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1.  Exploring the borders of European Phragmites within a cosmopolitan genus 
AoB Plants  2012;2012:pls020.
European Phragmites australis is one of four main cp-DNA haplotype clusters present worldwide. The European gene pool extends from North America to Far East Asia and South Africa. Extensive gene flow occurs only within the temperate region of Europe.
Background and aims
Two Phragmites australis taxa are recognized in Europe: P. australis ssp. altissimus, also known as Phragmites isiaca, in the Mediterranean region and P. australis in the temperate region. Another taxonomic group in the Mediterranean is Phragmites frutescens. European genotypes are diverse genetically, cytologically and morphologically, and are related to African, Asiatic and American genotypes. We investigated chloroplast DNA (cpDNA) diversity in Europe and defined the current borders of the European gene pool.
Methodology
We analysed chloroplast variation with parsimony and genetic distance methods, and compared it with that of nuclear amplified fragment length polymorphism and microsatellites. We also investigated the phenological pattern of 188 genotypes collected worldwide in a common garden in Denmark. We assumed that non-flowering genotypes could indicate climatic, geographic and/or reproductive barriers to dispersal and would have been recorded in the genetic pattern as groups genetically isolated from, or within, the European pool.
Principal results
The European P. australis gene pool extends from North America to the Far East and South Africa. However, African and North American genotypes are differentiating from the European genotypes. Mediterranean P. australis is genetically different from temperate P. australis and shares several similarities with Phragmites mauritianus in Africa and Phragmites karka in Asia. Phragmites frutescens shares the cpDNA sequences with both these tropical species. Two DNA bands can distinguish Mediterranean P. australis from P. frutescens and P. mauritianus and from temperate P. australis, and reveal possible hybrids among these species in the Mediterranean region. Phenological data confirmed possible gene flow within the temperate region of Europe, whereas the Mediterranean genotypes did not set inflorescences in Denmark, suggesting reproductive barriers between temperate and Mediterranean P. australis.
Conclusions
European P. australis appears as one of four main Phragmites groups known in the world. Further research is needed to understand the implications of long-distance dispersal at the population level.
doi:10.1093/aobpla/pls020
PMCID: PMC3435523  PMID: 22962631
2.  Hybridization of common reed in North America? The answer is blowing in the wind 
AoB Plants  2012;2012:pls022.
Hybridization of Phragmites has occurred in the Gulf Coast and likely is occurring elsewhere in North America. However, detection failure may be due to limited genetic tools. Additionally, nomenclature confusion necessitates a revision of the current classification system.
Background and aims
We review evidence for hybridization of Phragmites australis in North America and the implications for the persistence of native P. australis ssp. americanus populations in North America. We also highlight the need for an updated classification system, which takes P. australis intraspecific variation and hybridization into account.
Methodology
We reviewed available published, in press and in preparation literature to assess the likelihood of hybridization and interbreeding in genotypes of P. australis present in North America.
Principal results
Experimental results demonstrate that hybridization among introduced and native haplotypes is possible within the genus Phragmites, yet evidence that hybridization has occurred naturally is only starting to emerge. The lag in identifying hybridization in Phragmites in North America may be related to under-sampling in some parts of North America and to a lack of molecular tools that provide the capability to recognize hybrids.
Conclusions
Our understanding of the gene flow within and between species in the genus Phragmites is moving at a fast pace, especially on the east and Gulf coasts of North America. More attention should also be focused on the Great Lakes region, the southwestern and the west coast of the USA, where sympatry has created opportunities for hybridization. Where hybridizations have been detected, there are currently no published data on how hybridization affects plant vigour, morphology, invasiveness or conservation of the genetic integrity of the North American native subspecies. We conclude that the detection of more hybridization is highly likely and that there is a need to develop new markers for the different Phragmites species and lineages to fill current knowledge gaps. Finally, we suggest that the classification system for P. australis should be updated and published to help clarify the nomenclature.
doi:10.1093/aobpla/pls022
PMCID: PMC3444738  PMID: 22993684
3.  Jack-and-Master Trait Responses to Elevated CO2 and N: A Comparison of Native and Introduced Phragmites australis 
PLoS ONE  2012;7(10):e42794.
Global change is predicted to promote plant invasions world-wide, reducing biodiversity and ecosystem function. Phenotypic plasticity may influence the ability of introduced plant species to invade and dominate extant communities. However, interpreting differences in plasticity can be confounded by phylogenetic differences in morphology and physiology. Here we present a novel case investigating the role of fitness trait values and phenotypic plasticity to global change factors between conspecific lineages of Phragmites australis. We hypothesized that due to observed differences in the competitive success of North American-native and Eurasian-introduced P. australis genotypes, Eurasian-introduced P. australis would exhibit greater fitness in response to global change factors. Plasticity and plant performance to ambient and predicted levels of carbon dioxide and nitrogen pollution were investigated to understand how invasion pressure may change in North America under a realistic global change scenario. We found that the introduced Eurasian genotype expressed greater mean trait values in nearly every ecophysiological trait measured – aboveground and belowground – to elevated CO2 and nitrogen, outperforming the native North American conspecific by a factor of two to three under every global change scenario. This response is consistent with “jack and master” phenotypic plasticity. We suggest that differences in plant nitrogen productivity, specific leaf area, belowground biomass allocation, and inherently higher relative growth rate are the plant traits that may enhance invasion of Eurasian Phragmites in North America. Given the high degree of genotypic variability within this species, and our limited number of genotypes, our results must be interpreted cautiously. Our study is the first to demonstrate the potential importance of jack-and-master phenotypic plasticity in plant invasions when facing imminent global change conditions. We suggest that jack-and-master invasive genotypes and/or species similar to introduced P. australis will have an increased ecological fitness, facilitating their invasion in both stressful and resource rich environments.
doi:10.1371/journal.pone.0042794
PMCID: PMC3485286  PMID: 23118844
4.  Spatial Genetic Structure in Natural Populations of Phragmites australis in a Mosaic of Saline Habitats in the Yellow River Delta, China 
PLoS ONE  2012;7(8):e43334.
Determination of spatial genetic structure (SGS) in natural populations is important for both theoretical aspects of evolutionary genetics and their application in species conservation and ecological restoration. In this study, we examined genetic diversity within and among the natural populations of a cosmopolitan grass Phragmites australis (common reed) in the Yellow River Delta (YRD), China, where a mosaic of habitat patches varying in soil salinity was detected. We demonstrated that, despite their close geographic proximity, the common reed populations in the YRD significantly diverged at six microsatellite loci, exhibiting a strong association of genetic variation with habitat heterogeneity. Genetic distances among populations were best explained as a function of environmental difference, rather than geographical distance. Although the level of genetic divergence among populations was relatively low (F’ST = 0.073), weak but significant genetic differentiation, as well as the concordance between ecological and genetic landscapes, suggests spatial structuring of genotypes in relation to patchy habitats. These findings not only provided insights into the population dynamics of common reed in changing environments, but also demonstrated the feasibility of using habitat patches in a mosaic landscape as test systems to identify appropriate genetic sources for ecological restoration.
doi:10.1371/journal.pone.0043334
PMCID: PMC3420903  PMID: 22916244
5.  Moving from a regional to a continental perspective of Phragmites australis invasion in North America 
AoB Plants  2012;2012:pls040.
Here we describe the results of a regional comparison of introduced Phragmites australis and two other P. australis lineages found in North America. The regional similarities and differences in introduced P. australis invasion highlight the importance of continental-scale studies for decoding plant invasions.
Aims
We use a regional comparison of Phragmites australis (common reed) subsp. americanus, P. australis subsp. berlandieri and introduced P. australis (possibly five sublineages) in the Chesapeake Bay, the St Lawrence River, Utah and the Gulf Coast to inform a North American perspective on P. australis invasion patterns, drivers, impacts and research needs.
Findings and research needs
Our regional assessments reveal substantial diversity within and between the three main lineages of P. australis in terms of mode of reproduction and the types of environment occupied. For introduced P. australis, the timing of introduction also differed between the regions. Nevertheless, a common finding in these regions reinforces the notion that introduced P. australis is opportunistic and thrives in disturbed habitats. Thus, we expect to see substantial expansion of introduced P. australis with increasing anthropogenic disturbances in each of these regions. Although there have been some studies documenting the negative impacts of introduced P. australis, it also plays a beneficial role in some regions, and in some cases, the purported negative impacts are unproven. There is also a broader need to clarify the genetic and ecological relationships between the different introduced sublineages observed in North America, and their relative competitive ability and potential for admixture. This may be done through regional studies that use similar methodologies and share results to uncover common patterns and processes. To our knowledge, such studies have not been performed on P. australis in spite of the broad attention given to this species. Such research could advance theoretical knowledge on biological invasion by helping to determine the extent to which the patterns observed can be generalized or are sublineage specific or region specific.
Synthesis
Given what appears to be sometimes idiosyncratic invasion patterns when interpreted in isolation in the regions that we analysed, it may be time to consider initiatives on a continental (if not intercontinental) scale to tackle unresolved issues about P. australis.
doi:10.1093/aobpla/pls040
PMCID: PMC3676263  PMID: 23755351
6.  Vegetation Types Alter Soil Respiration and Its Temperature Sensitivity at the Field Scale in an Estuary Wetland 
PLoS ONE  2014;9(3):e91182.
Vegetation type plays an important role in regulating the temporal and spatial variation of soil respiration. Therefore, vegetation patchiness may cause high uncertainties in the estimates of soil respiration for scaling field measurements to ecosystem level. Few studies provide insights regarding the influence of vegetation types on soil respiration and its temperature sensitivity in an estuary wetland. In order to enhance the understanding of this issue, we focused on the growing season and investigated how the soil respiration and its temperature sensitivity are affected by the different vegetation (Phragmites australis, Suaeda salsa and bare soil) in the Yellow River Estuary. During the growing season, there were significant linear relationships between soil respiration rates and shoot and root biomass, respectively. On the diurnal timescale, daytime soil respiration was more dependent on net photosynthesis. A positive correlation between soil respiration and net photosynthesis at the Phragmites australis site was found. There were exponential correlations between soil respiration and soil temperature, and the fitted Q10 values varied among different vegetation types (1.81, 2.15 and 3.43 for Phragmites australis, Suaeda salsa and bare soil sites, respectively). During the growing season, the mean soil respiration was consistently higher at the Phragmites australis site (1.11 µmol CO2 m−2 s−1), followed by the Suaeda salsa site (0.77 µmol CO2 m−2 s−1) and the bare soil site (0.41 µmol CO2 m−2 s−1). The mean monthly soil respiration was positively correlated with shoot and root biomass, total C, and total N among the three vegetation patches. Our results suggest that vegetation patchiness at a field scale might have a large impact on ecosystem-scale soil respiration. Therefore, it is necessary to consider the differences in vegetation types when using models to evaluate soil respiration in an estuary wetland.
doi:10.1371/journal.pone.0091182
PMCID: PMC3946705  PMID: 24608636
7.  Understanding Plant-Microbe Interactions for Phytoremediation of Petroleum-Polluted Soil 
PLoS ONE  2011;6(3):e17961.
Plant-microbe interactions are considered to be important processes determining the efficiency of phytoremediation of petroleum pollution, however relatively little is known about how these interactions are influenced by petroleum pollution. In this experimental study using a microcosm approach, we examined how plant ecophysiological traits, soil nutrients and microbial activities were influenced by petroleum pollution in Phragmites australis, a phytoremediating species. Generally, petroleum pollution reduced plant performance, especially at early stages of plant growth. Petroleum had negative effects on the net accumulation of inorganic nitrogen from its organic forms (net nitrogen mineralization (NNM)) most likely by decreasing the inorganic nitrogen available to the plants in petroleum-polluted soils. However, abundant dissolved organic nitrogen (DON) was found in petroleum-polluted soil. In order to overcome initial deficiency of inorganic nitrogen, plants by dint of high colonization of arbuscular mycorrhizal fungi might absorb some DON for their growth in petroleum-polluted soils. In addition, through using a real-time polymerase chain reaction method, we quantified hydrocarbon-degrading bacterial traits based on their catabolic genes (i.e. alkB (alkane monooxygenase), nah (naphthalene dioxygenase) and tol (xylene monooxygenase) genes). This enumeration of target genes suggests that different hydrocarbon-degrading bacteria experienced different dynamic changes during phytoremediation and a greater abundance of alkB was detected during vegetative growth stages. Because phytoremediation of different components of petroleum is performed by different hydrocarbon-degrading bacteria, plants’ ability of phytoremediating different components might therefore vary during the plant life cycle. Phytoremediation might be most effective during the vegetative growth stages as greater abundances of hydrocarbon-degrading bacteria containing alkB and tol genes were observed at these stages. The information provided by this study enhances our understanding of the effects of petroleum pollution on plant-microbe interactions and the roles of these interactions in the phytoremediation of petroleum-polluted soil.
doi:10.1371/journal.pone.0017961
PMCID: PMC3060916  PMID: 21437257
8.  A Comparison of the Functional Traits of Common Reed (Phragmites australis) in Northern China: Aquatic vs. Terrestrial Ecotypes 
PLoS ONE  2014;9(2):e89063.
Common reed (Phragmites australis (Cav.) Trin. ex Steud.) is distributed widely throughout the world with various ecotypes. This research compares the functional traits and biomass allocation patterns of two contrasting reed ecotypes. Twelve pairs of aquatic and terrestrial reed samples were collected in northern China. Significant differences in functional traits between the two reed ecotypes were observed, while biomass allocation patterns of reed organs did not differ significantly except for at the root. The dry matter content (DMC) in the whole of the reed plant, leaf, root, and rhizome was higher; while the specific leaf area (SLA) and specific root length (SRL) were lower in terrestrial versus aquatic reed. The biomass allocation in organs of the two forms of reed was isometric, only root in the terrestrial habitat increased faster with an increase in the whole plant biomass. It can be affirmed that aquatic and terrestrial reed that adapt to different environments generally has distinct leaf and root functional traits but isometric biomass allocation patterns. This suggests different resource acquisition strategies: (1) aquatic reed grows faster with high SLA and SRL and is more responsive to the environment, while (2) terrestrial reed with high DMC grows slower and is less responsive to the adverse environment (e.g. dry soil conditions).
doi:10.1371/journal.pone.0089063
PMCID: PMC3929632  PMID: 24586505
9.  Ancient DNA Analyses Reveal Contrasting Phylogeographic Patterns amongst Kiwi (Apteryx spp.) and a Recently Extinct Lineage of Spotted Kiwi 
PLoS ONE  2012;7(8):e42384.
The little spotted kiwi (Apteryx owenii) is a flightless ratite formerly found throughout New Zealand but now greatly reduced in distribution. Previous phylogeographic studies of the related brown kiwi (A. mantelli, A. rowi and A. australis), with which little spotted kiwi was once sympatric, revealed extremely high levels of genetic structuring, with mitochondrial DNA haplotypes often restricted to populations. We surveyed genetic variation throughout the present and pre-human range of little spotted kiwi by obtaining mitochondrial DNA sequences from contemporary and ancient samples. Little spotted kiwi and great spotted kiwi (A. haastii) formed a monophyletic clade sister to brown kiwi. Ancient samples of little spotted kiwi from the northern North Island, where it is now extinct, formed a lineage that was distinct from remaining little spotted kiwi and great spotted kiwi lineages, potentially indicating unrecognized taxonomic diversity. Overall, little spotted kiwi exhibited much lower levels of genetic diversity and structuring than brown kiwi, particularly through the South Island. Our results also indicate that little spotted kiwi (or at least hybrids involving this species) survived on the South Island mainland until more recently than previously thought.
doi:10.1371/journal.pone.0042384
PMCID: PMC3410920  PMID: 22876319
10.  Genetics, novel weapons and rhizospheric microcosmal signaling in the invasion of Phragmites australis 
Plant Signaling & Behavior  2008;3(1):1-5.
Chemical communication and perception strategies between plants are highly sophisticated but are only partly understood. Among the different interactions, the suppressive interaction of a class of chemicals released by one plant through root exudates against the neighbouring plants (allelopathy) have been implicated in the invasiveness of many exotic weedy species. Phragmites australis (common reed) is one of the dominant colonizers of the North American wetland marshes and exhibits invasive behavior by virtually replacing the entire native vegetation in its niche. Recently, by adopting a systematic bioassay driven approach we elucidated the role of root derived allelopathy as one of the important mechanisms by which P. australis exerts its invasive behavior. Additionally, our recent preliminary data indicates the involvement of rhizobacterial signaling in the invasive success of P. australis. A better understanding of biochemical weaponry used by P. australis will aid scientists and technologists in addressing the impact of root secretions in invasiveness of weedy species and thus promote a more informed environmental stewardship.
PMCID: PMC2633947  PMID: 19516974
Phragmites australis; roots; phytotoxicity; reactive oxygen species; microtubules; microcosm
11.  Phenotypic Plasticity in Response to the Social Environment: Effects of Density and Sex Ratio on Mating Behaviour Following Ecotype Divergence 
PLoS ONE  2010;5(9):e12755.
The ability to express phenotypically plastic responses to environmental cues might be adaptive in changing environments. We studied phenotypic plasticity in mating behaviour as a response to population density and adult sex ratio in a freshwater isopod (Asellus aquaticus). A. aquaticus has recently diverged into two distinct ecotypes, inhabiting different lake habitats (reed Phragmites australis and stonewort Chara tomentosa, respectively). In field surveys, we found that these habitats differ markedly in isopod population densities and adult sex ratios. These spatially and temporally demographic differences are likely to affect mating behaviour. We performed behavioural experiments using animals from both the ancestral ecotype (“reed” isopods) and from the novel ecotype (“stonewort” isopods) population. We found that neither ecotype adjusted their behaviour in response to population density. However, the reed ecotype had a higher intrinsic mating propensity across densities. In contrast to the effects of density, we found ecotype differences in plasticity in response to sex ratio. The stonewort ecotype show pronounced phenotypic plasticity in mating propensity to adult sex ratio, whereas the reed ecotype showed a more canalised behaviour with respect to this demographic factor. We suggest that the lower overall mating propensity and the phenotypic plasticity in response to sex ratio have evolved in the novel stonewort ecotype following invasion of the novel habitat. Plasticity in mating behaviour may in turn have effects on the direction and intensity of sexual selection in the stonewort habitat, which may fuel further ecotype divergence.
doi:10.1371/journal.pone.0012755
PMCID: PMC2940798  PMID: 20862332
12.  Only a Few Fungal Species Dominate Highly Diverse Mycofloras Associated with the Common Reed 
Plants are naturally colonized by many fungal species that produce effects ranging from beneficial to pathogenic. However, how many of these fungi are linked with a single host plant has not been determined. Furthermore, the composition of plant-associated fungal communities has not been rigorously determined. We investigated these essential issues by employing the perennial wetland reed Phragmites australis as a model. DNA extracted from roots, rhizomes, stems, and leaves was used for amplification and cloning of internal transcribed spacer rRNA gene fragments originating from reed-associated fungi. A total of 1,991 clones from 15 clone libraries were differentiated by restriction fragment length polymorphism analyses into 345 operational taxonomical units (OTUs). Nonparametric estimators for total richness (Chao1 and ACE) and also a parametric log normal model predicted a total of about 750 OTUs if the libraries were infinite. Sixty-two percent of the OTUs sequenced were novel at a threshold of 3%. Several of these OTUs represented undocumented fungal species, which also included higher taxonomic levels. In spite of the high diversity of the OTUs, the mycofloras of vegetative organs were dominated by just a few typical fungi, which suggested that competition and niche differentiation influence the composition of plant-associated fungal communities. This suggestion was independently supported by the results of nested PCR assays specifically monitoring two OTUs over 3 years, which revealed significant preferences for host habitat and host organ.
doi:10.1128/AEM.72.2.1118-1128.2006
PMCID: PMC1392925  PMID: 16461657
13.  Can resource costs of polyploidy provide an advantage to sex? 
Heredity  2012;110(2):152-159.
The predominance of sexual reproduction despite its costs indicates that sex provides substantial benefits, which are usually thought to derive from the direct genetic consequences of recombination and syngamy. While genetic benefits of sex are certainly important, sexual and asexual individuals, lineages, or populations may also differ in physiological and life history traits that could influence outcomes of competition between sexuals and asexuals across environmental gradients. Here, we address possible phenotypic costs of a very common correlate of asexuality, polyploidy. We suggest that polyploidy could confer resource costs related to the dietary phosphorus demands of nucleic acid production; such costs could facilitate the persistence of sex in situations where asexual taxa are of higher ploidy level and phosphorus availability limits important traits like growth and reproduction. We outline predictions regarding the distribution of diploid sexual and polyploid asexual taxa across biogeochemical gradients and provide suggestions for study systems and empirical approaches for testing elements of our hypothesis.
doi:10.1038/hdy.2012.78
PMCID: PMC3554456  PMID: 23188174
sexual reproduction; ploidy; phosphorus; parthenogenesis; ecological stoichiometry; nutrient
14.  Tidal Flushing Restores the Physiological Condition of Fish Residing in Degraded Salt Marshes 
PLoS ONE  2012;7(9):e46161.
Roads, bridges, and dikes constructed across salt marshes can restrict tidal flow, degrade habitat quality for nekton, and facilitate invasion by non-native plants including Phragmites australis. Introduced P. australis contributes to marsh accretion and eliminates marsh surface pools thereby adversely affecting fish by reducing access to intertidal habitats essential for feeding, reproduction, and refuge. Our study assessed the condition of resident fish populations (Fundulus heteroclitus) at four tidally restricted and four tidally restored marshes in New England invaded by P. australis relative to adjacent reference salt marshes. We used physiological and morphological indicators of fish condition, including proximate body composition (% lipid, % lean dry, % water), recent daily growth rate, age class distributions, parasite prevalence, female gravidity status, length-weight regressions, and a common morphological indicator (Fulton’s K) to assess impacts to fish health. We detected a significant increase in the quantity of parasites infecting fish in tidally restricted marshes but not in those where tidal flow was restored to reduce P. australis cover. Using fish length as a covariate, we found that unparasitized, non-gravid F. heteroclitus in tidally restricted marshes had significantly reduced lipid reserves and increased lean dry (structural) mass relative to fish residing in reference marshes. Fish in tidally restored marshes were equivalent across all metrics relative to those in reference marshes indicating that habitat quality was restored via increased tidal flushing. Reference marshes adjacent to tidally restored sites contained the highest abundance of young fish (ages 0–1) while tidally restricted marshes contained the lowest. Results indicate that F. heteroclitus residing in physically and hydrologically altered marshes are at a disadvantage relative to fish in reference marshes but the effects can be reversed through ecological restoration.
doi:10.1371/journal.pone.0046161
PMCID: PMC3459893  PMID: 23029423
15.  Effects of oil on internal gas transport, radial oxygen loss, gas films and bud growth in Phragmites australis 
Annals of Botany  2008;103(2):333-340.
Background and Aims
Oil pollution of wetlands is a world-wide problem but, to date, research has concentrated on its influences on salt marsh rather than freshwater plant communities. The effects of water-borne light oils (liquid paraffin and diesel) were investigated on the fresh/brackish wetland species Phragmites australis in terms of routes of oil infiltration, internal gas transport, radial O2 loss (ROL), underwater gas films and bud growth.
Methods
Pressure flow resistances of pith cavities of nodes and aerenchyma of leaf sheaths, with or without previous exposure to oil, were recorded from flow rates under applied pressure. Convective flows were measured from living excised culms with oiled and non-oiled nodes and leaf sheaths. The effect of oil around culm basal nodes on ROL from rhizome and root apices was measured polarographically. Surface gas films on submerged shoots with and without oil treatment were recorded photographically. Growth and emergence of buds through water with and without an oil film were measured.
Key Results
Internodes are virtually impermeable, but nodes of senesced and living culms are permeable to oils which can block pith cavity diaphragms, preventing flows at applied pressures of 1 kPa, natural convective transport to the rhizome, and greatly decreasing ROL to phyllospheres and rhizospheres. Oil infiltrating or covering living leaf sheaths prevents humidity-induced convection. Oil displaces surface gas films from laminae and leaf sheaths. Buds emerge only a few centimetres through oil and die.
Conclusions
Oil infiltrates the gas space system via nodal and leaf sheath stomata, reducing O2 diffusion and convective flows into the rhizome system and decreasing oxygenation of phyllospheres and rhizospheres; underwater gas exchange via gas films will be impeded. Plants can be weakened by oil-induced failure of emerging buds. Plants will be most at risk during the growing season.
doi:10.1093/aob/mcn213
PMCID: PMC2707319  PMID: 18996951
Phragmites australis; oil pollution; convective flow; pressure flow resistance; phyllosphere oxygenation; rhizosphere oxygenation; underwater gas films; bud emergence; stomata; pith cavity diaphragms; leaf sheath aerenchyma; rhizome aeration
16.  Leaf-traits and growth allometry explain competition and differences in response to climatic change in a temperate forest landscape: a simulation study 
Annals of Botany  2011;108(5):885-894.
Background and Aims
The ability to simulate plant competition accurately is essential for plant functional type (PFT)-based models used in climate-change studies, yet gaps and uncertainties remain in our understanding of the details of the competition mechanisms and in ecosystem responses at a landscape level. This study examines secondary succession in a temperate deciduous forest in eastern China with the aim of determining if competition between tree types can be explained by differences in leaf ecophysiological traits and growth allometry, and whether ecophysiological traits and habitat spatial configurations among PFTs differentiate their responses to climate change.
Methods
A temperate deciduous broadleaved forest in eastern China was studied, containing two major vegetation types dominated by Quercus liaotungensis (OAK) and by birch/poplar (Betula platyphylla and Populus davidiana; BIP), respectively. The Terrestrial Ecosystem Simulator (TESim) suite of models was used to examine carbon and water dynamics using parameters measured at the site, and the model was evaluated against long-term data collected at the site.
Key Results
Simulations indicated that a higher assimilation rate for the BIP vegetation than OAK led to the former's dominance during early successional stages with relatively low competition. In middle/late succession with intensive competition for below-ground resources, BIP, with its lower drought tolerance/resistance and smaller allocation to leaves/roots, gave way to OAK. At landscape scale, predictions with increased temperature extrapolated from existing weather records resulted in increased average net primary productivity (NPP; +19 %), heterotrophic respiration (+23 %) and net ecosystem carbon balance (+17 %). The BIP vegetation in higher and cooler habitats showed 14 % greater sensitivity to increased temperature than the OAK at lower and warmer locations.
Conclusions
Drought tolerance/resistance and morphology-related allocation strategy (i.e. more allocation to leaves/roots) played key roles in the competition between the vegetation types. The overall site-average impacts of increased temperature on NPP and carbon stored in plants were found to be positive, despite negative effects of increased respiration and soil water stress, with such impacts being more significant for BIP located in higher and cooler habitats.
doi:10.1093/aob/mcr218
PMCID: PMC3177688  PMID: 21835816
Succession; watershed; ecophysiological trait; landscape carbon dynamics; temperate forests; competition; simulation; Quercus liaotungensis; Betula platyphylla; Populus davidiana
17.  Genetic Diversity and Differentiation of Juniperus thurifera in Spain and Morocco as Determined by SSR 
PLoS ONE  2014;9(2):e88996.
Juniperus thurifera L. is an important tree endemic to the western Mediterranean basin that it is able to grow in semi-arid climates. It nowadays exhibits a disjunct distribution pattern, occurring in North Africa, Spain, France and the Italian Alps. The Strait of Gibraltar has acted as an efficient barrier against gene flow between African and European populations, which are considered different subspecies by some authors. We aimed at describing the intraspecific genetic diversity of J. thurifera in populations from the Iberian Peninsula and Morocco and the phylogeographical relationships among these populations. The ploidy level of J. thurifera was examined and eleven nuclear microsatellites (nSSRs) developed for J. thurifera were assessed for genotyping this species. Six nSSRs were polymorphic and subsequently used to assess the genetic diversity and structure of the studied populations. Genotyping of the tetraploid J. thurifera using nuclear microsatellites supports the separation of Moroccan and Spanish populations into two genetically differentiated groups that correspond to the proposed subspecies africana and thurifera. High values of within population genetic diversity were found, that accounted for 90% of the total genetic variance, while population structure was weak. The estimators of genetic diversity were higher in populations of Spain than in populations of Morocco pointing for a possible loss of genetic diversity during the spread of this species to Africa from Europe.
doi:10.1371/journal.pone.0088996
PMCID: PMC3923062  PMID: 24533164
18.  Vegetative Ecological Characteristics of Restored Reed (Phragmites australis) Wetlands in the Yellow River Delta, China 
Environmental Management  2011;49(2):325-333.
In this study, we compared ecological characteristics of wetland vegetation in a series of restoration projects that were carried out in the wetlands of Yellow River Delta. The investigated characteristics include plant composition structure, species diversity and community similarity in three kinds of Phragmites australis wetlands, i.e. restored P. australis wetlands (R1, R2, R3 and R4: restored in 2002, 2005, 2007 and 2009, respectively), natural P. australis wetland (N) and degraded P. australis wetland (D) to assess the process of wetlands restoration. The coverage of the R1 was 99%, which was similar to natural wetland. Among all studied wetlands, the highest and lowest stem density was observed in R1 and R2, respectively, Plant height and stem diameter show the same trend as N > R2 > R1 > R3 > D > R4. Species diversity of restored P. australis wetlands became closed to natural wetland. Both species richness and Shannon–Wiener index had similar tendency: increased first and then decreased with restored time. The highest species richness and species diversity were observed in R2, while the lowest values of those parameters were found in natural P. australis wetland. Similarity indexes between restored wetlands and natural wetland increased with the restoration time, but they were still less than 50%. The results indicate that the vegetation of P. australis wetlands has experienced a great improvement after several years’ restoration, and it is feasible to restored degraded P. australis wetlands by pouring fresh water into those wetlands in the Yellow River Delta. However, it is notable that costal degraded P. australis wetland in this region may take years to decades to reach the status of natural wetland.
doi:10.1007/s00267-011-9757-6
PMCID: PMC3260433  PMID: 21968874
Coastal wetland; Wetland restoration; Yellow River Delta; Vegetation characteristics; Species diversity
19.  SELECTION ON LEAF ECOPHYSIOLOGICAL TRAITS IN A DESERT HYBRID HELIANTHUS SPECIES AND EARLY-GENERATION HYBRIDS 
Leaf ecophysiological traits related to carbon gain and resource use are expected to be under strong selection in desert annuals. We used comparative and phenotypic selection approaches to investigate the importance of leaf ecophysiological traits for Helianthus anomalus, a diploid annual sunflower species of hybrid origin that is endemic to active desert dunes. Comparisons were made within and among five genotypic classes: H. anomalus, its ancestral parent species (H. annuus and H. petiolaris), and two backcrossed populations of the parental species (designated BC2ann and BC2pet) representing putative ancestors of H. anomalus. Seedlings were transplanted into H. anomalus habitat at Little Sahara Dunes, Utah, and followed through a summer growing season for leaf ecophysiological traits, phenology, and fitness estimated as vegetative biomass. Helianthus anomalus had a unique combination of traits when compared to its ancestral parent species, suggesting that lower leaf nitrogen and greater leaf succulence might be adaptive. However, selection on leaf traits in H. anomalus favored larger leaf area and greater nitrogen, which was not consistent with the extreme traits of H. anomalus relative to its ancestral parents. Also contrary to expectation, current selection on the leaf traits in the backcross populations was not consistently similar to, or resulting in evolution toward, the current H. anomalus phenotype. Only the selection for greater leaf succulence in BC2ann and greater water-use efficiency in BC2pet would result in evolution toward the current H. anomalus phenotype. It was surprising that the action of phenotypic selection depended greatly on the genotypic class for these closely related sunflower hybrids grown in a common environment. We speculate that this may be due to either phenotypic correlations between measured and unmeasured but functionally related traits or due to the three genotypic classes experiencing the environment differently as a result of their differing morphology.
PMCID: PMC2562700  PMID: 15696747
Carbon isotope discrimination; fitness; leaf area; nitrogen; succulence; water-use efficiency
20.  Invasive Acer negundo outperforms native species in non-limiting resource environments due to its higher phenotypic plasticity 
BMC Ecology  2011;11:28.
Background
To identify the determinants of invasiveness, comparisons of traits of invasive and native species are commonly performed. Invasiveness is generally linked to higher values of reproductive, physiological and growth-related traits of the invasives relative to the natives in the introduced range. Phenotypic plasticity of these traits has also been cited to increase the success of invasive species but has been little studied in invasive tree species. In a greenhouse experiment, we compared ecophysiological traits between an invasive species to Europe, Acer negundo, and early- and late-successional co-occurring native species, under different light, nutrient availability and disturbance regimes. We also compared species of the same species groups in situ, in riparian forests.
Results
Under non-limiting resources, A. negundo seedlings showed higher growth rates than the native species. However, A. negundo displayed equivalent or lower photosynthetic capacities and nitrogen content per unit leaf area compared to the native species; these findings were observed both on the seedlings in the greenhouse experiment and on adult trees in situ. These physiological traits were mostly conservative along the different light, nutrient and disturbance environments. Overall, under non-limiting light and nutrient conditions, specific leaf area and total leaf area of A. negundo were substantially larger. The invasive species presented a higher plasticity in allocation to foliage and therefore in growth with increasing nutrient and light availability relative to the native species.
Conclusions
The higher level of plasticity of the invasive species in foliage allocation in response to light and nutrient availability induced a better growth in non-limiting resource environments. These results give us more elements on the invasiveness of A. negundo and suggest that such behaviour could explain the ability of A. negundo to outperform native tree species, contributes to its spread in European resource-rich riparian forests and impedes its establishment under closed-canopy hardwood forests.
doi:10.1186/1472-6785-11-28
PMCID: PMC3275484  PMID: 22115342
21.  Interspecific Interactions between Phragmites australis and Spartina alterniflora along a Tidal Gradient in the Dongtan Wetland, Eastern China 
PLoS ONE  2013;8(1):e53843.
The invasive species Spartina alterniora Loisel was introduced to the eastern coast of China in the 1970s and 1980s for the purposes of land reclamation and the prevention of soil erosion. The resulting interspecific competition had an important influence on the distribution of native vegetation, which makes studying the patterns and mechanisms of the interactions between Spartina alterniora Loisel and the native species Phragmites australis (Cav.) Trin ex Steud in this region very important. There have been some researches on the interspecific interactions between P. australis and S. alterniora in the Dongtan wetland of Chongming, east China, most of which has focused on the comparison of their physiological characteristics. In this paper, we conducted a neighbor removal experiment along a tidal gradient to evaluate the relative competitive abilities of the two species by calculating their relative neighbor effect (RNE) index. We also looked at the influence of environmental stress and disturbance on the competitive abilities of the two species by comparing interaction strength (I) among different tidal zones both for P. australis and S. alterniora. Finally, we measured physiological characteristics of the two species to assess the physiological mechanisms behind their different competitive abilities. Both negative and positive interactions were found between P. australis and S. alterniora along the environmental gradient. When the direction of the competitive intensity index for P. australis and S. alterniora was consistent, the competitive or facilitative effect of S. alterniora on P. australis was stronger than that of P. australis on S. alterniora. The interspecific interactions of P. australis and S. alterniora varied with environmental conditions, as well as with the method used, to measure interspecific interactions.
doi:10.1371/journal.pone.0053843
PMCID: PMC3547036  PMID: 23342017
22.  Dynamic Formation of Asexual Diploid and Polyploid Lineages: Multilocus Analysis of Cobitis Reveals the Mechanisms Maintaining the Diversity of Clones 
PLoS ONE  2012;7(9):e45384.
Given the hybrid genomic constitutions and increased ploidy of many asexual animals, the identification of processes governing the origin and maintenance of clonal diversity provides useful information about the evolutionary consequences of interspecific hybridization, asexuality and polyploidy. In order to understand the processes driving observed diversity of biotypes and clones in the Cobitis taenia hybrid complex, we performed fine-scale genetic analysis of Central European hybrid zone between two sexual species using microsatellite genotyping and mtDNA sequencing. We found that the hybrid zone is populated by an assemblage of clonally (gynogenetically) reproducing di-, tri- and tetraploid hybrid lineages and that successful clones, which are able of spatial expansion, recruit from two ploidy levels, i.e. diploid and triploid. We further compared the distribution of observed estimates of clonal ages to theoretical distributions simulated under various assumptions and showed that new clones are most likely continuously recruited from ancestral populations. This suggests that the clonal diversity is maintained by dynamic equilibrium between origination and extinction of clonal lineages. On the other hand, an interclonal selection is implied by nonrandom spatial distribution of individual clones with respect to the coexisting sexual species. Importantly, there was no evidence for sexually reproducing hybrids or clonally reproducing non-hybrid forms. Together with previous successful laboratory synthesis of clonal Cobitis hybrids, our data thus provide the most compelling evidence that 1) the origin of asexuality is causally linked to interspecific hybridization; 2) successful establishment of clones is not restricted to one specific ploidy level and 3) the initiation of clonality and polyploidy may be dynamic and continuous in asexual complexes.
doi:10.1371/journal.pone.0045384
PMCID: PMC3447977  PMID: 23028977
23.  A functional–structural model of rice linking quantitative genetic information with morphological development and physiological processes 
Annals of Botany  2011;107(5):817-828.
Background and Aims
Although quantitative trait loci (QTL) analysis of yield-related traits for rice has developed rapidly, crop models using genotype information have been proposed only relatively recently. As a first step towards a generic genotype–phenotype model, we present here a three-dimensional functional–structural plant model (FSPM) of rice, in which some model parameters are controlled by functions describing the effect of main-effect and epistatic QTLs.
Methods
The model simulates the growth and development of rice based on selected ecophysiological processes, such as photosynthesis (source process) and organ formation, growth and extension (sink processes). It was devised using GroIMP, an interactive modelling platform based on the Relational Growth Grammar formalism (RGG). RGG rules describe the course of organ initiation and extension resulting in final morphology. The link between the phenotype (as represented by the simulated rice plant) and the QTL genotype was implemented via a data interface between the rice FSPM and the QTLNetwork software, which computes predictions of QTLs from map data and measured trait data.
Key Results
Using plant height and grain yield, it is shown how QTL information for a given trait can be used in an FSPM, computing and visualizing the phenotypes of different lines of a mapping population. Furthermore, we demonstrate how modification of a particular trait feeds back on the entire plant phenotype via the physiological processes considered.
Conclusions
We linked a rice FSPM to a quantitative genetic model, thereby employing QTL information to refine model parameters and visualizing the dynamics of development of the entire phenotype as a result of ecophysiological processes, including the trait(s) for which genetic information is available. Possibilities for further extension of the model, for example for the purposes of ideotype breeding, are discussed.
doi:10.1093/aob/mcq264
PMCID: PMC3077984  PMID: 21247905
Functional–structural plant model; ecophysiology; QTL analysis; plant modelling; quantitative genetics
24.  Hybridization between Two Polyploid Cardamine (Brassicaceae) Species in North-western Spain: Discordance Between Morphological and Genetic Variation Patterns 
Annals of Botany  2007;99(6):1083-1096.
Background and Aims
Hybridization is an important evolutionary phenomenon, and therefore a detailed understanding of the dynamics of interspecific gene flow and resulting morphological and genetic patterns is of widespread interest. Here hybridization between the polyploids Cardamine pratensis and C. raphanifolia at four localities is explored. Using different types of data, the aim is to provide simultaneous and direct comparisons between genotype and phenotype variation patterns in the studied hybrid populations.
Methods
Evidence of hybridization has been gathered from morphology, molecular markers (amplified fragment length polymorphism and chloroplast DNA sequences), pollen viability, karyology and nuclear DNA content.
Key Results
All data support extensive gene flow occurring in the hybrid populations. A wide range of morphological and genetic variation is observed, which includes both parental and intermediate types. Unbalanced pollen fertility and several ploidy levels are recorded.
Conclusions
Incongruence reported between genotype and phenotype suggests that parental phenotypes are affected by introgression, and intermediate hybrid phenotypes can be genetically closer to one of the parents. Thus, it is evident that morphology, when used alone, can be misleading for interpreting hybridization, and critical evaluation of other data is needed.
doi:10.1093/aob/mcm056
PMCID: PMC3243574  PMID: 17495984
AFLP; Brassicaceae; Cardamine pratensis; Cardamine raphanifolia; flow cytometry; hybridization; morphometrics; polyploidy; Spain
25.  Phragmites australis root secreted phytotoxin undergoes photo-degradation to execute severe phytotoxicity 
Plant Signaling & Behavior  2009;4(6):506-513.
Our study organism, Phragmites australis (common reed), is a unique invader in that both native and introduced lineages are found coexisting in North America. This allows one to make direct assessments of physiological differences between these different subspecies and examine how this relates to invasiveness. Recent efforts to understand plant invasive behavior show that some invasive plants secrete a phytotoxin to ward-off encroachment by neighboring plants (allelopathy) and thus provide the invaders with a competitive edge in a given habitat. Here we show that a varying climatic factor like ultraviolet (UV) light leads to photo-degradation of secreted phytotoxin (gallic acid) in P. australis rhizosphere inducing higher mortality of susceptible seedlings. The photo-degraded product of gallic acid (hereafter GA), identified as mesoxalic acid (hereafter MOA), triggered a similar cell death cascade in susceptible seedlings as observed previously with GA. Further, we detected the biological concentrations of MOA in the natural stands of exotic and native P. australis. Our studies also show that the UV degradation of GA is facilitated at an alkaline pH, suggesting that the natural habitat of P. australis may facilitate the photo-degradation of GA. The study highlights the persistence of the photo-degraded phytotoxin in the P. australis's rhizosphere and its inhibitory effects against the native plants.
PMCID: PMC2688296  PMID: 19816146
ultraviolet; gallic acid; mesoxalic acid; novel weapons; invasive species; Phragmites australis

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