Lay Summaries

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

Lay summaries for the current issue, which includes our latest Special Feature: Ecosystems, Evolution and Plant–Soil Feedbacks.

 

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.

 

 

Conserving rare species when de-extinction is an option

Gwenllian Iacona, Richard F. Maloney, Iadine Chadès, Joseph R. Bennett, Philip J. Seddon, Hugh P. PossinghamThe Huia (Heteralocha acutirostris), is an extinct New Zealand bird species with an interesting dimorphism such that the female has a dramatically longer bill than the male. The last individuals may have survived until as recently as the 1960s. Species such as this are often suggested as candidates for de-extinction: they are recently lost species of significant conservation interest, and the threats that caused their extinction are known. This paper discusses how using a decision theory approach to conservation prioritization can help managers decide if de-extinction of such species is a good idea.   – photographer J.L . Kendrick. Photo courtesy of the New Zealand Department of Conservation.

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The technology to revive extinct species (de-extinction) may soon no longer be simply in the realm of science fiction. In the exciting rush to bring back populations of wild mammoths, or moa, or passenger pigeons, we need to take a step back and make sure that the conservation benefits of such an action outweighs any potential perverse negative impacts. We suggest that the decision tools used in modern conservation prioritization approaches can quantitatively and transparently weigh the pros and cons of de-extinction. This is especially relevant to managing a de-extinct species in the wild in systems where there are extant species of conservation concern. While outlining the steps to the process, we discuss the new considerations that would be important if de-extinction was a possible conservation action. One particularly interesting implication of de-extinction would be its capacity to change the biodiversity conservation problem from the current one that is similar to managing non-renewable natural resources, to a version where the management is of a potentially renewable natural resource. This switch opens up a new suite of time preference and risk aspects to rare species management which could change the strategies employed by managers and the possible conservation outcomes. We are not arguing for or against de-extinction. Instead, we are proposing that the technological advances need to be considered within the context of the existing conservation landscape, and that such considerations may include unprecedented modifications to the current species prioritization problem.

Image caption: The Huia (Heteralocha acutirostris), is an extinct New Zealand bird species with an interesting dimorphism such that the female has a dramatically longer bill than the male. The last individuals may have survived until as recently as the 1960s. Species such as this are often suggested as candidates for de-extinction: they are recently lost species of significant conservation interest, and the threats that caused their extinction are known. This paper discusses how using a decision theory approach to conservation prioritization can help managers decide if de-extinction of such species is a good idea. – photographer J.L . Kendrick. Photo courtesy of the New Zealand Department of Conservation.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Root heterogeneity along an arctic elevational gradient: the importance of resolution

Sabrina Träger & Scott D. WilsonRoots in arctic forest in a minirhizotron image (13.5 x 18 mm). Photo by S. Träger.

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The majority of ecological studies focus on aboveground parts of plants and their interaction with the environment. However, plant roots often account for 80 – 90 % of plant biomass, especially in the Arctic. Roots are the key link providing plants with nutrients and water, and providing organic carbon to soils. Patchy distribution of resources can lead to and in turn be influenced by patchy root growth.

The magnitude and spatial scale of root patchiness varies with the dominant vegetation type (e.g. forest or grassland). However, studies are limited to temperate regions and deal with scales ranging between a few kilometers to a few centimeters. At the same time, the root diameter and thus the scale of interaction with the environment can be as small as fractions of a millimeter. Knowledge about root patchiness at those scales is still missing.

We analyzed the magnitude and scale of fine root patchiness in the Arctic at resolutions ranging from 1 to 300 mm² along an arctic alpine gradient (500 to 1100 m above sea level) to cover a variety of vegetation types (from forest to tundra). To study roots in their natural environment and in a non-invasive way we used a minirhizotron camera.

Roots in all vegetation types responded to or generated very fine scales of spatial patchiness of a few millimeters, which are scales about five times smaller than those that have previously been found. The patchiness of roots was greatest at the highest elevation, tundra, where the smallest plants dominated, which stands in contrast to studies from temperate regions where patchiness increases with plant size. Both the magnitude and scale of heterogeneity varied with sampling resolution, suggesting resolutions as small as a few millimeters are relevant to studies of spatial root interactions and belowground processes.

Image caption: Roots in arctic forest in a minirhizotron image (13.5 x 18 mm). Photo by S. Träger.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Stress hormones may help handicapped moms produce young

James W. Rivers, Gretchen N. Newberry, Carl J. Schwarz and Daniel R. ArdiaPhoto provided by authors.

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Stress hormones are typically thought of as being bad for one’s health, but they can be beneficial to individuals over short-term periods of high energetic demand. In this study, we evaluated whether female violet-green swallows, small insect-eating birds found throughout western North America, had altered stress hormone concentrations while undergoing unplanned energetic challenges when rearing young. To test this idea, we experimentally removed a small number of wing feathers at two different intensities (low and high) in some individuals, whereas other individuals were handled in the same manner but had no feathers removed. We measured stress hormone concentrations at two points during the breeding season when females were feeding their young: immediately prior to feather removal, and 10 days later. We also assessed whether females in the three groups varied in how often they fed their offspring, as well as the quality and quantity of young that were raised.

Females in the three groups were initially similar in their body size and in their baseline stress hormone concentrations. However, females experiencing feather removal were found to have much greater increases in baseline stress hormones, and the amount of stress hormones was positively linked to the degree of feather removal. Despite this, females in both feather-removal groups were able to maintain feeding rates at levels similar to control females, and they produced a similar number of young. Offspring from mothers in the different groups did, however, have different levels of stress hormones, the reason for which remains unclear. Overall, this study suggests that energetic challenges are associated with increases in stress hormones, and such increases appear to allow female swallows to maintain feeding rates at a level typical of control females and produce a similar number of offspring. Thus, stress hormones may provide individuals with a way of ramping up their parental effort when they encounter unexpected energetic challenges, so they can produce the same number of young they would have done during a normal breeding season.

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

 

Effects of flooding on relationships between plants and soil fauna

Corentin Abgrall, Matthieu Chauvat, Estelle Langlois, Mickaël Hedde, David Mouillot, Sandrine Salmon, Bruna Winck and Estelle ForeyView of the considered flooding gradient from the mudflats (photo credit: Estelle Langlois-Saliou).

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Terrestrial ecosystems are composed of plants and soil animals (e.g. earthworms, small insects) with strong interactions between them that are central in ecosystem functioning. These interactions between plants, soil organisms and the soil itself regulate processes such as nutrient cycling or energy flow and control how plant and animal communities are structured. Simultaneous study of all these compartments can therefore provide additional information on how the ecosystem is structured and functions, more so than separate studies ever would. In this study we looked for links between plant and soil fauna characteristics (or traits) in relation to soil abiotic properties along a flooding gradient on the banks of the Seine River. Small and localized environmental gradients such as this one provide powerful tools to assess the effects of variations within a specific environmental variable (here flooding) on various processes. We sampled and identified soil fauna and plants in the field and used publically available databases to provide information on their traits. We observed a strong influence of flooding on the structuring of plant communities with particular traits, or adaptations, being selected by flooding intensity leading to the existence of functionally, and visually, different communities along the gradient. Springtails, small soil arthropods which we used as a proxy for the soil fauna, were not observed to be directly linked to variations in flooding intensity. Instead of being directly filtered by flooding, springtail traits were selected and filtered by variations within plant communities, especially their traits. We thus revealed an indirect influence of flooding intensity on soil fauna through its effects on plant communities. As this pattern has been previously observed for other gradients and species, our results enhance our understanding of how naturally-occurring communities can be influenced by other organisms as well as their physical and chemical environment.

Image caption: View of the considered flooding gradient from the mudflats (photo credit: Estelle Langlois-Saliou).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Salivary cues: Simulated deer browsing induces changes in plant hormones and defense compounds in tree saplings

Bettina Ohse, Almuth Hammerbacher, Carolin Seele, Stefan Meldau, Michael Reichelt, Sylvia Ortmann and Christian Wirth Simulating deer browsing by clipping a tree sapling’s apical bud and applying deer saliva on the fresh cut (here on Acer pseudoplatanus). Photo by Bettina Ohse.

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Young trees in temperate forests are often browsed by mammalian herbivores, such as deer. Studies on insect herbivory have shown that plants respond to herbivory by upregulating growth hormones and producing defense compounds. However, it remains unknown whether the same response mechanisms are induced when young trees are browsed by mammals. We also wanted to know if tree saplings can detect whether they are just injured mechanically, or whether they are browsed by deer. To answer these questions, we simulated deer browsing on field grown sycamore maple (Acer pseudoplatanus) and European beech (Fagus sylvatica) saplings by clipping their buds in winter and leaves in summer. For some of the saplings we additionally applied deer saliva with a pipette on the cut surface.

We found that two hours after clipping, wound hormones, called jasmonates, increased in the remaining maple buds and beech leaves. This is a well-known response to herbivory, but differed here between tree species and developmental stages. In maple buds, growth hormones (cytokinins) also increased after clipping, probably because if maple loses its one main apical bud through browsing, the upregulated growth hormones will help activate lateral buds for regrowth. Beech has more equal buds and may therefore not respond as strongly to clipping when losing one. Saliva application did not amplify wound hormone responses, but led to increased levels of the signaling hormone salicylic acid in beech leaves, suggesting that the trees were able to detect something in the deer saliva. Interestingly, changes in defense compounds were found only when deer saliva was also applied, which means that these compounds are only regulated specifically after deer browsing and not after any mechanical damage. Not all defense compounds changed in the same way. Mainly hydrolysable tannins increased, although they are not harmful to deer. Condensed tannins, which occurred only in beech and are known to be avoided by deer because they negatively impact digestion, did not change, and may rather act as a constitutive defense, i.e. one that is permanently present.

We conclude that tree saplings are able to detect and specifically respond to mammalian herbivory, although strategies to respond to mammalian browsing seem to be species-specific, probably based on distinct combinations of morphological and chemical characteristics.

Image caption: Simulating deer browsing by clipping a tree sapling’s apical bud and applying deer saliva on the fresh cut (here on Acer pseudoplatanus). Photo by Bettina Ohse.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

In, out or staying put? The landscape and the plant both have their say.

Alistair G. Auffret, Elsa Aggemyr, Jan Plue and Sara A.O. CousinsThe Stockholm archipelago from above (Photo: S. Cousins); Common Hepatica (Hepatica nobilis) responded well to grassland abandonment (Photo: A. Auffret);  However, Mountain Everlasting (Antennaria dioica) disappeared completely from the 27 islands  (Photo: A. Auffret); Harebell (Campanula rotundifolia) has characteristics of plants both able to persist and able to disperse (Photo: A. Auffret).

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Every summer, Stockholm's idyllic archipelago is alive with tourists. People arrive at an island, stay for a while, and then leave. During the 20th century, the same has happened to the islands' plant species, albeit much more slowly. Up until the 1950s, the area was a busy farming landscape. Fodder was grown in the meadows and cattle were transported from island to island during the summer. Since then, agriculture has been almost totally abandoned and now most of the land area is covered in forest. This has had a huge impact on the area's plant life.

We compared species lists of plants from 27 small islands in 1908, when farming was still thriving, with our own survey from 2008. This meant that for each island, we were able to see which plant species had arrived, which had disappeared and which had stayed put during 100 years of landscape change. It was much easier for plants to survive on and arrive at larger islands and those close to the mainland, but it also depended on the plants themselves. Taller plants, which were able to compete for light in the overgrown pastures, could persist and spread to new islands, while plants with long life spans or long-lasting seeds were also more able to survive adverse conditions. Plant species that prefer to move (disperse) rather than stay put did not fare so well. Even if one would expect such species to move to more suitable areas following grazing abandonment, the magnitude of change meant that there was simply nowhere for them to go.

We also compared the species listed in the grid squares used for the historical and present-day plant atlases covering the same area. In this case it was only the plants, not the landscape, which explained change over time. Understanding how plants and animals are affected by human activity over time is interesting for ecologists, and historical species lists are therefore very useful. However, our results show that it is important to understand that different sources of species observations can affect the patterns we see and what drives them.

Image caption: The Stockholm archipelago from above (Photo: S. Cousins); Common Hepatica (Hepatica nobilis) responded well to grassland abandonment (Photo: A. Auffret); However, Mountain Everlasting (Antennaria dioica) disappeared completely from the 27 islands (Photo: A. Auffret); Harebell (Campanula rotundifolia) has characteristics of plants both able to persist and able to disperse (Photo: A. Auffret).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Climate and atmospheric change impacts on sap-feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites

James M. W. Ryalls, Ben D. Moore, Markus Riegler, Lisa M. Bromfield, Aidan A. G. Hall and Scott N. Johnson Magnified pea aphids (Acyrthosiphon pisum) feeding on an experimental lucerne (Medicago sativa) leaf.

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‘Little things that run the world’ is how E.O. Wilson described insects and other invertebrates, but which ‘little things’ will run a future world with higher atmospheric carbon dioxide concentrations and warmer temperatures? We set about answering this for aphids feeding on lucerne and aimed to get at the underlying plant-mediated mechanisms for changes in their performance. We chose aphids because these troublesome insects transmit at least 50% of insect-vectored plant viruses and therefore cause widespread damage to crops worldwide - a troubling prospect considering that we’ll need to feed another 3 billion people by 2050. In addition, they can have disproportionately large impacts on foodwebs and insect community structure simply because they can reproduce so rapidly in response to favourable environmental conditions. Aphids have been repeatedly identified in reviews and meta-analyses as being a net beneficiary of predicted increases in atmospheric carbon dioxide concentrations, yet the exact mechanisms for this aren’t always clear. Our study addresses a missing piece of this jigsaw by investigating the underlying chemical mechanisms for their success and how concurrent climatic factors (elevated air temperature) interact with elevated CO2. We demonstrated that it was a specific group of amino acids that increased and decreased, respectively, under elevated CO2 and temperature, which was directly correlated with aphid performance. This consistent pattern across five plant genotypes explained why aphids benefited from elevated CO2, yet performance declined when elevated temperature was included. Understanding the chemical mechanisms underpinning insect responses to climate and atmospheric change raises the possibility of building resistance into new crop cultivars and gives us some foresight for preventing pest outbreaks and preserving ecosystem functions.

Image caption: Magnified pea aphids (Acyrthosiphon pisum) feeding on an experimental lucerne (Medicago sativa) leaf.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The honeybee leads the effect of an exotic plant on resident plant-pollinator communities

Ana Montero-Castaño and Montserrat VilàSubsample of the Mediterranean plant –pollinator community studied.

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Exotic plants that depend on pollinators for their reproduction usually become well integrated into the diet of generalist pollinators. This integration can affect the entire recipient plant-pollinator community; for instance, by attracting pollinators, or on the contrary, by stealing pollinators from the recipient communities. Understanding the factors that govern such variable effects is among the fundamental goals in invasion ecology.

Because species traits determine the interaction between plants and pollinators (e.g. size, shape and colour of flowers and body size or tongue length in pollinators), trait similarity among plants or among pollinators might modulate how they affect each other.

We conducted a flower removal experiment to investigate the effects of the exotic legume Hedysarum coronarium on the pollination patterns of a Mediterranean shrubland community. We explored if the number, frequency or identity of interactions were affected by the exotic and whether the effects were influenced by trait similarity. Specifically, we explored the influence of similarity in flower morphology with Hedysarum (i.e., whether natives were also legumes or not). And in the case of pollinators, we explored the influence of belonging to the same functional group (i.e., whether they were also bees or not) as the main pollinator of Hedysarum, the highly competitive honeybee. Other pollinators were flies and beetles.

Hedysarum was well integrated into the diet of 15 generalist pollinators. Such integration did not affect the pollination of native plants (irrespective of their flower morphology) in terms of number and frequency of interactions, despite a reduction in proportion of honeybee visits. On the other hand, Hedysarum reduced the visitation frequency of bees to both natives and Hedysarum. In addition, pollinators switched the plants they visited (i.e., interaction rewiring) according to the changes in the proportion of honeybee visits. That is, the bigger the change in the proportion of honeybee visits to a given plant, the greater the interaction rewiring.

In conclusion, pollinators respond to plant invasions with a plastic use of floral resources. When the exotic attracts highly competitive pollinators such as the honeybee, plasticity is especially significant for pollinators functionally close to that pollinator, i.e. other bees. The result is an interaction rewiring due to pollinators avoiding competition with the honeybee.

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

Review

 

Bridging frameworks to better understand the nutrition of animals in their environment

Erik Sperfeld, Nicole Wagner, Halvor Halvorson, Matthew Malishev, David RaubenheimerThe water flea Daphnia magna (photo: Silvia Heim), the grasshopper Locusta migratoria (adapted photo by Ferran Turmo Gort, CC BY 2.0), and the caddisfly larvae Pycnopsyche gentilis (courtesy of Bob Henricks)..

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It is essential for ecologists to understand the interaction between animal nutrition and the environment to better predict how animals will respond to our changing world. The research field investigating this animal nutrition-environment interface, nutritional ecology, has developed tremendously within recent decades. Steering this field are two prominent research frameworks, offering a toolbox of concepts to address the challenges of nutritional ecology. One framework, ‘Ecological Stoichiometry’ (ES), uses elements (e.g. carbon, nitrogen, phosphorus) to explore how imbalanced diets alter animal physiology, population dynamics, and nutrient cycling in ecosystems. The second framework, ‘Nutritional Geometry’ (NG), uses geometry to study feeding decisions of animals to maximize their fitness. ES originates from studies on element cycling, often using aquatic invertebrates (e.g. water fleas) as focal organisms, whereas NG originates from animal behaviour research, particularly on terrestrial insects (e.g. grasshoppers and cockroaches). Both origins have influenced the types of questions investigated and the type of nutrient currency used, with NG focusing on macronutrients (proteins, carbohydrates, and fats) and ES on elements.

Despite their inherently different perspectives, NG and ES are unified by a shared concept that contributes to collectively achieving the common goal of understanding the animal nutrition-environment interface. This concept, called homeostasis, drives animal nutrition and is broadly defined as an animal’s ability to regulate its internal nutrient status under a varying diet. ES uses an “are you what you eat?” approach to homeostasis by measuring internal nutrient composition, while NG adds individual behaviour to diet choice and food intake. In this paper, we illustrate how the complementary homeostasis approaches of NG and ES can be integrated in a conceptual, mathematical model that a) describes animal metabolism and tracks the flow of multiple nutrients through the body, and b) describes individual animal feeding behaviour in its environment in time and space. Our described modelling approach aims to advance nutritional ecology by better connecting organisms with their environments across different scales by using a shared concept well established in the field.

Image caption: The water flea Daphnia magna (photo: Silvia Heim), the grasshopper Locusta migratoria (adapted photo by Ferran Turmo Gort, CC BY 2.0), and the caddisfly larvae Pycnopsyche gentilis (courtesy of Bob Henricks)
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Experimental warming in a dryland community reduced plant photosynthesis and soil CO2 efflux, but didn't change the relationship between the fluxes

Timothy M. Wertin, Jayne Belnap and Sasha C. ReedClimate manipulation experiment in a semiarid grassland, with Achnatherum hymenoides (Indian ricegrass) as the focal plant species; photo by TM Wertin.

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As air temperatures warm and precipitation patterns shift, arid and semiarid grasslands, such as those typical of the southwestern US, are expected to expand throughout this century. At the global scale, drylands support up to 38% of the human population, a number that is expected to increase due to both population growth and climate change. Recent research also suggests dryland systems are a major factor dictating future carbon cycling and climate. From a regional perspective, arid and semiarid grasslands represent critical habitat for wildlife, agriculture, and livestock grazing. If climate change affects plant growth, it would have dramatic implications on the landscape’s ability to sustainably maintain food production and carbon stocks.

Nevertheless, our understanding of how dryland grasses will respond to climatic change remains notably poor. To test the effects of warming on arid grasslands we conducted a climate manipulation study where we artificially increased plant and soil temperature by ~2 oC, which is well within the expected range of temperature increase expected for the Southwest. Specific goals of this experiment were to determine how a change in temperature would affect photosynthesis (the process by which plants convert solar energy and CO2 into organic forms) and soil respiration (the conversion of plant carbon and soil organic matter into CO2 and energy). We conducted this experiment on Indian Rice Grass, a native plant that is heavily relied upon for native and domesticated animal grazing.

Our study showed that a relatively subtle increase in temperature reduced both photosynthesis and soil respiration. The close coupling between soil respiration and photosynthesis was surprising; although warmer temperature reduced both fluxes, it did not change the relationship between the fluxes. In our study site, soil organic matter is quite low, and our data suggest that soil CO2 efflux was strongly regulated by newly acquired photosynthetic products respired or exuded by roots. This finding may have dramatic implications for climate models, which are used to predict carbon cycling and climate, and also heralds concern for the important grasses of the Southwest.

Image caption: Climate manipulation experiment in a semiarid grassland, with Achnatherum hymenoides (Indian ricegrass) as the focal plant species; photo by TM Wertin.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

The Ecology of De-Extinction

How close can we get to bringing an extinct species back to life?

Beth Shapiro A researcher prepares a fragment of mammoth bone for DNA extraction in the Paleogenomics Lab at UC Santa Cruz. Credit: Beth Shapiro.

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Over the last five years, de-extinction, which is the term used to describe the idea that extinct species may soon be brought back to life, has received increasing attention in both scientific and public arenas. Discussions about de-extinction tend to concentrate on the ethical and political implications of resurrecting extinct species and, increasingly, to focus on the ecological consequences of releasing resurrected species into the wild. Relatively less attention has been paid, however, to the process of de-extinction itself, specifically whether the technology is sufficiently advanced to bring an extinct animal species back to life.

I review the three main technologies that are being considered at present for de-extinction: back-breeding, cloning via somatic cell nuclear transfer, and genetic engineering. Back-breeding aims to concentrate ancestral traits that persist within a population into a single individual using selective breeding. Cloning aims to create genetically identical copies of an extinct species from preserved cells, which means that this approach may not be feasible for long-dead organisms whose cells, and the genetic material within them, have decayed. Genetic engineering draws on recent advances in both ancient DNA and genome editing technologies, and aims to edit the genome sequence within a living cell so that the sequence more closely resembles that of a closely related extinct species. This edited cell would then be cloned, creating a genetic hybrid between the living and extinct species.

Because the phenotype of an organism is the consequence of the interaction between its genotype and the environment in which it develops and lives, none of these processes will create exact copies of the extinct species that they are attempting to resurrect. Precise replication, however, is not necessary to achieve the conservation-oriented goals of de-extinction. In the majority of ongoing de-extinction projects, the goal is to create functional equivalents of species that once existed: ecological proxies that are capable of filling the extinct species’ ecological niches. It is this application of de-extinction technologies that is likely to have the most positive impact on conservation.

Image caption: A researcher prepares a fragment of mammoth bone for DNA extraction in the Paleogenomics Lab at UC Santa Cruz. Credit: Beth Shapiro.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Advances and challenges in the study of ecological networks

Species and their interactions

Kristian Trøjelsgaard and Jens M. OlesenA food web consisting of a single top predator (bird), some intermediate species (parasitic wasp, caterpillar, and grasshopper) and a single primary producer (plant). The network is a quick way of illustrating the feeding relationship between the species.

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Virtually no organism lives in isolation, and biotic interactions (e.g. competition, predation, mutualism and parasitism) therefore play an important part in the biodiversity and distribution of species that we see today. One way of analysing complex systems of interacting species is through network analysis, a discipline that has grown considerably in recent decades. Ecological networks consist of nodes (typically species) that are connected because they somehow interact. A good example is food webs where predators are connected to prey, which in turn can be connected to plants, and as such, the food web demonstrates who eats whom. Interestingly, it has turned out that human networks like air transportation networks, the Internet, and sexual relationships between humans have many structural commonalities with the ecological networks we find in nature. For example, most species (or humans) have few interaction partners while a few nodes have disproportionately many interaction partners.

As stated, ecological networks provide a way of capturing whole communities of interacting species in a single analysable entity. The variability that ecological networks exhibit across space and time is likely to teach us how networks of interacting species will respond to e.g. future climate changes. Interestingly, temporal comparisons of ecological networks range from within season to across millions of years, and spatial comparisons have been done within a single km, across regions or even across the globe. Herein we review what such studies have taught us and list potential ways of moving forward.

We emphasize that although networks may look calm on the surface, when compared across space and time, there seems to be much variability underneath. For example, individual species may change with whom they interact, with how many they interact, and also their role in the community. This microscopic (i.e. below the network level) variability deserves further attention, and is likely to add another dimension to network variability.

Image caption: A food web consisting of a single top predator (bird), some intermediate species (parasitic wasp, caterpillar, and grasshopper) and a single primary producer (plant). The network is a quick way of illustrating the feeding relationship between the species.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Assessing vulnerability of functional diversity to species loss: a case in Mediterranean agricultural systems

Carlos P. Carmona, Irene Guerrero, Manuel B. Morales, Juan J. Oñate & Begoña PecoDetail of one of the agricultural fields included in the study.

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Increasing intensification of land use is leading to biodiversity losses worldwide, which in turn can alter the functioning of ecosystems. Agricultural intensification aims to increase yield through changes in management both at the local field and at the landscape level. Arable plants, which support services like biological pest control, as well as the presence of pollinators, birds and mammals, are one of the groups most notably affected by these practices. However, it is increasingly clear that not all species are equally important for ecosystem processes. Approaches based on the traits of plants (e.g. height or leaf area) have allowed ecologists to tackle questions regarding the effects of plants on ecosystem functioning, because these traits determine how species affect different ecosystem processes. Thus, whereas the loss of a species with unique functional traits from a community may result in a reduction in the capacity of the community to perform some function, the loss of a functionally redundant species should have a much smaller impact. Assessment of the changes in functional trait diversity –a proxy of the range of functions provided by a community– as species are lost appears as a promising tool to predict the impacts of land use intensification. Here, we modified a recently developed method that compares the changes in functional diversity caused by random losses of species with those expected under the most likely order of species losses. This approach allowed us to estimate the vulnerability of the functional diversity of biological communities. We applied this method to arable plant communities from 78 agricultural fields in the area of Madrid (Spain), across a gradient of agricultural intensification. We found that the vulnerability of functional diversity to species losses increased along with agricultural intensification. Importantly, vulnerability to intensification was markedly non-linear, with great increases in the first stages of intensification, and much smaller increases afterwards. Our results suggest that field-level agricultural intensification not only reduces the taxonomic and functional diversity of arable plant communities, but also eliminates functionally redundant species, thus increasing their vulnerability to further species losses.

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

 

Long-lasting effects from previous winter warming events suggest that an important sub-Arctic moss will be disadvantaged in a future sub-Arctic climate

Jarle W. Bjerke, Stef Bokhorst, Terry V. Callaghan & Gareth K. PhoenixA shoot of splendid feathermoss with fertile organs (sporophytes) protruding from the green shoot segments, which are partly blurred. Photo credit: Jarle W. Bjerke.

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Understanding the impacts of climate change on ecosystems is complex for many reasons. Firstly, there are many drivers of change and each driver has numerous interacting facets. Secondly, there are practical issues that hinder research, such as difficult species groups and winter research. Here we focus on a moss (an understudied plant group), the winter period (under-represented in field studies) and extreme warming events, that are both difficult to observe and even more difficult to predict. Winter is a period of dormancy for plants of cold environments. However, winter climate is changing, leading to an increasing frequency of warm weather events that temporarily reduce snow cover. These conditions can break dormancy for some plants and expose them to freeze-and-thaw stress. Mosses are a major component of northern lands, yet the longer-term impacts of such winter warming events on mosses remain unknown. Therefore, we undertook a field experiment to simulate these events over three consecutive winters in a sub-Arctic open woodland. The mat-forming splendid feathermoss (Hylocomium splendens), also known as the glittering woodmoss or stairstep moss, was the most abundant moss species at our site, and we studied it during both the experimental years and in the years following these events. This is probably one of the most abundant moss species in the World, and plays important roles such as insulating the ground. We found that the warming events reduced its vitality. Both photosynthesis and shoot growth rates declined considerably and were still much lower than in non-experimental plots even four years after the last warming event. These results suggest that this moss will be disadvantaged in a future sub-Arctic climate where a high frequency of winter warming events may become the norm. More broadly, this suggests the potential for large consequences for northern lands where mosses are often a major component of the vegetation and where the greatest increases in extreme winter events may be expected. This will again have a strong influence on ground temperature and moisture, cycling of nutrients and water, permafrost thaw and ecosystem carbon balance.

Image caption: A shoot of splendid feathermoss with fertile organs (sporophytes) protruding from the green shoot segments, which are partly blurred. Photo credit: Jarle W. Bjerke.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Joint effects of climate change and parasite infection on host in the wild

Matthieu Bruneaux, Marko Visse, Riho Gross, Lilian Pukk, Lauri Saks, Anti VasemägiEcologist at work. Photograph provided by authors.

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Climate change can affect ecosystems in several ways, through direct temperature effects on organisms (e.g. limiting metabolic capacity at high temperatures) or through indirect effects, such as an increased parasite burden or the introduction of new parasites. These negative effects can interact with potentially dramatic consequences, when high temperatures disrupt the immune function of the host and make it unable to resist a parasite infection, or when the parasite infection compromises the ability of the host to cope with elevated temperatures.

The physiological effects of parasites have been traditionally evaluated under controlled laboratory conditions. However, much less is known about the effect of emerging parasitic diseases on host performance in nature. We studied wild-caught juveniles of brown trout (Salmo trutta) and measured several physiological and performance traits to evaluate the effect of proliferative kidney disease (PKD), which is caused by the myxozoan parasite Tetracapsuloides bryosalmonae This parasite can result in high mortalities in salmonid species, both in farms and in natural ecosystems, and its range has extended in recent years. To understand how parasite load, metabolic rate and thermal resistance are related to each other in the fish host, we brought our physiological laboratory into the field to measure oxygen consumption and thermal tolerance of wild brown trout.

We found that fish exhibited varying degrees of disease severity, with a wide range of parasite load, kidney swelling and associated anemia. Importantly, the aerobic scope, which is the maximum amount of usable energy a fish can produce using its aerobic metabolism, was negatively correlated with the severity of PKD. In addition, the thermal tolerance of the fish was also negatively correlated with disease symptoms. Our results demonstrate how a wild fish population can be at risk under the double threat of increased water temperature and expanding parasite range, and of their interaction. Understanding if and how local populations can adapt to these selective pressures will be critical to assess the long term evolution of this type of ecosystem.

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

 

The effect of egg size on hatch time and metabolic rate: theoretical and empirical insights on developing insect embryos

James L. Maino, Elia I. Pirtle, and Michael R. KearneyGumleaf Grasshopper from Australia’s Dry Eucalypt Forest. This grasshopper resembles a dry gum leaf and lays its eggs in the leaf litter. Photograph by James Maino.

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As organisms change in size, they much also change in design to compensate for the mismatched scaling between surface-area and volume-based processes. Body size scaling relationships, combined with metabolic theory, allow biologists to study ecological phenomena in terms of processes at the organism level. By properly understanding biological processes at one level, higher level processes are able to be predicted and, in doing so, a mechanistic understanding is achieved. In this study we present a model based on simple energy and mass transfer processes during egg development that is able to explain how hatch time varies with species size and the time course of metabolic rate from egg lay to hatch. Our findings suggests that previous models made unrealistic assumptions regarding the metabolic activity of a freshly laid egg, leading to unreliable predictions. Metabolic theory is increasingly being applied in biology to understand a range of biological phenomena. Contributing to its success is its emphasis on the currencies of mass and energy, which are relevant at all scales of biology from the molecular to the ecosystem. Our presented model and supporting data on 98 species of insects advances our mechanistic understanding of egg development and highlights the usefulness of process-based models from which higher levels patterns can be derived.

Image caption: Gumleaf Grasshopper from Australia’s Dry Eucalypt Forest. This grasshopper resembles a dry gum leaf and lays its eggs in the leaf litter. Photograph by James Maino.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Positive species diversity and above-ground biomass relationships are ubiquitous across forest strata despite interference from overstorey trees

Yu Zhang, Han Y.H. Chen, Anthony R. TaylorOld growth red spruce (Picea rubens) stand, typical of eastern Canadian temperate forest.  Photo Credit: Anthony Taylor.

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There is growing concern over rates of global species diversity loss, given its important role in the healthy functioning of ecosystems and the many goods and services they provide. However, our knowledge of how diversity supports ecosystem function remains unclear. While positive relationships between tree species diversity and forest biomass production have been observed, forests are structurally complex, consisting of various understorey vegetation layers which also contribute to ecosystem functioning as they often account for the majority of species richness; however, the relationships between understorey vegetation diversity and function are largely unexplored. Further, few studies have simultaneously assessed how both overstorey and understorey vegetation interact and contribute to overall forest ecosystem function.

In our study, we used Canada’s National Forest Inventory data, covering many forest types across a wide spatial distribution, and a robust statistical modeling approach (structural equation modelling) to explore both overstorey and understorey relationships between species richness and forest biomass production while accounting for potentially confounding factors, including climate, physical site characteristics, and forest ageing. We found positive relationships between species richness and biomass production across all forest vegetation layers, but the relationship was strongest for the overstorey layer. Species richness of the understorey tree, shrub, and herb layers was positively related to overstorey species richness. However, overstorey biomass had a negative effect on the biomass production of all understorey layers. Our results suggest that resource filtering by overstorey trees might have reduced the strength of the positive diversity-productivity relationships in the forest understorey, supporting previous hypotheses that the magnitude and direction of diversity-productivity relationships is context specific and dependent on the conditions of the surrounding environment. Further, heterogeneity in understorey resources, as affected by overstorey trees, may promote niche complementarity (i.e. plants using different resources, or at different times or in different places) as the main mechanism driving diversity-productivity relationships in understorey vegetation.

Image caption: Old growth red spruce (Picea rubens) stand, typical of eastern Canadian temperate forest. Photo Credit: Anthony Taylor.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Do thermoregulatory costs limit altitude distributions of Andean forest birds?

Gustavo A. Londoño, Mark A. Chappell, Jill E. Jankowski and Scott K. Robinson Andean cock-of-the-rock. Image provided by authors.

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Tropical mountains contain the highest regional bird diversity in the world, largely because of high turnover of species with narrow altitudinal ranges. Understanding the mechanisms that limit so many species to narrow altitudinal distributions in the Andes is the central goal of our study. Our research is the first experimental approach to understanding the role of thermal physiology in limiting species’ altitudinal distributions. The biologist Daniel Janzen in 1967 hypothesized that tropical organisms should be specialized to a narrow range of temperatures because they experience little climatic variation in their ranges. As a result, they should be intolerant of temperatures outside of the optimal range, which would inhibit up- or downslope movements. Some tropical ectotherms (cold-blooded animals) fit Janzen’s predictions, but we do not know if endotherms, which maintain a constant internal temperature, are also excluded from environments outside their optimal temperature range. We measured several aspects of thermal physiology of 215 bird species across a 2.6-km altitude gradient in the Peruvian Andes. We predicted that highland species would show adaptation to the colder high-altitude climate, and that energy costs of thermoregulation might limit up-slope dispersal of lowland natives.

We found reductions in thermal conductance (amount of heat loss) and body temperature, and lower critical temperature (lowest temperature where metabolism increases) in highland birds compared to lowland species, all of which make birds of high elevations more resistant to heat loss. We did not, however, find convincing evidence that acute thermal limits or energy costs of thermoregulation constrained altitudinal distributions. However, to evaluate the amount of energy that low elevation birds would spend at high elevation, we built heat budget models that predicted low-to-moderate long-term costs at native altitudes. Costs increased for lowland natives modeled in the highland climate, but for all but a few species, these higher costs remained within putative expenditure limits as defined in the literature.

Although we did not test heat tolerances, we measured all species at temperatures similar to the hottest air temperatures at the lowland site. The lack of difference in basal metabolic rate at 30-34ºCdoes not suggest that high lowland temperatures preclude down-slope movements of highland birds. While thermal tolerances probably do not directly determine altitude occupancy by most species, there may be a tradeoff between the higher costs of thermoregulation experienced by lowland species moving up-slope and investment in important life history components such as breeding.

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

 

The plant you choose to make your home isn't always the one that protects you best

Jared G. Ali & Anurag A. Agrawal Image provided by authors.

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A herbivore’s ability to feed, avoid predation, and succeed on specific host plants are some of the most important factors in its life. What we find, though, is that not all herbivores are able to perform equally well on every plant they encounter. Therefore, we assume most herbivores have specialized on plants that allow them to achieve optimal measures of performance. An important question that remains in ecology is whether herbivores select hosts more because of interactions with their host alone (nutrition, plant defenses, growth, etc.) or if predators and parasites play a major role in the selection of a plant host. A very interesting phenomenon occurs in many herbivores that specialize on particular hosts; they often gain the ability not only to cope with plant defenses (toxins produced to ward off herbivores), but to also steal them and keep them in their bodies to protect themselves from their own enemies. In this experiment we tested two specialized insect herbivores’ ability to perform on alternative plant hosts. We evaluated their performance while measuring toxins that these specialist herbivores steal from plants that might protect them from parasitic worms. We find specialization is driven primarily by plant-herbivore interactions, rather than by threat of predation/ parasitization, and that not all measures of performance are highest on the herbivores’ preferred host plants. This tells us that measures of performance are complex and that ecological interactions between a plant and host are not always those that result in optimal performance on every trait.

 

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

 

Movement correlates of lizards' dorsal pigmentation patterns

Topaz Halperin, Liran Carmel and Dror HawlenaPhoto provided by authors.

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The reasons why some animals have cryptic body patterns, such as spots, reticulations and blotches, while others have conspicuous stripes, has long intrigued scientists. We provide a simple explanation for this quandary that is based on the balance between the animal’s need to eat and the need to avoid being eaten. Species that remain still during much of their activity time, such as animals that hunt from ambush, may benefit from cryptic body patterns that help them blend in to the environment. However, cryptic patterns are less beneficial for species that actively search for food. This is because visual predators can easily detect a moving prey regardless of their coloration. Conversely, these highly detectable active species may benefit from conspicuous stripes that improve their chances to survive predator attacks. Stripes can dazzle the predator’s motion perception and hamper its ability to intercept escaping prey. Thus, we suggest that species that forage less actively should have cryptic patterns while species that actively search for food should have stripes. We tested this hypothesis by studying the association between lizard foraging behaviors and their pigmentation patterns. Using an extensive literature survey, we found that lizards with stripes were indeed substantially more active than lizards with cryptic patterns. Our findings provide the first quantitative support for the hypothesized relationships between pigmentation-patterns and foraging behavior. These findings might be relevant to other animals besides lizards. We hope that future studies will test our movement-patterns hypothesis, ultimately applying meticulous manipulations to tease apart and test its mechanistic details.

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

 

Testosterone and the cloacal microbiome in a free-living bird

Camilo Escallón, Matthew H. Becker, Jenifer B. Walke, Roderick V. Jensen, Guy Cormier, Lisa K. Belden, Ignacio T. Moore Image provided by authors.

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Testosterone is a hormone that primarily functions to regulate reproduction in male vertebrates. It mediates processes such as sperm production, development of sexually-selected traits, and reproductive behaviors. There are many benefits for males maintaining high testosterone levels. However, it has been argued that maintaining high testosterone levels for prolonged periods also has costs, and could ultimately have negative consequences for long-term survival. One of the proposed pathways by which testosterone can affect survival is by increasing the risk of infection, including pathogenic bacteria.

We investigated testosterone and cloacal bacteria in free-living rufous-collared sparrows in the Ecuadorian Andes. Males of this species have high levels of testosterone during the breeding season, when they form socially monogamous unions with females. However, extra-pair paternity is common. We measured circulating testosterone concentrations, and assessed the diversity and types of bacteria living in their cloaca, which in birds functions as the opening from the gastrointestinal tract and is also the copulatory organ. Thus, it harbors bacteria that can be sexually transmitted.

We found that birds with higher levels of testosterone also had higher cloacal bacterial diversity, and had higher relative abundance of Chlamydiae, a group of bacteria that can be pathogenic. In addition, the cloacal microbes of low-testosterone birds were different from the rest of the males, seemingly because they were missing some bacteria that the other birds possessed. Two nonexclusive explanations for these results are that testosterone affects behaviors that lead to increased sexual contacts, and thus increased exposure to bacteria, or that testosterone is altering the bird’s immune system, thus making it easier for bacteria to colonize. Either way, these results suggests that increased exposure to sexually-transmitted pathogens in the form of cloacal bacteria could be a cost of maintaining high testosterone levels.

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

 

Host phenology and potential saprotrophism of ectomycorrhizal fungi in the boreal forest

Stefan F. Hupperts, Justine Karst, Karin Pritsch, Simon LandhäusserMature aspen trees during late summer, when leaves are fully expanded and photosynthesizing at full capacity. Carbon allocation to ectomycorrhizal fungi is likely high during this phenological stage. Photo credit: Erin Wiley.

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Ectomycorrhizal plants allocate some of their photosynthetically derived carbon to ectomycorrhizal fungi - organisms that colonize roots and provide mineral nutrients to their plant hosts in return for carbon compounds. With the onset of spring, trees will develop leaves for photosynthesis and then drop their leaves in autumn when temperatures decrease and daylight shortens. These seasonal changes in photosynthetic capacity induce fluctuations of carbon stored in tree roots, and may therefore influence the amount of carbon provided to ectomycorrhizal fungi.

Though traditionally considered dependent on living trees for carbon, recent work suggests that ectomycorrhizal fungi may be able to mobilize carbon from soil organic matter and plant litter (i.e. become saprotrophic). Two competing models exist to explain carbon mobilization by ectomycorrhizal fungi. Under the ‘saprotrophy model’, decreased allocation of carbon may induce saprotrophic behavior in ectomycorrhizal fungi, resulting in the decomposition of organic matter to provide the fungus with carbon if the supply from the host plant is inadequate. Alternatively, under the ‘nutrient acquisition model’, decomposition by ectomycorrhizal fungi may instead be driven by the acquisition of nutrients, such as nitrogen and phosphorus, locked within soil organic matter compounds, with carbon mobilization a secondary process.

We tested whether phenology-induced shifts in carbon reserves of fine roots of aspen affect potential activity of carbon-compound degrading extracellular enzymes by ectomycorrhizal fungi. Ectomycorrhizal roots from mature aspen were collected across eight sites in northeastern Alberta, Canada and analyzed during four distinct phenological stages: winter, spring, summer, and autumn. We predicted potential activity of carbon-compound degrading enzymes would be highest when root carbon reserves were lowest, should host phenology induce saprotrophism.

We found activity of EMF-derived carbon-compound degrading enzymes to be relatively constant across phenological stages. Furthermore, low-biomass ectomycorrhizal fungi appear to have a greater ability to degrade complex carbon compounds when compared to high-biomass ectomycorrhizal fungi. These findings support the nutrient acquisition model, and suggest that the degradation of soil organic matter and plant litter by ectomycorrhizal fungi is driven by nutrient foraging rather than saprotrophy.

Image caption: Mature aspen trees during late summer, when leaves are fully expanded and photosynthesizing at full capacity. Carbon allocation to ectomycorrhizal fungi is likely high during this phenological stage. Photo credit: Erin Wiley.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

New ranking algorithm can identify overall pattern from incomplete surveys, providing critical insight into complex problems

Timothy D. Swain, John Chandler, Vadim Backman, Luisa MarcelinoPhoto by Luisa A. Marcelino.

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As the third global coral bleaching episode is currently ongoing and expected to kill thousands of square kilometers of coral reefs, our ability to understand why some corals are killed while others survive is hampered by our capacity to consolidate previous knowledge. Corals are a combination of simple animals and algae that work in highly efficient unison to collect sunlight to make food. This association is sensitive to changes in temperature; when stressed by heat, the combination unravels in the bleaching response, leaving corals weakened and starving. Rising ocean temperatures caused by global climate change have made bleaching more frequent and severe, and understanding the mechanisms underlying the bleaching response is an urgent ecological problem. It is known that the algae associated with coral are highly diverse, and that some types are better at helping corals resist thermal stress than others. This insight originates from many experiments and surveys that, for reasons necessitated by the biology of the organisms themselves, can only provide detailed information on small subsets of the algae types; meaning that we know a lot about the relative performance of short lists of algae types, but almost nothing about the relative performance of all types. It turns out that this problem, of having lots of information about the ranking of small partial lists and little information about the ranking of an entire population, is common in many fields including search engines, election schemes, ‘best of’ rankings, and theoretical and applied sciences and engineering. To overcome this problem we devised a new ranking algorithm that can accept these partial lists and return a consensus ranking of all the elements in the lists even when there are disagreements among lists. We also validated the performance and accuracy of the algorithm with known rankings; the algorithm is very robust at uncovering new comparisons absent from the initial lists and has a low misranking error. This novel tool has broad application potential to a variety of ranking problems and will provide critical insight into coral bleaching mechanisms.

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

 

Fire impacts on soil organisms

Jennifer L. Soong, Marie Dam, Diana H. Wall, M. Francesca CotrufoImage provided by authors.

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Fires occur in nearly all terrestrial ecosystems. The occurrence rate and severity of fires depends on many factors. One important impact of fires is the combustion of aboveground plant material. This plant material would typically die and be considered “litter” to be decomposed by soil microbes and other organisms, such as nematodes, who help to recycle the nutrients held in the litter for subsequent plant production. When plant litter is combusted during a fire, much of its biomass is volatilized and lost from the ecosystem but a small fraction remains as partially burned residues, or the black charred material remaining on the soil surface after a fire. Here we used pyrolized organic matter as a substance resembling the charred material left behind by fires.

We examined how soil microbes, nematodes and plant roots use organic matter from decomposing litter and pyrolized organic matter in order to understand how the alteration of decomposition inputs to the soil by burning affects soil biological processes. We found that while litter provides a carbon and nitrogen food source to soil microbes, nematodes and growing roots, pyrogenic organic matter remains in the soil mostly unused. We also saw that this litter food source shifts the structure of the belowground food web. These results help to explain the impact of fire on belowground biological processes. For example, if aboveground biomass is removed during fires there is less material remaining to fuel belowground organisms, and the partially combusted material remaining is not easily decomposed and recycled.

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

 

Phytopathogens affect plant volatile emissions and the attraction of parasitoid wasps

Camille Ponzio, Berhane T. Weldegergis, Marcel Dicke and Rieta GolsThe parasitic wasp Cotesia glomerata, parasitizing on 1st instar larvae of the large cabbage white butterfly, Pieris brassicae. Photo copyright Hans Smid / Bugsinthepicture.com.

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As natural enemies of plant feeding insects, parasitoid wasps lay their eggs in the bodies of these other insects, and develop inside. The wasps find their herbivorous hosts by using plant odors to find the infested plant. When a plant is attacked by an insect herbivore, the volatile odors that it emits are modified, and these changes provide the foraging wasps with important information on the location of its hosts. If more than one species of insect herbivore attacks the plant, this can affect the plant odors, and in turn affect the ability of the wasps to find hosts.

However, plants are attacked not only by insects, but also by plant pathogens, and these can also change the odor of the plants. This has been rarely studied, and researchers usually focus on plant pathogens that cause disease. Yet plants can also be resistant to a pathogen, and this may also affect the emitted plant odors.

We investigated how two strains of a plant pathogen, with the plants resistant to one and susceptible to the other, affected the composition of the induced odors and the ability of the wasps to find their hosts. We studied plants infected either with a pathogen, caterpillar hosts of the wasps, or a combination of both. We found that the two strains produced odors that were different from each other, but that the odors from plants infected with the disease-causing strain were similar to the odors induced by feeding caterpillars. The parasitoid wasps preferred plants that had both caterpillars and a pathogen over plants with only caterpillars, and they were even attracted to odors from plants challenged with only a pathogen.

This research shows that plant pathogens can have as strong influence as insects on plant odors and their use by parasitoids. It is important to combine research on plant-insect and plant-pathogen interactions in the future if we are to have a better understanding of how plants defend themselves against both types of attackers.

Image caption: The parasitic wasp Cotesia glomerata, parasitizing on 1st instar larvae of the large cabbage white butterfly, Pieris brassicae. Photo copyright Hans Smid / Bugsinthepicture.com.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Linking the respiration of fungal sporocarps with their nitrogen concentration: variation among species, tissues, and guilds

Lidia K. Trocha, Elżbieta Rudy, Weile Chen, Miroslawa Dabert, David M. EissenstatMeasuring respiration of a piece of sporocarp of Lactarius sp. using the the oxygraph: a chamber containing the silver electrode which detects oxygen consumption; photo captured by Lidia Trocha.

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Respiration (RS) has been widely correlated with tissue nitrogen concentration in plants. Worldwide results show positive N-RS relationships across plant species, plant functional groups, and plant organs. We wanted to determine if similar responses exist in fungal sporocarps (spore-producing bodies) either among fungal species representing different guilds (ectomycorrhizal, saprotrophic, and parasitic) or between fungal caps and stipes representing different “tissues”.

Similar to plants, fungal sporocarps exhibit positive N-RS relationships across 93 species, which was consistent across fungal guilds, and across fungal “tissues”. However, in contrast to plants, nitrogen concentration could only explain relatively little (26%) of the RS variation among fungal species. This result may reflect fungal sporocarp nitrogen allocation, which may be partially metabolically inactive.

Forest fungi belonging to different guilds (ectomycorrhizal, saprotrophic, and parasitic) gain food through diverse strategies: by decomposition of organic matter (saprotrophic) or through symbiosis with plants (ectomycorrhizal and parasitic). Thus, feeding strategy of a fungus influences fungal metabolic activity as different amounts of energy resources are required depending on the chemical recalcitrance of the food source.

We found that fungal guild can be linked to sporocarp respiration and nitrogen concentration. Saprotrophic species have the fastest respiration and highest N concentration and ectomycorrhizal species have the lowest, with parasites intermediate. We also found that caps are more active than stipes, which reflects sporocarp “organ” specification: the caps are responsible for producing spores, while stipes mostly lift the caps.

Image caption: Measuring respiration of a piece of sporocarp of Lactarius sp. using the the oxygraph: a chamber containing the silver electrode which detects oxygen consumption; photo captured by Lidia Trocha.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Limited flexibility in heat tolerance suggests vulnerability to climate change

Belinda van Heerwaarden, Vanessa Kellermann and Carla M. SgròPhotograph provided by author.

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Rises in average temperature (as much as 2-4° C), as well as increases in the frequency of extreme temperature events, are likely to pose a major risk to many species. Tolerance of high temperatures is flexible (plastic) and can change depending on the temperatures a species encounters prior to experiencing stressfully high temperatures. Whether flexibility (plasticity) in heat tolerance can buffer the increases in temperature predicted with climate change is not known. We examined the plasticity of heat tolerance in tropical and temperate flies exposed to constant or fluctuating temperatures that reflect average temperatures experienced in nature during development (developmental plasticity), as well as after a short term stressful, but not lethal, temperature as adults (hardening plasticity) representing extreme high temperature events. While we observed some increases in heat tolerance when flies were exposed to higher average temperatures during development (developmental plasticity) and extreme temperatures as adults (hardening plasticity), heat tolerance was improved only by a maximum of 1.01° C. These results imply that overheating risk will only be minimally reduced by plasticity in heat resistance. We also found that increased heat tolerance after exposure to short term non-lethal stressful temperatures (hardening) was lower in flies exposed to warmer average developmental temperatures, indicating that increases in heat resistance at warmer temperatures may come at the cost of a reduced capacity to respond to short term extreme heat events via hardening plasticity. This study suggests that plastic increases in heat tolerance, particularly at warmer temperatures, may not be sufficient to keep pace with temperature increases predicted under climate change.

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

Ecosystems, Evolution, and Plant Soil Feedbacks

Eco-evolutionary feedbacks in an invasive plant

Jeffrey A. Evans, Richard A. Lankau, Adam S. Davis, S. Raghu and Douglas A. Landis Photograph provided by authors.

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Ecological and evolutionary processes are often assumed to operate at very different speeds. People typically think of ecological interactions as fast (such as a predator hunting for prey or two plants competing for water). In contrast we usually think of evolutionary change as very slow (for example, it took many millions of years for mammals to evolve from reptiles). But these processes can, in fact, both work relatively quickly and affect each other on mutually relevant time scales. We call these eco-evolutionary feedbacks. Our study shows how an eco-evolutionary feedback between population growth and plant chemistry shapes the invasion process in a weedy invasive plant, garlic mustard (Alliaria petiolata).

Garlic mustard produces a chemical called sinigrin that it releases into the soil, where it acts as a competitive “weapon” against other plant species early in the invasion process. We show that garlic mustard plants that produce more sinigrin have higher survival rates early in their life cycle, particularly as seedlings and during the summer. These life history stages are important drivers of population growth. Populations that produce more sinigrin grow and spread faster and ultimately reach higher plant densities. Once an established population has pushed out other competitors though, garlic mustard plants primarily compete with each other. Because sinigrin is only useful to garlic mustard in competition with other species, populations evolve to produce less sinigrin as they age. These lower-sinigrin populations grow and spread more slowly and have lower average plant densities.

Our results illustrate how the evolution of a trait (sinigrin production) can influence the ecology of a species over periods from just a few years to decades, altering its trajectory of population growth and interactions with other species in the soil and the plant communities it invades. They confirm predictions that eco-evolutionary feedbacks occur in natural populations. Furthermore, they improve our conceptual understanding of what drives population growth, by highlighting the relationship of survival and reproduction to a critical competitive trait whose advantages decrease as populations age.

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

 

Searching for prey in a three-dimensional environment: hierarchical movements enhance foraging success in northern elephant seals

Taiki Adachi, Daniel P. Costa, Patrick W. Robinson, Sarah H. Peterson, Masato Yamamichi, Yasuhiko Naito and Akinori TakahashiFemale northern elephant seals during moulting season at Año Nuevo State Reserve, CA, USA. Photo taken by T. Adachi in the morning on May 23, 2011.

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In nature, prey is often patchily distributed. Therefore, to enhance foraging success, predators are expected to concentrate search paths in areas where prey is more abundant. This style of searching is generally called “area-restricted search (ARS)”, which is characterized by sinuous search paths of predators with increased turning frequency. ARS has been suggested as an optimal search strategy in a patchy environment for both terrestrial and marine predators. However, due to the technological challenge of coupling search paths of animals with records of feeding events (prey captures), it remains unclear if ARS actually enhances foraging success in free-ranging animals, especially in marine animals that forage in a three-dimensional (3D) underwater environment.

Here, we reconstructed fine-scale 3D dive paths of a deep-diving (occasionally over 1000 m) marine predator, the northern elephant seal, coupled with recording feeding events using accelerometers attached on their jaws. Then, we quantified the 3D foraging behavior to test if seals enhance foraging success by employing “volume-restricted search” (VRS, termed for ARS in three-dimensions) while exploring a 3D environment.

Our results showed that most feeding events occurred when seals employed VRS. Also, we found that there was a hierarchical structure to the VRS; most small-VRS (95%) were nested within large-VRS (nested VRS). Importantly, nested VRS had significantly higher feeding rates than non-nested VRS, because nested VRS contained small- and large-VRS with higher and lower feeding rates, respectively. These results provided the first empirical evidence that underwater sinuous search paths (VRS) are strongly linked to higher foraging success, especially when the search paths are hierarchically structured, suggesting that seals forage on prey in a hierarchical patch system where high-density patches at small scales are nested within low-density patches at larger scales.

For all animals that search for prey, it is a central question how to adjust search paths according to the spatial distribution of prey to enhance foraging success. Our results suggest that northern elephant seals enhance foraging success by employing hierarchical decision making to concentrate search paths in areas where prey appeared to be hierarchically structured in patches over a range of 3D spatial scales.

Image caption: Female northern elephant seals during moulting season at Año Nuevo State Reserve, CA, USA. Photo taken by T. Adachi in the morning on May 23, 2011.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Litter microbial and soil faunal communities stimulated in the wake of a volcanic eruption in a semiarid woodland

Paula Berenstecher, Daniela Gangi, Adelia González-Arzac, M. Laura Martínez, Eliseo J. Chaves, Eduardo A. Mondino and Amy T. AustinMeliquina Valley, Argentina, several months after the massive eruption of the Puyehue volcano in December, 2011.  This site is approximately 70 km from the epicenter of the eruption.  The area is a mixture of natural woodland vegetation and exotic ponderosa pine (Pinus ponderosa) plantations.  Inset shows depth of ash deposition in the woodland ecosystem. Photo courtesy of P. Berenstecher.

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Large-scale natural disturbances, such as hurricanes, fires, frosts and volcanic eruptions, are important factors that affect natural ecosystems, but generalities regarding their effects are difficult due to their infrequent and unpredictable nature. Volcanic eruptions figure as one of the most prominent of these natural disturbances, but the effects on microbes and soil fauna (ground-dwelling arthropods, such as ants, beetles or mites, and nematodes, microscopic round-worms) are relatively unknown. These organisms are important because they are key players in the formation of soil organic matter and turnover of nutrients which then become available for plants. We evaluated ecosystem changes induced by the dramatic Puyehue-Cordón Caulle eruption of June 2011 in Patagonia, Argentina. We were interested in how these microbes and soil animals responded to heavy ash deposition in both natural woodland vegetation and a pine plantation in the Meliquina Valley, located 70 km west of the epicenter of the eruption. As ash can be quite abrasive and is, in fact, used as an insecticide, we hypothesized that volcanic ash deposition would have marked negative effects on the soil biota and consequently on decomposition. We were extremely fortunate to have made pre-eruption measurements in the same sites in the year prior to the volcanic eruption, which provided a rare opportunity to make a real comparison before and after the ash deposition.

We measured environmental variables of soil and litter (moisture, pH, organic matter) and biotic variables (abundance of ground-dwelling arthropods, nematodes, microbial biomass and microbial activity in soil and litter) in both natural woodland and pine plantation sites. We were surprised to find that ground-dwelling arthropods actually dramatically increased in abundance after the eruption, while soil nematodes were negatively impacted. More surprising, however, was that evaluating the effects of ash on litter decomposition showed more than doubled rates of carbon turnover in litter from the native woodland. It seems that the effect of the ash deposition may be related to your habitat, with those who reside in the soil being negatively affected while the litter dwelling microbes and fauna were actually favoured by the conditions of the eruption. This study provides insight into the effects of large disturbances on the underappreciated soil biota, and highlights that these disturbances do not always result in the catastrophic effects that we might imagine.

Image caption: Meliquina Valley, Argentina, several months after the massive eruption of the Puyehue volcano in December, 2011. This site is approximately 70 km from the epicenter of the eruption. The area is a mixture of natural woodland vegetation and exotic ponderosa pine (Pinus ponderosa) plantations. Inset shows depth of ash deposition in the woodland ecosystem. Photo courtesy of P. Berenstecher.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Using functional responses to quantify interaction effects among predators

Ryan J. Wasserman, Mhairi E. Alexander, Tatenda Dalu, Bruce R. Ellender, Horst Kaiser and Olaf L.F. WeylSouthern mouthbrooder (Pseudocrenilabrus philander- foreground) and banded tilapia (Tilapia sparrmanii- background). Photo provided by authors.

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The relationship between prey consumption by a predator and prey availability is known as the functional response. Functional response studies on predators are useful as they provide valuable information on the nature of prey consumption by a predator. For example, the proportion of prey that a predator consumes when there are lots of prey around may be different to the proportion consumed when there are few prey. This is because some predators are better at finding prey at low densities than others, while certain predators are particularly good at eating lots of prey when they are available. Understanding differences amongst predators is important as across most ecosystems, biodiversity levels are changing as a result of extinctions and invasions associated with anthropogenic activities. This is also true for predatory species and many environments have been altered to the point where predatory species have been either lost or gained. It has been shown that predators interact with one another and interactions among predators can diminish or enhance their effects on prey, depending on the nature of the interaction between the predators. These are known as multiple predator effects (MPEs) and are relevant within the context of predator species loss or gain.

While functional response and MPE studies are common in the literature and their value is well recognised, few studies have assessed both aspects of predation simultaneously. In a laboratory study we use three fish species with different functional traits as model predators (bluegill Lepomis macrochirus, southern mouthbrooder Pseudocrenilabrus philander and banded tilapia Tilapia sparrmanii) and assess intra- and inter-specific predator interaction outcomes on predator-prey dynamics. We contrasted the observed functional responses of combinations of predators, of the same or different species, with expected responses based on those of individual predators. We show that prey risk varies as a result of predator-predator effects, both within and between species. This study therefore represents a step closer to real world scenarios where multiple predators interact with one another, and with prey at different prey densities. We therefore propose that the incorporation of predator combinations into classic functional response investigations would be useful for the development of competition and predation ecology.

Image caption: Southern mouthbrooder (Pseudocrenilabrus philander- foreground) and banded tilapia (Tilapia sparrmanii- background). Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Fertilization changes goldenrod’s defensive response to grasshoppers

Karin T. Burghardt Photo credit: Karin T. Burghardt.

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Most plants are not able to actively move away from animals that want to eat them, however they are far from passive in their response. Many species can reduce herbivore feeding by producing an arsenal of chemical and structural anti-herbivore defenses. Such resistance may always be produced by a plant at baseline levels or only after an herbivore attacks. Alternatively, a plant can tolerate herbivore damage and simply reallocate resources to promote regrowth, thereby minimizing the negative impact of the herbivore on reproduction. The strategy a plant uses may depend on nutrient availability because the cost-benefit trade-off between growth and defense changes across nutrient environments.

In this study, I investigated how defensive strategy changes across a nutrient (fertilization) gradient within tall goldenrod. This plant is an extraordinarily common species found within abandoned fields and along roadsides across eastern North America. Clones of 9 genotypes (collected from an old-field) were grown in a greenhouse at varying nutrient levels and some were exposed to grasshoppers collected from the same field.

I found that genetically identical individuals changed their defensive strategy across the nutrient gradient. At low nutrient levels, plants tolerated herbivory and exhibited low to moderate levels of baseline resistance. In contrast, fertilized plants did not invest in baseline resistance, opting to wait and invest in high levels of resistance only when attacked by grasshoppers. It is important to note that plant defensive trait changes occur within the context of many other whole-plant changes. Therefore, I also studied how a plant’s defensive strategy changed in concert with 26 other plant traits including leaf nutrient content and belowground allocation.

This study highlights how flexible genetically identical plants can be in terms of resource allocation patterns across developmental environments. In addition, quantifying the way in which a dominant species alters traits in response to nutrients enables us to predict how human-caused nitrogen deposition (a known occurrence in the northeastern U.S.A) will impact old-field communities. Finally, understanding how soil nutrient environment changes plant defensive traits and productivity is of critical importance to agriculturists interested in reducing pesticide use while maximizing yield.

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

 

Predator-prey mass ratio revisited: Does preference of relative prey body size depend on individual predator size?

Cheng-Han Tsai, Chih-hao Hsieh and Takefumi NakazawaPhoto provided by authors.

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Food webs are complex systems including many species and interactions and thus are difficult to understand. A promising way of understanding food-web dynamics and their responses to environmental changes is to focus on body size relationships between interacting predator and prey, because their relative body sizes (i.e. predator-prey mass ratio, abbreviated as PPMR) largely determine the strength of predator-prey interactions. Specifically, it is expected that predators should not eat too big or too small sized prey. If we know the optimal relative prey size, it may help to simplify the structure of complex food-web models and allow us to more easily assess food-web responses to environmental changes. This optimal relative prey size is called preferred PPMR.

So far, previous studies of several dietary datasets have reported that PPMR increases with predator body size, meaning that large predators consume proportionally smaller prey. Problematically, this pattern contradicts the conventional assumption that all predators should have a similar value of preferred PPMR, and thus those studies have argued that more complex food-web models are needed to better describe food-web dynamics.

However, we point out that this apparent inconsistency arises because previous measurement of PPMR have been based only on dietary data (i.e. realised PPMR in diet) and have not appropriately assessed prey size selectivity of predators (i.e. preferred PPMR) by considering effects of prey composition in the environment. In this study, comparing long-term changes in prey size composition in both the diet and the environment of a fish species, we appropriately assessed preferred PPMR for the first time, and observed that preferred PPMR does not vary with predator body size, in accordance with the original theoretical expectation. Although this is a case study using a single predator species, our findings represent an important first step in establishing size-based food-web studies. In addition, our approach can be generally applied to other species and systems, which would allow us to test the plausibility of previous theoretical predictions based on the assumption of size-invariant preferred PPMR.

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

 

 

 

 

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