Sir Arthur Tansley’s ecosystem concept

Virtual Issue Articles: Units of nature or processes across scales? The ecosystem concept at age 75 William S. Currie Effects of multiple climate change factors on the tall fescue–fungal endophyte symbiosis: infection frequency and tissue chemistry Glade B. Brosi, Rebecca L. McCulley, Lowell P. Bush, Jim A. Nelson, Aimée T. Classen, Richard J. Norby Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland Feike A. Dijkstra, Dana Blumenthal, Jack A. Morgan, Elise Pendall, Yolima Carrillo, Ronald F. Follett Heatwave 2003: high summer temperature, rather than experimental fertilization, affects vegetation and CO2 exchange in an alpine bog Renato Gerdol, Luca Bragazza, Lisa Brancaleoni Establishing a missing link: warm summers and winter snow cover promote shrub expansion into alpine tundra in Scandinavia Martin Hallinger, Michael Manthey, Martin Wilmking Recovery of ectomycorrhiza after ‘nitrogen saturation’ of a conifer forest Peter Högberg, Christian Johannisson, Stephanie Yarwood, Ingeborg Callesen, Torgny Näsholm, David D. Myrold, Mona N. Högberg Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis Chengzhang Liao, Ronghao Peng, Yiqi Luo, Xuhui Zhou, Xiaowen Wu, Changming Fang, Jiakuan Chen, Bo Li

Global patterns of ectomycorrhizal introductions Else C. Vellinga, Benjamin E. Wolfe, Anne Pringle The origin and evolution of lignin biosynthesis Jing-Ke Weng, Clint Chapple Global methane emission estimates from ultraviolet irradiation of terrestrial plant foliage A. Anthony Bloom, Julia Lee-Taylor, Sasha Madronich, David J. Messenger, Paul I. Palmer, David S. Reay, Andy R. McLeod Phytotoxicity, not nitrogen immobilization, explains plant litter inhibitory effects: evidence from solid-state 13C NMR spectroscopy Giuliano Bonanomi, Guido Incerti, Elisa Barile, Manuela Capodilupo, Vincenzo Antignani, Antonio Mingo, Virginia Lanzotti, Felice Scala, Stefano Mazzoleni Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest Gregory P. Asner, Roberta E. Martin Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis Stephan Hättenschwiler, Sylvain Coq, Sandra Barantal, Ira Tanya Handa Can we predict carbon stocks in tropical ecosystems from tree diversity? Comparing species and functional diversity in a plantation and a natural forest Maria C. Ruiz-Jaen, Catherine Potvin Genes to ecosystems: exploring the frontiers of ecology with one of the smallest biological units Adam S. Wymore, Annika T. H. Keeley, Kasey M. Yturralde, Melanie L. Schroer, Catherine R. Propper, Thomas G. Whitham

Virtual Issue Articles: Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest M. Öpik, M. Metsis, T. J. Daniell, M. Zobel, M. Moora 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases Leho Tedersoo, R. Henrik Nilsson, Kessy Abarenkov, Teele Jairus, Ave Sadam, Irja Saar, Mohammad Bahram, Eneke Bechem, George Chuyong, Urmas Kõljalg Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing Alex J. Dumbrell, Peter D. Ashton, Naveed Aziz, Gu Feng, Michaela Nelson, Calvin Dytham, Alastair H. Fitter, Thorunn Helgason Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere A. Jumpponen, K. L. Jones 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity M. Buée, M. Reich, C. Murat, E. Morin, R. H. Nilsson, S. Uroz, F. Martin

Cover image: A mosaic of natural grassland and forest ecosystems in southern temperate Patagonia, Lanín National Park, Argentina. Photo courtesy of C. Ballaré.

Celebrating the ecosystem’s three-quarter century:

Introduction to a Virtual Special Issue on Sir Arthur

Tansley´s ecosystem concept Ecosystem ecology has played a central role in our understanding of the natural world, and the importance of plants as the organisms that define the amount and flow of energy entering the ecosystem demonstrates the fundamental role of plant science in our understanding of how ecosystems function. New Phytologist has a tradition of publishing original research papers and reviews focused on the interface between plant and ecosystem science. But there is an additional reason for the collection in this Virtual Special Issue (www.newphytologist.com/virtualissues), which is the commemoration of the publication of a seminal paper by Sir Arthur Tansley (1935) (the founding Editor of New Phytologist and after whom the Tansley Reviews are named), which was fundamental in establishing the ecosystem concept in biological studies. And so, three quarters of a century on we celebrate the ecosystem concept, with a series of New Phytologist publications that span the range from the gene to the globe, from the tropics to the tundra, with an eye on the visionary influence of Sir Arthur Tansley on modern ecosystem science.

http://www.newphytologist.com/virtualissues

http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2011.03931.x/full

Tansley review

Units of nature or processes across scales? The ecosystem concept at age 75

Author for correspondence: William S. Currie Tel: +1 734 764 2550 Email:[email protected]

William S. Currie

New Phytologist (2010) 190: 21-34 doi: 10.1111/j.1469-8137.2011.03646.x

Keywords: community; complexity; ecosystem and ecosystem services; energetics; global change; nutrient cycling and primary production; social–ecological systems; theoretical ecology

Summary

The ecosystem has served as a central organizational concept in ecology for nearly a half century and continues to evolve. As a level in the biotic hierarchy, ecosystems are often viewed as ecological communities integrated with their abiotic environments. This has always been imperfect because of a mismatch of scales between communities and ecosystem processes as they are made operational for field study. Complexity theory has long been forecasted to provide a renewed foundation for ecosystem theory but has been slow to do so. Partly this has arisen from a difficulty in translating theoretical tenets into operational terms for testing in field studies. Ecosystem science has become an important applied science for studying global change and human environmental impacts. Vigorous and important directions in the study of ecosystems today include a growing focus on human-dominated landscapes and development of the concept of ecosystem services for human resource supply and well-being. Today, terrestrial ecosystems are viewed less as well-defined entities or as a level in the biotic hierarchy. Instead, ecosystem processes are being increasingly viewed as the elements in a hierarchy. These occur alongside landscape processes and socioeconomic processes, which combine to form coupled social–ecological systems across a range of scales.

http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2011.03646.x/abstract

Effects of multiple climate change factors on the tall fescue–fungal endophyte symbiosis: infection frequency and tissue chemistry

Glade B. Brosi, Rebecca L. McCulley, Lowell P. Bush, Jim A. Nelson, Aimée T. Classen, Richard J. Norby

Author for correspondence: Rebecca L. McCulley Tel: +1 859 2576388 Email: [email protected]

New Phytologist (2010) 189: 797–805 doi: 10.1111/j.1469-8137.2010.03532.x

Summary

• Climate change (altered CO2, warming, and precipitation) may affect plant–microbial interactions, such as the Lolium arundinaceum–Neotyphodium coenophialum symbiosis, to alter future ecosystem structure and function. • To assess this possibility, tall fescue tillers were collected from an existing climate manipulation experiment in a constructed old-field community in Tennessee (USA). Endophyte infection frequency (EIF) was determined, and infected (E+) and uninfected (E−) tillers were analysed for tissue chemistry. • The EIF of tall fescue was higher under elevated CO2 (91% infected) than with ambient CO2 (81%) but was not affected by warming or precipitation treatments. Within E+ tillers, elevated CO2 decreased alkaloid concentrations of both ergovaline and loline, by c. 30%; whereas warming increased loline concentrations 28% but had no effect on ergovaline. Independent of endophyte infection, elevated CO2 reduced concentrations of nitrogen, cellulose, hemicellulose, and lignin. • These results suggest that elevated CO2, more than changes in temperature or precipitation, may promote this grass–fungal symbiosis, leading to higher EIF in tall fescue in old-field communities. However, as all three climate factors are likely to change in the future, predicting the symbiotic response and resulting ecological consequences may be difficult and dependent on the specific atmospheric and climatic conditions encountered.

KEYWORDS: alkaloids;climate change; fungal endophyte; plant–microbe symbiosis; tall fescue; tissue chemistry


Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland

Feike A. Dijkstra, Dana Blumenthal, Jack A. Morgan, Elise Pendall, Yolima Carrillo, Ronald F. Follett

Author for correspondence: Feike A. Dijkstra Tel: +1 970 492 7126 Email: f [email protected]


Summary

• Simulation models indicate that the nitrogen (N) cycle plays a key role in how other ecosystem processes such as plant productivity and carbon (C) sequestration respond to elevated CO2 and warming. However, combined effects of elevated CO2 and warming on N cycling have rarely been tested in the field. • Here, we studied N cycling under ambient and elevated CO2 concentrations (600 μmol mol−1), and ambient and elevated temperature (1.5 : 3.0°C warmer day:night) in a full factorial semiarid grassland field experiment in Wyoming, USA. We measured soil inorganic N, plant and microbial N pool sizes and NO3

− uptake (using a 15N tracer). • Soil inorganic N significantly decreased under elevated CO2, probably because of increased microbial N immobilization, while soil inorganic N and plant N pool sizes significantly increased with warming, probably because of increased N supply. We observed no CO2 × warming interaction effects on soil inorganic N, N pool sizes or NO3

− uptake in plants and microbes. • Our results indicate a more closed N cycle under elevated CO2 and a more open N cycle with warming, which could affect long-term N retention, plant productivity, and C sequestration in this semiarid grassland.

KEYWORDS: 15N tracer; elevated CO2; free-air CO2 enrichment (FACE); heating; microbial nitrogen immobilization; net nitrogen mineralization; soil inorganic nitrogen; soil moisture


Heatwave 2003: high summer temperature, rather than experimental fertilization, affects vegetation and CO2 exchange in an alpine bog Renato Gerdol, Luca Bragazza, Lisa Brancaleoni

Author for correspondence: Renato Gerdol Tel: +39 (0)532 293775 Fax:+39 (0)532 208561 Email: [email protected]


Summary

• Nitrogen and phosphorus were added experimentally in a bog in the southern Alps. It was hypothesized that alleviating nutrient limitation will increase vascular plant cover. As a consequence, more carbon will be fixed through higher rates of net ecosystem CO2 exchange (NEE). • The vascular cover did increase at the expense of Sphagnum mosses. However, such vegetation changes were largely independent of the treatment and were probably triggered by an exceptional heatwave in summer 2003. • Contrary to the tested hypothesis, NEE was unaffected by the nutrient treatments but was strongly influenced by temperature and water-table depth. In particular, ecosystem respiration in the hot summer of 2003 increased dramatically, presumably owing to enhanced heterotrophic respiration in an increased oxic peat layer. • At the end of the experiment, the Sphagnum cover decreased significantly in the nitrogen-fertilized treatment at hummock microhabitats. In the long term, this will imply a proportionally greater accumulation of vascular litter, more easily decomposable than the recalcitrant Sphagnum litter. As a result, rates of carbon fixation may decrease because of stimulated respiration.

KEYWORDS: atmospheric nitrogen deposition; climate change; decomposition; gas exchange; nutrient; peat; photosynthesis; respiration


Establishing a missing link: warm summers and winter snow cover promote shrub expansion into alpine tundra in Scandinavia Martin Hallinger, Michael Manthey, Martin Wilmking

Author for correspondence: Martin Hallinger Tel: +49 3834 86 4094 Email: [email protected]


Summary

• Shrub expansion in alpine and arctic areas is a process with possibly profound implications for ecosystem functioning. The recent shrub expansion has been mainly documented by remote sensing techniques, but the drivers for this process largely remain hypotheses. • Here, we outline a dendrochronological method, adapted to shrubs, to address these hypotheses and then present a mechanism for the current shrub expansion by linking recent climate change to shrub growth performance in northern Sweden. • A pronounced increase in radial and vertical growth during recent decades along an elevational gradient from treeline to shrubline indicates an ongoing shrub expansion. Age distribution of the shrub population indicates the new colonization of shrubs at high elevations. • Shrub growth is correlated with warm summers and winter snow cover and suggests the potential for large-scale ecosystem changes if climate change continues as projected.

KEYWORDS: climate change; Juniperus nana; Scandinavia; serial sectioning; shrub expansion; shrub rings; subarctic vegetation


Recovery of ectomycorrhiza after ‘nitrogen saturation’ of a conifer forest Peter Högberg, Christian Johannisson, Stephanie Yarwood, Ingeborg Callesen, Torgny Näsholm, David D. Myrold, Mona N. Högberg

Author for correspondence: Peter Högberg Tel: +46 786 8353 Email: [email protected]


Summary

• Trees reduce their carbon (C) allocation to roots and mycorrhizal fungi in response to high nitrogen (N) additions, which should reduce the N retention capacity of forests. The time needed for recovery of mycorrhizas after termination of N loading remains unknown. • Here, we report the long-term impact of N loading and the recovery of ectomycorrhiza after high N loading on a Pinus sylvestrisforest. We analysed the N% and abundance of the stable isotope 15N in tree needles and soil, soil microbial fatty acid biomarkers and fungal DNA. • Needles in N-loaded plots became enriched in 15N, reflecting decreased N retention by mycorrhizal fungi and isotopic discrimination against 15N during loss of N. Meanwhile, needles in N-limited (control) plots became depleted in 15N, reflecting high retention of 15N by mycorrhizal fungi. N loading was terminated after 20 yr. The δ15N and N% of the needles decreased 6 yr after N loading had been terminated, and approached values in control plots after 15 yr. This decrease, and the larger contributions compared with N-loaded plots of a fungal fatty acid biomarker and ectomycorrhizal sequences, suggest recovery of ectomycorrhiza. • High N loading rapidly decreased the functional role of ectomycorrhiza in the forest N cycle, but significant recovery occurred within 6–15 yr after termination of N loading.

KEYWORDS: 15N natural abundance; boreal forest; ecosystem nitrogen retention; ectomycorrhizal fungi; nitrogen deposition; soil microbial community


Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis Chengzhang Liao, Ronghao Peng, Yiqi Luo, Xuhui Zhou, Xiaowen Wu, Changming Fang, Jiakuan Chen, Bo Li

Author for correspondence: Bo Li Tel: +86 21 65642178 Fax: +86 21 55664990 Email: [email protected]


Summary

• Plant invasion potentially alters ecosystem carbon (C) and nitrogen (N) cycles. However, the overall direction and magnitude of such alterations are poorly quantified. • Here, 94 experimental studies were synthesized, using a meta-analysis approach, to quantify the changes of 20 variables associated with C and N cycles, including their pools, fluxes, and other related parameters in response to plant invasion. • Pool variables showed significant changes in invaded ecosystems relative to native ecosystems, ranging from a 5% increase in root carbon stock to a 133% increase in shoot C stock. Flux variables, such as above-ground net primary production and litter decomposition, increased by 50–120% in invaded ecosystems, compared with native ones. Plant N concentration, soil and concentrations were 40, 30 and 17% higher in invaded than in native ecosystems, respectively. Increases in plant production and soil N availability indicate that there was positive feedback between plant invasion and C and N cycles in invaded ecosystems. • Invasions by woody andN-fixing plants tended to have greater impacts on C and N cycles than those by herbaceous and non N-fixing plants, respectively. The responses to plant invasion are not different among forests, grasslands, and wetlands. All of these changes suggest that plant invasion profoundly influences ecosystem processes.

KEYWORDS: carbon and nitrogen pools and fluxes; litter quality; meta-analysis; plant invasion; soil nitrogen availability


Global patterns of ectomycorrhizal introductions

Else C. Vellinga, Benjamin E. Wolfe, Anne Pringle

Author for correspondence: Anne Pringle Tel:+1 617 496 9707 Fax:+1 617 495 8848 Email: [email protected]


Summary

• Plants have often been moved across the globe with intact root systems. These roots are likely to have housed symbiotic ectomycorrhizal (EM) fungi and the movement of plants may have facilitated the introduction of EM fungi. • Here, we report data compiled from a newly created database of EM fungal introductions. We estimate the magnitude of EM fungal introductions around the world and examine patterns associated with these introductions. We also use the data to develop a framework for understanding the invasion biology of EM fungi. • At least 200 species of basidiomycete and ascomycete EM fungi have been moved from native ranges to novel habitats. The majority of recorded introductions are associated with Pinus or Eucalyptus plantations in the southern hemisphere. Most introduced species appear to be constrained from spreading in novel habitats and associate only with their introduced hosts. Aspects of life history, including host range, may influence the ability of EM species to establish or invade. • Human-caused introductions of EM fungi are a common and global phenomenon. The mechanisms controlling EM fungi in novel habitats and potential impacts of EM fungal introductions are almost entirely unknown.

KEYWORDS: ascomycete and basidiomycete; forestry; fungal biodiversity; fungal biogeography; fungi; host specificity; invasion or conservation biology; symbiosis


Tansley review

The origin and evolution of lignin biosynthesis

Author for correspondence: Clint Chapple Tel: +1 765 494 0494 Email: [email protected]

Jing-Ke Weng, Clint Chapple


Keywords: biofuel; cell wall; convergent evolution; diversification; land colonization; lycophyte; P450; phenylpropanoid

Summary

Lignin, a phenolic polymer derived mainly from hydroxycinnamyl alcohols, is ubiquitously present in tracheophytes. The development of lignin biosynthesis has been considered to be one of the key factors that allowed land plants to flourish in terrestrial ecosystems. Lignin provides structural rigidity for tracheophytes to stand upright, and strengthens the cell wall of their water-conducting tracheary elements to withstand the negative pressure generated during transpiration. In this review, we discuss a number of aspects regarding the origin and evolution of lignin biosynthesis during land plant evolution, including the establishment of its monomer biosynthetic scaffold, potential precursors to the lignin polymer, as well as the emergence of the polymerization machinery and regulatory system. The accumulated knowledge on the topic, as summarized here, provides us with an evolutionary view on how this complex metabolic system emerged and developed.


Global methane emission estimates from ultraviolet irradiation of terrestrial plant foliage

A. Anthony Bloom, Julia Lee-Taylor, Sasha Madronich, David J. Messenger, Paul I. Palmer, David S. Reay, Andy R. McLeod

Author for correspondence: Andy McLeod Tel: +44 131 650 5434 Email: [email protected]


Summary

• Several studies have reported in situ methane (CH4) emissions from vegetation foliage, but there remains considerable debate about its significance as a global source. Here, we report a study that evaluates the role of ultraviolet (UV) radiation-driven CH4emissions from foliar pectin as a global CH4 source. • We combine a relationship for spectrally weighted CH4 production from pectin with a global UV irradiation climatology model, satellite-derived leaf area index (LAI) and air temperature data to estimate the potential global CH4 emissions from vegetation foliage. • Our results suggest that global foliar CH4 emissions from UV-irradiated pectin could account for 0.2–1.0 Tg yr−1, of which 60% is from tropical latitudes, corresponding to < 0.2% of total CH4 sources. • Our estimate is one to two orders of magnitude lower than previous estimates of global foliar CH4 emissions. Recent studies have reported that pectin is not the only molecular source of UV-driven CH4 emissions and that other environmental stresses may also generate CH4. Consequently, further evaluation of such mechanisms of CH4 generation is needed to confirm the contribution of foliage to the global CH4 budget.

KEYWORDS: foliage; methane (CH4); pectin; ultraviolet radiation; vegetation


Phytotoxicity, not nitrogen immobilization, explains plant litter inhibitory effects: evidence from solid-state 13C NMR spectroscopy

Giuliano Bonanomi, Guido Incerti, Elisa Barile, Manuela Capodilupo, Vincenzo Antignani, Antonio Mingo, Virginia Lanzotti, Felice Scala, Stefano Mazzoleni

Author for correspondence: Giuliano Bonanomi Tel: +39 081 2539379 Email: [email protected]


Summary

• Litter decomposition provides nutrients that sustain ecosystem productivity, but litter may also hamper root proliferation. The objectives of this work were to assess the inhibitory effect of litter decomposition on seedling growth and root proliferation; to study the role of nutrient immobilization and phytotoxicity; and to characterize decomposing litter by 13C NMR spectroscopy. • A litter-bag experiment was carried out for 180 d with 16 litter types. Litter inhibitory effects were assessed by two bioassays: seed germination and root proliferation bioassays. Activated carbon (C) and nutrient solutions were used to evaluate the effects of phytotoxic factors and nutrient immobilization. • An inhibitory effect was found for all species in the early phase of decomposition, followed by a decrease over time. The addition of activated C to litter removed this inhibition. No evidence of nutrient immobilization was found in the analysis of nitrogen dynamics. NMR revealed consistent chemical changes during decomposition, with a decrease in O-alkyl and an increase in alkyl and methoxyl C. • Significant correlations were found among inhibitory effects, the litter decay rate and indices derived from NMR. The results show that it is possible to predict litter inhibitory effects across a range of litter types on the basis of their chemical composition.

KEYWORDS: 13C cross-polarization magic angle spinning NMR; activated carbon; allelopathy; carbon: nitrogen ratio; decomposition; litter quality; nutrient cycling; root proliferation


Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest Gregory P. Asner, Roberta E. Martin

Author for correspondence: Gregory P. Asner Tel: +1 650 462 1047 Email: [email protected]


Summary

• Canopy chemistry and spectroscopy offer insight into community assembly and ecosystem processes in high-diversity tropical forests, but phylogenetic and environmental factors controlling chemical traits underpinning spectral signatures remain poorly understood. • We measured 21 leaf chemical traits and spectroscopic signatures of 594 canopy individuals on high-fertility Inceptisols and low-fertility Ultisols in a lowland Amazonian forest. The spectranomics approach, which explicitly connects phylogenetic, chemical and spectral patterns in tropical canopies, provided the basis for analysis. • Intracrown and intraspecific variation in chemical traits varied from 1.4 to 36.7% (median 9.3%), depending upon the chemical constituent. Principal components analysis showed that 14 orthogonal combinations were required to explain 95% of the variation among 21 traits, indicating the high dimensionality of canopy chemical signatures among taxa. Inceptisols and lianas were associated with high leaf nutrient concentrations and low concentrations of defense compounds. Independent of soils or plant habit, an average 70% (maximum 89%) of chemical trait variation was explained by taxonomy. At least 10 traits were quantitatively linked to remotely sensed signatures, which provided highly accurate species classification. • The results suggest that taxa found on fertile soils carry chemical portfolios with a deep evolutionary history, whereas taxa found on low-fertility soils have undergone trait evolution at the species level. Spectranomics provides a new connection between remote sensing and community assembly theory in high-diversity tropical canopies.

KEYWORDS: Amazon; community assembly; leaf chemistry; leaf traits; Peru; remote sensing; spectranomics; tropical forest


Research review

Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis

Author for correspondence: S. Hättenschwiler Tel: +33 467 61 22 36 Email: [email protected]

Stephan Hättenschwiler, Sylvain Coq, Sandra Barantal, Ira Tanya Handa


Keywords: energy starvation; French Guiana; litter quality; mycorrhizas; nutrient cycling; nutrient limitation; phosphorus; soil fauna

Summary

Proper estimates of decomposition are essential for tropical forests, given their key role in the global carbon (C) cycle. However, the current paradigm for litter decomposition is insufficient to account for recent observations and may limit model predictions for highly diverse tropical ecosystems. In light of recent findings from a nutrient-poor Amazonian rainforest, we revisit the commonly held views that: litter traits are a mere legacy of live leaf traits; nitrogen (N) and lignin are the key litter traits controlling decomposition; and favourable climatic conditions result in rapid decomposition in tropical forests. Substantial interspecific variation in litter phosphorus (P) was found to be unrelated to variation in green leaves. Litter nutrients explained no variation in decomposition, which instead was controlled primarily by nonlignin litter C compounds at low concentrations with important soil fauna effects. Despite near-optimal climatic conditions, tropical litter decomposition proceeded more slowly than in a climatically less favourable temperate forest. We suggest that slow decomposition in the studied rainforest results from a syndrome of poor litter C quality beyond a simple lignin control, enforcing energy starvation of decomposers. We hypothesize that the litter trait syndrome in nutrient-poor tropical rainforests may have evolved to increase plant access to limiting nutrients via mycorrhizal associations.


Can we predict carbon stocks in tropical ecosystems from tree diversity? Comparing species and functional diversity in a plantation and a natural forest Maria C. Ruiz-Jaen, Catherine Potvin

Author for correspondence: Maria C. Ruiz-Jaen Tel: +1 514 3986726 Email: [email protected]


Summary

• Linking tree diversity to carbon storage can provide further motivation to conserve tropical forests and to design carbon-enriched plantations. Here, we examine the role of tree diversity and functional traits in determining carbon storage in a mixed-species plantation and in a natural tropical forest in Panama. • We used species richness, functional trait diversity, species dominance and functional trait dominance to predict tree carbon storage across these two forests. Then we compared the species ranking based on wood density, maximum diameter, maximum height, and leaf mass per area (LMA) between sites to reveal how these values changed between different forests. • Increased species richness, a higher proportion of nitrogen fixers and species with low LMA increased carbon storage in the mixed-species plantation, while a higher proportion of large trees and species with high LMA increased tree carbon storage in the natural forest. Furthermore, we found that tree species varied greatly in their absolute and relative values between study sites. • Different results in different forests mean that we cannot easily predict carbon storage capacity in natural forests using data from experimental plantations. Managers should be cautious when applying functional traits measured in natural populations in the design of carbon-enriched plantations.

KEYWORDS: dominance; functional trait diversity; functional traits; mixed-species plantations; Panama; species diversity; tree carbon storage; tropical forests


Tansley review

Genes to ecosystems: exploring the frontiers of ecology with one of the smallest biological units

Author for correspondence: Thomas G. Whitham Tel: +1 928 523 7215 Email: [email protected]

Adam S. Wymore, Annika T. H. Keeley, Kasey M. Yturralde, Melanie L. Schroer, Catherine R. Propper, Thomas G. Whitham


Keywords: climate change; community genetics postulates; ecosystem services; foundation species; genes-to-ecosystems; invasive species; pollution

Summary

Genes and their expression levels in individual species can structure whole communities and affect ecosystem processes. Although much has been written about community and ecosystem phenotypes with a few model systems, such as poplar and goldenrod, here we explore the potential application of a community genetics approach with systems involving invasive species, climate change and pollution. We argue that community genetics can reveal patterns and processes that otherwise might remain undetected. To further facilitate the community genetics or genes-to-ecosystem concept, we propose four community genetics postulates that allow for the conclusion of a causal relationship between the gene and its effect on the ecosystem. Although most current studies do not satisfy these criteria completely, several come close and, in so doing, begin to provide a genetic-based understanding of communities and ecosystems, as well as a sound basis for conservation and management practices.


Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest M. Öpik, M. Metsis, T. J. Daniell, M. Zobel, M. Moora

Author for correspondence: M. Öpik Tel:+372 737 6224 Email: [email protected]


Summary

• Knowledge of the diversity of arbuscular mycorrhizal fungi (AMF) in natural ecosystems is a major bottleneck in mycorrhizal ecology. Here, we aimed to apply 454 sequencing – providing a new level of descriptive power – to assess the AMF diversity in a boreonemoral forest. • 454 sequencing reads of the small subunit ribosomal RNA (SSU rRNA) gene of Glomeromycota were assigned to sequence groups by BLAST searches against a custom-made annotated sequence database. • We detected 47 AMF taxa in the roots of 10 plant species in a 10 × 10 m plot, which is almost the same as the number of plant species in the whole studied forest. There was a significant difference between AMF communities in the roots of forest specialist plant species and in the roots of habitat generalist plant species. Forest plant species hosted 22 specialist AMF taxa, and the generalist plants shared all but one AMF taxon with forest plants, including globally distributed generalist fungi. These AMF taxa that have been globally recorded only in forest ecosystems were significantly over-represented in the roots of forest plant species. • Our findings suggest that partner specificity in AM symbiosis may occur at the level of ecological groups, rather than at the species level, of both plant and fungal partners.

KEYWORDS: 454 sequencing; arbuscular mycorrhizal fungi; diversity; forest ecosystem; habitat specificity; host specificity; soil microbial community; SSU rDNA


454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases

Leho Tedersoo, R. Henrik Nilsson, Kessy Abarenkov, Teele Jairus, Ave Sadam, Irja Saar, Mohammad Bahram, Eneke Bechem, George Chuyong, Urmas Kõljalg

Author for correspondence: Leho Tedersoo Tel: +372 7376222 Email: [email protected]


Summary

• Compared with Sanger sequencing-based methods, pyrosequencing provides orders of magnitude more data on the diversity of organisms in their natural habitat, but its technological biases and relative accuracy remain poorly understood. • This study compares the performance of pyrosequencing and traditional sequencing for species’ recovery of ectomycorrhizal fungi on root tips in a Cameroonian rain forest and addresses biases related to multi-template PCR and pyrosequencing analyses. • Pyrosequencing and the traditional method yielded qualitatively similar results, but there were slight, but significant, differences that affected the taxonomic view of the fungal community. We found that most pyrosequencing singletons were artifactual and contained a strongly elevated proportion of insertions compared with natural intra- and interspecific variation. The alternative primers, DNA extraction methods and PCR replicates strongly influenced the richness and community composition as recovered by pyrosequencing. • Pyrosequencing offers a powerful alternative for the identification of ectomycorrhizal fungi in pooled root samples, but requires careful selection of molecular tools. A well-populated backbone database facilitates the detection of biological and technical artifacts. The pyrosequencing pipeline is available at http://unite.ut.ee/454pipeline.tgz.

KEYWORDS: 454 massively parallel pyrosequencing; artifacts; biodiversity; community structure; ectomycorrizal fungi; Korup National Park; PCR bias

http://unite.ut.ee/454pipeline.tgz


Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing Alex J. Dumbrell, Peter D. Ashton, Naveed Aziz, Gu Feng, Michaela Nelson, Calvin Dytham, Alastair H. Fitter, Thorunn Helgason

Author for correspondence: Alex J. Dumbrell Tel: +44 01206 873370 Email: [email protected]


Summary

• Understanding the dynamics of rhizosphere microbial communities is essential for predicting future ecosystem function, yet most research focuses on either spatial or temporal processes, ignoring combined spatio-temporal effects. • Using pyrosequencing, we examined the spatio-temporal dynamics of a functionally important community of rhizosphere microbes, the arbuscular mycorrhizal (AM) fungi. We sampled AM fungi from plant roots growing in a temperate grassland in a spatially explicit manner throughout a year. • Ordination analysis of the AM fungal assemblages revealed significant temporal changes in composition and structure. Alpha and beta diversity tended to be negatively correlated with the climate variables temperature and sunshine hours. Higher alpha diversity during colder periods probably reflects more even competitive interactions among AM fungal species under limited carbon availability, a conclusion supported by analysis of beta diversity which highlights how resource limitation may change localized spatial dynamics. • Results reveal distinct AM fungal assemblages in winter and summer at this grassland site. A seasonally changing supply of host-plant carbon, reflecting changes in temperature and sunshine hours, may be the driving force in regulating the temporal dynamics of AM fungal communities. Climate change effects on seasonal temperatures may therefore substantially alter future AM fungal community dynamics and ecosystem functioning.

KEYWORDS: 454 pyrosequencing; beta diversity; Glomeromycota; microbial diversity; seasonal dynamics; soil fungi; SSU rDNA; temporal diversity


Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere A. Jumpponen, K. L. Jones

Author for correspondence: A. Jumpponen Tel: +1 785 532 6751 Email: [email protected]


Summary

• This study targeted the fungal communities in the phyllosphere of Quercus macrocarpa and compared the fungal species richness, diversity and community composition among trees located within and outside a small urban center using recently developed 454 sequencing and DNA tagging. • The results indicate that the fungal phyllosphere communities are extremely diverse and strongly dominated by ascomycetes, with Microsphaeropsis [two Operational Taxonomic Units (OTUs); 23.6%], Alternaria (six OTUs; 16.1%), Epicoccum (one OTU; 6.0%) and Erysiphe (two OTUs; 5.9%) as the most abundant genera. • Although the sequencing effort averaged 1000 reads per tree and detected nearly 700 distinct molecular OTUs at 95% internal transcribed spacer 1 similarity, the richness of the hyperdiverse phyllosphere communities could not be reliably estimated as nearly one-half of the molecular OTUs were singletons. • The fungal communities within and outside the urban center differed in richness and diversity, which were lower within the urban development. The two land-use types contained communities that were distinct and more than 10% of the molecular OTUs differed in their frequency.

KEYWORDS: endophyte; epiphyte; foliar; fungi; Quercus; urbanization


454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity

M. Buée, M. Reich, C. Murat, E. Morin, R. H. Nilsson, S. Uroz, F. Martin

Author for correspondence: Marc Buée Tel: +33 383 39 40 72 Email: [email protected]


Summary

• Soil fungi play a major role in ecological and biogeochemical processes in forests. Little is known, however, about the structure and richness of different fungal communities and the distribution of functional ecological groups (pathogens, saprobes and symbionts). • Here, we assessed the fungal diversity in six different forest soils using tag-encoded 454 pyrosequencing of the nuclear ribosomal internal transcribed spacer-1 (ITS-1). No less than 166 350 ITS reads were obtained from all samples. In each forest soil sample (4 g), approximately 30 000 reads were recovered, corresponding to around 1000 molecular operational taxonomic units. • Most operational taxonomic units (81%) belonged to the Dikarya subkingdom (Ascomycota and Basidiomycota). Richness, abundance and taxonomic analyses identified the Agaricomycetes as the dominant fungal class. The ITS-1 sequences (73%) analysed corresponded to only 26 taxa. The most abundant operational taxonomic units showed the highest sequence similarity to Ceratobasidium sp., Cryptococcus podzolicus, Lactarius sp. and Scleroderma sp. • This study validates the effectiveness of high-throughput 454 sequencing technology for the survey of soil fungal diversity. The large proportion of unidentified sequences, however, calls for curated sequence databases. The use of pyrosequencing on soil samples will accelerate the study of the spatiotemporal dynamics of fungal communities in forest ecosystems.

KEYWORDS: 454 pyrosequencing; community structure; ectomycorrhizal fungi; environmental samples; fungal diversity; nuclear ribosomal internal transcribed spacers


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Sir Arthur Tansley’s ecosystem concept

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