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1.  Silicon’s organic pool and biological cycle in moso bamboo community of Wuyishan Biosphere Reserve*  
Biomineralization of Si by plants into phytolith formation and precipitation of Si into clays during weathering are two important processes of silicon’s biogeochemical cycle. As a silicon-accumulating plant, the widely distributed and woody Phyllostachys heterocycla var. pubescens (moso bamboo) contributes to storing silicon by biomineralization and, thus, prevents eutrophication of nearby waterbodies through silicon’s erosion of soil particles.
A study on the organic pool and biological cycle of silicon (Si) of the moso bamboo community was conducted in Wuyishan Biosphere Reserve, China. The results showed that: (1) the standing crop of the moso bamboo community was 13355.4 g/m2, of which 53.61%, 45.82% and 0.56% are represented by the aboveground and belowground parts of moso bamboos, and the understory plants, respectively; (2) the annual net primary production of the community was 2887.1 g/(m2·a), among which the aboveground part, belowground part, litterfalls, and other fractions, accounted for 55.86%, 35.30%, 4.50% and 4.34%, respectively; (3) silicon concentration in stem, branch, leaf, base of stem, root, whip of bamboos, and other plants was 0.15%, 0.79%, 3.10%, 4.40%, 7.32%, 1.52% and 1.01%, respectively; (4) the total Si accumulated in the standing crop of moso bamboo community was 448.91 g/m2, with 99.83% of Si of the total community stored in moso bamboo populations; (5) within moso bamboo community, the annual uptake, retention, and return of Si were 95.75, 68.43, 27.32 g/(m2·a), respectively; (6) the turnover time of Si, which is the time an average atom of Si remains in the soil before it is recycled into the trees or shrubs, was 16.4 years; (7) the enrichment ratio of Si in the moso bamboo community, which is the ratio of the mean concentration of nutrients in the net primary production to the mean concentration of nutrients in the biomass of a community, was 0.64; and lastly, (8) moso bamboo plants stored about 1.26×1010 kg of silicon in the organic pool made up by the moso bamboo forests in the subtropical area of China.
PMCID: PMC1635818  PMID: 17048297
Phyllostachys heterocycla var. pubescens; Moso bamboo community; Silicon-accumulating; Silicon biological cycle; Wuyishan Biosphere Reserve
2.  Sensitivity of the Invasive Geophyte Oxalis pes-caprae to Nutrient Availability and Competition 
Annals of Botany  2007;99(4):637-645.
Background and Aims
Invasion by alien plants may be partially related to disturbance-related increases in nutrient availability and decreases of competition with native species, and to superior competitive ability of the invader. Oxalis pes-caprae is an invasive winter geophyte in the Mediterranean Islands that reproduces vegetatively via bulbs. An investigation was made into the relative responses of O. pes-caprae and the native annual grass Lolium rigidum to nutrient availability and to competition with each other in order to understand patterns of invasion in the field. Because Oxalis accumulates oxalic acid in its leaves, which could ameliorate soil phosphorous availability, field observations were made to determine whether the presence of Oxalis alters soil P availability.
A full-factorial glasshouse experiment was conducted with nutrient availability (high and low) and competition (Lolium alone, Oxalis alone, and Lolium and Oxalis together). Plant performance was assessed by determining (1) above- and below-ground biomass at the time of Oxalis maximum biomass and (2) reproductive output of Oxalis and Lolium at the end of their respective growth cycles. Measurements were also taken for leaf N and P content. Soil samples were taken in the field from paired Oxalis-invaded and non-invaded plots located in Menorca (Balearic Islands) and available P was determined.
Key Results
High nutrient availability increased Oxalis and Lolium vegetative biomass and reproductive output to a similar degree. Competition with Lolium had a much stronger negative effect on Oxalis bulb production than reduced nutrients. Lolium was a superior competitor than Oxalis; the latter did not affect Lolium maximum biomass and spike production. Significantly greater soil-P availability in Oxalis-invaded field soils relative to paired non-invaded soils suggest that Oxalis influences soil P cycling.
Oxalis is a poor competitor. This is consistent with the preferential distribution of Oxalis in disturbed areas such as ruderal habitats, and might explain its low influence on the cover of native species in invaded sites. The results also suggest that certain disturbances (e.g. autumn ploughing) may greatly enhance Oxalis invasion.
PMCID: PMC2802929  PMID: 17298990
Oxalis pes-caprae; invasive species; competition; nutrients; Lolium rigidum; asexual reproduction; Mediterranean Islands
3.  Large herbivores may alter vegetation structure of semi-arid savannas through soil nutrient mediation 
Oecologia  2011;165(4):1095-1107.
In savannas, the tree–grass balance is governed by water, nutrients, fire and herbivory, and their interactions. We studied the hypothesis that herbivores indirectly affect vegetation structure by changing the availability of soil nutrients, which, in turn, alters the competition between trees and grasses. Nine abandoned livestock holding-pen areas (kraals), enriched by dung and urine, were contrasted with nearby control sites in a semi-arid savanna. About 40 years after abandonment, kraal sites still showed high soil concentrations of inorganic N, extractable P, K, Ca and Mg compared to controls. Kraals also had a high plant production potential and offered high quality forage. The intense grazing and high herbivore dung and urine deposition rates in kraals fit the accelerated nutrient cycling model described for fertile systems elsewhere. Data of a concurrent experiment also showed that bush-cleared patches resulted in an increase in impala dung deposition, probably because impala preferred open sites to avoid predation. Kraal sites had very low tree densities compared to control sites, thus the high impala dung deposition rates here may be in part driven by the open structure of kraal sites, which may explain the persistence of nutrients in kraals. Experiments indicated that tree seedlings were increasingly constrained when competing with grasses under fertile conditions, which might explain the low tree recruitment observed in kraals. In conclusion, large herbivores may indirectly keep existing nutrient hotspots such as abandoned kraals structurally open by maintaining a high local soil fertility, which, in turn, constrains woody recruitment in a negative feedback loop. The maintenance of nutrient hotspots such as abandoned kraals by herbivores contributes to the structural heterogeneity of nutrient-poor savanna vegetation.
PMCID: PMC3057003  PMID: 21225433
Bush encroachment; Tree–grass competition; Nutrient hotspot; Seedling; Predation
4.  The Root Herbivore History of the Soil Affects the Productivity of a Grassland Plant Community and Determines Plant Response to New Root Herbivore Attack 
PLoS ONE  2013;8(2):e56524.
Insect root herbivores can alter plant community structure by affecting the competitive ability of single plants. However, their effects can be modified by the soil environment. Root herbivory itself may induce changes in the soil biota community, and it has recently been shown that these changes can affect plant growth in a subsequent season or plant generation. However, so far it is not known whether these root herbivore history effects (i) are detectable at the plant community level and/or (ii) also determine plant species and plant community responses to new root herbivore attack. The present greenhouse study determined root herbivore history effects of click beetle larvae (Elateridae, Coleoptera, genus Agriotes) in a model grassland plant community consisting of six common species (Achillea millefolium, Plantago lanceolata, Taraxacum officinale, Holcus lanatus, Poa pratensis, Trifolium repens). Root herbivore history effects were generated in a first phase of the experiment by growing the plant community in soil with or without Agriotes larvae, and investigated in a second phase by growing it again in the soils that were either Agriotes trained or not. The root herbivore history of the soil affected plant community productivity (but not composition), with communities growing in root herbivore trained soil producing more biomass than those growing in untrained soil. Additionally, it influenced the response of certain plant species to new root herbivore attack. Effects may partly be explained by herbivore-induced shifts in the community of arbuscular mycorrhizal fungi. The root herbivore history of the soil proved to be a stronger driver of plant growth on the community level than an actual root herbivore attack which did not affect plant community parameters. History effects have to be taken into account when predicting the impact of root herbivores on grasslands.
PMCID: PMC3575479  PMID: 23441201
5.  Herbaceous Forage and Selection Patterns by Ungulates across Varying Herbivore Assemblages in a South African Savanna 
PLoS ONE  2013;8(12):e82831.
Herbivores generally have strong structural and compositional effects on vegetation, which in turn determines the plant forage species available. We investigated how selected large mammalian herbivore assemblages use and alter herbaceous vegetation structure and composition in a southern African savanna in and adjacent to the Kruger National Park, South Africa. We compared mixed and mono-specific herbivore assemblages of varying density and investigated similarities in vegetation patterns under wildlife and livestock herbivory. Grass species composition differed significantly, standing biomass and grass height were almost twice as high at sites of low density compared to high density mixed wildlife species. Selection of various grass species by herbivores was positively correlated with greenness, nutrient content and palatability. Nutrient-rich Urochloa mosambicensis Hack. and Panicum maximum Jacq. grasses were preferred forage species, which significantly differed in abundance across sites of varying grazing pressure. Green grasses growing beneath trees were grazed more frequently than dry grasses growing in the open. Our results indicate that grazing herbivores appear to base their grass species preferences on nutrient content cues and that a characteristic grass species abundance and herb layer structure can be matched with mammalian herbivory types.
PMCID: PMC3865094  PMID: 24358228
6.  Efficacy of Biosolids in Assisted Phytostabilization of Metalliferous Acidic Sandy Soils with Five Grass Species 
The role of sewage sludge as an immobilising agent in the phytostabilization of metal-contaminated soil was evaluated using five grass species viz., Dactylis glomerata L., Festuca arundinacea Schreb., F. rubra L., Lolium perenne L., L. westerwoldicum L. The function of metal immobilization was investigated by monitoring pH, Eh and Cd, Pb, and Zn levels in column experiment over a period of 5-months. Grasses grown on sewage sludge-amendments produced high biomass in comparison to controls. A significant reduction in metal uptake by plants was also observed as a result of sewage sludge application, which was attributed to decreased bioavailability through soil stabilisation. We have observed that the sludge amendment decreased metal bioavailability and concentrations in soil at a depth of 25 cm, in contrast to untreated columns, where metal concentrations in the soil solution were very high.
PMCID: PMC3827663
grass species; trace elements; sewage sludge; phytostabilisation; column experiment; soil solution; redox potential
7.  Impacts of seedling herbivory on plant competition and implications for species coexistence 
Annals of Botany  2009;103(8):1347-1353.
Background and Aims
Although the causes and consequences of seedling herbivory for plant community composition are well understood, the mechanisms by which herbivores influence plant species recruitment to the established phase remain less clear. The aim was to examine how variation in the intensity of seedling herbivory interacts with growth-defence trade-offs and herbivore feeding preferences to affect plant community development.
Using 14-d-old seedlings of Trifolium pratense and T. repens, relative growth and susceptibility to herbivory by the snail Helix aspersa was quantified to elucidate putative growth-defence trade-offs for these species. Then mixed assemblages of 14-d-old Trifolium seedlings were exposed to herbivory by zero, two, five or ten snails and determined how variation in the intensity of herbivory affected competitive interactions into the mature phase (as measured by total plant biomass at 120 d old).
Key Results
In the absence of herbivory, communities were dominated by T. pratense; a result expected on the basis that it yielded larger and presumably more competitive seedlings. However, when seedlings were exposed to herbivory, the balance of competition shifted. At low levels of herbivory (two snails), both Trifolium species contributed equally to total plant biomass. More intense herbivory (five snails) resulted in almost total mortality of T. pratense and dominance of the mature community by T. repens. The most intense herbivory (ten snails) effectively removed all seedlings from the experimental community.
The study illustrates a mechanism whereby spatio-temporal fluctuations in seedling herbivory, when coupled with species-specific variation in competitive ability and sensitivity to herbivore attack, can differentially influence plant recruitment into the mature phase. This mechanism may be a key element in our attempts to understand plant species coexistence, since fluctuations in plant recruitment are fundamental to the many theories that view coexistence as a consequence of a spatio-temporal lottery for dominance over regeneration micro-sites.
PMCID: PMC2685311  PMID: 19351683
Growth-defence trade-off; lottery models; plant–animal interactions; plant size variability; seedling acceptability; seedling defence; spatio-temporal niches; Trifolium pratense; Trifolium repens
8.  The Terrestrial Silica Pump 
PLoS ONE  2012;7(12):e52932.
Silicon (Si) cycling controls atmospheric CO2 concentrations and thus, the global climate, through three well-recognized means: chemical weathering of mineral silicates, occlusion of carbon (C) to soil phytoliths, and the oceanic biological Si pump. In the latter, oceanic diatoms directly sequester 25.8 Gton C yr−1, accounting for 43% of the total oceanic net primary production (NPP). However, another important link between C and Si cycling remains largely ignored, specifically the role of Si in terrestrial NPP. Here we show that 55% of terrestrial NPP (33 Gton C yr−1) is due to active Si-accumulating vegetation, on par with the amount of C sequestered annually via marine diatoms. Our results suggest that similar to oceanic diatoms, the biological Si cycle of land plants also controls atmospheric CO2 levels. In addition, we provide the first estimates of Si fixed in terrestrial vegetation by major global biome type, highlighting the ecosystems of most dynamic Si fixation. Projected global land use change will convert forests to agricultural lands, increasing the fixation of Si by land plants, and the magnitude of the terrestrial Si pump.
PMCID: PMC3534122  PMID: 23300825
9.  Fate and Uptake of Pharmaceuticals in Soil–Plant Systems 
Pharmaceuticals have been detected in the soil environment where there is the potential for uptake into crops. This study explored the fate and uptake of pharmaceuticals (carbamazepine, diclofenac, fluoxetine, propranolol, sulfamethazine) and a personal care product (triclosan) in soil–plant systems using radish (Raphanus sativus) and ryegrass (Lolium perenne). Five of the six chemicals were detected in plant tissue. Carbamazepine was taken up to the greatest extent in both the radish (52 μg/g) and ryegrass (33 μg/g), whereas sulfamethazine uptake was below the limit of quantitation (LOQ) (<0.01 μg/g). In the soil, concentrations of diclofenac and sulfamethazine dropped below the LOQ after 7 days. However, all pharmaceuticals were still detectable in the pore water at the end of the experiment. The results demonstrate the ability of plant species to accumulate pharmaceuticals from soils with uptake apparently specific to both plant species and chemical. Results can be partly explained by the hydrophobicity and extent of ionization of each chemical in the soil.
PMCID: PMC3908740  PMID: 24405013
plant uptake; pharmaceuticals; fate; soil; bioavailability; carbamazepine; diclofenac; fluoxetine; propranolol; sulfamethazine; triclosan
10.  Rapid Plant Identification Using Species- and Group-Specific Primers Targeting Chloroplast DNA 
PLoS ONE  2012;7(1):e29473.
Plant identification is challenging when no morphologically assignable parts are available. There is a lack of broadly applicable methods for identifying plants in this situation, for example when roots grow in mixture and for decayed or semi-digested plant material. These difficulties have also impeded the progress made in ecological disciplines such as soil- and trophic ecology. Here, a PCR-based approach is presented which allows identifying a variety of plant taxa commonly occurring in Central European agricultural land. Based on the trnT-F cpDNA region, PCR assays were developed to identify two plant families (Poaceae and Apiaceae), the genera Trifolium and Plantago, and nine plant species: Achillea millefolium, Fagopyrum esculentum, Lolium perenne, Lupinus angustifolius, Phaseolus coccineus, Sinapis alba, Taraxacum officinale, Triticum aestivum, and Zea mays. These assays allowed identification of plants based on size-specific amplicons ranging from 116 bp to 381 bp. Their specificity and sensitivity was consistently high, enabling the detection of small amounts of plant DNA, for example, in decaying plant material and in the intestine or faeces of herbivores. To increase the efficacy of identifying plant species from large number of samples, specific primers were combined in multiplex PCRs, allowing screening for multiple species within a single reaction. The molecular assays outlined here will be applicable manifold, such as for root- and leaf litter identification, botanical trace evidence, and the analysis of herbivory.
PMCID: PMC3257244  PMID: 22253728
11.  New chloroplast microsatellite markers suitable for assessing genetic diversity of Lolium perenne and other related grass species 
Annals of Botany  2012;110(6):1327-1339.
Background and Aims
Lolium perenne (perennial ryegrass) is the most important forage grass species of temperate regions. We have previously released the chloroplast genome sequence of L. perenne ‘Cashel’. Here nine chloroplast microsatellite markers are published, which were designed based on knowledge about genetically variable regions within the L. perenne chloroplast genome. These markers were successfully used for characterizing the genetic diversity in Lolium and different grass species.
Chloroplast genomes of 14 Poaceae taxa were screened for mononucleotide microsatellite repeat regions and primers designed for their amplification from nine loci. The potential of these markers to assess genetic diversity was evaluated on a set of 16 Irish and 15 European L. perenne ecotypes, nine L. perenne cultivars, other Lolium taxa and other grass species.
Key Results
All analysed Poaceae chloroplast genomes contained more than 200 mononucleotide repeats (chloroplast simple sequence repeats, cpSSRs) of at least 7 bp in length, concentrated mainly in the large single copy region of the genome. Nucleotide composition varied considerably among subfamilies (with Pooideae biased towards poly A repeats). The nine new markers distinguish L. perenne from all non-Lolium taxa. TeaCpSSR28 was able to distinguish between all Lolium species and Lolium multiflorum due to an elongation of an A8 mononucleotide repeat in L. multiflorum. TeaCpSSR31 detected a considerable degree of microsatellite length variation and single nucleotide polymorphism. TeaCpSSR27 revealed variation within some L. perenne accessions due to a 44-bp indel and was hence readily detected by simple agarose gel electrophoresis. Smaller insertion/deletion events or single nucleotide polymorphisms detected by these new markers could be visualized by polyacrylamide gel electrophoresis or DNA sequencing, respectively.
The new markers are a valuable tool for plant breeding companies, seed testing agencies and the wider scientific community due to their ability to monitor genetic diversity within breeding pools, to trace maternal inheritance and to distinguish closely related species.
PMCID: PMC3478042  PMID: 22419761
Lolium perenne; perennial ryegrass; Poaceae; chloroplast microsatellite markers; chloroplast genome; genetic diversity
12.  Phytolith Assemblages and Systematic Associations in Grassland Species of the South-Eastern Pampean Plains, Argentina 
Annals of Botany  2006;98(6):1155-1165.
• Background and Aims Phytolith descriptions of South American plant species are scarce. This knowledge is crucial for the interpretation of the fossil phytolith record of a region. In this study phytolith assemblages and systematic relationships of the main grasses and Asteraceae species of Paspalum quadrifarium grassland are described.
• Methods Phytoliths from leaves of Poaceae and Asteraceae species were extracted by using a calcination technique. For each species, 350–400 phytoliths were counted and the relative frequency of each morphotype was calculated. Phytolith assemblages were subject to principal components analysis (PCA) and cluster analysis (Morisita index).
• Key Results PCA and cluster analysis showed family (Poaceae vs. Asteraceae) and subfamily (within Poaceae) differentiation. Exceptions to general trends described for other species were detected. Floristic variants of Paspalum quadrifarium grassland can be separated by their phytolith assemblages.
• Conclusions The study provides a reference collection of phytolith assemblages of the main Poaceae and Asteraceae species of Paspalum quadrifarium grassland and describes some phytolith morphotypes/systematic relationships useful for the analysis of fossil phytolith assemblages of the Pampean region.
PMCID: PMC3292269  PMID: 17030553
Paspalum quadrifarium; Asteraceae; Poaceae; phytolith assemblages; Argentina; Southern Pampa
13.  Transport of silicon from roots to panicles in plants 
Silicon (Si) is the most abundant minerals in soil and exerts beneficial effects on plant growth by alleviating various stresses. The transport of Si from soil to the panicles is mediated by different transporters. Lsi1, belonging to a NIP group of the aquaporin family, is responsible for the uptake of Si from soil into the root cells in both dicots and monocots although its expression patterns and cellular localization differ with plant species. The subsequent transport of Si out of the root cells towards the stele is medicated by an active efflux transporter, Lsi2. Lsi1 and Lsi2 are polarly localized at the distal and proximal sides, respectively, of both exodermis and endodermis in rice root. Silicon in the xylem sap is presented in the form of monosilicic acid and is unloaded by Lsi6, a homolog of Lsi1 in rice. Lsi6 is also involved in the inter-vascular transfer of Si at the node, which is necessary for preferential Si distribution to the panicles.
PMCID: PMC3171283  PMID: 21785256
localization; distribution; uptake; silicon; transporter
14.  Olivine Weathering in Soil, and Its Effects on Growth and Nutrient Uptake in Ryegrass (Lolium perenne L.): A Pot Experiment 
PLoS ONE  2012;7(8):e42098.
Mineral carbonation of basic silicate minerals regulates atmospheric CO2 on geological time scales by locking up carbon. Mining and spreading onto the earth's surface of fast-weathering silicates, such as olivine, has been proposed to speed up this natural CO2 sequestration (‘enhanced weathering’). While agriculture may offer an existing infrastructure, weathering rate and impacts on soil and plant are largely unknown. Our objectives were to assess weathering of olivine in soil, and its effects on plant growth and nutrient uptake. In a pot experiment with perennial ryegrass (Lolium perenne L.), weathering during 32 weeks was inferred from bioavailability of magnesium (Mg) in soil and plant. Olivine doses were equivalent to 1630 (OLIV1), 8150, 40700 and 204000 (OLIV4) kg ha−1. Alternatively, the soluble Mg salt kieserite was applied for reference. Olivine increased plant growth (+15.6%) and plant K concentration (+16.5%) in OLIV4. At all doses, olivine increased bioavailability of Mg and Ni in soil, as well as uptake of Mg, Si and Ni in plants. Olivine suppressed Ca uptake. Weathering estimated from a Mg balance was equivalent to 240 kg ha−1 (14.8% of dose, OLIV1) to 2240 kg ha−1 (1.1%, OLIV4). This corresponds to gross CO2 sequestration of 290 to 2690 kg ha−1 (29 103 to 269 103 kg km−2.) Alternatively, weathering estimated from similarity with kieserite treatments ranged from 13% to 58% for OLIV1. The Olsen model for olivine carbonation predicted 4.0% to 9.0% weathering for our case, independent of olivine dose. Our % values observed at high doses were smaller than this, suggesting negative feedbacks in soil. Yet, weathering appears fast enough to support the ‘enhanced weathering’ concept. In agriculture, olivine doses must remain within limits to avoid imbalances in plant nutrition, notably at low Ca availability; and to avoid Ni accumulation in soil and crop.
PMCID: PMC3415406  PMID: 22912685
15.  Climate Extreme Effects on the Chemical Composition of Temperate Grassland Species under Ambient and Elevated CO2: A Comparison of Fructan and Non-Fructan Accumulators 
PLoS ONE  2014;9(3):e92044.
Elevated CO2 concentrations and extreme climate events, are two increasing components of the ongoing global climatic change factors, may alter plant chemical composition and thereby their economic and ecological characteristics, e.g. nutritional quality and decomposition rates. To investigate the impact of climate extremes on tissue quality, four temperate grassland species: the fructan accumulating grasses Lolium perenne, Poa pratensis, and the nitrogen (N) fixing legumes Medicago lupulina and Lotus corniculatus were subjected to water deficit at elevated temperature (+3°C), under ambient CO2 (392 ppm) and elevated CO2 (620 ppm). As a general observation, the effects of the climate extreme were larger and more ubiquitous in combination with elevated CO2. The imposed climate extreme increased non-structural carbohydrate and phenolics in all species, whereas it increased lignin in legumes and decreased tannins in grasses. However, there was no significant effect of climate extreme on structural carbohydrates, proteins, lipids and mineral contents and stoichiometric ratios. In combination with elevated CO2, climate extreme elicited larger increases in fructan and sucrose content in the grasses without affecting the total carbohydrate content, while it significantly increased total carbohydrates in legumes. The accumulation of carbohydrates in legumes was accompanied by higher activity of sucrose phosphate synthase, sucrose synthase and ADP-Glc pyrophosphorylase. In the legumes, elevated CO2 in combination with climate extreme reduced protein, phosphorus (P) and magnesium (Mg) contents and the total element:N ratio and it increased phenol, lignin, tannin, carbon (C), nitrogen (N) contents and C:N, C:P and N:P ratios. On the other hand, the tissue composition of the fructan accumulating grasses was not affected at this level, in line with recent views that fructans contribute to cellular homeostasis under stress. It is speculated that quality losses will be less prominent in grasses (fructan accumulators) than legumes under climate extreme and its combination with elevated CO2 conditions.
PMCID: PMC3966776  PMID: 24670435
16.  Above- and below-ground vertebrate herbivory may each favour a different subordinate species in an aquatic plant community 
Oecologia  2009;162(1):199-208.
At least two distinct trade-offs are thought to facilitate higher diversity in productive plant communities under herbivory. Higher investment in defence and enhanced colonization potential may both correlate with decreased competitive ability in plants. Herbivory may thus promote coexistence of plant species exhibiting divergent life history strategies. How different seasonally tied herbivore assemblages simultaneously affect plant community composition and diversity is, however, largely unknown. Two contrasting types of herbivory can be distinguished in the aquatic vegetation of the shallow lake Lauwersmeer. In summer, predominantly above-ground tissues are eaten, whereas in winter, waterfowl forage on below-ground plant propagules. In a 4-year exclosure study we experimentally separated above-ground herbivory by waterfowl and large fish in summer from below-ground herbivory by Bewick’s swans in winter. We measured the individual and combined effects of both herbivory periods on the composition of the three-species aquatic plant community. Herbivory effect sizes varied considerably from year to year. In 2 years herbivore exclusion in summer reinforced dominance of Potamogeton pectinatus with a concomitant decrease in Potamogeton pusillus, whereas no strong, unequivocal effect was observed in the other 2 years. Winter exclusion, on the other hand, had a negative effect on Zannichellia palustris, but the effect size differed considerably between years. We suggest that the colonization ability of Z. palustris may have enabled this species to be more abundant after reduction of P. pectinatus tuber densities by swans. Evenness decreased due to herbivore exclusion in summer. We conclude that seasonally tied above- and below-ground herbivory may each stimulate different components of a macrophyte community as they each favoured a different subordinate plant species.
PMCID: PMC2776151  PMID: 19756762
Aquatic macrophytes; Waterfowl; Tubers; Competition colonization trade-off; Bare patch formation
17.  Interspecific Variation in Compensatory Regrowth to Herbivory Associated with Soil Nutrients in Three Ficus (Moraceae) Saplings 
PLoS ONE  2012;7(9):e45092.
Plant compensatory regrowth is an induced process that enhances plant tolerance to herbivory. Plant behavior against herbivores differs between species and depends on resource availability, thus making general predictions related to plant compensatory regrowth difficult. To understand how soil nutrients determine the degree of compensatory regrowth for different plant species, we selected saplings of three Ficus species and treated with herbivore insects and artificial injury in both glasshouse conditions and in the field at two soil nutrient levels. Compensatory regrowth was calculated by biomass, relative growth rate and photosynthetic characteristics. A similar pattern was found in both the glasshouse and in the field for species F. hispida, where overcompensatory regrowth was triggered only under fertile conditions, and full compensatory regrowth occurred under infertile conditions. For F. auriculata, overcompensatory regrowth was stimulated only under infertile conditions and full compensatory regrowth occurred under fertile conditions. Ficus racemosa displayed full compensatory regrowth in both soil nutrient levels, but without overcompensatory regrowth following any of the treatments. The three Ficus species differed in biomass allocation following herbivore damage and artificial injury. The root/shoot ratio of F. hispida decreased largely following herbivore damage and artificial injury, while the root/shoot ratio for F. auriculata increased against damage treatments. The increase of shoot and root size for F. hispida and F. auriculata, respectively, appeared to be caused by a significant increase in photosynthesis. The results indicated that shifts in biomass allocation and increased photosynthesis are two of the mechanisms underlying compensatory regrowth. Contrasting patterns among the three Ficus species suggest that further theoretical and empirical work is necessary to better understand the complexity of the plant responses to herbivore damage.
PMCID: PMC3440311  PMID: 22984616
18.  Density-dependent aposematism in the desert locust. 
The ecological processes underlying locust swarm formation are poorly understood. Locust species exhibit phenotypic plasticity in numerous morphological, physiological and behavioural traits as their population density increases. These density-dependent changes are commonly assumed to be adaptations for migration under heterogeneous environmental conditions. Here we demonstrate that density-dependent nymphal colour change in the desert locust Schistocerca gregaria (Orthoptera: Acrididae) results in warning coloration (aposematism) when the population density increases and locusts consume native, toxic host plants. Fringe-toed lizards (Acanthodactylus dumerili (Lacertidae)) developed aversions to high-density-reared (gregarious-phase) locusts fed Hyoscyamus muticus (Solanaceae). Lizards associated both olfactory and visual cues with locust unpalatability, but only gregarious-phase coloration was an effective visual warning signal. The lizards did not associate low rearing density coloration (solitarious phase) with locust toxicity. Predator learning of density-dependent warning coloration results in a marked decrease in predation on locusts and may directly contribute to outbreaks of this notorious pest.
PMCID: PMC1690497  PMID: 10670954
19.  Earthworm and belowground competition effects on plant productivity in a plant diversity gradient 
Oecologia  2009;161(2):291-301.
Diversity is one major factor driving plant productivity in temperate grasslands. Although decomposers like earthworms are known to affect plant productivity, interacting effects of plant diversity and earthworms on plant productivity have been neglected in field studies. We investigated in the field the effects of earthworms on plant productivity, their interaction with plant species and functional group richness, and their effects on belowground plant competition. In the framework of the Jena Experiment we determined plant community productivity (in 2004 and 2007) and performance of two phytometer plant species [Centaurea jacea (herb) and Lolium perenne (grass); in 2007 and 2008] in a plant species (from one to 16) and functional group richness gradient (from one to four). We sampled earthworm subplots and subplots with decreased earthworm density and reduced aboveground competition of phytometer plants by removing the shoot biomass of the resident plant community. Earthworms increased total plant community productivity (+11%), legume shoot biomass (+35%) and shoot biomass of the phytometer C. jacea (+21%). Further, phytometer performance decreased, i.e. belowground competition increased, with increasing plant species and functional group richness. Although single plant functional groups benefited from higher earthworm numbers, the effects did not vary with plant species and functional group richness. The present study indicates that earthworms indeed affect the productivity of semi-natural grasslands irrespective of the diversity of the plant community. Belowground competition increased with increasing plant species diversity. However, belowground competition was modified by earthworms as reflected by increased productivity of the phytometer C. jacea. Moreover, particularly legumes benefited from earthworm presence. Considering also previous studies, we suggest that earthworms and legumes form a loose mutualistic relationship affecting essential ecosystem functions in temperate grasslands, in particular decomposition and plant productivity. Further, earthworms likely alter competitive interactions among plants and the structure of plant communities by beneficially affecting certain plant functional groups.
PMCID: PMC2719079  PMID: 19526252
Aboveground–belowground interactions; Diversity–productivity relationship; Grassland; Positive interactions
20.  On the origin of the desert locust Schistocerca gregaria (Forskål) (Orthoptera: Acrididae: Cyrtacanthacridinae). 
The locust genus Schistocerca (Stål) has a transatlantic disjunction, which has been controversial for more than a century. Among 50 species within the genus, only one species, the desert locust (S. gregaria Forskål), occurs in the Old World, and the rest occur in the New World. Earlier taxonomists suggested that the desert locust is a migrant from America, but this view was strongly challenged when a large swarm of the desert locust successfully crossed the Atlantic Ocean from West Africa to the West Indies in 1988. The currently accepted view, supported by this incident, is that the New World species are descendants of a gregaria-like ancestor, and the desert locust would be ancestral to the rest of the genus. However, there is surprisingly little evidence to support this view other than the 1988 swarm. I present the most comprehensive phylogenetic study that suggests that the desert locust originated from the New World, contrary to the accepted view. I also present a hypothesis about how the ancestral Schistocerca might have colonized the New World in the first place in light of phylogenetic relationships with other cyrtacanthacridine genera.
PMCID: PMC1691763  PMID: 15306312
21.  Effects of the Fungal Endophyte, Neotyphodium lolii, on Net Photosynthesis and Growth Rates of Perennial Ryegrass (Lolium perenne) are Independent of In Planta Endophyte Concentration 
Annals of Botany  2006;98(2):379-387.
• Background and Aims Neotyphodium lolii is a fungal endophyte of perennial ryegrass (Lolium perenne), improving grass fitness through production of bioactive alkaloids. Neotyphodium species can also affect growth and physiology of their host grasses (family Poaceae, sub-family Pooideae), but little is known about the mechanisms. This study examined the effect of N. lolii on net photosynthesis (Pn) and growth rates in ryegrass genotypes differing in endophyte concentration in all leaf tissues.
• Methods Plants from two ryegrass genotypes, Nui D and Nui UIV, infected with N. lolii (E+) differing approx. 2-fold in endophyte concentration or uninfected clones thereof (E−) were grown in a controlled environment. For each genotype × endophyte treatment, plant growth rates were assessed as tillering and leaf extension rates, and the light response of Pn, dark respiration and transpiration measured in leaves of young (30–45 d old) and old (>90 d old) plants with a single-chamber open infrared gas-exchange system.
• Key Results Neotyphodium lolii affected CO2-limited rates of Pn, which were approx. 17 % lower in E+ than E− plants (P < 0·05) in the young plants. Apparent photon yield and dark respiration were unaffected by the endophyte (P > 0·05). Neotyphodium lolii also decreased transpiration (P < 0·05), but only in complete darkness. There were no endophyte effects on Pn in the old plants (P > 0·05). E+ plants grew faster immediately after replanting (P < 0·05), but had approx. 10 % lower growth rates during mid-log growth (P < 0·05) than E− plants, but there was no effect on final plant biomass (P > 0·05). The endophyte effects on Pn and growth tended to be more pronounced in Nui UIV, despite having a lower endophyte concentration than Nui D.
• Conclusions Neotyphodium lolii affects CO2 fixation, but not light interception and photochemistry of Pn. The impact of N. lolii on plant growth and photosynthesis is independent of endophyte concentration in the plant, suggesting that the endophyte mycelium is not simply an energy drain to the plant. However, the endophyte effects on Pn and plant growth are strongly dependent on the plant growth phase.
PMCID: PMC2803460  PMID: 16735403
Lolium perenne; Neotyphodium lolii; perennial ryegrass; grass endophyte; net photosynthesis; tillering rate; leaf extension rate; plant fitness
22.  Plants Can Benefit from Herbivory: Stimulatory Effects of Sheep Saliva on Growth of Leymus chinensis 
PLoS ONE  2012;7(1):e29259.
Plants and herbivores can evolve beneficial interactions. Growth factors found in animal saliva are probably key factors underlying plant compensatory responses to herbivory. However, there is still a lack of knowledge about how animal saliva interacts with herbivory intensities and how saliva can mobilize photosynthate reserves in damaged plants.
Methodology/Principal Findings
The study examined compensatory responses to herbivory and sheep saliva addition for the grass species Leymus chinensis in three experiments over three years. The first two experiments were conducted in a factorial design with clipping (four levels in 2006 and five in 2007) and two saliva treatment levels. The third experiment examined the mobilization and allocation of stored carbohydrates following clipping and saliva addition treatments. Animal saliva significantly increased tiller number, number of buds, and biomass, however, there was no effect on height. Furthermore, saliva effects were dependent on herbivory intensities, associated with meristem distribution within perennial grass. Animal saliva was found to accelerate hydrolyzation of fructans and accumulation of glucose and fructose.
The results demonstrated a link between saliva and the mobilization of carbohydrates following herbivory, which is an important advance in our understanding of the evolution of plant responses to herbivory. Herbivory intensity dependence of the effects of saliva stresses the significance of optimal grazing management.
PMCID: PMC3251555  PMID: 22235277
23.  Plant Nitrogen Dynamics and Nitrogen-use Strategies under Altered Nitrogen Seasonality and Competition 
Annals of Botany  2007;100(4):821-830.
Background and Aims
Numerous studies have examined the effects of climatic factors on the distribution of C3 and C4 grasses in various regions throughout the world, but the role of seasonal fluctuations in temperature, precipitation and soil N availability in regulating growth and competition of these two functional types is still not well understood. This report is about the effects of seasonality of soil N availability and competition on plant N dynamics and N-use strategies of one C3 (Leymus chinensis) and one C4 (Chloris virgata) grass species.
Leymus chinensis and C. virgata, two grass species native to the temperate steppe in northern China, were planted in a monoculture and a mixture under three different N seasonal availabilities: an average model (AM) with N evenly distributed over the growing season; a one-peak model (OM) with more N in summer than in spring and autumn; and a two-peak model (TM) with more N in spring and autumn than in summer.
Key Results
The results showed that the altered N seasonality changed plant N concentration, with the highest value of L. chinensis under the OM treatment and C. virgata under the TM treatment, respectively. N seasonality also affected plant N content, N productivity and N-resorption efficiency and proficiency in both the C3 and C4 species. Interspecific competition influenced N-use and resorption efficiency in both the C3 and C4 species, with higher N-use and resorption efficiency in the mixture than in monoculture. The C4 grass had higher N-use efficiency than the C3 grass due to its higher N productivity, irrespective of the N treatment or competition.
The observations suggest that N-use strategies in the C3 and C4 species used in the study were closely related to seasonal dynamics of N supply and competition. N seasonality might be involved in the growth and temporal niche separation between C3 and C4 species observed in the natural ecosystems.
PMCID: PMC2749635  PMID: 17704500
Competition; C3 and C4 grasses; nitrogen seasonality; nitrogen productivity; mean residence time; temperate steppe
24.  Animal or Plant: Which Is the Better Fog Water Collector? 
PLoS ONE  2012;7(4):e34603.
Occasional fog is a critical water source utilised by plants and animals in the Namib Desert. Fog basking beetles (Onymacris unguicularis, Tenebrionidae) and Namib dune bushman grass (Stipagrostris sabulicola, Poaceae) collect water directly from the fog. While the beetles position themselves optimally for fog water collection on dune ridges, the grass occurs predominantly at the dune base where less fog water is available. Differences in the fog-water collecting abilities in animals and plants have never been addressed. Here we place beetles and grass side-by-side in a fog chamber and measure the amount of water they collect over time. Based on the accumulated amount of water over a two hour period, grass is the better fog collector. However, in contrast to the episodic cascading water run-off from the grass, the beetles obtain water in a steady flow from their elytra. This steady trickle from the beetles' elytra to their mouth could ensure that even short periods of fog basking – while exposed to predators – will yield water. Up to now there is no indication of specialised surface properties on the grass leafs, but the steady run-off from the beetles could point to specific property adaptations of their elytra surface.
PMCID: PMC3318004  PMID: 22509331
25.  Ancient trans-Atlantic flight explains locust biogeography: molecular phylogenetics of Schistocerca 
The desert locust (Schistocerca gregaria) has been an important agricultural pest at least since biblical times. Although the ecology, physiology and behaviour of this insect species have been well characterized, its biogeographical origins and evolutionary history are more obscure. Schistocerca gregaria occurs throughout Africa, the Middle East and Western Asia, but all other species in the genus Schistocerca are found in the New World. Because S. gregaria has the capacity for extreme long-distance movement associated with swarming behaviour, dispersal may have played an important role in determining current distribution patterns. Some authors have argued that S. gregaria is the product of an eastward trans-Atlantic dispersal from North America to Africa; others consider it more likely that the New World taxa are the product of westward dispersal from Africa. Here, we present a mitochondrial DNA phylogeny of Schistocerca species that supports the monophyly of New World species (including the Galapagos endemic Halmenus) relative to S. gregaria. In concert with observed patterns of molecular divergence, and in contrast to previous morphological studies, our analysis indicates a single trans-Atlantic flight from Africa to South America, followed by extensive speciation and ecological divergence in the New World.
PMCID: PMC1560218  PMID: 16618668
Schistocerca; desert locust; biogeography; molecular phylogeny; gregarious behaviour; swarming

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