Lay Summaries

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

 

Lay summaries for the current issue, including lay summaries for the new Special Feature: Defensive Symbiosis

 

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.

 

Nitrogen cycle response to precipitation change.

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

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

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

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

 

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

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

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

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

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

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

 

Transgenerational plasticity in marine sticklebacks: maternal effects mediate impacts of a warming ocean.

Lisa N.S. Shama, Anneli Strobel, Felix C. Mark and K. Mathias WegnerSize differences in offspring of mothers acclimated to different temperatures.

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Our climate is changing at an alarming rate, and nowhere is this more apparent than in the world´s oceans. The key question now being asked is whether marine species will be able to adapt fast enough to keep pace with changing environments. Evidence is accumulating that marine species might be able to adapt to rapid environmental change if they have sufficient genetic variation (the raw material for evolutionary change) and/or plasticity to mount fast responses. In the case of plasticity, organisms adjust to the changed conditions by a change in morphology or behaviour without altering their genetic composition. Plasticity can work very fast. For example, if the environment becomes warmer, any trait that is plastic with respect to temperature can shift. Moreover, plasticity can occur both within a generation (individual responds to environment) and across generations (transgenerational e.g. maternal and paternal effects), making it a highly effective mechanism. The evolutionary potential of populations can thus be influenced by both genetic adaptation and non-genetic inheritance mechanisms such transgenerational plasticity.

Our study shows that transgenerational effects, in particular maternal effects, will play an important role in populations’ adaptive responses to climate change. We acclimated marine stickleback parents to either ambient or elevated sea water temperatures, produced offspring in all possible parental temperature combinations, and then reared offspring at both temperatures. Our results suggest that stickleback mothers are programming offspring growth via adjustments to offspring metabolism to grow better in the predicted future environment (her acclimation temperature), and this programming is particularly strong at elevated temperature, suggesting that maternal effects will be highly relevant for climate change scenarios in this system. Genetic variation was lower at elevated temperature, and the interaction of genotype and environment (within generation plasticity) also played an important role in shaping offspring growth trajectories at different temperatures.

Taken together, our data suggest that elevated temperature may be a particular problem for these fish, but stronger maternal programming under stressful conditions may help to alleviate some of the negative effects. Hence, both non-genetic and genetic inheritance will influence the adaptive potential of marine stickleback populations in the face of a rapidly changing ocean climate. Transgenerational plasticity can buffer short-term detrimental effects of climate warming and may buy time for genetic adaptation to catch up, therefore markedly contributing to the persistence of populations under climate change.

Image caption: Size differences in offspring of mothers acclimated to different temperatures.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Non-random patterns of functional redundancy revealed in ground beetle communities facing an extreme flood event.

Michael Gerisch

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Why are there so many species? And why are some species more similar in what they do than others? These questions have fascinated ecologists for decades, because they might explain why some populations, communities, or ecosystems are resilient to disturbances – and some are less. Functional redundancy is an increasingly applied concept to understand such biodiversity-stability relationships. It predicts that certain species can get lost from ecosystems (e.g., through disturbances) without affecting its integrity, because the remaining species perform similar roles and in doing so, maintain ecological functioning. However, recent studies report that functional redundancy is often lower than expected, and its importance for ecosystem stability is still unclear. Here I ask whether functional redundancy exists in ground beetles experiencing different levels of flood disturbance, and how it connects to the resilience of communities after an extreme flood event.

Functional redundancy was measured as the proportion of species having neutral effects on functional diversity if they were removed from the community. I compared the functional redundancy between artificial and observed communities to estimate if the functional redundancy “in the field” is higher or lower than what can be expected from a random draw. In fact, it was random, or even lower than expected, in many cases. Only in habitats with high flood disturbance or low groundwater depth (e.g., the most dynamic habitats), was functional redundancy considerably higher than expected. I also found functional redundancy to be higher in spring than in autumn. Most likely, the regular flood disturbance in spring facilitates many species to be functionally redundant in order to insure ecological functioning despite environmental stochasticity. However, in the course of extreme flood events, this mechanism was not very effective. The study shows that the role of functional redundancy for ecosystem stability is not permanent, but changes with environmental conditions, time after disturbances, and species composition.

Image caption: Dike burst during the extreme summer flood in August 2002 at the Elbe River, Germany, near the city of Dessau. Photo by Andre Künzelmann, UFZ.
This paper can be found online here.

 

Seedling resistance, tolerance and escape from herbivores: insights from co-dominant canopy tree species in a resource-poor African rain forest.

Julian M. Norghauer, Gaёtan Glauser & David M. Newbery In the foreground is a large seedling of zebrawood (Microberlinia bisulcata) at Korup, Cameroon, with mature and new leaves that had been protected from insect herbivores. In the background is a typical mesh cage built to exclude these herbivores in the experiment. Photo by Julian Norghauer.

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Since plants are largely immobile a crucial function for them is to reduce the potential impacts of being found and especially their leaves being repeatedly eaten by herbivores. Plants can defend themselves in three principal ways. One, by having chemical and/or physical traits that make them resistant to being eaten, two by having growth traits that instead enable them to be tolerant, e.g. by rapidly replacing lost leaves; and three, by having seed dispersal traits that allow escape in space, so they can avoid being found. How these different traits trade off to form the various strategies among co-occurring species within tropical tree communities is of essential interest as they have important consequences for recruitment, replacement and forest dynamics.

Compared with other tropical regions, much less is known about the defense strategies of African tree species. This study attempts to redress the imbalance.

The primary rain forest at Korup in the Republic of Cameroon offers a unique site for studying tree seedling defenses. The three co-dominant canopy tree species, all of the family Caesalpiniaeae, are taxonomically very closely related and share the same ballistic mode of seed dispersal. The most abundant of them is Microberlinia bisulcata or zebrawood, which forms large groves at Korup. The 4-year field experiment was set up within a large permanent grove plot. Fine nylon mesh cages were placed over new seedlings to protect them from insect herbivores — mesh roofs only for unprotected seedlings — in many pairs of well-lighted forest gaps and contrastingly shaded understorey locations. Seedling growth rates were related to leaf chemistry to estimate resistance and tolerance traits. Using mapped tree locations around seedlings mechanisms of escape could be evaluated.

The three tree species have apparently evolved quite different defense strategies which result from a trade-off between fast growth in response to light (hence raised tolerance) and effective escape associated with low resistance, and slow (shade-tolerant) growth and less successful escape associated with high resistance. A small conceptual model encapsulates these ideas. By reducing direct competition between them in this way (creating niche separation), trait differences are thought to contribute importantly to the species’ co-existence at Korup.

Image caption: In the foreground is a large seedling of zebrawood (Microberlinia bisulcata) at Korup, Cameroon, with mature and new leaves that had been protected from insect herbivores. In the background is a typical mesh cage built to exclude these herbivores in the experiment. Photo by Julian Norghauer.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Within-species variability is the main driver of community-level responses of traits of epiphytes across a long term chronosequence.

Johan Asplund and David A. WardlePhoto by Johan Asplund..

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Ecosystem succession is characterized by an initial build-up phase where nutrient availability increases until a maximum biomass phase is reached. However, in the prolonged absence of major disturbances (often in the order of millennia) the ecosystem enters a phase of retrogression which is characterized by increasing limitation in the availability of soil nutrients, notably phosphorous but in several cases also nitrogen. Chronosequences, areas that vary in time since major disturbance but otherwise are similar, can be used as “natural experiments”. In this study we used such a chronosequence involving 30 lake islands in northern Sweden spanning 5000 years in time since latest fire. We used this system to study how changes in soil fertility during retrogression affect lichens which are organism-like associations between fungi and algae. We measured how secondary compounds (defensive compounds), nutrient concentrations and the ratio between biomass and area changed in lichens growing on birch trees across this gradient. We measured these responses at the individual species level to see if lichens of the same species change across the gradient. We further calculated the responses as community weighted means where the responses of more common species have more influence than less common species. As such, community weighted responses can be affected by changes in the relative species composition and / or the response of individual species. We found older, less fertile islands had lichens with much higher nutrient concentration and higher biomass per unit area. At the community-level this was explained by higher values in individual species rather than a switch to species with higher values.

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

 

Invasion and root heterogeneity.

Brenda M. Vaness, Scott D. Wilson and Andrew S. MacDougallPrairie crocus (Pulsatilla patens), a native species, is part of the diverse natural community lost following invasion by introduced grasses. Credit: S. Wilson.

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Plant invasions are a widespread cause of global change. In North America, Eurasian grass species have invaded vast tracts of native prairie, altering wildlife habitat and producing species-poor “diversity deserts” that resist the reintroduction of native species.

We found that soil beneath invaded grasslands is consistently filled with roots. In contrast, soil beneath native prairie has more empty spaces that are available for invasive species to colonize. Overall, the patchiness of root length is about 30% lower beneath invaded grassland than native prairie.

Our results partly explain why native prairie is susceptible to invasion: soil beneath prairie has unoccupied spaces available for invaders to exploit. They also account for the difficulty of restoring native diversity to invaded grasslands: soil beneath the invaders is more fully occupied, leaving few opportunities for the reintroduction of native species.

Image caption: Prairie crocus (Pulsatilla patens), a native species, is part of the diverse natural community lost following invasion by introduced grasses. Credit: S. Wilson.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Frugivorous birds use a network of fruiting trees to move seeds across the landscape.

Javier Rodríguez-Pérez, Daniel García and Daniel MartínezCantabrian forest and potential network of fleshy-fruited trees. Tree species are represented by coloured nodes potentially linked by dashed lines. Courtesy of Daniel Martínez.

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Many birds eat the fleshy fruits of trees. After feeding, these frugivores carry the seeds within their guts and could defecate seeds in sites different from where they were consumed, and hence move tree genes, individuals and species across the landscape. Birds spend much time feeding on fruits, also perching on trees just to rest, and flying from one tree to another. Thus, fruiting trees may act as static elements that “channelize” the transport of seeds by animals. In ecological terms, fruiting trees would determine the connectivity of seed dispersal, that is the effect of the landscape on the flow of seeds through it.

We studied the movement of seeds by birds in a forest of the northern Iberian Peninsula, considering the fruiting trees as potential sites for perching, and thus the areas below them as potential sites for seed deposition. To this end, we translated the landscape into a network of fruiting trees (nodes) and the likely movements of fruit-eating birds as links between those trees.

We found that trees with higher connectivity accumulated larger seed clumps below them. This result suggests that trees surrounded by many others are more visited by frugivore birds for defecating. This favours the movement of seeds from different parts of the landscape, that is from trees with few neighbours to trees surrounded by others. This result, however, varies between years, which further suggests that the network of fleshy-fruited trees could be “disconnected” due to yearly changes in the fruiting landscape. Our findings reveal that fruiting plants and the activity of birds are essential to describe the transport of seeds throughout the landscape.

Image caption: Cantabrian forest and potential network of fleshy-fruited trees. Tree species are represented by coloured nodes potentially linked by dashed lines. Courtesy of Daniel Martínez.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Does body mass convey a digestive advantage for large herbivores?.

Patrick Steuer, Karl-Heinz Südekum, Thomas Tütken, Dennis W. H. Müller, Jacques Kaandorp, Martin Bucher Marcus Clauss & Jürgen HummelGrévy´s Zebra (Equus grevyi). Photograph provided by authors.

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In many ancient and present ecosystems around the world, assemblies of ungulates (a group of large herbivorous mammals) make use of the available plant matter; herbivore faunas of the ice-age (“Pleistocene mammoth steppe”) or of present African savannahs represent fascinating examples. Their members range from relatively small creatures like antelopes/deer over cattle or horses up to real “megaherbivores” like giraffes, rhinos and elephants.

It has long been debated how all these herbivores manage to co-exist in an area and how they share their common food resources. Body size is considered to be a key trait. It is thought that large animals have to rely on low quality food (because they cannot select for the best plant parts), but that at the same time this disadvantage is balanced by their higher capacity to digest plant food (due to the longer time the food stays in their guts, allowing gut microbes more time to digest plant cellulose).

Our project wanted to test to what extent such scenarios are true. Two samples of herbivores of a considerable range of body sizes (from goats/antelopes to African elephants) were available: The first (17 species, kept in a large zoo and several other institutions) was fed on a uniform food resource (grass hay), whereas the second (19 species) was selecting a natural diet (free-ranging herbivores of East Africa). A proxy from faecal material (faecal protein content, largely depending on the amount of microbial biomass built during the digestive process) was used to evaluate digestibility realized by the animals.

No dependence of digestibility (faecal protein) on body mass was found for the animals fed on the uniform diet (grass hay), while for the free-ranging animals, a considerable decrease in digestibility was found. The first result contradicts an advantage of large over small animals in digestive ability. The considerable decrease of digestibility with increasing body mass found in the free-ranging herbivores strongly indicates that large animals like elephants had to select a diet of considerably lower digestibility than smaller herbivores, and that this lower quality was not balanced by a higher digestive ability in large herbivores.

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

 

Outcrossing in sessile organisms: a feat perfected in Darwin’s primroses.

Barbara Keller, James D. Thomson and Elena ContiA flower of the distylous Primula elatior probed by a hairy-footed flower bee (Anthophora plumipes). Photograph credit: Barbara Keller..

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Plants are sessile organisms, thus vectors (e.g., insects) are needed to transfer male reproductive cells between individuals, effecting sexual reproduction and increasing genetic variation. Most flowering plants have male (anthers) and female (stigmas) sexual organs within the same flower, a condition that enables pollen produced by one flower to fertilize ovules of the same flower (selfing). Selfing, however, is often associated with inbreeding depression, which tends to lower offspring fitness. Various strategies aimed at reducing selfing have evolved in flowering plants, including spatial separation of sexual organs within a flower (herkogamy). However, there is often a tradeoff between avoidance of selfing and promotion of cross-pollination (outcrossing). For instance, herkogamy, which decreases self-pollination, might hamper cross-pollination via the spatial mismatch between anthers of pollen-donor and stigmas of pollen-recipient flowers. The dilemma is thought to be largely resolved in distylous species by producing two types of plants (morphs) with male and female sexual organs placed reciprocally in their flowers. The reciprocal placement facilitates cross-pollination, while the separation between anthers and stigmas within flowers limits self-pollination. Furthermore, a pollen-incompatibility system prevents seed set after self- and intra-morph pollination. The combination of the peculiar sexual-organ arrangement and incompatibility system is expected to maximize outcrossing by favoring inter-morph over intra-morph pollen transfer, while restricting intra-floral and intra-morph pollination. But does distyly really work as expected?

Despite the long-standing interest in distyly, dating back to Darwin’s studies on primroses, the specific predictions of its functional roles have never been tested in the same system. Here we perform controlled pollination experiments in the primrose and the oxlip - popular and commercially important spring-flowering ornamentals - using hairy-footed flower bees as pollen vectors. Consistent with our expectations, we find that more pollen is transferred between than within morphs, herkogamy lowers self- and intra-morph pollination, self-pollen does not set seed, and the presence of incompatible pollen on a stigma does not significantly diminish seed set by inter-morph pollen. Our study provides experimental validation for the predictions that distyly promotes cross-pollination and restricts gamete wastage to self-fertilization, thus optimizing outcrossing in sessile organisms.

Image caption: A flower of the distylous Primula elatior probed by a hairy-footed flower bee (Anthophora plumipes) . Photograph credit: Barbara Keller.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Cytokines and Eco-immunology: Studying the signalling molecule of the immune system

Laura M. Zimmerman, Rachel M. Bowden and Laura A. Vogel Ecologist at work. Photo provided by authors

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Animals face the constant threat of pathogens, and the immune system has evolved to combat this threat. Despite the obvious benefits of a strong immune response, we often observe great variation in the abilities of animals to mount an immune response. Eco-immunology is a field where scientists are concerned with figuring out why this variation occurs in natural populations. Eco-immunologists examine many aspects of the immune system, and in this review we discuss the applicability to eco-immunology of examining cytokines. Cytokines are the signaling molecule of the immune system and they form a complex network that controls virtually all types of immune responses. We also discuss potential ways to measure these cytokines.

Some functions of cytokines include directing cells to the site of infection, causing cells to multiply, and stimulating them to produce antibodies. Some cytokines work together to produce a certain immune response, while some actually cancel out the effect of other cytokines. Methods of measuring cytokines can look at aspects of cytokine production such as the total amount of a cytokine present in a sample, identify the cells that produce them, or examine gene expression of the cytokine. The method used is based on the type of question the eco-immunologist wants to answer.

Most of what we know about cytokines comes from studies in mice and humans and, currently, over 60 different cytokines have been identified in these species. Recently, more research has focused on cytokines in fish, birds, reptiles, and amphibians, and we know now that not all types of animals produce the same cytokines. Different types of animals also face different challenges in their environment. For example, the immune system of reptiles is affected by environmental temperature, while that of birds is less likely to be similarly affected. This could potentially impact the cytokine production of cold-blooded animals and, ultimately, their immune response to a pathogen. Understanding how cytokines work in this wider range of animals can provide important information to eco-immunologists about why immune responses in wild animals are not always kept at a high, constant level.

Image caption: Ecologist at work. Photo provided by authors

 

Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds.

Jared G. Ali and Anurag A. AgrawalCaterpillar. Photograph by Ellen Woods.

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In the past two decades it has been well established that distinct herbivore species can indirectly interact through a shared host plant. An asymmetric interaction has been hypothesized for insects in different feeding guilds, such as aphids (‘suckers’) and caterpillars (‘chewers’). The general pattern observed is that by inducing the plant hormone salicylic acid, aphids enhance performance of caterpillars by reducing the induction of production of jasmonic acid, a hormone involved in plant defense. Although most of this work has been done using model plant species or crops, we present one of the few studies that have tested the assumptions of aphid-caterpillar interactions in wild plants, with herbivore species that naturally co-occur. This study confirms that aphids enhance performance of caterpillars (of the specialist monarch butterfly) and yet caterpillars reduce aphid performance on Common Milkweed. But on a closely related plant, Butterfly Milkweed, there were different induced responses after herbivory: aphids did not promote caterpillar performance, and caterpillars did not reduce aphid performance. That closely related wild species differ in their responses to aphids and caterpillars suggests that during their evolution they have diverged in their responses to these insects.

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

 

Complementary plant nutrient-acquisition strategies promote growth of neighbour species.

Francois P. Teste, Erik J. Veneklaas, Kingsley W. Dixon, and Hans Lambers Roots interacting, Photograph provided by author.

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Diverse plant assemblages in biodiversity hotspots tend to occur on nutrient-poor soils. Plant diversity is thought to be partly maintained by complementary nutrient-acquisition strategies and mycorrhizal networks that can increase plant growth. Greater understanding of positive interspecific interactions in nutrient-poor soils is a priority, particularly in phosphorus- (P) limited ecosystems where plants with contrasting nutrient-acquiring strategies co-occur. It is also relevant to agro-ecosystems, since global P stocks are being depleted. In this study, conducted in the SW Australia biodiversity hotspot, we assess positive interactions between coexisting plants with contrasting nutrient-acquiring strategies from highly P-impoverished soils.

Using a novel glasshouse ‘common garden’ approach, we explore enhanced growth and nutrient uptake among plants with different root morphologies that help them satisfy their nutritional needs. The first type of root was the cluster roots that mine soil phosphorus (Banksia). The second root type was the ‘ectomycorrhizal’ (literally fungus on outside of root) typical of Eucalyptus trees. The third root type was the ‘arbuscular mycorrhizal’ that commonly forms on Verticordia. Finally, we had a root type that had both ectomycorrhiza and arbuscular mycorrhiza (Melaleuca). These plants were grown together with or without root contact and with or without fertiliser. We measured plant performance, the nutrient concentrations in the leaves, and root characteristics at the end of the experiment.

Growth was best when Melaleuca grew beside Banksia and Eucalyptus. This ameliorated growth was only seen when roots could not intermingle and when the plants were not fertilised, that is when they grew in nutrient-poor soils. Facilitated uptake of nutrients such as P and manganese were likely responsible for the enhanced growth. Some root types formed more abundantly when plants grew beside neighbours with the ectomycorrhizal root type. We think that this root type was partly responsible for the enhanced growth and nutrients in Melaleuca.

This research improves our understanding of how plant roots interact with each other and how such interactions can contribute to the formation of diverse plant communities in natural areas on nutrient-poor soils. It will also deepen our understanding of mechanisms involved in plant coexistence and ecological restoration under changing precipitation regimes.

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

 

Meristem limitation explains lags in the response of productivity to changes in precipitation in arid grasslands.

Lara G. Reichmann and Osvaldo E. Sala Rainout shelter used in the rainfall manipulation experiment at the Jornada LTER. Dr. Reichmann (pictured) and Dr. Sala studied lags in the response of productivity to changes in precipitation.

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Ecologists have assumed for a long time that arid and semiarid ecosystems are mostly limited by water availability. Surprisingly, the strong relationship between mean annual precipitation and primary production that exists across regional precipitation gradients contrasts with the low correlation between current-year precipitation and production at individual sites. Although arid ecosystems account for 40% of land surface and are home for 30% of human population, we still have a limited understanding of mechanisms controlling inter-annual variability of primary production. Lags in the response of ecosystems to changes in precipitation explain why current-year precipitation accounts for only a small fraction of the variability in production from year to year. Results showed that legacies occur through changes in the density of meristems (plant growing points). Previous dry or wet years differentially affected the components of asexual reproduction, which in grasses are tiller (shoot) density, stolon density, tiller growth, axillary bud density and percent viable axillary buds of black grama. Stolon and tiller density were the most sensitive parameters to changes in precipitation and were responsible for the observed lags in production. On the contrary, percent of active axillary buds was insensitive to changes in precipitation.

This work contributed to our understanding of temporal controls of ecosystem functioning in water-limited regions. Current-year production depends on current-year precipitation and previous-year precipitation. The effect of the latter is mediated by changes in stolon and tiller density. In addition, this work highlighted the differences between temporal and spatial controls on primary production.

Image caption: Rainout shelter used in the rainfall manipulation experiment at the Jornada LTER. Dr. Reichmann (pictured) and Dr. Sala studied lags in the response of productivity to changes in precipitation.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Cellular adaptation to temperature in natural populations of Drosophila melanogaster.

Brandon S. Cooper, Loubna A. Hammad, Kristi L. Montooth Drosophila melanogaster. Image provided by authors..

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Membranes composed of phospholipids (fats with an attached phosphate group) separate cells from the external environment and provide structures where critical cellular functions, such as aerobic respiration, occur. Environmental factors like temperature can perturb these membranes with negative effects on cellular function. The vast majority of organisms on our planet are ectotherms, including the insects, whose body temperatures largely match the external thermal environment. Because of this, the cell membranes of ectotherms can become too fluid when the environment warms and too rigid when the environment cools. Insects at temperate latitudes experience seasonal and daily changes in temperature, and respond by behaviorally regulating their body temperatures (e.g., flying to a more comfortable temperature), or by adjusting their physiology (e.g., remodeling cell membranes to match their current environment). We were interested in how the model ectotherm, the fruit fly Drosophila melanogaster, evolves to respond physiologically to changes in temperature.

We previously showed that populations of D. melanogaster flies exposed for many generations to variable temperatures in the laboratory evolved an increased ability to remodel their cell membranes in response to temperature (i.e., they have greater cell membrane plasticity). These populations also have greater fecundity than flies from populations evolved under constant temperatures. These plastic physiological responses presumably enable flies to maintain cell function across a range of temperatures, but it remained unclear how this trait evolves in nature. In this paper, we show that a natural population of D. melanogaster from a variable thermal environment also has greater cell membrane plasticity than populations from less variable thermal environments, suggesting that similar evolutionary processes shape this trait in nature and in the lab. We also investigated the genetic basis of this trait and show that individuals that respond strongly during development as larvae also respond strongly as adults. However, adults that respond strongly to warm environments do not necessarily respond strongly to cool environments. Our data provide insights into genetic and physiological mechanisms of thermal adaptation in temporally variable environments.

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

 

Maternal effects and warning signal honesty in eggs and offspring of an aposematic ladybird beetle.

Anne E. Winters, Martin Stevens, Chris Mitchell, Simon P. Blomberg & Jonathan D. BlountSeven-spotted ladybird. Photo provided by authors.

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Eggs are often subject to intense predation. One parental strategy to deter predators is to produce eggs that are laced with noxious chemicals and are conspicuously coloured as a warning signal (known as aposematism). Ladybird eggs are yellow/orange and contain toxins known as alkaloids; these traits are believed to function in concert as visual signal and chemical defence respectively. However, it remains unclear whether such aposematic signals reveal the strength (rather than simply the existence) of chemical defences. Furthermore, additional functions of egg pigments and toxins could apply; in particular mothers might deposit such resources into eggs to aid the development of offspring, or to provide resources that could contribute to aposematic traits in offspring.

We bred seven-spot ladybird beetles in the laboratory, and then measured relationships between egg colouration (in terms of the colouration metrics ‘brightness’, ‘hue’, and ‘saturation’) and toxin concentrations (the alkaloids precoccinelline and coccinelline). We also measured relationships between egg levels of carotenoid pigments and egg colouration. Finally, for a subset of eggs that were allowed to develop and the offspring reared until adulthood, we measured relationships between the colouration of the wing cases (an aposematic signal) and body toxin concentrations. As expected, we found that egg colour saturation correlated positively with egg levels of carotenoid pigments. In addition, egg concentrations of precoccinelline were positively correlated with egg colour saturation and hue. However, there were no significant relationships between egg coccinelline concentration and any measure of egg colouration. In young adults of both sexes, wing case colour saturation was significantly correlated with egg saturation and hue. Finally, body concentrations of coccinelline were significantly correlated with wing case hue. These results suggest that the colouration of 7-spot ladybird eggs is a reliable signal of the strength of the chemical defences they contain, but in addition, maternal investment of pigments and toxins into eggs may serve to influence the reliability of aposematic signalling in resultant offspring.

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

 

Scaling leaf respiration in a tropical forest.

Martijn Slot, Camilo Rey-Sánchez, Klaus Winter and Kaoru KitajimaPhoto provided by authors.

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Plants respire to produce energy and building blocks for growth. A waste product of respiration is CO2. As temperature increases, more energy is needed to maintain cellular functions, and consequently, more CO2 is released back into the atmosphere. The flux of CO2 released by respiration to the atmosphere is almost as large as the opposite flux, in which photosynthesis takes up CO2 from the atmosphere, and almost a third of the total respiration flux comes from leaves. Quantifying leaf respiration in relation to temperature is thus important to estimate the carbon balance of forest ecosystems.

Tropical forests are an important contributor to the global carbon cycle, but their diversity and their height makes it difficult to measure respiration fluxes for all species. In this study we quantified respiration of leaves of 28 species of trees and lianas (woody vines) in the upper-canopy of a tropical forest in Panamá —making use of a construction crane to access the canopy— and we correlated respiration rates, and the sensitivity of respiration to short-term temperature change, to other leaf traits that are easier to measure. Using these trait-correlations and long-term temperature data at our study site, we predicted temperature-dependent respiration of the whole canopy from the behaviour of individual leaves.

In contrast to predictions from global datasets, leaf phosphorus was a stronger correlate of respiration than leaf nitrogen. The combination of leaf phosphorus content, photosynthetic capacity, and leaf mass per unit leaf area could explain 64% of the variation in respiration at a set temperature, while the sensitivity of respiration to short-term temperature changes could be predicted from the concentration of sugars and starch in leaves and the growth form of the species (trees versus lianas). Respiration scaled to the stand level from these traits was estimated to release 7.4 ton of carbon per hectare per year. Similar fluxes have been estimated for other tropical forests, suggesting that using correlations with easy to measure traits instead of tedious direct measurements of respiration may make it easier to predict carbon fluxes in tropical forests in relation to temperature at a larger spatial scale.

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

 

Lifetime consequences of food protein-carbohydrate content for an insect herbivore.

Karl A. Roeder and Spencer T. BehmerCaterpillar. Photo provided by authors.

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All animals eat to acquire nutrients. For herbivores, two particularly important nutrients are protein and digestible carbohydrates. However, protein and digestible carbohydrate content in plants is often highly variable – both within and between plants. Herbivores can overcome this variability because they have a strong ability to regulate their protein-carbohydrate intake by practising dietary self-selection. In some situations, though, herbivores may not be able to practise dietary self-selection. For example, predators might block access to certain plant tissues, or abiotic factors (e.g., drought) may limit the range of available protein and carbohydrates. Where this happens, herbivores will be forced to eat whatever is available. The effect of food protein-carbohydrate content has been studied in a number of different herbivores, especially in insect herbivores, but usually only over a short time period, and never over a herbivore’s entire lifetime. In this study we reared newly hatched caterpillars (the tobacco budworm, Heliothis virescens) on a range of diets that differed in their protein-carbohydrate (p:c) ratio; the diets used spanned p:c ratios that can be observed in plants that would normally be eaten by this caterpillar. We recorded larval survival, time to pupation, pupal mass, survival rates and time to eclosion (emergence from the pupa), and pupal body lipid content. Additionally, for each diet, we mated successfully eclosed males and females and measured egg production and viability. Our results suggest that larval performance may not be overly sensitive to food p:c ratio, except when this differs widely from the self-selected p:c ratio. However, as food protein-carbohydrate content becomes increasingly imbalanced relative to the self-selected p:c ratio, pupal performance, most notably eclosion success, decreases. Additionally, males are more sensitive than females to protein-carbohydrate imbalances. Finally, when food protein-carbohydrate effects are explored at the population level, by combining larval and pupal performance with reproductive output (to generate estimates of population size and generation time), it becomes clear that there is a specific p:c ratio that is functionally optimal, and that small deviations away from this optimal ratio can have strong negative repercussions.

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

 

Causal networks clarify productivity–richness interrelations, bivariate plots do not.

James B. Grace, Peter B. Adler, W. Stanley Harpole, Elizabeth T. Borer, and Eric W. Seabloom Causal analysis of Grime’s Humped-Back Model involves converting his pictorial abstraction (left panel) into a causal diagram (right panel) where the logical connections between hypothesized processes are made explicit and testable implications are revealed.

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Species diversity and productivity are among the most fundamental characteristics of ecosystems. While the importance of these ecological properties is universally agreed upon, the mechanisms connecting these two variables have been debated for decades without resolution. In an attempt to achieve a synthetic understanding of the collective effects of proposed mechanisms, some ecologists have turned to the examination of bivariate plots to see if particular patterns are consistently observed in nature.

In a recent study, Adler et al. (2011, Science) reported only weak correlations between richness and productivity in grasslands from around the world and urged future studies to “focus on fresh, mechanistic approaches to understanding the multivariate links between productivity and richness.” While some have applauded this call for a fresh approach, others remain focused on the study of simple scatterplots. Most recently, Pierce (2013, Functional Ecology) has reexamined the original data reported in the Adler et al. (2011) study using boundary regression and claimed that there are strongly predictive, humped boundary relationships between richness and productivity. Pierce goes on to argue that failure to support one particular model, referred to as the Humped-Back Model (HBM), undermines conservation efforts.

In our paper, we illustrate that Pierce’s analyses are invalid and that defensible statistical methods for examining boundary relationships confirm that any relationship between productivity and richness in the Adler data is weak at best. The main focus of our presentation, however, is on explaining why scatterplot patterns cannot help us understand controlling mechanisms.

In our paper we examine the HBM through the lens of causal networks. We begin by translating the HBM into a causal diagram, which shows explicitly how multiple processes are hypothesized to control biomass production and richness. We then evaluate the causal diagram using example data, showing that alternative mechanisms cannot be distinguished through the examination of scatterplots. Going further, we show that more sophisticated multivariate approaches are far more useful for both understanding ecological systems and informing conservation efforts.

Image caption: Causal analysis of Grime’s Humped-Back Model involves converting his pictorial abstraction (left panel) into a causal diagram (right panel) where the logical connections between hypothesized processes are made explicit and testable implications are revealed.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Lifespan in the wild: the role of activity and climate in bees.

Jakub Straka, Kateřina Černá, Lenka Macháčková, Monika Zemenová and Petr KeilSolitary bee Anthophora plumipes on flower; photo credit Pavel Krásenský (macrophotography.cz).

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Animal lifespan is potentially constrained by a number of environmental and physiological factors (temperature, humidity, metabolic rate, oxidative stress, etc.). Many of these have been studied in controlled conditions, but little is known about what influences animal lifespan in the wild. We assessed in situ environmental predictors of lifespan of two solitary bee species: a pollen specialist Andrena vaga (Andrenidae) and a pollen generalist Anthophora plumipes (Apidae). These bees forage and care for their offspring in the nests, and thus it is possible to observe them daily during most of their lives. For both species we collected extensive data on length of life, activity patterns during life and on environmental conditions, such as temperature, precipitation, sunshine, and pollen availability.

We found that lifespan is driven both directly by climate and indirectly by climate-dependent activity patterns. Specifically, we found a strong negative relationship between proportion of active days and length of life, and this proportion was related to climate. Also, individuals active during warm and/or wet days lived longer. Surprisingly, precipitation was a more important determinant of lifespan than temperature. Timing of the first appearance at the site was also an important predictor of the bee lifespan. Individuals that first appeared closer to the end of season lived for a shorter time than individuals that appeared earlier. Unsurprisingly, the exact timing of this first appearance was correlated with seasonal climate (temperature and precipitation).

Our study presents evidence that, in the wild, lifespan is constrained by an interplay of physical activity, precipitation, temperature, and food availability, and that this happens over at least two temporal scales (daily and seasonal). Understanding these constraints is important from both basic and applied perspectives. For instance, the prominent relationship between climate, activity patterns and lifespan suggest that climate change will have a profound effect on ecosystem services (e.g. pollination) that are directly dependent on animal activity and length of life.

Image caption: Solitary bee Anthophora plumipes on flower; photo credit Pavel Krásenský (macrophotography.cz).
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Community assembly effects shape the biodiversity-ecosystem functioning relationships.

Benoît Jaillard, Alain Rapaport, Jérôme Harmand, Alain Brauman, & Naoise NunanInteracting classes of species in a community .

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It is important to understand correctly how diversity influences the functioning of ecosystems, given the current loss of biodiversity and its likely effects on ecosystems. Many studies have tried to explain this relation in different environments such as plant, aquatic or microbial ecology. Usually scientists choose species at random from a given fixed species pool and test experimentally how assembling their behaviour influences the overall function of the ecosystem. They most often find that productivity increases with increasing biodiversity. Conversely, some people consider that ecosystems are dominated by a small number of species. With this idea, we decided to build a theoretical model based on the probability of interaction between species. We arbitrarily assigned species to one of three classes, subordinate, dominant and super-dominant species, ordered in a simple dominance hierarchy. Community functioning is determined by prevalent dominance rules. We tested two rules. One was the simple presence of a species determined if it dominated the ecosystem. The other was that the dominant species had to be present as a majority of species in order to achieve their dominant position. To our surprise we found that the system became rapidly very complex, even when only three species classes were present. We were also surprised to discover that all species, even the subordinate species, played a role in the functioning of the ecosystem. The model fitted experimental observations well. This parsimonious model provides a new framework for studying ecosystems, whatever their environment.

Image caption: Interacting classes of species in a community .
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Tolerance landscapes in thermal ecology.

Enrico L. Rezende, Luis E. Castañeda and Mauro Santos Thermal tolerance landscapes describe how survival is affected concomitantly by temperature and exposure times.

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Scientists predict that average temperatures may rise globally up to 4 ºC by 2100. In a warming world with increasingly extreme summers and winters, which organisms may be susceptible to, and threatened by, thermal stress? Answering this question is of paramount importance to predict, quite literally, who lives and who dies as a direct result of temperature changes in the forthcoming years.

The general approach to address this question has been to measure the highest or lowest temperature that an organism can tolerate. In practice, this involves subjecting the animal to increasingly warmer or colder temperatures, often in an oven or a freezer, until it can no longer respond. The temperature at which the animal eventually collapses in known as a critical thermal limit, and the temperature range that this animal can tolerate lies within the boundaries set by the hottest and coldest temperature it can cope with (that is, its upper and lower critical thermal limits).

Critical thermal limits have been measured in hundreds of species (mostly insects, and many fishes, amphibians and lizards), and results are puzzling. The hottest or coldest temperature that an organism can tolerate varies depending on how it is measured. With one protocol, a fly can tolerate 45ºC whereas with a different protocol it might collapse at 39 ºC, jeopardizing any attempt to predict the conditions in which this fly could be under thermal stress in nature.

In our perspective paper we discuss the limitations of this approach. The question is not only which temperature can an organism tolerate, but also for how long? In a sauna bath, just as the fly, a human being can tolerate 45 ºC for several minutes but would be in great danger if the exposure lasted hours or days. Because the harmful effects of temperature accumulate over time, the length of the exposure to stressful conditions matters. We quantify how much it matters and, by doing so, describe how temperature draws the thin line between life and death as exposure times change.

Image caption: Thermal tolerance landscapes describe how survival is affected concomitantly by temperature and exposure times.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Variation in early life testosterone within a wild population of red deer.

Alyson T Pavitt, Craig A Walling, Alan S McNeilly, Josephine M Pemberton & Loeske E. B Kruuk Female red deer (Cervus elaphus) with calf on the Isle of Rum, Scotland.

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The sex hormone testosterone is usually associated with male reproduction, but its effects are far broader than this. Concentrations can differ substantially between individuals, and whilst high levels can benefit males in the breeding season, they can also reduce survival by making animals of both sexes more vulnerable to parasites and disease. Most research in this area has focussed on adults so far, however we were interested in whether there were any effects of varying testosterone in juvenile animals. We measured testosterone in blood plasma collected from wild Scottish red deer calves across a 17 year period, as part of a long-running red deer study on the Isle of Rum. We were interested in whether the condition of either the mother or calf caused testosterone to differ between calves, and particularly whether this affected a calf’s chances of survival.

Despite calves being only around two days old, testosterone was already higher in males, although both sexes showed a striking decline across the first day of life which flattened off at low levels after 24 hours. Interestingly, male calves had lower testosterone if they were born in the years after an older brother than if they had an older sister or were a firstborn. This sibling effect could be mediated by the condition of the mother, as we know sons are more costly to raise than daughters in this population (male calves are born larger and suckle longer than females).

Whilst testosterone did not seem to relate to survival across all calves, firstborn males (a group particularly vulnerable to mortality) were less likely to survive their first year if their testosterone concentrations were above average. This suggests that a young deer’s testosterone concentration can negatively affect their survival, but that these effects are only apparent if they are already at a higher risk of death.

Image caption: Female red deer (Cervus elaphus) with calf on the Isle of Rum, Scotland.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Individual (co)variation in thermal reaction norms of standard and maximal metabolic rates in wild-caught slimy salamanders.

Vincent Careau, Matthew E. Gifford & Peter A. BiroSlimy salamander. Photo provided by authors..

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We all intuitively know that humans differ from each other in almost every aspect of their morphology (e.g., body mass), physiology (e.g., alcohol tolerance), and behaviour (e.g., shy vs. bold). Not surprisingly, these individual differences also exist – and are naturally interesting to study – within species of wild animals.

Individual differences are often viewed as the “raw” material on which natural selection can act, as individuals with certain variants of a given trait may survive and reproduce more than individuals with other variants. Individual variation itself can also be considered as the result of natural selection, as certain types of selection (correlational or balancing) can generate and maintain variation among individuals within populations.

Over the last ~30 years, evolutionary physiologists have studied individual variation in a variety of traits, including the standard (lowest) and maximal (highest) metabolic rate that can be expressed by ectotherms (i.e., “cold-blooded” animals). Standard and maximal metabolic rates are fundamental measures in ecology and evolution because they set the range of conditions within which animals can perform activities that directly affect Darwinian fitness. Several studies revealed that individuals of similar body mass show 1.5 to 3-fold differences in metabolic rate within a single population.

Although metabolism is typically measured at a constant temperature to eliminate this important source of variation, we intentionally measured standard and maximal metabolic rates from 10 to 25°C in wild-caught slimy salamanders. We found that individual differences persisted across this temperature range, but the magnitude of individual variation (expressed relative to the total phenotypic variation) was ~60% lower than regularly reported in studies conducted at a single temperature.

This result was somewhat expected because temperature introduces variation within individuals. Such variation within individuals has traditionally been overlook as it was considered as “noise” that obscures interesting differences among individuals. Yet, we have shown that part of this within-individual variation was due to differences in how individuals responded to changes in temperature.

These among-individual differences in thermal sensitivity represent additional raw material on which natural selection can act, and/or sources of adaptive (co)variation. Thus, our study reveals the importance of considering within-individual variation in these apparently co-adapted traits.

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

 

Community assembly and functional diversity along succession post-management

Radika Bhaskar, Todd E. Dawson, and Patricia BalvaneraTropical dry forest, Chamela Biological Reserve, Mexico. Photo by R. Bhaskar.

Ecologists have long been interested in whether plant communities recover in some predictable progression following a severe natural disturbance, such as a hurricane. Ecological theory suggests post-disturbance conditions are stressful, thus only the few species that can tolerate the harsh environmental filter will establish. With time, as conditions improve through recovery of vegetation and soil, a larger number of species can be supported, that then compete for resources.

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The analysis of vegetation recovery takes on new urgency in light of extensive human modification, particularly in the tropics. Anthropogenic disturbance may not be analogous to ‘natural’ disturbance, and may change the pattern of recovery in unknown ways. Tropical dry forests (TDFs), characterized by seasonal drought, are experiencing unprecedented clearing. Though they have received much less scientific attention than wet forests, TDFs are important as habitat and for human welfare. Understanding how recovery proceeds post-management can aid in restoration efforts of this vulnerable and critical system.

Morphological characteristics of plants, or plant traits, can be used to assess responses to environmental conditions, to detect environmental filters and competition. We evaluated the recovery of a TDF in western Mexico following cattle ranching. We measured leaf and stem traits in plots recovering for 1 - 15 years after the ending of ranching and compared them to neighboring conserved TDF.

Forest recovery was only partially consistent with ecological theory. One leaf trait response indicated a progression from a narrow to a wider range of trait values, related to a transition from uniformly high light availability to dense shade, however the other two traits contradicted theoretical expectations. Analysis of a stem trait suggested water limits species establishment at all stages of recovery, and may be a resource particularly important in TDFs. Unexpected patterns not consistent with solely environmental or competitive processes may be a result of management legacy; individual adult trees exist in modified sites because farmers have kept them in pastures while clearing surrounding forests. In addition some TDF species can respond to clearing by resprouting, growing new stems from previous trunks or roots.

Our results suggest that to understand vegetation recovery post-management we need to take into account the influence of human interventions and the particularities of tropical dry forests.

Image caption: Tropical dry forest, Chamela Biological Reserve, Mexico. Photo by R. Bhaskar.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Variation in elemental stoichiometry and RNA:DNA in four phyla of benthic organisms from coral reefs.

Catherine Lovelock, Ruth Reef & John Pandolfi Reef-scape, Lizard Island lagoon. Photograph by Dr Ruth Reef.

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The elemental composition of organisms, including carbon (C), nitrogen (N) and phosphorus (P) composition, is proposed to be linked to levels of RNA in organisms, which in turn influences rates of growth. In coral reefs, benthic corals and macroalgae (seaweeds) co-occur, competing for space on the reef. For these reasons we investigated elemental composition and RNA in reef corals and macroalgae at Lizard Island in the northern Great Barrier Reef lagoon. We surveyed species from four phyla and 53 genera, assessing the RNA:DNA ratio as an integrated measure of investment in nucleic acids to support growth. We tested a range of hypotheses aimed at increasing our knowledge of variation in elemental composition and RNA on coral reefs, including the role of phylogeny (genera, family, phyla) and of functional form. We found substantial support for links between elemental composition and RNA:DNA ratio in corals and algae. The RNA:DNA ratio was more closely correlated with N (and C:N ratio) than with P. Corals had higher concentrations of P and RNA:DNA ratios than macroalgae. Among the macrolagal lineages, consistent with hypotheses that predict higher C:P in lineages with low levels of complexity of their forms, C:P was higher in brown algae compared to red and green algal phyla. Genera of macroalgae with larger sizes tended to have higher N concentrations in their tissues than smaller forms. Analysis of phylogenetic sources of variation (family and genus) in elemental composition and RNA found that genus accounted for 15 – 47% of variation in both corals and macroalgae , but the largest source of variation (50-97%) was unexplained by our statistical model and thus most likely attributable to species, individual and environmental factors. Overall, variation in elemental composition of macroalgae was relatively low compared to that reported for terrestrial plants and was similar to that of corals. Our study shows that element ratios in marine macroalgae are different to terrestrial plants, which may underlie some of the differences between aquatic and terrestrial ecosystems, including more grazing but fewer specialist grazers in aquatic habitats. Additionally, our study indicates that theoretical models based on variation in RNA and elemental composition of corals and algae may be useful for predicting ecological interactions on coral reefs, although an enhanced understanding of uptake and storage of elements will be important for the development of models.

Image caption: Reef-scape, Lizard Island lagoon. Photograph by Dr Ruth Reef.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range.

Sarah R. McCann, Lee A. Rollins, Simon C. Griffith & William A. ButtemerThe cane toad (Rhinella marina, formerly Bufo marinus) is a large toxic anuran from South and Central America, currently spreading through its introduced range in Australia. Our studies on a montane cool-climate population of this invasive species show that toads can acclimate to low temperatures after only a few hours exposure. That rapid acclimation enhances the toad’s invasion success, and may allow it to spread into cooler regions than have been predicted by previous bioclimatic models. Photograph by Matt Greenlees.

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All around the world, invading species are causing problems for native ecosystems. In order to deal with the invaders, we need to know how far they are likely to spread in their invaded range. Several methods have been developed to do this, and one of the most accurate is to examine the range of climatic conditions that are available to the invader in its new home. In general, we expect invaders to be able to occupy only areas that have conditions fairly similar to those in which they usually live.

Sometimes, however, invaders have surprised us, by spreading into areas that we thought were unsuitable for them. For example, the large and highly toxic cane toad has colonized much of tropical Australia, including areas much more arid than its home in the rainforests of South and Central America. Cane toads are now also moving into areas of southeastern Australia that were thought to be too cold for them. How can this tropical amphibian survive in the high, cold Border Ranges region of northeastern new South Wales?

We measured the cane toad’s ability to function at low temperatures by catching toads and cooling them down, to assess the temperature at which a toad was unable to flip itself back over if placed on its back. As we expected, toads from higher colder areas were able to function at lower temperatures than toads from nearby warmer places. Remarkably, however, even a few hours of being kept at low temperatures improved a toad’s thermal tolerance. Cane toads can rapidly adjust their physiology to deal with cold conditions.

That ability to adapt to low temperatures suggests that cane toads may be able to spread even further in Australia than is predicted by current models. More generally, animals that can acclimate quickly to extreme conditions may be especially troublesome invaders, extending further than we ever thought possible.

Image caption: The cane toad (Rhinella marina, formerly Bufo marinus) is a large toxic anuran from South and Central America, currently spreading through its introduced range in Australia. Our studies on a montane cool-climate population of this invasive species show that toads can acclimate to low temperatures after only a few hours exposure. That rapid acclimation enhances the toad’s invasion success, and may allow it to spread into cooler regions than have been predicted by previous bioclimatic models. Photograph by Matt Greenlees.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Changing leaf nitrogen and canopy height quantify processes leading to plant and butterfly diversity loss in agricultural landscapes.

John G. Hodgson , Jerry Tallowinc, Roger L. H. Dennis , Ken Thompson, Peter Poschlod, Mewa S. Dhanoa, Mike Charles, Glynis Jones, Peter Wilson, Stuart R. Band, Amy Bogaard, Carol Palmer, Gaylynne Carter, Alison Hynd.The English countryside: a mosaic of farmed and unfarmed components. Photo provided by authors..

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Agri-environment schemes that support wildlife friendly farming practices aim to counterbalance impacts of intensive agriculture on biodiversity in the countryside. Using England as an example, this paper attempts to quantify the effectiveness of these schemes not, in the traditional way, by identifying ‘winners’ and ‘losers’, but by examining the impact of key processes that determine the species composition of the countryside.

We compared three independent numerical measures for the English countryside: the farmer’s viewpoint (as identified by governmental agricultural statistics), the nature conservationist’s (using distribution atlases of plant and butterfly species) and the ecologist’s (using published functional traits of individual plant species to quantify their tolerance to changes in environmental variables such as soil fertility and frequency of management ).

We show that despite the implementation of agri-environment schemes and other conservation measures, diversity of native English plants remains strongly negatively correlated with agricultural intensity, as assessed from governmental agricultural statistics: heavily farmed English counties are disproportionately poor in species. Moreover, this lower biodiversity in the most intensively-farmed parts of England results from two separate processes. On farmland itself, the exclusion of slow-growing species of infertile soils, intolerant of ‘active’ management processes designed to boost crop yields (e.g. fertilizer additions and herbicide application to eliminate competition by weeds) was most complete in intensively farmed landscapes. However, much floristic diversity probably now resides (at least within arable regions) in unmanaged (or infrequently-managed) habitats outside the ‘working agricultural landscape’ (field margins, old quarries, track and roadsides) and here, associated with an increase in plant height, more ‘passive’ processes are at work. In these unmanaged parts of intensively farmed regions, tall species have been encouraged at the expense of shorter ones. Moreover, these continuing changes, both ‘active’ and ‘passive’, are not confined to plants. The butterflies considered most at risk of extinction feed, both as larvae and as adults, on slow- and low-growing food plants.

Analyses of this type can help improve conservation policies. For example, efficiency can be increased simply by integrating policies for conserving biodiversity within and outside farmland. Future improvements should be generated not, as in the past, by ‘learning from mistakes’ but by predicting and anticipating potential problems by reference to ecological and economic theory and through experimentation and data analysis.

Image caption: The English countryside: a mosaic of farmed and unfarmed components. Photo provided by authors..
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Interlopers pay the rent in nitrogen rather than protection in an ant-plant.

Joyshree Chanam, M.S. Sheshshayee, Srinivasan Kasinathan, Amaraja Jagdeesh, Kanchan A. Joshi and Renee M. BorgesLay Summary Photograph Caption:  Ants on a young leaf outside an ant shelter or domatium. Photocredit: Joyshree Chanam.

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Myrmecophytes are special plants with unusual interactions with ants. Such plants produce nesting shelters called domatia for ants and could also provide ants with liquid or solid food. These benefits to ants have traditionally been considered to be in exchange for protection services that the ants provide against herbivores. The production of domatia was considered to be a strong incentive for protective ants to reside within these plants. However, whether plants with domatia had greater reproductive success in terms of fruit set owing to the presence of domatia has been difficult to examine because myrmecophytes almost always produce domatia, and it is difficult to remove domatia from plants. However, in the unique myrmecophyte Humboldtia brunonis, found only in the Western Ghats of India, only some individuals bear domatia on some of their branches, each domatium formed by modified swollen and hollow internodes, while all individuals produce extrafloral nectar. Moreover, these domatia meant for protective ants are prone to interloping residents because they have a self-opening slit that allows access to the domatium interior. Consequently, domatia in H. brunonis are occupied not only by many ant species, of which only one provides protection against herbivores, but also by numerous other invertebrates, most unusually an arboreal earthworm, which has antagonistic interactions with ants. Earlier studies have established that domatia-bearing H. brunonis plants have greater fruit set, hence greater reproductive success, than those without domatia. We show that plant tissues near domatia received 17% and 9% of their nitrogen from the ants (protective and non-protective) and the earthworm respectively. We also demonstrate that the absorbed nutrients travelled to distant branches; hence, fruit set was not different between branches with and without domatia. This is the first study to demonstrate that non-protective interlopers in the domatia pay the rent by contributing to plant nutrition. This can explain why even before the establishment of a specialised protection-based symbiosis with ants, plants bearing domatia may be favoured because of the nutritional benefits provided by a motley set of domatia residents that could even include arboreal earthworms.

Image caption: Lay Summary Photograph Caption: Ants on a young leaf outside an ant shelter or domatium. Photocredit: Joyshree Chanam.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

A close arrangement of insect olfactory cells improves discrimination of odour sources.

Muhammad Binyameen, Júlia Jankuvová, Miroslav Blaženec, Rastislav Jakuš, Liwen Song, Fredrik Schlyter & Martin N. AnderssonEuropean spruce bark beetle, Ips typographus (left), and field trapping site (right). Photo courtesy of Fredrik Schlyter and Júlia Jankuvová..

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How does an insect find food and mates over a distance, avoiding nearby stale food, defence chemicals, and competitors? It has been suggested that a specific, very close arrangement of olfactory cells inside olfactory hairs helps insects to find attractive sources of odour that are in close proximity to unpleasant odours. If two cells detecting two different odours are located within the same hair (“co-localised” cells), the insect should in theory be able to more precisely determine whether the odours emanate from the same source or from two closely separated ones, as compared to if the cells were located further apart on the antenna. For example, when two odours are released from the same source, they will activate the co-localised cells at exactly the same time, while odours that emanate from different sources would activate the cells at slightly different time points, providing the brain with a different temporal response pattern.

We show that the close arrangement of olfactory cells in olfactory hairs improves discrimination of odour sources in an important forest pest, the bark beetle Ips typographus, under natural field conditions. This beetle coordinates mass-attacks on trees by using an aggregation pheromone, but some odours released from attacked trees reduce the pheromone attraction. A tree defence compound, cineole, is one such odour, and verbenone is another. The beetles use the latter compound to avoid trees in late attack phases with low nutritional value, and the two compounds reduce pheromone attraction to similar levels. The olfactory cells for cineole, but not those for verbenone, are found in the same olfactory hairs as the cells for an essential pheromone component.

We used this olfactory subsystem to test the beetle response to the two inhibitors when they were placed at different distances from the pheromone on traps in the field. Beetle trap catch increased at shorter distance between the pheromone and cineole sources than between the pheromone and verbenone sources, demonstrating a better olfactory acuity for odours that are detected in the same olfactory hairs. This finding is of general importance for understanding principles of form and functions of the insect olfactory sense and will help to inform the utilisation of inhibitors for forest protection against bark beetles.

Image caption: European spruce bark beetle, Ips typographus (left), and field trapping site (right). Photo courtesy of Fredrik Schlyter and Júlia Jankuvová.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Chemical compounds in fruits defend against pests.

Susan R. Whitehead and M. Deane BowersSibaria englemani feeding on an immature infructescence of Piper sancti-felicis. Photo credited to Susan R. Whitehead.

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Plants produce fruits primarily to attract fruit-feeding animals, who benefit plants by inadvertently transporting seeds to new sites. However, the same nutritional rewards produced in fruits to attract beneficial animals can also attract a variety of pests and pathogens, which feed on fruits without providing any service to the plant. In this study, we examined whether some of the natural chemical compounds produced in fruits function to defend plants against fruit pests and pathogens. We focused on the plant genus Piper, a diverse group of tropical plants. Many plants in this group produce complex mixtures of chemical compounds called amides. For example, amides are responsible for the spicy heat of black peppercorns, which are the dried fruits of Piper nigrum. Our results show that amides also serve an important role in fruit defense. Certain amides deterred feeding by an insect seed predator and also strongly reduced the growth rates of several strains of fruit-associated fungi. We tested a variety of individual amides and mixtures of amides, and all showed some bioactivity against insects and/or fungi, although the strength of the effects were variable depending on the specific mixture of compounds and species of fruit pest being tested. In addition, our results showed that certain amides interacted with each other when they occurred in combination, such that the effects of the amide mixtures could not be predicted by simply adding up the effects of the individual compounds present. In some cases, the compounds interacted synergistically, leading to a stronger than expected effect, and in other cases they interacted antagonistically, leading to a weaker than expected effect. Overall, this study provides new evidence of the importance of fruit chemistry in plant defense against fruit-feeding pests and also emphasizes the potential complexity of effects on pests when compounds are present in mixtures.

 

Image caption: Sibaria englemani feeding on an immature infructescence of Piper sancti-felicis. Photo credited to Susan R. Whitehead.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Epiphytes improve host plant water use by microenvironment modification.

Daniel Stanton, Jackelyn Huallpa Chávez, Luis Villegas, Francisco Villasante, Juan Armesto, Lars Hedin and Henry Horn Epiphytes such as these fog-soaked lichens can greatly change the microclimate of the host canopy in arid environments.

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Epiphytes, plants that grow on other plants (including mosses, lichens, ferns and flowering plants) are often overlooked when we study forest ecology. Nonetheless, they can occur in very large quantities and researchers have shown them to contribute significantly to water and nutrient cycles in forests. Getting a clear picture of how much impact epiphytes can have is challenging: comparing trees with different epiphyte loads can confound factors (are the conditions different due to the differing amounts of epiphytes, or do the amounts of epiphytes differ because of conditions) and removing epiphytes involves difficult and dangerous tree-climbing.

However, not all epiphyte-covered trees are large. By working at two desert sites that receive large amounts of fog (one in northern Chile, one in southern Peru) we were able to strip epiphytes from naturally growing plants that were small (1-5m) and separate (so that overlapping canopies did not interfere). We removed either all of the epiphytes (from Caesalpinia spinosa trees in Peru) or half of the epiphytes (from the north or south-facing sides of Eulychnia spinosa cacti in Chile) and studied the effects of soil water and microclimate for the host. Furthermore, we complemented these experiments by constructing artificial cactus mimics that could be decked with epiphytes and studying soil moisture and microclimate in the absence of root water uptake and host transpiration.

Although we expected the epiphytes to increase the water inputs to the soil (by intercepting more fog that could then drip to the ground), we found the opposite: epiphytes held water in the canopy and decreased inputs to the soil. This water retention wasn't bad for the host though; plants with epiphytes took up soil water more slowly. This is explained by the epiphytes creating a significantly cooler and moister environment in the host plant canopy, with the potential to greatly reduce losses through transpiration. These results show that, at least in some ecosystems where epiphytes are abundant, epiphytes can have big impacts on the trees, and should be considered in models of forest ecosystem processes.

Image caption: Epiphytes such as these fog-soaked lichens can greatly change the microclimate of the host canopy in arid environments.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Carbon and phosphorus linkages in Daphnia growth are determined by growth rate, not species or diet.

James M. Hood and Robert W. Sterner Daphnia. Photo credited to James Hood and Robert Sterner.

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All living things require a unique combination of chemical elements to grow and reproduce; therefore, the chemical composition of organisms can provide clues about the life and history of individuals and species. For example, the phosphorus (P) content of invertebrate bodies is one trait used to explain invertebrate distributions across gradients of P (which varies widely among water bodies and commonly limits algal growth). Because a large proportion of the P in invertebrates is associated with biomolecules involved in growth, several authors have predicted that the P content of invertebrates (a snapshot of their past and, possibly, future demand for P) should be positively correlated with a species’ growth rate, sensitivity to P limitation of growth and hence, abundance. This linkage between P and growth has a strong biological basis, but there is mixed support for relationships between fitness and the simple measure of body P. This study shows that growth-P linkages are revealed when a more realistic measure of demand is used.

We measured the growth of seven Daphnia (water flea) species on algal diets with low and high phosphorus contents and used this information to test predictions about relationships among body P content, growth rate, and sensitivity to P limitation. Like several other studies, we did not find support for the predicted relationships among these traits. However, by using an alternative approach -examining the linkage between carbon (C) and P accumulation in juvenile growth- we did find support for the principle that the P requirements of growth creates a tradeoff between maximizing growth and minimizing susceptibility to growth depression on low P diets.

Our results indicate that examination of C and P linkages in growth can replace body P content in predicting P demand, competitive tradeoffs, and perhaps even the role of species in nutrient cycling. Furthermore, our new approach appears to work better under the constantly changing conditions of aquatic systems. We hope that the approach we identified can be used to better understand how biochemical linkages between elements influence organisms and shape elemental cycles.

Image caption: Daphnia. Photo credited to James Hood and Robert Sterner.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

How to blend in.

Sami Merilaita and Marina DimitrovaCatching blue tits. Photo provided by authors.

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Background matching means that an animal blends into its background due to visual similarity between its colour pattern and the environment. Background-matching coloration is a common form of protective coloration that has evolved in a broad range of animals. Although the similarity between the colour pattern of an animal and its natural background can be measured in many different ways, from an ecological and evolutionary viewpoint it is the degree of similarity experienced by a natural predator of the animal that is important as it determines the detectability of the pattern and hence its protective value. We explored the relationship between similarity and detectability by testing how stepwise changes in similarity in geometry between prey colour pattern and the visual background are reflected in its detectability. We conducted a predation experiment using artificial prey items and backgrounds. As predators we used wild-caught birds, blue tits, which typically search for camouflaged prey items for food. We trained the birds to search for artificial prey items that each concealed a piece of peanut as reward. In the experiment each bird received twelve presentations of prey with body colour patterns that to different degrees resembled the background, and we recorded the time it took the birds to detect the prey items. We found that initially the relationship between similarity and detectability was not linear. Instead, for prey that had high background matching, similarity had a larger impact on detectability than for prey with lower background matching. Most animals live in visually variable environments, and we also investigated background matching in an environment consisting of two different backgrounds. Obviously a colour pattern cannot simultaneously resemble perfectly several different background patterns, and therefore maximisation of background matching in a variable environment is more problematic. We found that a colour pattern that was a compromise between the two different backgrounds did equally well as the prey pattern that matched perfectly one of the backgrounds and mismatched the other. In conclusion, close similarity is strongly favoured in a single background, but in a variable environment a compromise pattern that only loosely resembles both backgrounds can provide relatively good protection.

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

 

Exploring the nutritional basis of starvation resistance in Drosophila melanogaster.

Kwang Pum Lee and Taehwan Jang Drosophila melanogaster under starvation. Photo courtesy of authors.

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Hunger is the most common stress encountered by all animals living in natural conditions where food is often scarce. Those individuals that withstand starvation better are more likely to pass on their genes to the next generations. It is common sense that how long animals can live without food depends partly on how much energy is stored in their body, which is in turn determined by the amounts and types of nutrients in foods they have been eating. It is not yet clear whether it is the quantity or the blend of nutrients that really matters for animals facing extreme food shortages. In this study, we used Drosophila fruit flies to tackle this tricky issue. Flies were fed diets with varying concentrations and ratios of protein and carbohydrate before they were plunged into the state of hunger. We found that flies that were previously fed low-protein, high-carbohydrate diets survived starvation longer than those fed high-protein, low-carbohydrate diets. Against our expectation, the amount of calories and nutrients eaten by flies had little influence on their resistance to starvation. These results tell us that the dietary balance between ingested nutrients is more important than the mere sum of caloric intake for flies when fighting hunger. To understand what really goes on inside the bodies of starving flies, we carefully tracked how their body nutrient reserves changed during starvation. According to our results, flies preferentially utilized non-fat substrates in the body to support life during the early stage of starvation. But once these resources were used up, they switched to burn off body fats throughout the remaining period of starvation. Flies died of starvation when fat reserves were emptied. Collectively, this study highlights that the way that animals cope with starvation is basically a nutritional process. For this reason, any phenotypic or genetic changes in starvation responses should be understood in a nutritional context.

Image caption: Drosophila melanogaster under starvation. Photo courtesy of authors.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Leaf plumbing systems: efficiency and safety across biomes.

Andrea Nardini and Jessica Luglio  Photo provided by authors.

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Leaves must transport huge amounts of water in order to keep cells hydrated and allow them to photosynthesise. In fact, CO2 uptake is unavoidably coupled to massive water flow to the atmosphere, exposing plants to the risk of fatal desiccation. Water transport in the plant is based on negative pressures i.e. water is pulled from the soil through roots, stems and leaves via a network of conduits inter-connected to each other. If water pressures within these conduits become too low, either because of high air temperatures forcing evaporation and/or because of low precipitation making water less available in the soil, the water transport system can be damaged by air entry into the generally water-filled conduits, leading to plant desiccation and death. The intricate vein system of the leaf is apparently very vulnerable to such damage when compared to the main stem.

We have compared the leaf hydraulic efficiency and safety toward drought-induced damage by comparing values reported in the literature for 130 woody flowering plants growing throughout the globe. We found that tropical plants have leaves that are very efficient in transporting water but relatively less drought resistant when compared to plant inhabiting temperate and dry woodlands. Clear relationships emerged across three major biomes between leaf hydraulic efficiency and vulnerability, and mean annual precipitation of each species' habitat.

Also, 'safer' leaves of plants inhabiting dry habitats were relatively less efficient in hydraulic terms, as they invested more carbon and dry mass into the construction of their plumbing system, probably leading to their inherently lower growth rates when compared to plants growing in more humid habitats.

This study suggests that plants need to optimize the compromise between efficiency and safety when building their leaves. Hence, leaf hydraulic features play a very important role in shaping vegetation at different scales, from micro-climatic niches up to extended biomes.

Image caption: Photo credited to Andrea Nardini.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Confusing Females: Colour Differences May Make Female Butterflies Difficult for Males to Identify.

Lisa B. Limeri and Nathan I. Morehouse  Orange-and-black (left) and white-and-black (right) females of the Orange Sulfur butterfly, Colias eurytheme. Photo courtesy of authors.

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The diversity of colour patterns in nature has long fascinated biologists. Particularly puzzling are cases where members of the same species are colored differently. Common examples of this phenomenon, known as color polymorphism, include human hair color and eye color. However, how and why different color forms are maintained in populations over long periods of time is often not well understood. In the Orange Sulfur butterfly, a common agricultural pest that feeds on alfalfa, females come in two different color forms: black-and-orange or black-and-white. Black-and-white females, called ‘albas’, produce their less colorful patterns by reducing the amount of pigmentation in their wings, a strategy which allows them to reinvest these resources in faster development and increased egg production. Biologists have suggested that this strategy comes at a cost to ‘alba’ females, because males prefer to mate with the black-and-orange females. However, although some evidence for a male mating bias against ‘alba’ females does exist, little is known about why males would discriminate against these females, especially considering their higher egg production ability. We evaluated the hypotheses that either 1) males find ‘alba’ females difficult to see in their natural environments, or 2) males experience difficulties telling ‘alba’ females apart from other black-and-white butterfly species that live in the same habitats. Using detailed information about the vision of these animals, we “viewed” ‘alba’ and non-‘alba’ females through male eyes using mathematical models of butterfly vision. We find mixed evidence for the idea that ‘alba’ females may be more difficult to see against common backgrounds. However, we do find that males should face challenges discriminating between ‘alba’ females and other white butterflies commonly found in their environment. This suggests that the difficulties associated with properly distinguishing ‘albas’ from other species may be one reason underlying male mate biases against these black-and-white females. Such mating biases may counteract the other advantages of being an ‘alba’ female. Thus, limitations to male visual abilities may be important in maintaining both female color forms in this butterfly.

Image caption: Orange-and-black (left) and white-and-black (right) females of the Orange Sulfur butterfly, Colias eurytheme. Photo courtesy of authors.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Changing drivers of species dominance during tropical forest succession.

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

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

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

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

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

 

Smart limpets: complex behaviour in "simple" animals.

Giacomo Santini, Avis Ngan, Michael T. Burrows, Guido Chelazzi and Gray A. Williams  Observing the behavior of Cellana grata at Cape d’Aguilar, Hong Kong.  Photo credit: Avis Ngan.

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Most animals have the ability to respond to environmental challenges, adopting complex behavioural patterns that maximize their survival and reproductive output (i.e. their 'fitness'). Limpets, marine rocky shore molluscs, are no exception. Many limpet species live in the rocky intertidal: a narrow belt between the land and sea which experiences cyclical changes in environmental conditions dictated by the rise and fall of the tide. In such an environment, even a seemingly simple decision such as deciding when to move from a safe area to forage, has to be balanced against a number of changing constraints and stressors (e.g. heat stress, dehydration or predation).

Clarifying if an animal adopts optimal, fitness-maximising, solutions to foraging problems is a complex challenge, which can be addressed using mathematical models which allow predicted optimal behavioural decisions to be compared to real, observed, behaviours. Among the possible modelling approaches one could employ, the so-called 'State Dependent Models' (SDM) represents a powerful, although poorly exploited, option. Basically, such models monitor how the internal state of an animal changes as a consequence of its behaviour, and how such changes may affect further decisions. For example, if an individual has recently obtained food, this satiated state will make the individual less likely to immediately foraging to obtain more food. One of the main criticisms directed to such models is the large amounts of information which have to be initially collected to produce realistic models of behaviour. In this paper we developed a SDM model for the temporal organization of foraging in the intertidal zone, using the tropical limpet Cellana grata as a test species. Estimates of all the relevant variables affecting its behaviour were obtained to build the most realistic model possible. The derived model was able to satisfactorily reproduce the foraging behaviour of the limpet, which clearly organized its activity in a way that maximized its fitness. In addition, the results highlighted several emergent details of the limpets behaviour which were not immediately apparent or predicted using simpler models, demonstrating the benefits of this modelling approach.

Image caption: Observing the behavior of Cellana grata at Cape d’Aguilar, Hong Kong. Photo credit: Avis Ngan.
Image caption: Epiphytes such as these fog-soaked lichens can greatly change the microclimate of the host canopy in arid environments.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

 

Cycad cones’ thermogenic signals govern pollinators’ behaviour

L. Irene Terry, Robert B. Roemer, Gimme H. Walter and David BoothTwo male cycad plants in Brisbane Forest Park near Brisbane, Australia, each with a cone in the pollination phase.  The plant on the left is in about day 1 of the pollination period (of about 10 days duration) and the right hand plant’s cone is near day 3.

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The discovery that reproductive organs of some plants self-heat to high temperatures was made centuries ago, but its function(s) remain something of a mystery. The organs involved can switch rapidly from a resting metabolic rate that produces negligible heating to values as high as 10 W/kg in cycad cones, for example, a value comparable to an exercising human. Although many investigators have speculated on the role this energetically costly thermogenesis plays in pollinator behavior, few studies have investigated how associated chemical changes influence the pollination process. Thermogenic heating is a by-product of the plants’ ramped up metabolic activity, which also increases CO2 emissions and relative humidity and, in some cycad cones, volatile organic compound emissions. We studied the effects of all of these factors on the behavior of a specific pollinator of cycads, the thrips insect, Cycadothrips chadwicki. This species is the sole pollinator of the cycads Macrozamia lucida and M. macleayi, and relies entirely on these plants for its own reproduction. In addition, these cycads depend on this insect to vector pollen from male to female plants.

During each cone’s pollination phase of about 10 days, male and female cycad cones go through a daily, mid-day burst of elevated metabolism that causes a temperature rise of up to 12-15°C. Cones also emit high levels of water vapor, CO2 and ß-myrcene, the primary volatile component, during these metabolic spurts. At this time, thrips fly from the cone en masse (each male cone hosts thousands of these tiny insects). Later in the day, when cone metabolism has subsided, thrips forced out of a male cone earlier in the day return carrying pollen on their body surface . Thrips that enter female cones may then fertilize the ovule.

We investigated the responses of thrips to light, different temperatures, low to high concentrations of ß-myrcene, CO2, and water vapor. We expected that elevated levels of all of the signals (which occur as a consequence of cone thermogenesis in nature) would repel thrips based on our previous field observations. We found that thrips responded to all of these signals except CO2, and the response depended on temperature. At low, overnight temperatures, thrips movement was minimal, and they avoided light. By contrast, they were highly attracted to light at higher temperatures, and they avoided the high temperatures found inside cones during peak thermogenesis. ß-myrcene was repellent at high concentrations but was slightly attractive at low concentrations, regardless of temperature. Thus the increases in temperature and chemical concentrations associated with thermogenesis act together to drive thrips from cones, and at high levels none of the signals attract thrips. Other signals must attract them back to cones later in the day when thermogenic metabolic activity has declined. The pollination system is therefore a push-pull system regulated by the plants.

Image caption: Two male cycad plants in Brisbane Forest Park near Brisbane, Australia, each with a cone in the pollination phase. The plant on the left is in about day 1 of the pollination period (of about 10 days duration) and the right hand plant’s cone is near day 3.
This paper can be found online in its As Accepted form (not typeset or proofed) here.

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