Mechanisms of xylem embolism repair in woody plants: Research progress and questions

To maintain long-distance water transport in woody plants is critical for their survival, growth and development. Water under tension is in a metastable state and prone to cavitation and embolism, which leads to loss of hydraulic conductance, reduced productivity, and eventually plant death. In face to water stress-induced cavitation, plants either reduce frequency of embolism occurrence through cavitation resistance with specialized anatomical struc- ture, or/and form a metabolically active embolism repair mechanism. For the xylem embolism and repair, however, there are controversies regarding the occurring frequency, conditions and underlying mechanisms. In this review paper, we first examined the process, temporal dynamics and frequency of xylem embolism and repair. Then, we summarized hypotheses for the mechanisms of the novel refilling in xylem embolism repair, including the osmotic hypothesis, the reverse osmotic hypothesis, the phloem-driven refilling hypothesis, and the phloem unloading hypothesis. We further compared differences in xylem embolism and repair between conifers and angiosperms tree species, and examined the trade-offs between cavitation resistance and xylem recovery performance. Finally, we proposed four priorities in future research in this field: (1) to improve measuring technology of xylem embolism; (2) to test hypotheses for the mechanisms of the novel refilling in xylem embolism repair and the signal triggering xylem refilling; (3) to explore species-specific trait differences related to xylem embolism and repair and their underlying trade-off relationships; and (4) to enhance studies on the relationship between the involvement of carbon metabolism and aquaporins expression in xylem embolism and repair.     

Going to great lengths: selection for long corolla tubes in an extremely specialized bat–flower mutualism

In a hypothesis that has remained controversial since its inception, Darwin suggested that long-tubed flowers and long-tongued pollinators evolved together in a coevolutionary race, with each selecting for increasing length in the other. Although the selective pressures that flowers impose on tongue length are relatively straightforward, in that longer tongues allow access to more nectar, selective pressures that pollinators impose on flower length are less clear. Here, we test for such selective pressures in the highly specialized mutualism between the nectar bat Anoura fistulata, which can extend its tongue twice as far as other nectar bats, and Centropogon nigricans, which has flowers of a similar length (8–9 cm). We used flight cage experiments to examine the effects of artificially manipulated flower lengths on (i) bat behaviour and (ii) pollen transfer. Increased length produced longer visits, but did not affect the force bats applied during visits. In the second experiment, flower length increased both the male and female components of flower function: long male flowers delivered more pollen grains and long female flowers received more pollen grains. However, pollen transfer was not correlated with visit duration, so the mechanism behind differences in pollen transfer remains unclear. By demonstrating that bats select for increasing flower length, these results are consistent with the hypothesis that A. fistulata evolved its remarkable tongue in a coevolutionary race with long-tubed flowers similar to that envisioned by Darwin.     

Unearthening Old Data: Darwin was Indeed Correct About Earthworm Behavior

Charles Darwin is well known for his studies on the expression of emotions in animals and humans and as founding father of the concept of sexual selection. Yet it is commonly believed that the various arguments Darwin developed about behavior were usually illustrated only by anecdotes and observations recounted by explorers, naturalists, or zookeepers, and lacking any experimental approach. Here we show that this is not true. In his last book, The Formation of Vegetable Mould Through the Action of Worms (1881), Darwin mentions a series of meticulous experiments he ran to test his hypotheses about why earthworms plug their burrows and comes to the conclusion that earthworms seem to act in an intelligent way. His study can still function as a prime example of how to design an experiment for testing hypotheses. Only one part was missing in Darwin’s research: statistical analyses. We retrieved his data and analyzed them statistically. Based on these results, we cannot reject his conclusion as the statistical analyses confirmed Darwin was right. This shows that Charles Darwin already used a hypothetico-deductive approach, and he can thus be seen as the first true behavioral ecologist—a representative of a discipline that has been recognized for only about a hundred years.     

Darwin Core: an evolving community-developed biodiversity data standard

Biodiversity data derive from myriad sources stored in various formats on many distinct hardware and software platforms. An essential step towards understanding global patterns of biodiversity is to provide a standardized view of these heterogeneous data sources to improve interoperability. Fundamental to this advance are definitions of common terms. This paper describes the evolution and development of Darwin Core, a data standard for publishing and integrating biodiversity information. We focus on the categories of terms that define the standard, differences between simple and relational Darwin Core, how the standard has been implemented, and the community processes that are essential for maintenance and growth of the standard. We present case-study extensions of the Darwin Core into new research communities, including metagenomics and genetic resources. We close by showing how Darwin Core records are integrated to create new knowledge products documenting species distributions and changes due to environmental perturbations.     

Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs

Understanding which species are able to recover from drought, under what conditions, and the mechanistic processes involved, will facilitate predictions of plant mortality in response to global change. In response to drought, some species die because of embolism-induced hydraulic failure, whilst others are able to avoid mortality and recover, following rehydration. Several tree species have evolved strategies to avoid embolism, whereas others tolerate high embolism rates but can recover their hydraulic functioning upon drought relief. Here, we focus on structures and processes that might allow some plants to recover from drought stress via embolism reversal. We provide insights into how embolism repair may have evolved, anatomical and physiological features that facilitate this process, and describe possible trade-offs and related costs. Recent controversies on methods used for estimating embolism formation/repair are also discussed, providing some methodological suggestions. Although controversial, embolism repair processes are apparently based on the activity of phloem and ray/axial parenchyma. The mechanism is energetically demanding, and the costs to plants include metabolism and transport of soluble sugars, water and inorganic ions. We propose that embolism repair should be considered as a possible component of a ‘hydraulic efficiency-safety’ spectrum. We also advance a framework for vegetation models, describing how vulnerability curves may change in hydrodynamic model formulations for plants that recover from embolism.     

Metaorganismusforschung trifft Schule

The Darwin Day: modern science meets school During the Darwin Day at the University of Kiel high school students are introduced to recent research fields in modern biology. In 2018 the holistic view of a metaorganism offered the students new scientific ways of thinking and working, which are important for a profound understanding of biological interrelations as well as current clinical disorders. In order to bring new insights from biological research and modern science to school, different formats of science communication can be used. One possibility is the visit of extracurricular learning opportunities such as the Darwin Day at the University of Kiel. By linking current biological research with an out-of-school learning place, the importance of science communication can be illustrated. For this purpose, the Darwin Day and an accompanying teaching unit are presented in this article. Furthermore, insights into the evaluation of this outreach format are given.     

Darwin,Malthus, Süssmilch,and Euler: The Ultimate Origin of the Motivation for the Theory of Natural Selection

It is fairly well known that Darwin was inspired to formulate his theory of natural selection by reading Thomas Malthus’s Essay on the Principle of Population. In fact, by reading Darwin’s notebooks, we can even locate one particular sentence which started Darwin thinking about population and selection. What has not been done before is to explain exactly where this sentence – essentially Malthus’s ideas about geometric population growth – came from. In this essay we show that eighteenth century mathematician Leonhard Euler is responsible for this sentence, and in fact forms the beginning of the logical chain which leads to the creation of the theory of natural selection. We shall examine the fascinating path taken by a mathematical calculation, the many different lenses through which it was viewed, and the path through which it eventually influenced Darwin.     

Character displacement and the origins of diversity

In The Origin of Species, Darwin proposed his principle of divergence of character (a process now termed "character displacement") to explain how new species arise and why they differ from each other phenotypically. Darwin maintained that the origin of species and the evolution of differences between them is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin's principle, specifically that (1) competition promotes divergent trait evolution, (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors, (3) divergence can occur within species, and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how (1) divergence can arise from selection acting to lessen reproductive interactions, (2) divergence is fueled by the intersection of character displacement and sexual selection, and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify.     

Seasonal patterns in biomass smoke pollution and the mid 20th-century transition from Aboriginal to European fire management in northern Australia

Aim Globally, most landscape burning occurs in the tropical savanna biome, where fire is a characteristic of the annual dry season. In northern Australia there is uncertainty about how the frequency and timing of dry season fires have changed in the transition from Aboriginal to European fire management. Location In the tropical eucalypt savannas that surround the city of Darwin in the northwest of the Northern Territory of Australia. Methods Our study had three parts: (1) we developed a predictive statistical model of mean mass (µg) of particulates 10 µm or less per cubic metre of air (PM₁₀) using visibility and other meteorological data in Darwin during the dry seasons of 2000 and 2004; (2) we tested the model and its application to the broader air shed by (a) matching the prediction of this model to PM₁₀ measurements made in Darwin in 2005, (b) matching the predictions to independent measurements at two locations 20 km to the north and south of Darwin and (c) matching peaks in PM₁₀ to known major fire events in the region (2000–01 dry seasons); and (3) we used the model to explore changes in air quality over the last 50 years, a period that spans the transition from Aboriginal to European land management. Results We demonstrated that visibility data can be used reliably as a proxy for biomass burning across the largely uncleared tropical savannas inland of Darwin. Validations using independent measurements demonstrated that our predictive model was robust, and geographically and temporally representative of the regional airshed. We used the model to hindcast and found that seasonal air quality has changed since 1955, with a trend to increasing PM₁₀ concentrations in the early dry season. Main conclusions The results suggest that the transition from Aboriginal to European land management has been associated with an increase in fire activity in the early months of the dry season.     

Aesthetic evolution by mate choice: Darwin's really dangerous idea

Darwin proposed an explicitly aesthetic theory of sexual selection in which he described mate preferences as a 'taste for the beautiful', an 'aesthetic capacity', etc. These statements were not merely colourful Victorian mannerisms, but explicit expressions of Darwin's hypothesis that mate preferences can evolve for arbitrarily attractive traits that do not provide any additional benefits to mate choice. In his critique of Darwin, A. R. Wallace proposed an entirely modern mechanism of mate preference evolution through the correlation of display traits with male vigour or viability, but he called this mechanism natural selection. Wallace's honest advertisement proposal was stridently anti-Darwinian and anti-aesthetic. Most modern sexual selection research relies on essentially the same Neo-Wallacean theory renamed as sexual selection. I define the process of aesthetic evolution as the evolution of a communication signal through sensory/cognitive evaluation, which is most elaborated through coevolution of the signal and its evaluation. Sensory evaluation includes the possibility that display traits do not encode information that is being assessed, but are merely preferred. A genuinely Darwinian, aesthetic theory of sexual selection requires the incorporation of the Lande-Kirkpatrick null model into sexual selection research, but also encompasses the possibility of sensory bias, good genes and direct benefits mechanisms.     

Embolism formation during freezing in the wood of Picea abies

Freeze-thaw events can cause embolism in plant xylem. According to classical theory, gas bubbles are formed during freezing and expand during thawing. Conifers have proved to be very resistant to freeze-thaw induced embolism, because bubbles in tracheids are small and redissolve during thawing. In contrast, increasing embolism rates upon consecutive freeze-thaw events were observed that cannot be explained by the classical mechanism. In this study, embolism formation during freeze-thaw events was analyzed via ultrasonic and Cryo-scanning electron microscope techniques. Twigs of Picea abies L. Karst. were subjected to up to 120 freeze-thaw cycles during which ultrasonic acoustic emissions, xylem temperature, and diameter variations were registered. In addition, the extent and cross-sectional pattern of embolism were analyzed with staining experiments and Cryo-scanning electron microscope observations. Embolism increased with the number of freeze-thaw events in twigs previously dehydrated to a water potential of -2.8 MPa. In these twigs, acoustic emissions were registered, while saturated twigs showed low, and totally dehydrated twigs showed no, acoustic activity. Acoustic emissions were detected only during the freezing process. This means that embolism was formed during freezing, which is in contradiction to the classical theory of freeze-thaw induced embolism. The clustered pattern of embolized tracheids in cross sections indicates that air spread from a dysfunctional tracheid to adjacent functional ones. We hypothesize that the low water potential of the growing ice front led to a decrease of the potential in nearby tracheids. This may result in freezing-induced air seeding.     

木本植物木质部的冻融栓塞应对研究进展

冻融栓塞在中高纬度地区木本植物中普遍存在。抗冻融栓塞能力对在寒冷环境中木本植物的生长和安全越冬十分关键, 这直接决定植物分布范围。冻融栓塞是由于冰中气体溶解度低, 木质部水分在低温下冷冻, 使之前水中溶解的气体逸出到导管中, 随后木质部中的冰融化又使气泡扩张而引发的栓塞现象。木质部解剖结构的差异会影响植物的抗冻融栓塞能力, 植物还可以通过调节木质部正压、代谢耗能等方式主动修复冻融栓塞, 也可通过增加树液溶质含量等逃避冷冻, 以减少低温损伤。然而, 与干旱栓塞相比, 目前对木质部冻融栓塞的形成以及植物响应和调节机制的理解不足。为此, 该文首先综述了木质部冻融栓塞的形成机制和植物的逃避、忍耐、修复等3种冻融栓塞的应对策略, 然后总结了木质部抗低温胁迫能力的生理表现、影响因子和评价指标, 并在此基础上讨论了低温抗性、干旱抗性和水力效率之间的多元权衡关系, 最后提出今后该领域中的5个优先研究问题: (1)不同植物冰冻的最低温度阈值; (2)是否存在应对低温胁迫的水力脆弱性分割机制; (3)冻融栓塞修复与代谢消耗的关系; (4)低温抗性、干旱抗性和水力效率之间的权衡关系; (5)抗冻融栓塞性状是否能够纳入经济性状谱系。     

The role of population size in molecular evolution.

The results of a computer simulation study of the role of population size in population genetical models of molecular evolution are presented. If the mutation rate and strength of selection are held fixed and the population size increased, the eight models examined fall into three domains based on their rates of substitution. In the Ohta domain, the rate of substitution decreases with increasing population size; in the Kimura domain, the rate of substitution remains close to the mutation rate; in the Darwin domain, the rate of substitution increases without bound. In the Kimura and Darwin domains, the rate of substitution is much less sensitive to the population size than suggested by two-allele theories. Remarkably, the overdominance model converges to the neutral model with increasing N. The variation at a neutral locus linked to a selected locus is found to be insensitive to the population size for certain models of selection. A selected locus can actually cause the rate of substitution of deleterious alleles at a linked locus to increase with increasing population size. These unexpected results illustrate that intuition based on two-allele theory is often misleading.     

Limiting similarity and Darwin’s naturalization hypothesis: understanding the drivers of biotic resistance against invasive plant species

Several hypotheses have been proposed to explain biotic resistance of a recipient plant community based on reduced niche opportunities for invasive alien plant species. The limiting similarity hypothesis predicts that invasive species are less likely to establish in communities of species holding similar functional traits. Likewise, Darwin’s naturalization hypothesis states that invasive species closely related to the native community would be less successful. We tested both using the invasive alien Ambrosia artemisiifolia L. and Solidago gigantea Aiton, and grassland species used for ecological restoration in central Europe. We classified all plant species into groups based on functional traits obtained from trait databases and calculated the phylogenetic distance among them. In a greenhouse experiment, we submitted the two invasive species at two propagule pressures to competition with communities of ten native species from the same functional group. In another experiment, they were submitted to pairwise competition with native species selected from each functional group. At the community level, highest suppression for both invasive species was observed at low propagule pressure and not explained by similarity in functional traits. Moreover, suppression decreased asymptotically with increasing phylogenetic distance to species of the native community. When submitted to pairwise competition, suppression for both invasive species was also better explained by phylogenetic distance. Overall, our results support Darwin’s naturalization hypothesis but not the limiting similarity hypothesis based on the selected traits. Biotic resistance of native communities against invasive species at an early stage of establishment is enhanced by competitive traits and phylogenetic relatedness.     

The Trouble with Triplets in Biodiversity Informatics: A Data-Driven Case against Current Identifier Practices

The biodiversity informatics community has discussed aspirations and approaches for assigning globally unique identifiers (GUIDs) to biocollections for nearly a decade. During that time, and despite misgivings, the de facto standard identifier has become the “Darwin Core Triplet”, which is a concatenation of values for institution code, collection code, and catalog number associated with biocollections material. Our aim is not to rehash the challenging discussions regarding which GUID system in theory best supports the biodiversity informatics use case of discovering and linking digital data across the Internet, but how well we can link those data together at this moment, utilizing the current identifier schemes that have already been deployed. We gathered Darwin Core Triplets from a subset of VertNet records, along with vertebrate records from GenBank and the Barcode of Life Data System, in order to determine how Darwin Core Triplets are deployed “in the wild”. We asked if those triplets follow the recommended structure and whether they provide an easy and unambiguous means to track from specimen records to genetic sequence records. We show that Darwin Core Triplets are often riddled with semantic and syntactic errors when deployed and curated in practice, despite specifications about how to construct them. Our results strongly suggest that Darwin Core Triplets that have not been carefully curated are not currently serving a useful role for relinking data. We briefly consider needed next steps to overcome current limitations.     

Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance

Hydraulic conductance of leaves (K(leaf)) typically decreases with increasing water stress and recent studies have proposed different mechanisms responsible for decreasing K(leaf) . We measured K(leaf) concurrently with ultrasonic acoustic emissions (UAEs) in dehydrating leaves of several species to determine whether declining K(leaf) was associated with xylem embolism. In addition, we performed experiments in which the surface tension of water in the leaf xylem was reduced by using a surfactant solution. Finally, we compared the hydraulic vulnerability of entire leaves with the leaf lamina in three species. Leaf hydraulic vulnerability based on rehydration kinetics and UAE was very similar, except in Quercus garryana. However, water potentials corresponding to the initial decline in K(leaf) and the onset of UAE in Q. garryana were similar. In all species tested, reducing the surface tension of water caused K(leaf) to decline at less negative water potentials compared with leaves supplied with water. Microscopy revealed that as the fraction of embolized xylem increased, K(leaf) declined sharply in Q. garryana. Measurements on leaf discs revealed that reductions in lamina hydraulic conductance with dehydration were not as great as those observed in intact leaves, suggesting that embolism was the primary mechanism for reductions in K(leaf) during dehydration.     

Interactions between all pairs of neighboring trees in 16 forests worldwide reveal details of unique ecological processes in each forest,and provide windows into their evolutionary histories

When Darwin visited the Galapagos archipelago, he observed that, in spite of the islands’ physical similarity, members of species that had dispersed to them recently were beginning to diverge from each other. He postulated that these divergences must have resulted primarily from interactions with sets of other species that had also diverged across these otherwise similar islands. By extrapolation, if Darwin is correct, such complex interactions must be driving species divergences across all ecosystems. However, many current general ecological theories that predict observed distributions of species in ecosystems do not take the details of between-species interactions into account. Here we quantify, in sixteen forest diversity plots (FDPs) worldwide, highly significant negative density-dependent (NDD) components of both conspecific and heterospecific between-tree interactions that affect the trees’ distributions, growth, recruitment, and mortality. These interactions decline smoothly in significance with increasing physical distance between trees. They also tend to decline in significance with increasing phylogenetic distance between the trees, but each FDP exhibits its own unique pattern of exceptions to this overall decline. Unique patterns of between-species interactions in ecosystems, of the general type that Darwin postulated, are likely to have contributed to the exceptions. We test the power of our null-model method by using a deliberately modified data set, and show that the method easily identifies the modifications. We examine how some of the exceptions, at the Wind River (USA) FDP, reveal new details of a known allelopathic effect of one of the Wind River gymnosperm species. Finally, we explore how similar analyses can be used to investigate details of many types of interactions in these complex ecosystems, and can provide clues to the evolution of these interactions.     

Charles Robert Darwin and Alfred Russel Wallace: their dispute over the units of selection

Charles Darwin and Alfred Russel Wallace independently discovered the mechanism of natural selection for evolutionary change. However, they viewed the working of selection differently. For Darwin, selection was always focused on the benefit for the individual. For Wallace, selection was as much something of benefit for the group as for the individual. This difference is traced to their different background political–economic views, with Darwin in favor of Adam Smith's view of society and Wallace following Robert Owen in being a socialist.     

The prominent absence of Alfred Russel Wallace at the Darwin anniversaries in Germany in 1909, 1959 and 2009

It is well known that the contribution of Alfred Russell Wallace (1823–1913) to the development of the “Darwinian” principle of natural selection has often been neglected. Here we focus on how the three anniversaries to celebrate the origin of the Darwin–Wallace theory in Germany in 1909, in 1959 in the divided country, as well as in 2009, have represented Charles Robert Darwin’s and Alfred Russell Wallace’s contributions. We have analyzed books and proceedings volumes related to these anniversaries, and the main result is that Wallace was almost always ignored, or only mentioned in passing. In 1909, Ernst Haeckel gave a talk in Jena, later published under the title The worldview of Darwin and Lamarck (Das Weltbild von Darwin und Lamarck), but not as the Darwin–Wallace concept. Haeckel mentions Wallace only once. In two important proceedings volumes from the 1959 anniversaries, Wallace was ignored. The only fair treatment of Wallace is given in another book, a collection of documents edited by Gerhard Heberer, for which the author selected nine key documents and reprinted excerpts (1959). Three of them were articles by Wallace, including the Sarawak- and Ternate-papers of 1855 and 1858, respectively. An analysis of the dominant themes during the celebrations of 2009 shows that none of the six topics had much to do with Wallace and his work. Thus, the tendency to exclude Alfred Russell Wallace is an international phenomenon, and largely attributable to the “Darwin industry”.     

Darwin's Manufactory Hypothesis Is Confirmed and Predicts the Extinction Risk of Extant Birds

In the Origin of Species Darwin hypothesized that the “manufactory” of species operates at different rates in different lineages and that the richness of taxonomic units is autocorrelated across levels of the taxonomic hierarchy. We confirm the manufactory hypothesis using a database of all the world''s extant avian subspecies, species and genera. The hypothesis is confirmed both in correlations across all genera and in paired comparisons controlling for phylogeny. We also find that the modern risk of extinction, as measured by “Red List” classifications, differs across the different categories of genera identified by Darwin. Specifically, species in “manufactory” genera are less likely to be threatened, endangered or recently extinct than are “weak manufactory” genera. Therefore, although Darwin used his hypothesis to investigate past evolutionary processes, we find that the hypothesis also foreshadows future changes to the evolutionary tree.