

Moving Beyond Body Condition Indices as an Estimate of Fitness in Ecological and Evolutionary Studies

Shawn M. Wilder, David Raubenheimer and Stephen J. SimpsonCallipers used for measuring. Photo provided by authors.

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Ecologists, physiologists and evolutionary biologists are often interested in measuring the state or condition of animals. One shortcut that has been taken to estimate condition is the use of body condition indices, which measure the mass of an animal relative to frame or skeleton size. For example, in humans, the Body Mass Index (BMI; mass / height2) has been used as a body condition index. However, BMI is only a coarse measure of body composition and people with the same BMI can have very different body composition (e.g., weight lifter vs. obese person). Similarly, body condition indices used in ecological and evolutionary studies of a range of other animals are coarse or poor estimates of body composition (e.g., the relative amounts of lipid, protein and other components of the body). Another problem with body condition indices is that they are often used as a surrogate for body lipid content. The lipid content of an animal can be important for health or fitness but there are many other characteristics that could also be related to health. Furthermore, high body condition values are often assumed to reflect high health or fitness. However, as we know from studies of humans, individuals with intermediate condition index values may have higher health or fitness than individuals with very high (e.g., obesity) or low (e.g., malnutrition) values.

As a consequence of these problems with condition indices, we argue that biologists should abandon body condition indices in favor of more descriptive or detailed measures of the physiology or composition of animals. Methodological advances have resulted in a range of techniques to accurately measure many aspects of animal physiology and composition, including many noninvasive techniques. For example, in humans and many other animals, dual-energy x-ray absorptiometry can be used to provide an accurate and noninvasive measure of body lipid, lean mass and skeleton content. More accurate data on animal physiology and composition will provide us with a better understanding of the ways in which animals respond to their environment and the connections between behavior, physiology and ecology.

Image caption: Callipers used for measuring. 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.

 

Jack of all foods or master of one: symbiotic bacteria determine the diet of an insect pest

Steven M Wagner, , Adam J. Martinez, Yong-ming Ruan, Kyungsun L. Kim, Paul A. Lenhart, Allison C. Dehnel, Kerry M. Oliver, and Jennifer A. WhiteColony of Aphis craccivora infesting young locust tree (Robinia pseudoacaciae). Image provided by authors.

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Unseen microbes can affect the patterns observed at the macroscopic level in nature, mediating ecological interactions among plants and animals. Many herbivorous insect species are found to feed on multiple plant species, yet individual insects often perform well on only a subset of these plant species. Because infection with specific microbes often correlates with the use of particular plants, there has been much speculation, yet limited experimental evidence, that microbes promote dietary specialization. Here we investigated whether bacterial symbionts influence the diet of the cowpea aphid, which feeds on diverse plant species, including economically important crops. We first show that cowpea aphid clonal lines, each isolated from a single female, vary in their ability to use different plant species, which in turn correlates with patterns of infection by particular maternally-inherited bacteria. We next focused on aphid clones that naturally performed better on locust trees than other plant species, and which were infected with a common insect symbiont called Arsenophonus. We used antibiotics to remove Arsenophonus from two aphid clones and found that elimination of this symbiont dramatically reduced performance on locust, while generally increasing performance on other plant species. In fact, the uninfected aphids from "locust-specialist" lines didn't perform any better on locust than alfalfa-specialist lines, indicating that the bacteria are a critical component for effective use of locust as a food plant. We also experimentally infected an alfalfa-specialist aphid line with Arsenophonus, which instantaneously improved aphid performance on locust and decreased performance on alfalfa, effectively transforming an alfalfa specialist into a jack-of-all food plants. Inherited bacteria, including Arsenophonus, are widespread in insects and periodically gained or lost by host insect lines through natural processes; our results show that such transitions can abruptly change the food plant range of an herbivore, either restricting or facilitating use of particular plant species. If these changes improve performance on economically important food plant species, inherited microbes have the potential to transform innocuous herbivores into pests of consequence.

Image caption: Colony of Aphis craccivora infesting young locust tree (Robinia pseudoacaciae). 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.

 

Perspective

Does history matter in plant interactions?

Susanne Wurst &Takayuki OhgushiMultiple interactions including galling midges, aphids, and ants on a willow, Salix eriocarpa.

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Plants interact with a wide range of organisms above and below the ground. These spatially separated organisms can indirectly affect each other through changes in plant characteristics which do not stop at the plant level, but can also affect the zones of influence of the plants both above (the ‘phyllosphere’) and below ground (the ‘rhizosphere’).

Here, we ask if biotic interactions of plants below- and aboveground can have long-term legacy effects on future biotic interactions. In other words: does the history of biotic interactions matter for future biotic interactions of plants?

We propose that history (or legacy) effects are mainly transferred by changes in plant and/or soil characteristics. Changes in plant and soil characteristics caused by biotic interactions such as feeding on plant materials can be short- or long-term. For example, plants can react with a rapid defense response against feeders that often vanishes when the feeding ceases. This is seen as a short-term response. On the other hand, plants can also invest in new leaves or roots to compensate for feeding damage or translocate nutrients to unattacked plant parts. These are more long-term changes and are more likely to persist and affect future interactions of plants. In soil, carbon input into the rhizosphere can be changed in the short term and affect the activity of the microbial community in the rhizosphere, while litter quality changed by feeding may affect decomposition and soil biota communities in the longer term. We also ask about the potential consequences of long-term and history effects in terrestrial ecosystems. The fitness of plants, the composition of biotic communities and the functions of ecosystems may all be affected by past biotic interactions. We conclude that the history of past interactions should be included in studies on biotic interactions for a better understanding of the current community organization.

Image caption: Multiple interactions including galling midges, aphids, and ants on a willow, Salix eriocarpa.
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.

 

Predicting drought tolerance for Amazonian forest trees

Isabelle Maréchaux, Megan K. Bartlett, Lawren Sack, Christopher Baraloto, Julien Engel, Emilie Joetzjer & Jérôme ChaveCredits: Isabelle Maréchaux.

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Droughts are predicted to become increasingly frequent and intense in Amazonia, and empirical evidence for the vulnerability of Amazonian trees to drought has accumulated over the past decade. However, little is known about the mechanisms or the diversity of drought tolerance in tropical trees. Indeed, it has been difficult to quantify drought tolerance in tropical trees, due to a lack of consensus on a relevant tree functional trait, practical to measure for the hundreds of tree species occurring in tropical forests.

One potential trait has been proposed recently: the leaf water potential at wilting or turgor loss point (πtlp), which determines the tolerance of leaves to drought stress. We estimated πtlp for 165 trees of 71 species, at three sites within forests in French Guiana, using a new method, based on a demonstrated association between πtlp and another trait, the leaf osmotic water potential at full hydration. This new method is much faster than the standard one. Our dataset represents a significant increase in information for tropical tree species.

We found that πtlp varied little within species and significantly across species. Some species were much more drought tolerant than others. Measures for πtlp were consistent with the few direct observations of species vulnerability in long-term drought experiments in Amazonia. We also found that πtlp showed only a weak or no correlation with other commonly measured plant traits.

The variability in πtlp among species indicates the potential for a range of species responses to drought within Amazonian forest communities. Vegetation models seeking to predict forest response to drought may profit from more direct measurements of hydraulics-related plant functional traits such as πtlp.

Image caption: Credits: Isabelle Maréchaux.
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 double-edged sword of immune defence and damage control: Do food availability and immune challenge alter the balance?

Zachary R. Stahlschmidt, Madison Acker, Ilya Kovalko and Shelley A. AdamoFemale Texas field cricket. Photograph by ZRS.

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Although immune resistance is necessary to kill pathogens, it may also cause damage to hosts. Thus, animal immune systems must adaptively balance aggressive immune resistance (ability to destroy pathogens) with infection tolerance (ability to withstand the self-damage caused by immune resistance). Insects offer unique insight into this balancing act because phenoloxidase (PO)-mediated melanisation is a key feature of immune resistance, but PO activation causes inevitable self-damage. The antioxidant glutathione (GSH) may reduce this damage, but high levels of GSH can impair melanisation. We first showed that GSH may be a mechanism of infection tolerance because GSH levels in crickets correlated with fecundity (egg-laying) despite bacterial growth—that is, crickets with high levels of GSH in their hemolymph (blood) were able to maintain reproductive output despite increased levels of bacterial infection. Next, we used crickets to examine whether the relative balance between a component of immune resistance (i.e., PO) and protection from self-damage (i.e., GSH) shifted due to food availability or immune challenge. Although GSH and PO were positively correlated with one another, the PO:GSH ratio was robust and not affected by food availability or immune challenge. Thus, increased investment in a mechanism of immune resistance may require an increase in GSH to reduce self-damage (i.e., increase infection tolerance). Chronic immune challenge led to greater tolerance of oxidative stress suggesting that repeated immune challenge up-regulates infection tolerance mechanisms. Food limitation led to reduced PO activity, but not GSH concentration. This result suggests that mechanisms of immune resistance may be more sensitive to food availability than mechanisms of infection tolerance. In sum, mechanisms of immune resistance and infection tolerance can be correlated, and they can be affected by food availability or immune challenge.

Image caption: Female Texas field cricket. Photograph by ZRS.
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.

 

Darwin’s dream: a manipulative experiment for measuring natural selection in animal populations

José Luis Bartheld, Juan Diego Gaitán-Espitia, Paulina Artacho, Cristian Salgado-Luarte, Ernesto Gianoli and Roberto F. NespoloImage provided by authors.

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Natural selection is one of the most important ideas in the history of science, but for a long time, testing it experimentally was elusive. As Darwin thought, natural selection was supposed to be too subtle to be accurately measured. However, ecologists and evolutionary biologists have shown that rapid evolution is commonplace, and that applying the appropriate procedures (e.g., using closed system such as islands, applying reciprocal transplant experiments) both the magnitude and shape of selection could be measured with precision.

In order to characterize fitness profiles –that is, the shape of selection- individuals in animal populations need to be marked, measured and recaptured. We chose to do such an experiment with the garden snail, an animal easy to collect in large numbers and also easy to mark and recapture. Also, it is distributed over a broad geographic range.

We tested one of the most important tenets of physiological ecology (and the one that shaped its development during the eighties and nineties): the assumption that energy allocation in organisms and populations is adaptive (i.e., a target of natural selection).

To do this, we performed a reciprocal transplant experiment using distant populations, which were bred in captivity and then released (about 1500 snails) at both extremes of their range, 1300 kms apart. Before release, we measure a suite of physiological, morphological and life-history traits.

Our results were surprising. The results in general are not consistent with the occurrence of local adaptation (i.e., higher fitness at home), and in spite of the very different climates of the original populations, we found that only two traits (energy metabolism and body size) were the target of selection. This strikingly homogeneous result suggests that some general rule for adaptive optimization exists in these snails.

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.

 

Neighbour presence reduces root allocation

Bin J. W. Chen , Heinjo J. During, Peter J. Vermeulen, Hans de Kroon, Hendrik Poorter and Niels P. R. AntenTwo split-root pea plants sit on the edges of two pots and place their roots in both pots. Thus, each plant has access to the volume of two pots, and share soil nutrients with the neighbour.

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Increasing evidence suggests that plants are able to detect the presence of belowground neighbours. Such detection allows them to change their investment strategies in root growth and seed production. However, there is a debate about the direction and extent of the associated changes. Several studies propose that plants should grow more roots even at the expense of seed production to defeat their opponents (neighbours). Evidently such findings would have large significance for agriculture where maximum seed production is often the objective. Yet, studies that documented these effects are confounded by the fact that pot volume and plant size were insufficiently accounted for.

We developed an experimental approach in which the effects of neighbour presence and the effects of rooting volume and plant size are disentangled. We grew pea plants in the presence or absence of a belowground neighbour at a range of soil volumes, while providing equal amount of nutrients per plant. Then, we used a statistical approach that accounts for plant size, rooting volume and neighbour presence effects. We found pea plants were smaller and had less roots in the presence of a neighbour, which contradicts the above-mentioned results and suggests that neighbour-induced root overproliferation did not occur in our study.

More broadly our results indicate that if the effects of rooting volume and plant size are not taken into account, the effect of neighbours on plant growth can be misinterpreted. Our results do help to reconcile various results of neighbour effects published in the literature, by reasoning what the effect of rooting volume would be in other published studies.

Image caption: Two split-root pea plants sit on the edges of two pots and place their roots in both pots. Thus, each plant has access to the volume of two pots, and share soil nutrients with the neighbour.
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.

 

Burn or rot: leaf traits explain why flammability and decomposability are decoupled across species.

Saskia Grootemaat, Ian J. Wright, Peter M. van Bodegom, Johannes H. C. Cornelissen and William K. CornwellThe ignition of a leaf. Photo credit: S. Grootemaat.

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When leaves fall from a tree basically two things can happen: the leaves will either be decomposed by soil organisms or, in fire prone areas, the leaves can burn in a wildfire. Different plant species have different leaf characteristics. It is generally accepted that leaf characteristics, like lignin and phosphorus-concentrations, drive the speed of the decomposition process. This means that some species have leaves that decompose faster than others, depending on their physical and chemical characteristics. In contrast, less is known about the effects of leaf characteristics on leaf flammability. In this study on 32 species from eastern Australia we investigated which leaf characteristics determine the flammability of species. Both leaf dimensions and chemistry affected the ease of ignition and the burning time of individual leaves. For example, species with thinner leaves or leaves consisting of less dense material ignited more quickly. Leaves with higher moisture content took longer to ignite. Species with large, heavy leaves burned for longer than smaller (light) leaves. Furthermore, species with higher nutrient concentrations had shorter flame durations, suggesting that nitrogen and phosphorus work as flame retardants.

When we compared the sets of leaf characteristics driving decomposability and flammability respectively, we found no relationship between the two litter fates. This means that leaves that decompose quickly are not necessarily those that are most likely to burn or burn quickly. This study gives us important information because knowing which plant species (and leaf characteristics) make the vegetation more flammable, either directly or indirectly through litter accumulation as a consequence of slow decomposition, can inform fire behaviour models. The results can help to predict where a fire is likely to start and, once a fire has started, some estimates can be made of the likely fire intensity and spread. This can help policy makers, fire fighters and residents to make better informed decisions.

Image caption: The ignition of a leaf. Photo credit: S. Grootemaat.
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 availability and seasonal reproductive activation in a songbird

Scott Davies, Thomas Cros, Damien Richard, Simone L. Meddle, Kazuyoshi Tsutsui, and Pierre DevicheAn Abert’s Towhee. Photograph by Christofer Bang.

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Many animals have an outstanding ability to forecast when they need to be in breeding condition, yet much remains to be learned about how they achieve this. Most temperate zone songbirds, in particular, have to be exceptional forecasters because their reproductive system is shutdown during the winter and, to be able to breed, must be activated in the spring. Activation involves dramatic rises in the secretion of reproductive hormones and gonadal growth. This process takes time, so songbirds need to start it well before they need to breed and use cues from the environment that forecast when suitable environmental conditions are approaching. For decades, scientists have recognized that food availability is important because seasonal reproductive activation takes longer if birds are energetically constrained. However, our understanding of the physiological mechanisms that link food availability to activation of the reproductive system is limited.

To address this issue, we food-restricted captive adult male Abert’s Towhees, Melozone aberti, during reproductive activation. We investigated whether energy deficiency constrains multiple aspects of reproductive activation, in particular the growth of the testes. Since testis growth is the culmination of an endocrine cascade that begins in the brain, we also aimed to understand which steps of this cascade are affected by energetic constraint and, to do so, measured endocrine activity at all three points of this cascade (i.e., brain, anterior pituitary gland, and testes). Consistent with the majority of studies in songbirds, we found no effect of food restriction on testis growth. However, food restriction influenced plasma levels of hormones from all levels of the cascade responsible for reproductive activation.

These results suggest that energetic constraint modulates reproductive activation not through changes in the growth of the testes, but through changes in the plasma levels of hormones. In other words, even when constrained by energy deficiency, male songbirds can morphologically enter breeding condition, but delay increasing reproductive endocrine activity. This delay may be beneficial as it presumably decreases the expression of energetically costly behaviors, such as aggression and singing, which are stimulated by reproductive hormones.

Image caption: An Abert’s Towhee. Photograph by Christofer Bang.
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 size really matter in predicting bite force in bats?

Juliana Senawi, Daniela Schmieder, Björn Siemers and Tigga Kingston Juliana Senawi with bats great and small from the study site, Krau Wildlife Reserve, Malaysia. At around 200 g, Cheiromeles torquatus or the Naked Bat is recognized as the largest insectivorous bat in the world, while Kerivoula intermedia or the Small Woolly Bat weighs a mere 3 g (less than a sheet of an A4 paper!!) and is one of the very smallest.  Photograph by Nurul Ain Elias.

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Would you rather be bitten by a big dog or by a small dog? Neither, of course, but if you had to choose, which one would it be? According to researchers, bite force (bite strength) increases with size in most animals, so the small dog is likely the better bet! Previous research in South and Central America indicates this relationship holds in bats too – bigger bats bite harder than smaller bats. We wanted to test whether this was the case in Asian forests, where the bat fauna is equally diverse, but dominated by very different families of bats.

So how do we measure how hard an animal bites without losing any fingers? The bats were encouraged to bite a pair of metal plates hinged at one end by a transducer, which converts the pressure of the bite to a readable output of the force. We recorded the maximum bite force and measures of size (body mass, forearm length, head width, head height and head length) of 35 insect-eating bat species captured in Krau Wildlife Reserve, Malaysia. The bats ranged in size from 3 g to 200 g and belonged to 7 families. We also measured jaw features responsible for generating bite force using museum specimens of the same species, and used these to calculate the mechanical advantage (jaw effectiveness) adjusted by the size of the species.

So, did bigger bats bite harder? The answer was yes, but the relationship between size and bite force differed among the bat families. The effectiveness of the jaw (mechanical advantage) also played a role, regardless of the size of the bat. All 35 species of bats in this study eat insects in the same forest, so they have developed strategies to avoid competition. Having a different bite force than your neighbour may be one – while some species may focus on hard crunchy prey like beetles, others may specialize on softer fare like flying termites and moths.

Image caption: Juliana Senawi with bats great and small from the study site, Krau Wildlife Reserve, Malaysia. At around 200 g, Cheiromeles torquatus or the Naked Bat is recognized as the largest insectivorous bat in the world, while Kerivoula intermedia or the Small Woolly Bat weighs a mere 3 g (less than a sheet of an A4 paper!!) and is one of the very smallest. Photograph by Nurul Ain Elias.
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.

 

Cane toad impacts native species reproduction

Edward J. Narayan, Tim S. Jessop and Jean-Marc HeroCane toads present within terrestrial breeding habitats of the endangered Fijian ground frogs (Photograph by Dr Edward Narayan).

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Invasive species, major drivers of global change, cause unprecedented impacts on biodiversity. Their influence is most apparent on small oceanic islands where invasive species are the main cause of extinction. Understanding the mechanisms that make invasive species devastating is central to addressing their ecological impacts on the islands. One idea is that colonization of “simple” small islands affords invaders greater capacity to diversify and intensify their ecological roles beyond those seen in their native or invaded continental distributions.

Here, we used natural and manipulative field experiments to test if density-mediated competitive interactions from the highly-invasive cane toad could cause indirect effects and fitness loss to a small island population of the endemic and endangered Fijian ground frog. Over 13 successive monthly field surveys we collected 5000 non-invasive urine samples and measured body condition, survival and reproductive success of the Fijian ground frog. Samples were then analysed for reproductive and stress hormones. These data provided detailed accounts of how exposure to high-densities of cane toads caused major alterations in the nutritional status, physiological stress and reproductive physiology of ground frogs in both field enclosures and natural habitats. Most telling was that ground frogs in high toad density enclosures experienced extremely poor breeding success.

Despite a wealth of knowledge on the cane toad’s ecological consequences in invaded continents, such as Australia, our results reveal them to have extremely novel ecological roles and consequences on islands. Clearly, our results demonstrated how invasive cane toad competition, through extremely strong indirect effects, triggers major physiological changes that led to the reproductive collapse in Fijian ground frogs. Further, our study suggests it is important to limit alterations to island habitats to reduce the strength of invader-native species interactions. Thus, our results provide a striking example of why invasive species can disproportionately impact island endemics to potentially increase extinction risk.

Image caption: Cane toads present within terrestrial breeding habitats of the endangered Fijian ground frogs (Photograph by Dr Edward Narayan).
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.

 

Bacterial diversity enhances plant growth

Simone Weidner, Robert Koller, Ellen Latz, George Kowalchuk, Michael Bonkowski, Stefan Scheu and Alexandre JoussetPhoto of thale cress (Arabidopsis thaliana associated with bacterial community of Pseudomonas spp. (taken by Simone Weidner).

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In order to grow, plants need to take up soil minerals such as nitrogen. Nitrogen is however often limited and when present locked in the soil matrix. To make nutrients accessible to the plant, soil particles have to be broken down by enzymes. Since plants are not efficient in doing this themselves, they have to rely on soil microbes to make nitrogen available. To ensure an optimal nitrogen supply, plants “hire” soil bacteria by pumping huge amounts of sugars into the soil. By doing so, they attract and feed a dense bacterial community that in turn produces the required enzymes. Feeding bacteria is a huge investment for the plant and the effort is only worthwhile if bacteria do contribute to the required functions.

In this study we wanted to know how this function of making nitrogen available is influenced by the diversity of the bacterial community. We performed an experiment in which plants completely depended on the nitrogen supply from the bacteria and added bacterial communities to the plant that differed in their diversity.

Our study shows that bacterial diversity is an essential driver for the feedback of investment to the plant. Bacteria living alone produce less enzymes, slowing down nutrient cycling and plant growth. Mixing different species causes the bacteria to upregulate enzymatic activity, probably as part of a strategy to exploit resources better than their competitors. This helps to make more nitrogen available, and enhances plant growth.

Alterations of soil bacterial diversity, for instance by poor agricultural management, may thus have deleterious effects on plant growth. We propose that preservation of soil microbial diversity should be taken into account when it comes to agricultural management strategies. In addition, we propose that soil microbial diversity could be enhanced by reintroducing the missing species in order to improve nutrient mobilization and minimize the need for fertilizers.

Image caption: Photo of thale cress (Arabidopsis thaliana associated with bacterial community of Pseudomonas spp. (taken by Simone Weidner).
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.

 

Investigating isotopic functional indices to reveal changes in the structure and functioning of benthic communities

Carinne Rigolet, Eric Thiébaut, Anik Brind’Amour and Stanislas F. DuboisHaploops nirae, a gregarious tubiculous amphipod (crustacean) species (top picture) colonizing muddy marine sediments and engineering a unique habitat (bottom picture) while largely affecting associated species assemblages.

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The number of species is a key element for ecosystem functioning. However, not all species play the same functional role and/or respond to changes in the same way. Approaches to study species functions and interactions are mostly based on morphology (e.g. size, shape) or behaviour (e.g. feeding guild, motility). Using many such biological traits, one can calculate functional indices. They measure a potential functional niche of species assemblage (community). We suggest using stable isotopic compositions of species to provide a realized functional niche. Indeed, stable isotopes (i.e. 13C and 15N) in species’ tissues are directly linked with the species’ diet. As a result, they reflect information about the use of the physical habitat (e.g. size, hydro-climatic conditions) and the use of its resources (e.g. diversity, foraging strategy), two crucial factors in defining the ecological realized niche. In this study, we examine the ecological significance of newly defined isotopic functional indices, using a large set of associated species from two marine benthic communities widely reported in coastal shallow waters: the common brittle star Amphiura filiformis community competing with the crustacean amphipod Haploops nirae community.

We showed that Isotopic Functional Richness (a measure of the extent of the community trophic niche) is higher in the Haploops community due to a higher diversity in food sources but also due to longer food chains. Isotopic Functional Evenness (the regularity in all species distribution) showed that the biomass originates from other primary production sources, besides the phytoplankton.

These isotopic metrics responded according to expectations, based on the extensive knowledge of those communities. They provide new insights into how the structure of energy accumulation as biomass between species is likely to underpin the structure of the communities.

Image caption: Haploops nirae, a gregarious tubiculous amphipod (crustacean) species (top picture) colonizing muddy marine sediments and engineering a unique habitat (bottom picture) while largely affecting associated species assemblages.
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.

 

Convergence of three mangrove species towards freeze-tolerant phenotypes at an expanding range edge

Susan C. Cook-Patton, Michael Lehmann and John D. ParkerBranch samples collected from adult trees (photo credit: Susan Cook-Patton).

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Although many species are moving around as the climate changes, they are not all moving at the same rate. To help explain why three species of mangroves are migrating northwards at different rates, we examined variation in their ability to tolerate freezing temperatures. We sampled mangrove adults and seedlings along most of Florida’s eastern shoreline and exposed them to freezing temperatures. We also measured a suite of leaf and branch traits to examine how plants were changing as they grew closer to the range edge. We found that black mangroves, the most northerly and fastest migrating mangrove species, showed the greatest freeze tolerance, followed by red, and then white mangroves, the least northerly and most slowly migrating species. However, freeze tolerance as well as other traits were not fixed within species, but instead varied systematically with latitude. Adults from black and red mangroves showed higher freeze tolerance towards the range edge, and the leaves of all three species became denser, tougher, and smaller in the north than in the south. Thus, freeze tolerance appears to determine where mangrove species can move and at what rate. As freeze events become more and more uncommon, these species are likely to continuing moving northwards, but at different rates, possibly breaking apart plant communities that historically co-occurred.

Image caption: Branch samples collected from adult trees (photo credit: Susan Cook-Patton).
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.

 

Stress, hormones, and blood- the devil’s in the details

Jeffrey M. Goessling, Heather Kennedy, Mary T. Mendonça, and Alan E. WilsonA sample blood smear from an adult Gopher Tortoise (Gopherus polyphemus) with an elevated heterophil:lymphocyte ratio consistent with an acute stress response. Image credit: J.M. Goessling.

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Who hasn’t been stressed out? Although one could easily define what it feels like to be under stress, few could quantify their level of stress. So, what is stress? In the strict sense, it is a term to describe the physical pressure on a system from an outside source. For example, the weight of a floor resting on an I-beam. Historically, biologists have used the tools of endocrinology to measure stress on animal populations (that is to measure the degree to which the environment is exerting pressure on individuals). Specifically, hormones aptly referred to as “stress hormones” have been measured in individuals, and compared between “stressed” and “non-stressed” populations. However, while convenient, recent studies have indicated that stress hormones may not be reliable in indicating if animals are exposed to long-term stressors. One new approach to measuring stress is quantifying relationships among cells of the immune system, as it is well-known that stressors can elicit a change in how the immune system functions. In this paper, we quantitatively synthesized relevant literature (in a meta-analysis) to compare the traditional measure of stress (stress hormone concentration) to the more novel measure of stress (proportion of white blood cells) in studies that have been published using both methods. We found that both measures are in fact increased in populations exposed to stress. However, an important difference between the two measures is how individuals physiologically adapt to stressors over time. Specifically, elevated stress hormones are reduced in response to long-duration stressors, up to a point where they reach levels of non-stressed populations. This reduction in response to stress was not seen in the white blood cell counts. This suggests that the immune cell measure remains elevated in populations that have been exposed to stressors for a prolonged period. Therefore, conclusions from our study indicate that the white blood cell parameter could be very useful as a tool to test whether populations have been exposed to long-term stressors, while stress hormone concentrations should be interpreted cautiously as they may not be indicative of responses to long-term stress.

Image caption: A sample blood smear from an adult Gopher Tortoise (Gopherus polyphemus) with an elevated heterophil:lymphocyte ratio consistent with an acute stress response. Image credit: J.M. Goessling.
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.

 

Early life stages dictate the future: plant species sorting along water availability gradients

Rob G.A. Fraaije, Cajo J.F. ter Braak, Betty Verduyn, Leonieke B.S. Breeman, Jos T.A. Verhoeven and Merel B. Soons Ecologists at work.  Photo provided by authors.

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Plant species differ widely in their requirements and tolerances to environmental conditions. Though many studies are available on such requirements and tolerances, it often remains unclear at which stage of a plant’s life cycle such characteristics are mainly determined. Early stages in a plant’s life cycle are known to be sensitive to the environment, but several steps can be distinguished within the early stages, including seed germination, seedling survival, and seedling growth.

Stream ecosystems and their surrounding terrestrial areas, known as riparian zones, provide an example of highly diverse ecosystems, harbouring many different plant species that typically have individual preferences along a gradient from wet (in the stream) to moist (close to the stream) to dry conditions (further upland). This presents an ideal study system to test how early stages in a plant’s life cycle may contribute to a species preferred position along this gradient. We tested this by sowing seeds and planting seedlings of 17 riparian plant species across a riparian gradient from wet to dry conditions, while closely studying their responses afterwards.

The moisture gradient had a very strong effect on germination, seedling survival and seedling growth of all 17 plant species. All three processes were strongly inhibited at the wet and dry ends of the gradient. Moreover, the individual plant species showed their own specific preference along the gradient, especially during seed germination and seedling growth, corresponding to their preferred habitat as an adult plant. This showed that these early stages already set the template for vegetation patterns along streams, and that they contribute to a high biodiversity by separating species along moisture gradients. This is important knowledge given the major declines in riparian plant species diversity, and may help future conservation and restoration programs.

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

 

How does a winter desert annual cope with two challenges in the desert: summer rains and winter rain unpredictability

Alejandra Martínez-Berdeja Exequiel Ezcurra & Mauricio TorresRigid spineflower skeleton at the end of the growth season. Photo: Alejandra Martínez-Berdeja.

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The rigid spineflower (Chorizanthe rigida) is a winter desert annual that grows in the Mojave and Sonoran deserts. Most winter annuals disintegrate and disperse their seeds at the end of spring, but the dead spineflower plants form dry rigid skeletons that stay in the field for several years, releasing seeds in response to winter rain events. C. rigida’s unique dispersal mechanism seems to allow it to synchronize seed release with available soil moisture, a scarce and precious resource in deserts. However, in order to do so effectively, the plant needs to overcome two challenges. On the one hand, it has to be able to differentially respond to seasonal precipitation patterns and avoid germination after summer rains, when the scorching temperatures could kill them. On the other hand, the plants also face winter rainfall unpredictability in the desert: any single rain event that might cause seeds to germinate might or might not be followed by additional rainfall, putting germinated seeds at a risk of dying from dehydration.

Our study shows that the stalk that attaches the seeds to the plant in spineflowers is much thicker in bi-seasonal deserts with summer rains, allowing the plants to retain seeds beyond summer and release them to more favorable winter rainfall cues. Secondly, we found that seeds in C. rigida individuals from populations experiencing highly unpredictable winter rainfall are much more variable in size than those from more predictable desert sites. Subsequent germination trials showed that larger seeds need more water to germinate and therefore have lower short-term germination and display a more “cautious” germination strategy. Thus, highly variable seed sizes allow C. rigida individuals to exhibit a heterogeneous germination response in extreme deserts, thus avoiding the loss of large fractions of seeds after a false moisture cue. Our study shows how desert organisms can adapt to both rain seasonality and unpredictability through simple changes in reproductive morphology.

Image caption: Rigid spineflower skeleton at the end of the growth season. Photo: Alejandra Martínez-Berdeja.
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 Energy Allocation Influences Reproductive Success in the Southernmost Breeding Mammal, the Weddell seal

Michelle R. Shero, Riley T. Krotz, Daniel P. Costa, Julie P. Avery & Jennifer M. BurnsWeddell seal, photo provided by authors.

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The ability of animals to stay in good health despite drastically changing environmental conditions is important for individual survival and reproductive success. An animal that is in good health can catch enough food to maintain their own body mass, and gain weight in the form of fat (lipid) or lean tissue reserves. The allocation of ingested calories is regulated by a suite of hormones, such as cortisol, thyroid hormones, growth hormone, and insulin-like growth factor-1. In seals, both the condition of females at the end of their fasting period, and the amount of energy gained while at sea, may influence a female’s probability of producing a pup the next year, as females that are too skinny may not be able to start a pregnancy or carry a foetus to term.

Weddell seals (Leptonychotes weddellii) are the southernmost breeding mammal in the world, and they live and reproduce in an extreme and rapidly changing environment. During the austral summer, females give birth, nurse their pups, breed, and moult while also reducing foraging efforts. By contrast, during the winter and pregnancy, animals forage intensively. In this study, we assess whether females that end the moult in better health (larger, more lipid stores) are more likely to return with a pup the next year, and whether pregnant seals “prepare themselves” for the upcoming lactation period by gaining more fat during the winter than non-reproductive females. Surprisingly, our study showed that both reproductive and non-reproductive seals gained similar amounts of mass and lipid during winter foraging. However, pregnant Weddell seals gain less mass during gestation than other seal species, explaining why previous studies show they must forage during lactation. Post-moult females with higher thyroid hormone concentrations were more likely to produce a pup the next year. Similarly, decreasing level of cortisol (stress) and maintaining growth hormone across the winter was shown to correlate with higher pupping probabilities. This study suggests that multiple hormones involved with energy allocation may also be indicative of positive reproductive outcomes. Understanding physiological factors that influence the probability of reproduction is important for assessing the species’ vulnerability to changes in ecosystem structure.

Image caption: Weddell seal, 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.

 

Active prey mixing as an explanation for polyphagy in predatory arthropods

Renata Vieira Marques, Renato Almeida Sarmento, Felipe Lemos, Marçal Pedro-Neto, Maurice W. Sabelis, Madelaine Venzon, Angelo Pallini & Arne JanssenPicture provided by authors.

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The question of why some species specialize on one or a few food types, whereas others consume many, continues to puzzle scientists. The existence of both strategies suggests that there are advantages and disadvantages to being a specialist or a generalist. Advantages to consuming various foods are to enable balancing of nutrients in the diet or diluting toxins present in each food type. In either case, a mixed diet yields a better reproductive performance of the animal than a single diet. Indeed, for us humans this comes as no surprise as we fare better on a mixed, varied diet.

Although there are many studies on the effects of mixed diets in animals, only a few show that animals actively search for different food types to obtain a mixed diet. In most studies, the different foods are offered together, so that the animals have plenty of food in the same area and can obtain a mixed diet without any effort. In this paper, we show that two species of tiny predatory mites (adults smaller than 1 mm) perform better on a mixed diet of two prey species, herbivorous mites that are pests of a biodiesel plant (Jatropha curcas) in Brazil. We show that females of each of the two predator species produce twice as many eggs on a diet consisting of the two prey species than when feeding on either of the two prey separately.

Moreover, we also show that the predators actually actively search for a mixed diet. This was done in the laboratory by offering the predators each prey species on a separate leaf of their host plant and by connecting the two leaves using a plastic bridge. So in order to feed on a mixed diet, the predators needed to spend time and energy to cross the bridge. Indeed they did so when the two leaves contained different prey species and much less when both leaves contained the same prey species. So the predators do what is good for them albeit at a cost: they actively commute between the two prey patches so as to obtain a mixed diet, thereby maximizing their reproductive performance.

Image caption: Picture 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.

 

The genetics of plant-plant interactions

Etienne Baron, Julien Richirt, Romain Villoutreix, Laurent Amsellem and Fabrice RouxPhoto provided by authors.

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Plant-plant interactions like competition are ecological and evolutionary processes that deeply influence natural communities. Studying their underlying mechanisms may be a key to understanding the structure and functioning of plant communities, which may in turn help to predict the response of plant communities to global change. However, we are only beginning to understand the genetics of competition. Notably, the identity of the genes involved in plant competitive ability still deserves deeper investigation. This exciting challenge calls for a multidisciplinary approach at the frontier between evolutionary ecology and genomics.

In this study, we adopted an ecological genomics approach to test whether the genetics of competitive ability of a local population of the model annual plant Arabidopsis thaliana was dependent on the identity of the competitor species. In a common garden experiment, the response of 48 A. thaliana genotypes to competition was estimated by looking at a suite of nine plant traits (including a proxy of seed production) in six competitive environments: absence of competition, intraspecific competition and interspecific competition with four species frequently associated with A. thaliana in natural plant communities (i.e. Poa annua, Stellaria media, Trifolium repens and Veronica arvensis). In addition, the biomass of its corresponding competitor was estimated in order to quantify the competitive effect of A. thaliana.

We showed that variation in the identity of the competitor might promote maintenance of genetic variation of A. thaliana at the local population scale and species coexistence at the community scale. We also demonstrated that the optimal strategies of A. thaliana in response to competition depend on the identity of the competitor species. Finally, we found that the genomic regions associated with the response of A. thaliana to competition depend on the identity of the competitor. This genomic map allowed us to identify the candidate genes related to plant-plant interactions.

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.

 

UV radiation causes darkening of the larval cuticle, at the expense of adult immune function

Sara Debecker, Ruben Sommaruga, Tim Maes and Robby StoksMale Azure Damselfly (Coenagrion puella). Photo credit: Robby Stoks.

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Many animals, just like humans, get a tan when exposed to the ultraviolet radiation (UV) in sunlight. This darkening of the skin or cuticle is a result of the accumulation of the molecule melanin, which absorbs the harmful UV radiation and protects the body from damage. In addition, melanin performs several other functions inside the body. In many invertebrates, for example, it is also an important component of the innate immune system, where it is used to encapsulate pathogens, such as bacteria and parasites, with the aim of neutralising them. This process is called “melanotic encapsulation”. The formation of melanin used for UV defence and for immune function relies on the same enzyme pathway and the same resources, which are taken up through the diet and therefore, their availability can be limited. Consequently, there might be a link, or even a trade-off, between the quantity of melanin used for UV defence and immune function. Furthermore, it has never been studied whether UV radiation can affect the immune system in an invertebrate. Additionally, in animals that have distinct larval and adult stages, such as insects and amphibians, little is known about the mechanisms by which stressors experienced in the larval stage affect the adult after metamorphosis.

In this study, we exposed larvae of the Azure Damselfly (Coenagrion puella) to UV radiation to evaluate whether UV affects the accumulation of melanin in the cuticle. After metamorphosis, we measured the strength of the immune system in adults as the melanotic encapsulation response. We found that larvae that were exposed to UV accumulated more melanin in their cuticle and metamorphosed later and at a smaller mass than animals reared without UV. After metamorphosis, they also had a reduced melanotic encapsulation response, constituting the first proof for UV affecting immune function in an invertebrate. Importantly, animals that accumulated more melanin in their cuticle as larvae had a more severely impaired immune function as adults, meaning melanin was traded off between its different functions. Therefore, we identified a new mechanism by which stressors experienced in the larval stage carry over to the adult stage.

Image caption: Male Azure Damselfly (Coenagrion puella). Photo credit: Robby Stoks.
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.

 

Intensity, not strategy is key for estimating trait values

C. E. Timothy Paine, Christopher Baraloto and Sandra DiazDr Claire Fortunel measures leaf toughness at Nouragues Biological Station, French Guiana.

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Functional traits are attributes of plants and animals that affect their rates of growth, survival and reproduction. They affect the responses of organisms to their environment, and also reflect the effects of the environment on organisms. For example, consider wood density, a commonly measured functional trait, which affects how stiff and strong an individual tree’s trunk is. If known for all trees in a forest, it also indicates how much carbon is stored within that forest. Thus, because of their myriad effects, functional traits are used to answer many questions about individual species and ecological communities. The challenge addressed in this paper is that, in species-rich ecosystems, it is very difficult to measure the functional traits of every species, as many of them are vanishingly rare. We report the optimal method for sampling trees to estimate the functional traits of diverse forests.

We began with nine hectares of tropical forest in French Guiana, in which eight functional traits had been measured on every tree. This gave us the true values of each trait in each plot. We then, using computer simulations, applied 12 different trait-sampling strategies. To take a few examples, some of the strategies emphasised very common species, others a range of sizes, and others particular clumps of individuals. Because we wanted to optimize the sampling of functional traits, we simulated applying the strategies over a range of intensities, from 1% of the individual trees up to 50% of them.

The take-home message is that the way to successfully estimate the distribution of trait values in a species-rich forest is through intense field sampling. In other words, the more trees you sample, the better your estimate of functional traits. Of less importance is the strategy applied. Increased sampling improved the performance of all strategies. Importantly, a commonly applied strategy, looking up trait values out of a database, yielded poor results, especially in estimating the variation in trait values within a forest. Our conclusion is that there is no substitute for extensive sampling to accurately characterize the distribution of functional trait values in species-rich forests.

Image caption: Dr Claire Fortunel measures leaf toughness at Nouragues Biological Station, French Guiana.
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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