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1.  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.
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.
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.
PMCID: PMC3444738  PMID: 22993684
2.  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.
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.
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.
PMCID: PMC3676263  PMID: 23755351
3.  Interactive effects of elevated temperature and CO2 on two phylogeographically distinct clones of common reed (Phragmites australis) 
AoB Plants  2013;5:pls051.
One European and one Mediterranean Phragmites australis genotype (DK clone and ALG clone, respectively) showed distinct aboveground growth and physiology in response to different treatment combinations of elevated CO2 and temperature according to their genetic background. The DK clone was the most responsive clone.
The aboveground growth, physiological and biochemical parameters of two clones of the cosmopolitan wetland grass Phragmites australis, grown at four treatment combinations of temperature and CO2, were investigated to elucidate whether their climate response differed due to inherent differences in their ecological adaptation. The two phylogeographically distinct P. australis clones (DK clone, European genetic background; ALG clone, Mediterranean genetic background) were grown for 151 days in phytotrons at 19/12 °C (day/night temperature) and 390 ppm CO2, and at elevated temperature (+5 °C) and CO2 (700 ppm) with treatment factors alone or in combination. The ALG clone had 2–4 times higher aboveground biomass, higher light-saturated rates of photosynthesis (Pmax), maximum electron transport rates (ETRmax) and Rubisco activity, and higher photosynthetic nitrogen-use efficiency than the DK clone. The DK clone, however, produced more shoots, leaves and side-shoots, and had 9–51 % higher specific leaf area and 15–39 % higher leaf nitrogen concentration than the ALG clone. Although elevated atmospheric CO2 alone barely affected the aboveground growth of the two P. australis clones, simultaneously elevated temperature and CO2 stimulated growth and aboveground biomass. Overall, elevated CO2 stimulated photosynthesis, but the clones responded differently to a concomitant increase in CO2 and temperature, depending on the phylogeographic background of the plant. The DK clone showed overall stronger responses, and can be considered the more plastic of the two clones with respect to CO2 and temperature. Thus, the DK clone may be better adapted to climate change than the ALG clone, at least in the short term.
PMCID: PMC4104621
Algeria; climate change; Denmark; Mediterranean Phragmites; RERAF phytotron; temperate Phragmites
4.  Phenotypic traits of Phragmites australis clones are not related to ploidy level and distribution range 
AoB Plants  2012;2012:pls017.
The present study reveals significant genetically determined differences in a range of growth and ecophysiological traits between different Phragmites australis genotypes, and provides evidence that the differences are neither related to ploidy level per se nor to the phylogeographic relationships of the genotypes.
Background and aims
Phragmites australis is a wetland grass with high genetic variability, augmented by its cosmopolitan distribution, clonal growth form and large variation in chromosome numbers. Different ploidy levels and ecotypes differ in morphology and ecophysiological traits, and may possess different levels of phenotypic variation. The aim of this study was to quantify the natural variation in ecophysiological characteristics of P. australis, and to explore whether differences in ecophysiological traits can be related to ploidy levels or to the geographic origin of the clones.
Fifteen clones of P. australis from Europe and Asia/Australia, representing five ploidy levels (4x, 6x, 8x, 10x and 12x), were grown in a common garden design for 119 days. Plant growth and light-saturated rate of photosynthesis (Pmax), stomatal conductance (gs), water use efficiency (WUE) and concentrations of photosynthetic pigments and mineral ions in the leaves were measured.
Principal results
The growth of the plants and most ecophysiological parameters differed significantly between clones. The mean maximum shoot height varied from 0.9 to 1.86 m, Pmax from 9.7 to 27 µmol m−2 s−1, gs from 0.22 to 1.41 mol m−2 s−1 and WUE from 13 to 47 µmol mol−1. The concentrations of chlorophylls did not vary significantly between clones, but the chlorophyll a/b ratio and the concentrations of total carotenoids did. The observed differences were not explained either by the ploidy level per se or by the geographic origin or phylogenetic relationships of the clones.
Phylogeographic relationships in P. australis on a global scale do not mirror the environment where the adaptations have evolved, and high phenotypic variation among and within clones complicates comparative studies. Future studies aimed at explaining differences in plant behaviour between P. australis populations should be careful in the selection of target genotypes and/or populations, and should avoid generalizing their findings beyond the genotypes and/or populations studied.
PMCID: PMC3407373  PMID: 22848787
5.  Preadaptation and post-introduction evolution facilitate the invasion of Phragmites australis in North America 
Ecology and Evolution  2014;4(24):4567-4577.
Compared with non-invasive species, invasive plant species may benefit from certain advantageous traits, for example, higher photosynthesis capacity and resource/energy-use efficiency. These traits can be preadapted prior to introduction, but can also be acquired through evolution following introduction to the new range. Disentangling the origins of these advantageous traits is a fundamental and emerging question in invasion ecology. We conducted a multiple comparative experiment under identical environmental condition with the invasive haplotype M lineage of the wetland grass Phragmites australis and compared the ecophysiological traits of this invasive haplotype M in North America with those of the European ancestor and the conspecific North American native haplotype E lineage, P. australis ssp. americanus. The invasive haplotype M differed significantly from the native North American conspecific haplotype E in several ecophysiological and morphological traits, and the European haplotype M had a more efficient photosynthetic apparatus than the native North American P. australis ssp. americanus. Within the haplotype M lineage, the introduced North American P. australis exhibited different biomass allocation patterns and resource/energy-use strategies compared to its European ancestor group. A discriminant analysis of principal components separated the haplotype M and the haplotype E lineages completely along the first canonical axis, highly related to photosynthetic gas-exchange parameters, photosynthetic energy-use efficiency and payback time. The second canonical axis, highly related to photosynthetic nitrogen use efficiency and construction costs, significantly separated the introduced P. australis in North America from its European ancestor. Synthesis. We conclude that the European P. australis lineage was preadapted to be invasive prior to its introduction, and that the invasion in North America is further stimulated by rapid post-introduction evolution in several advantageous traits. The multicomparison approach used in this study could be an effective approach for distinguishing preadaptation and post-introduction evolution of invasive species. Further research is needed to link the observed changes in invasive traits to the genetic variation and the interaction with the environment.
PMCID: PMC4278810  PMID: 25558352
Biomass allocation; common reed; common-environment experiment; discriminant analysis; ecophysiological trade-off; functional traits; invasion ecology; leaf construction cost; photosynthesis; standardized major axis (SMA)
6.  Phragmites australis management in the United States: 40 years of methods and outcomes 
AoB Plants  2014;6:plu001.
We reviewed all available studies on Phragmites australis management in the United States. Our results show that there is a heavy emphasis on herbicides to manage Phragmites, relative to other methods, and a lack of information on what types of plant communities establish once Phragmites is removed. Our model of Phragmites establishment and reproduction describes the invasion as a symptom of watershed-scale land use and disturbance. We advocate more holistic approaches to control and management that focus on improving water quality and minimizing human disturbance to deter future invasion and improve resilience of native plant communities.
Studies on invasive plant management are often short in duration and limited in the methods tested, and lack an adequate description of plant communities that replace the invader following removal. Here we present a comprehensive review of management studies on a single species, in an effort to elucidate future directions for research in invasive plant management. We reviewed the literature on Phragmites management in North America in an effort to synthesize our understanding of management efforts, identify gaps in knowledge and improve the efficacy of management. Additionally, we assessed recent ecological findings concerning Phragmites mechanisms of invasion and integrated these findings into our recommendations for more effective management. Our overall goal is to examine whether or not current management approaches can be improved and whether they promote reestablishment of native plant communities. We found: (i) little information on community-level recovery of vegetation following removal of Phragmites; and (ii) most management approaches focus on the removal of Phragmites from individual stands or groups of stands over a relatively small area. With a few exceptions, recovery studies did not monitor vegetation for substantial durations, thus limiting adequate evaluation of the recovery trajectory. We also found that none of the recovery studies were conducted in a landscape context, even though it is now well documented that land-use patterns on adjacent habitats influence the structure and function of wetlands, including the expansion of Phragmites. We suggest that Phragmites management needs to shift to watershed-scale efforts in coastal regions, or larger management units inland. In addition, management efforts should focus on restoring native plant communities, rather than simply eradicating Phragmites stands. Wetlands and watersheds should be prioritized to identify ecosystems that would benefit most from Phragmites management and those where the negative impact of management would be minimal.
PMCID: PMC4038441  PMID: 24790122
Common reed; ecological restoration; herbicide; invasive plant; invasive species; management; Phragmites australis; watershed restoration.
7.  Differences in salinity tolerance of genetically distinct Phragmites australis clones 
AoB Plants  2013;5:plt019.
The common reed (Phragmites australis) is a clonal wetland grass with high genetic variability. Clone-specific differences are reflected in morphological and physiological traits, and hence in the ability to cope with environmental stress. The responses to progressively increasing salinity of fifteen distinct Phragmites australis clones reveal genotype-related strategies of salt avoidance and exclusion. The salinity-induced inhibition in shoot elongation rate and photosynthesis varies widely between clones. The differences can be partially attributed to their geographic range, but not correlated to ploidy level. Thus, the genetic background is a major factor influencing the salinity tolerance of distinct Phragmites australis clones.
Different clones of the wetland grass Phragmites australis differ in their morphology and physiology, and hence in their ability to cope with environmental stress. We analysed the responses of 15 P. australis clones with distinct ploidy levels (PLs) (4n, 6n, 8n, 10n, 12n) and geographic origins (Romania, Russia, Japan, Czech Republic, Australia) to step-wise increased salinity (8, 16, 24, 32, 40, 56 and 72 ppt). Shoot elongation rate, photosynthesis and plant part-specific ion accumulation were studied in order to assess if traits associated with salinity tolerance can be related to the genetic background and the geographic origin of the clones. Salt stress affected all clones, but at different rates. The maximum height was reduced from 1860 mm in control plants to 660 mm at 40 ppt salinity. The shoot elongation rate of salt-exposed plants varied significantly between clones until 40 ppt salinity. The light-saturated photosynthesis rate (Pmax) was stimulated by a salinity of 8 ppt, but decreased significantly at higher salinities. The stomatal conductance (gs) and the transpiration rate (E) decreased with increasing salinity. Only three clones survived at 72 ppt salinity, although their rates of photosynthesis were strongly inhibited. The roots and basal leaves of the salt-exposed plants accumulated high concentrations of water-extractable Na+ (1646 and 1004 µmol g−1 dry mass (DM), respectively) and Cl− (1876 and 1400 µmol g−1 DM, respectively). The concentrations of water-extractable Mg2+ and Ca2+ were reduced in salt-exposed plants compared with controls. The variation of all the measured parameters was higher among clones than among PLs. We conclude that the salinity tolerance of distinct P. australis clones varies widely and can be partially attributed to their longitudinal geographic origin, but not to PL. Further investigation will help in improving the understanding of this species' salt tolerance mechanisms and their connection to genetic factors.
PMCID: PMC4104622
Common reed; ecophysiology; geographic range; ion concentration; ploidy level; salt-stress tolerance
8.  Physiological ecology and functional traits of North American native and Eurasian introduced Phragmites australis lineages 
AoB Plants  2013;5:plt048.
Biological invasion pose serious threats to biodiversity and ecosystem services worldwide. While the effects of invasive species are well-documents, less is known about which specific plant traits convey “invasiveness” because most studies compare closely related, but different species which can confound results. A review of the literature by Mozdzer and other scientists compared genetic lineages of the same species, those native to North American and a lineage introduced from Europe to address this complex issue. The authors found that the ability to change both physiologically and morphologically were the key to success of the introduced genetic lineage under current and predicted global change conditions.
Physiological ecology and plant functional traits are often used to explain plant invasion. To gain a better understanding of how traits influence invasion, studies usually compare the invasive plant to a native congener, but there are few conspecific examples in the literature. In North America, the presence of native and introduced genetic lineages of the common reed, Phragmites australis, presents a unique example to evaluate how traits influence plant invasion. We reviewed the literature on functional traits of P. australis lineages in North America, specifically contrasting lineages present on the Atlantic Coast. We focused on differences in physiology between the lineage introduced from Eurasia and the lineage native to North America, specifically seeking to identify the causes underlying the recent expansion of the introduced lineage. Our goals were to better understand which traits may confer invasiveness, provide predictions of how these lineages may respond to interspecific competition or imminent global change, and provide guidance for future research. We reviewed published studies and articles in press, and conducted personal communications with appropriate researchers and managers to develop a comparative dataset. We compared the native and introduced lineages and focused on plant physiological ecology and functional traits. Under both stressful and favourable conditions, our review showed that introduced P. australis consistently exhibited greater ramet density, height and biomass, higher and more plastic relative growth rate, nitrogen productivity and specific leaf area, higher mass specific nitrogen uptake rates, as well as greater phenotypic plasticity compared with the native lineage. We suggest that ecophysiological and other plant functional traits elucidate potential mechanisms for the introduced lineage's invasiveness under current and predicted global change conditions. However, our review identified a disconnect between field surveys, experiments, natural competition and plant ecophysiology that must be addressed in future field studies. Given the likelihood of hybridization between lineages, a better understanding of plant traits in native, non-native and hybrid lineages is needed to manage current invasions and to predict the outcome of interactions among novel genotypes. Comparative physiology and other plant functional traits may provide additional tools to predict the trajectory of current and potential future invasions.
PMCID: PMC4104623
Conspecific; global change; invasive; nitrogen; nitrogen productivity; phenotypic plasticity; relative growth rate; specific leaf area; wetland.
9.  Photosynthesis of co-existing Phragmites haplotypes in their non-native range: are characteristics determined by adaptations derived from their native origin? 
AoB Plants  2013;5:plt016.
Several Phragmites lineages differing in origin and phenotype co-exist in the Gulf Coast of North America. We collected rhizomes of four lineages and propagated them in a common environment to compare photosynthetic characteristics. We observed substantial differences among and within lineages. As the lineages originating in Africa and in the Mediterranean region had higher photosynthetic capacity than the lineages originating in Eurasia, and showed typical ecophysiological traits of plants adapted to warm and arid climates, we concluded that the differences observed are due to adaptations acquired in the native ranges. The four lineages can therefore be regarded as ecotypes.
The Gulf Coast of North America (GC) is a ‘hot spot’ of Phragmites diversity as several lineages (defined according to the haplotypes of their chloroplast DNA) differing in origin, genetic traits and phenotype co-exist and interbreed in this area. We analysed differences in photosynthetic characteristics among and within four haplotypes to understand if differences in gas exchange can be attributed to adaptations acquired in their native ranges. We collected rhizomes of four GC haplotypes (I2, M1, M and AI; including the phenotypes ‘Land-type’, ‘Delta-type’, ‘EU-type’ and ‘Greeny-type’) and propagated them in a common controlled environment to compare photosynthesis–irradiance responses, CO2 responses, chlorophyll fluorescence, the activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), specific leaf area (SLA), pigment contents, stomatal density and guard cell length. The maximum light-saturated photosynthetic rate, Amax, in the haplotype I2 (Land-type) and haplotype M1 (Delta-type) (34.3–36.1 µmol CO2 m−2 s−1) was higher than that in the invasive Eurasian haplotype M (22.4 ± 2.3 µmol CO2 m−2 s−1). The Amax of haplotype AI (Greeny3-type) was 29.1 ± 4.0 µmol CO2 m−2 s−1 and did not differ from the Amax of the other haplotypes. The carboxylation rate (Vcmax) and electron transport rate (Jmax) followed the same pattern as Amax. The haplotypes also differed in SLA (17.0–24.3 m2 kg−1 dry mass) and pigment content, whereas stomatal density and guard cell length, Rubisco activity and chlorophyll fluorescence did not differ significantly among haplotypes. The high photosynthetic activity and gas-exchange capacity of the two haplotypes originating in tropical Africa and the Mediterranean area (haplotypes I2 and M1) are apparently adaptations derived from their native ranges. Hence, the haplotypes can be regarded as ecotypes. However, it remains unclear how these differences relate to plant competitiveness and fitness in the GC of North America environment.
PMCID: PMC4104645
Adaptations; Gulf Coast of North America; genotypes; haplotypes; invasion; photosynthesis; Phragmites
10.  Livestock as a potential biological control agent for an invasive wetland plant 
PeerJ  2014;2:e567.
Invasive species threaten biodiversity and incur costs exceeding billions of US$. Eradication efforts, however, are nearly always unsuccessful. Throughout much of North America, land managers have used expensive, and ultimately ineffective, techniques to combat invasive Phragmites australis in marshes. Here, we reveal that Phragmites may potentially be controlled by employing an affordable measure from its native European range: livestock grazing. Experimental field tests demonstrate that rotational goat grazing (where goats have no choice but to graze Phragmites) can reduce Phragmites cover from 100 to 20% and that cows and horses also readily consume this plant. These results, combined with the fact that Europeans have suppressed Phragmites through seasonal livestock grazing for 6,000 years, suggest Phragmites management can shift to include more economical and effective top-down control strategies. More generally, these findings support an emerging paradigm shift in conservation from high-cost eradication to economically sustainable control of dominant invasive species.
PMCID: PMC4178463  PMID: 25276502
Top-down control; Salt marshes; Invasive species; Biocontrol
11.  Ecosystem services of Phragmites in North America with emphasis on habitat functions 
AoB Plants  2013;5:plt008.
In North America, Phragmites australis (common reed) has generally been regarded as a weed to be controlled. This paper shows that Phragmites-dominated vegetation provides important non-habitat ecosystem services (e.g., carbon sequestration, water quality maintenance) in proportion to its biomass, and many habitat functions for other organisms that vary depending on characteristics of the vegetation and surrounding landscape. Phragmites has both detrimental and beneficial functions; therefore decision-makers must clarify their management goals and understand the local situation. Extensive dense Phragmites may be managed to optimize ecosystem services by partial removal of biomass for a bioenergy feedstock.
Phragmites australis (common reed) is widespread in North America, with native and non-native haplotypes. Many ecologists and wetland managers have considered P. australis a weed with little value to the native biota or human society. I document important ecosystem services of Phragmites including support for many common and rare species of plants and animals. This paper is based on an extensive review of the ecology and natural history literature, discussions with field workers, and observations in 13 US states and one Canadian province during the past 40 years. Phragmites sequesters nutrients, heavy metals and carbon, builds and stabilizes soils, and creates self-maintaining vegetation in urban and industrial areas where many plants do not thrive. These non-habitat ecosystem services are proportional to biomass and productivity. Phragmites was widely used by Native Americans for many purposes; the most important current direct use is for the treatment of wastes. Most of the knowledge of non-habitat ecosystem services is based on studies of P. australis haplotype M (an Old World haplotype). Phragmites also has habitat functions for many organisms. These functions depend on the characteristics of the landscape, habitat, Phragmites stand, species using Phragmites and life history element. The functions that Phragmites provides for many species are optimal at lower levels of Phragmites biomass and extent of stands. Old World Phragmites, contrary to many published statements, as well as North American native Phragmites, provide valuable ecosystem services including products for human use and habitat functions for other organisms. Phragmites stands may need management (e.g. thinning, fragmentation, containment or removal) to create or maintain suitable habitat for desired species of animals and plants.
PMCID: PMC4104640
Bio-energy; ecosystem services; habitat functions; invasive plants; management; methodology; non-native species; Phragmites
12.  A phylogenetic re-evaluation of Arthrinium 
IMA Fungus  2013;4(1):133-154.
Although the genus Arthrinium (sexual morph Apiospora) is commonly isolated as an endophyte from a range of substrates, and is extremely interesting for the pharmaceutical industry, its molecular phylogeny has never been resolved. Based on morphology and DNA sequence data of the large subunit nuclear ribosomal RNA gene (LSU, 28S) and the internal transcribed spacers (ITS) and 5.8S rRNA gene of the nrDNA operon, the genus Arthrinium is shown to belong to Apiosporaceae in Xylariales. Arthrinium is morphologically and phylogenetically circumscribed, and the sexual genus Apiospora treated as synonym on the basis that Arthinium is older, more commonly encountered, and more frequently used in literature. An epitype is designated for Arthrinium pterospermum, and several well-known species are redefined based on their morphology and sequence data of the translation elongation factor 1-alpha (TEF), beta-tubulin (TUB) and internal transcribed spacer (ITS1, 5.8S, ITS2) gene regions. Newly described are A. hydei on Bambusa tuldoides from Hong Kong, A. kogelbergense on dead culms of Restionaceae from South Africa, A. malaysianum on Macaranga hullettii from Malaysia, A. ovatum on Arundinaria hindsii from Hong Kong, A. phragmites on Phragmites australis from Italy, A. pseudospegazzinii on Macaranga hullettii from Malaysia, A. pseudosinense on bamboo from The Netherlands, and A. xenocordella from soil in Zimbabwe. Furthermore, the genera Pteroconium and Cordella are also reduced to synonymy, rejecting spore shape and the presence of setae as characters of generic significance separating them from Arthrinium
PMCID: PMC3719201  PMID: 23898419
Apiospora; Apiosporaceae; ITS; LSU; Ascomycota; Sordariomycetes; Systematics
13.  Positive Effects of Nonnative Invasive Phragmites australis on Larval Bullfrogs 
PLoS ONE  2012;7(8):e44420.
Nonnative Phragmites australis (common reed) is one of the most intensively researched and managed invasive plant species in the United States, yet as with many invasive species, our ability to predict, control or understand the consequences of invasions is limited. Rapid spread of dense Phragmites monocultures has prompted efforts to limit its expansion and remove existing stands. Motivation for large-scale Phragmites eradication programs includes purported negative impacts on native wildlife, a view based primarily on observational results. We took an experimental approach to test this assumption, estimating the effects of nonnative Phragmites australis on a native amphibian.
Methodology/Principal Findings
Concurrent common garden and reciprocal transplant field experiments revealed consistently strong positive influences of Phragmites on Rana catesbeiana (North American bullfrog) larval performance. Decomposing Phragmites litter appears to contribute to the effect.
Positive effects of Phragmites merit further research, particularly in regions where both Phragmites and R. catesbeiana are invasive. More broadly, the findings of this study reinforce the importance of experimental evaluations of the effects of biological invasion to make informed conservation and restoration decisions.
PMCID: PMC3431391  PMID: 22952976
14.  Soil As Levels and Bioaccumulation in Suaeda salsa and Phragmites australis Wetlands of the Yellow River Estuary, China 
BioMed Research International  2015;2015:301898.
Little information is available on As contamination dynamics in the soil-plant systems of wetlands. Total arsenic (As) in soil and plant samples from Suaeda salsa and Phragmites australis wetlands was measured in the Yellow River Estuary (YRE) in summer and autumn of 2007 to investigate the seasonal changes in As concentrations in different wetlands. The results showed that soil As levels greatly exceeded the global and regional background values. As levels in soil and the roots and stems of both types of plants were much higher in summer than in autumn, whereas leaf As showed higher level in autumn. Soil sulfur was the main factor influencing As levels in Suaeda salsa wetlands, whereas soil porosity was the most important factor for Phragmites australis wetlands. The contamination factor (CF) showed moderately to considerably polluted levels of As in both wetland soils. Plant roots and leaves of Suaeda salsa had higher As concentrations and biological concentration factors (BCFs) than stems, while the leaves and stems of Phragmites australis showed higher As levels and BCFs than roots. Compared to Phragmites australis, Suaeda salsa generally showed higher translocation factor (TF), while TF values for both plant species were higher in summer than in autumn.
PMCID: PMC4317578
15.  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.
PMCID: PMC3485286  PMID: 23118844
16.  Expression of major photosynthetic and salt-resistance genes in invasive reed lineages grown under elevated CO2 and temperature 
Ecology and Evolution  2014;4(21):4161-4172.
It is important to investigate the molecular causes of the variation in ecologically important traits to fully understand phenotypic responses to climate change. In the Mississippi River Delta, two distinct, sympatric invasive lineages of common reed (Phragmites australis) are known to differ in several ecophysiological characteristics and are expected to become more salt resistant due to increasing atmospheric CO2 and temperature. We investigated whether different patterns of gene expression can explain their ecophysiological differences and increased vigor under future climatic conditions. We compared the transcript abundance of photosynthetic genes of the Calvin cycle (Rubisco small subunit, RbcS; Phosphoglycerate kinase, PGK; Phosphoribulokinase, PRK), genes related with salt transport (Na+/H+ antiporter, PhaNHA) and oxidative stress response genes (Manganese Superoxide dismutase, MnSOD; Glutathione peroxidase, GPX), and the total aboveground biomass production between two genotypes representing the two lineages. The two genotypes (Delta-type, Mediterranean lineage, and EU-type, Eurasian lineage) were grown under an ambient and a future climate scenario with simultaneously elevated CO2 and temperature, and under two different soil salinities (0‰ or 20‰). We found neither differences in the aboveground biomass production nor the transcript abundances of the two genotypes, but soil salinity significantly affected all the investigated parameters, often interacting with the climatic conditions. At 20‰ salinity, most genes were higher expressed in the future than in the ambient climatic conditions. Higher transcription of the genes suggests higher abundance of the protein they code for, and consequently increased photosynthate production, improved stress responses, and salt exclusion. Therefore, the higher expression of these genes most likely contributed to the significantly ameliorated salinity impact on the aboveground biomass production of both P. australis genotypes under elevated temperature and CO2. Although transcript abundances did not explain differences between the lineages, they correlated with the increased vigor of both lineages under anticipated future climatic conditions.
PMCID: PMC4242567  PMID: 25505541
Common reed; Delta-type; EU-type; Mississippi River Delta; Phragmites australis; US Gulf Coast
17.  Gene flow and genetic structure in the Galician population (NW Spain) according to Alu insertions 
BMC Genetics  2008;9:79.
The most recent Alu insertions reveal different degrees of polymorphism in human populations, and a series of characteristics that make them particularly suitable genetic markers for Human Biology studies. This has led these polymorphisms to be used to analyse the origin and phylogenetic relationships between contemporary human groups. This study analyses twelve Alu sequences in a sample of 216 individuals from the autochthonous population of Galicia (NW Spain), with the aim of studying their genetic structure and phylogenetic position with respect to the populations of Western and Central Europe and North Africa, research that is of special interest in revealing European population dynamics, given the peculiarities of the Galician population due to its geographical situation in western Europe, and its historical vicissitudes.
The insertion frequencies of eleven of the Alu elements analysed were within the variability range of European populations, while Yb8NBC125 proved to be the lowest so far recorded to date in Europe.
Taking the twelve polymorphisms into account, the GD value for the Galician population was 0.268. The comparative analyses carried out using the MDS, NJ and AMOVA methods reveal the existence of spatial heterogeneity, and identify three population groups that correspond to the geographic areas of Western-Central Europe, Eastern Mediterranean Europe and North Africa. Galicia is shown to be included in the Western-Central European cluster, together with other Spanish populations. When only considering populations from Mediterranean Europe, the Galician population revealed a degree of genetic flow similar to that of the majority of the populations from this geographic area.
The results of this study reveal that the Galician population, despite its geographic situation in the western edge of the European continent, occupies an intermediate position in relation to other European populations in general, and Iberian populations in particular. This confirms the important role that migratory movements have had in the European gene pool, at least since Neolithic times. In turn, the MDS and NJ analyses place Galicia within the group comprised of Western-Central European populations, which is justified by the influence of Germanic peoples on the Galician population during the Middle Ages. However, it should also be noted that some of the markers analysed have a certain degree of differentiation, possibly due to the region's position as a 'cul-de-sac' in terms of Iberian population dynamics.
PMCID: PMC2630999  PMID: 19055739
18.  Introducing the Algerian Mitochondrial DNA and Y-Chromosome Profiles into the North African Landscape 
PLoS ONE  2013;8(2):e56775.
North Africa is considered a distinct geographic and ethnic entity within Africa. Although modern humans originated in this Continent, studies of mitochondrial DNA (mtDNA) and Y-chromosome genealogical markers provide evidence that the North African gene pool has been shaped by the back-migration of several Eurasian lineages in Paleolithic and Neolithic times. More recent influences from sub-Saharan Africa and Mediterranean Europe are also evident. The presence of East-West and North-South haplogroup frequency gradients strongly reinforces the genetic complexity of this region. However, this genetic scenario is beset with a notable gap, which is the lack of consistent information for Algeria, the largest country in the Maghreb. To fill this gap, we analyzed a sample of 240 unrelated subjects from a northwest Algeria cosmopolitan population using mtDNA sequences and Y-chromosome biallelic polymorphisms, focusing on the fine dissection of haplogroups E and R, which are the most prevalent in North Africa and Europe respectively. The Eurasian component in Algeria reached 80% for mtDNA and 90% for Y-chromosome. However, within them, the North African genetic component for mtDNA (U6 and M1; 20%) is significantly smaller than the paternal (E-M81 and E-V65; 70%). The unexpected presence of the European-derived Y-chromosome lineages R-M412, R-S116, R-U152 and R-M529 in Algeria and the rest of the Maghreb could be the counterparts of the mtDNA H1, H3 and V subgroups, pointing to direct maritime contacts between the European and North African sides of the western Mediterranean. Female influx of sub-Saharan Africans into Algeria (20%) is also significantly greater than the male (10%). In spite of these sexual asymmetries, the Algerian uniparental profiles faithfully correlate between each other and with the geography.
PMCID: PMC3576335  PMID: 23431392
19.  Interactions among Plant Species and Microorganisms in Salt Marsh Sediments 
The interactions among Spartina patens and sediment microbial populations and the interactions among Phragmites australis and sediment microbial populations were studied at monotypic sites in Piermont Marsh, a salt marsh of the Hudson River north of New York, N.Y., at key times during the growing season. Arbuscular mycorrhizal fungi (AMF) effectively colonized S. patens but not P. australis, and there were seasonal increases and decreases that coincided with plant growth and senescence (17 and 6% of the S. patens root length were colonized, respectively). In sediment samples from the Spartina site, the microbial community and specific bacterial populations were at least twice as large in terms of number and biomass as the microbial community and specific bacterial populations in sediment samples from the Phragmites site, and peak values occurred during reproduction. Members of the domain Bacteria, especially members of the α-, γ-, and δ-subdivisions of the Proteobacteria, were the most abundant organisms at both sites throughout the growing season. The populations were generally more dynamic in samples from the Spartina site than in samples from the Phragmites site. No differences between the two sites and no differences during the growing season were observed when restriction fragment length polymorphism analyses of nifH amplicons were performed in an attempt to detect shifts in the diversity of nitrogen-fixing bacteria. Differences were observed only in the patterns generated by PCR or reverse transcription-PCR for samples from the Spartina site, suggesting that there were differences in the overall and active populations of nitrogen-fixing bacteria. Regression analyses indicated that there was a positive interaction between members of the δ-subdivision of the Proteobacteria and root biomass but not between members of the δ-subdivision of the Proteobacteria and macroorganic matter at both sites. In samples from the Spartina site, there were indications that there were bacterium-fungus interactions since populations of members of the α-subdivision of the Proteobacteria were negatively associated with AMF colonization and populations of members of the γ-subdivision of the Proteobacteria were positively associated with AMF colonization.
PMCID: PMC123761  PMID: 11872463
20.  Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments 
The effect of plant invasion on the microorganisms of soil sediments is very important for estuary ecology. The community structures of methanogens and sulfate-reducing bacteria (SRB) as a function of Spartina alterniflora invasion in Phragmites australis-vegetated sediments of the Dongtan wetland in the Yangtze River estuary, China, were investigated using 454 pyrosequencing and quantitative real-time PCR (qPCR) of the methyl coenzyme M reductase A (mcrA) and dissimilatory sulfite-reductase (dsrB) genes. Sediment samples were collected from two replicate locations, and each location included three sampling stands each covered by monocultures of P. australis, S. alterniflora and both plants (transition stands), respectively. qPCR analysis revealed higher copy numbers of mcrA genes in sediments from S. alterniflora stands than P. australis stands (5- and 7.5-fold more in the spring and summer, respectively), which is consistent with the higher methane flux rates measured in the S. alterniflora stands (up to 8.01 ± 5.61 mg m−2 h−1). Similar trends were observed for SRB, and they were up to two orders of magnitude higher than the methanogens. Diversity indices indicated a lower diversity of methanogens in the S. alterniflora stands than the P. australis stands. In contrast, insignificant variations were observed in the diversity of SRB with the invasion. Although Methanomicrobiales and Methanococcales, the hydrogenotrophic methanogens, dominated in the salt marsh, Methanomicrobiales displayed a slight increase with the invasion and growth of S. alterniflora, whereas the later responded differently. Methanosarcina, the metabolically diverse methanogens, did not vary with the invasion of, but Methanosaeta, the exclusive acetate utilizers, appeared to increase with S. alterniflora invasion. In SRB, sequences closely related to the families Desulfobacteraceae and Desulfobulbaceae dominated in the salt marsh, although they displayed minimal changes with the S. alterniflora invasion. Approximately 11.3 ± 5.1% of the dsrB gene sequences formed a novel cluster that was reduced upon the invasion. The results showed that in the sediments of tidal salt marsh where S. alterniflora displaced P. australis, the abundances of methanogens and SRB increased, but the community composition of methanogens appeared to be influenced more than did the SRB.
PMCID: PMC3750361  PMID: 23986751
dissimilatory sulfite reductase B (dsrB); methyl coenzyme M reductase A (mcrA); spartina alterniflora; phragmites australis; estuarine marsh
21.  Fungal Planet description sheets: 69–91 
Novel species of microfungi described in the present study include the following from Australia: Bagadiella victoriae and Bagadiella koalae on Eucalyptus spp., Catenulostroma eucalyptorum on Eucalyptus laevopinea, Cercospora eremochloae on Eremochloa bimaculata, Devriesia queenslandica on Scaevola taccada, Diaporthe musigena on Musa sp., Diaporthe acaciigena on Acacia retinodes, Leptoxyphium kurandae on Eucalyptus sp., Neofusicoccum grevilleae on Grevillea aurea, Phytophthora fluvialis from water in native bushland, Pseudocercospora cyathicola on Cyathea australis, and Teratosphaeria mareebensis on Eucalyptus sp. Other species include Passalora leptophlebiae on Eucalyptus leptophlebia (Brazil), Exophiala tremulae on Populus tremuloides and Dictyosporium stellatum from submerged wood (Canada), Mycosphaerella valgourgensis on Yucca sp. (France), Sclerostagonospora cycadis on Cycas revoluta (Japan), Rachicladosporium pini on Pinus monophylla (Netherlands), Mycosphaerella wachendorfiae on Wachendorfia thyrsifolia and Diaporthe rhusicola on Rhus pendulina (South Africa). Novel genera of hyphomycetes include Noosia banksiae on Banksia aemula (Australia), Utrechtiana cibiessia on Phragmites australis (Netherlands), and Funbolia dimorpha on blackened stem bark of an unidentified tree (USA). Morphological and culture characteristics along with ITS DNA barcodes are provided for all taxa.
PMCID: PMC3160798  PMID: 22025808
ITS DNA barcodes; LSU; novel fungal species; systematics
22.  Loss of genetic diversity as a signature of apricot domestication and diffusion into the Mediterranean Basin 
BMC Plant Biology  2012;12:49.
Domestication generally implies a loss of diversity in crop species relative to their wild ancestors because of genetic drift through bottleneck effects. Compared to native Mediterranean fruit species like olive and grape, the loss of genetic diversity is expected to be more substantial for fruit species introduced into Mediterranean areas such as apricot (Prunus armeniaca L.), which was probably primarily domesticated in China. By comparing genetic diversity among regional apricot gene pools in several Mediterranean areas, we investigated the loss of genetic diversity associated with apricot selection and diffusion into the Mediterranean Basin.
According to the geographic origin of apricots and using Bayesian clustering of genotypes, Mediterranean apricot (207 genotypes) was structured into three main gene pools: ‘Irano-Caucasian’, ‘North Mediterranean Basin’ and ‘South Mediterranean Basin’. Among the 25 microsatellite markers used, only one displayed deviations from the frequencies expected under neutrality. Similar genetic diversity parameters were obtained within each of the three main clusters using both all SSR loci and only 24 SSR loci based on the assumption of neutrality. A significant loss of genetic diversity, as assessed by the allelic richness and private allelic richness, was revealed from the ‘Irano-Caucasian’ gene pool, considered as a secondary centre of diversification, to the northern and southwestern Mediterranean Basin. A substantial proportion of shared alleles was specifically detected when comparing gene pools from the ‘North Mediterranean Basin’ and ‘South Mediterranean Basin’ to the secondary centre of diversification.
A marked domestication bottleneck was detected with microsatellite markers in the Mediterranean apricot material, depicting a global image of two diffusion routes from the ‘Irano-Caucasian’ gene pool: North Mediterranean and Southwest Mediterranean. This study generated genetic insight that will be useful for management of Mediterranean apricot germplasm as well as genetic selection programs related to adaptive traits.
PMCID: PMC3511222  PMID: 22510209
23.  First artificial hybrid of the eel species Anguilla australis and Anguilla anguilla 
Studies on artificial hybridization of different Anguilla species were conducted recently, i.e. female A. australis with male A. dieffenbachii, and female A. japonica with male A. anguilla. The existence of these artificial hybrids was however not demonstrated by independent genetic methods. Two species - A. anguilla and A. australis - that are phylogenetically close but have different sexual maturation times (12-25 weeks and 6-8 weeks, respectively), were expected to produce favourable hybrids for reproduction studies.
A modification of the protocol for the reproduction of Anguilla japonica was used to produce eight-day Anguilla australis larvae, with a success rate of 71.4%. Thus ten out of 14 females produced eggs that could be fertilized, and three batches resulted in mass hatching. Hybrid larvae from female A. australis x male A. Anguilla survived for up to seven days post fertilization (dpf). The early development of the hybrid showed typical characteristics of A. anguilla tail pigmentation at 50 hours post fertilization (hpf), indicating expression of genes derived from the father.
In this paper we describe the first production of hybrid larvae from male A. anguilla and female A. australis and their survival for up to 7 dpf. A species-specific nucleotide difference in the 18 S rDNA gene confirmed that genes from both A. australis and A. anguilla were present in the hybrids. The developmental stages of the hybrid eel embryos and larvae are described using high resolution images. Video footage also indicated a heart beat in 5-dpf larva.
PMCID: PMC3063818  PMID: 21396126
24.  The genetic structure of Arabidopsis thaliana in the south-western Mediterranean range reveals a shared history between North Africa and southern Europe 
BMC Plant Biology  2014;14:17.
Deciphering the genetic structure of Arabidopsis thaliana diversity across its geographic range provides the bases for elucidating the demographic history of this model plant. Despite the unique A. thaliana genomic resources currently available, its history in North Africa, the extreme southern limit in the biodiversity hotspot of the Mediterranean Basin, remains virtually unknown.
To approach A. thaliana evolutionary history in North Africa, we have analysed the genetic diversity and structure of 151 individuals collected from 20 populations distributed across Morocco. Genotyping of 249 genome-wide SNPs indicated that Morocco contains substantially lower diversity than most analyzed world regions. However, IBD, STRUCTURE and PCA clustering analyses showed that genetic variation is strongly geographically structured. We also determined the genetic relationships between Morocco and the closest European region, the Iberian Peninsula, by analyses of 201 populations from both regions genotyped with the same SNPs. These analyses detected four genetic groups, but all Moroccan accessions belonged to a common Iberian/Moroccan cluster that appeared highly differentiated from the remaining groups. Thus, we identified a genetic lineage with an isolated demographic history in the south-western Mediterranean region. The existence of this lineage was further supported by the study of several flowering genes and traits, which also found Moroccan accessions similar to the same Iberian group. Nevertheless, genetic diversity for neutral SNPs and flowering genes was higher in Moroccan than in Iberian populations of this lineage. Furthermore, we analyzed the genetic relationships between Morocco and other world regions by joint analyses of a worldwide collection of 337 accessions, which detected an additional weak relationship between North Africa and Asia.
The patterns of genetic diversity and structure of A. thaliana in Morocco show that North Africa is part of the species native range and support the occurrence of a glacial refugium in the Atlas Mountains. In addition, the identification of a genetic lineage specific of Morocco and the Iberian Peninsula indicates that the Strait of Gibraltar has been an A. thaliana migration route between Europe and Africa. Finally, the genetic relationship between Morocco and Asia suggests another migration route connecting north-western Africa and Asia.
PMCID: PMC3890648  PMID: 24411008
Arabidopsis thaliana; Population genetics; Natural variation; Genetic diversity; Genetic structure; Demographic history; North Africa; Mediterranean Basin; Glacial refugium/refugia
25.  Ancient DNA Analysis of 8000 B.C. Near Eastern Farmers Supports an Early Neolithic Pioneer Maritime Colonization of Mainland Europe through Cyprus and the Aegean Islands 
PLoS Genetics  2014;10(6):e1004401.
The genetic impact associated to the Neolithic spread in Europe has been widely debated over the last 20 years. Within this context, ancient DNA studies have provided a more reliable picture by directly analyzing the protagonist populations at different regions in Europe. However, the lack of available data from the original Near Eastern farmers has limited the achieved conclusions, preventing the formulation of continental models of Neolithic expansion. Here we address this issue by presenting mitochondrial DNA data of the original Near-Eastern Neolithic communities with the aim of providing the adequate background for the interpretation of Neolithic genetic data from European samples. Sixty-three skeletons from the Pre Pottery Neolithic B (PPNB) sites of Tell Halula, Tell Ramad and Dja'de El Mughara dating between 8,700–6,600 cal. B.C. were analyzed, and 15 validated mitochondrial DNA profiles were recovered. In order to estimate the demographic contribution of the first farmers to both Central European and Western Mediterranean Neolithic cultures, haplotype and haplogroup diversities in the PPNB sample were compared using phylogeographic and population genetic analyses to available ancient DNA data from human remains belonging to the Linearbandkeramik-Alföldi Vonaldiszes Kerámia and Cardial/Epicardial cultures. We also searched for possible signatures of the original Neolithic expansion over the modern Near Eastern and South European genetic pools, and tried to infer possible routes of expansion by comparing the obtained results to a database of 60 modern populations from both regions. Comparisons performed among the 3 ancient datasets allowed us to identify K and N-derived mitochondrial DNA haplogroups as potential markers of the Neolithic expansion, whose genetic signature would have reached both the Iberian coasts and the Central European plain. Moreover, the observed genetic affinities between the PPNB samples and the modern populations of Cyprus and Crete seem to suggest that the Neolithic was first introduced into Europe through pioneer seafaring colonization.
Author Summary
Since the original human expansions out of Africa 200,000 years ago, different prehistoric and historic migration events have taken place in Europe. Considering that the movement of the people implies a consequent movement of their genes, it is possible to estimate the impact of these migrations through the genetic analysis of human populations. Agricultural and husbandry practices originated 10,000 years ago in a region of the Near East known as the Fertile Crescent. According to the archaeological record this phenomenon, known as “Neolithic”, rapidly expanded from these territories into Europe. However, whether this diffusion was accompanied or not by human migrations is greatly debated. In the present work, mitochondrial DNA –a type of maternally inherited DNA located in the cell cytoplasm- from the first Near Eastern Neolithic populations was recovered and compared to available data from other Neolithic populations in Europe and also to modern populations from South Eastern Europe and the Near East. The obtained results show that substantial human migrations were involved in the Neolithic spread and suggest that the first Neolithic farmers entered Europe following a maritime route through Cyprus and the Aegean Islands.
PMCID: PMC4046922  PMID: 24901650

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