Nitrogen-based symbioses,phosphorus availability,and accounting for a modern world more productive than the Paleozoic

Evolution of high-productivity angiosperms has been regarded as a driver of Mesozoic ecosystem restructuring. However, terrestrial productivity is limited by availability of rock-derived nutrients such as phosphorus for which permanent increases in weathering would violate mass balance requirements of the long-term carbon cycle. The potential reality of productivity increases sustained since the Mesozoic is supported here with documentation of a dramatic increase in the evolution of nitrogen-fixing or nitrogen-scavenging symbioses, including more than 100 lineages of ectomycorrhizal and lichen-forming fungi and plants with specialized microbial associations. Given this evidence of broadly increased nitrogen availability, we explore via carbon cycle modeling how enhanced phosphorus availability might be sustained without violating mass balance requirements. Volcanism is the dominant carbon input, dictating peaks in weathering outputs up to twice modern values. However, times of weathering rate suppression may be more important for setting system behavior, and the late Paleozoic was the only extended period over which rates are expected to have remained lower than modern. Modeling results are consistent with terrestrial organic matter deposition that accompanied Paleozoic vascular plant evolution having suppressed weathering fluxes by providing an alternative sink of atmospheric CO₂. Suppression would have then been progressively lifted as the crustal reservoir's holding capacity for terrestrial organic matter saturated back toward steady state with deposition of new organic matter balanced by erosion of older organic deposits. Although not an absolute increase, weathering fluxes returning to early Paleozoic conditions would represent a novel regime for the complex land biota that evolved in the interim. Volcanism-based peaks in Mesozoic weathering far surpass the modern rates that sustain a complex diversity of nitrogen-based symbioses; only in the late Paleozoic might these ecologies have been suppressed by significantly lower rates. Thus, angiosperms are posited to be another effect rather than proximal cause of Mesozoic upheaval.     

Volcanic perturbations of the marine environment in South China preceding the latest Permian mass extinction and their biotic effects

The Dongpan section in southern Guangxi Province records the influence of local volcanic activity on marine sedimentation at intermediate water depths (~200-500 m) in the Nanpanjiang Basin (South China) during the late Permian crisis. We analyzed ~100 samples over a 12-m-thick interval, generating palynological, paleobiological, and geochemical datasets to investigate the nature and causes of environmental changes. The section records at least two major volcanic episodes that culminated in deposition of approximately 25- to 35-cm-thick ash layers (bentonites) and that had profound effects on conditions in both the Dongpan marine environment and adjacent land areas. Intensification of eruptive activity during each volcanic cycle resulted in a shift toward conifer forests, increased wildfire intensity, and elevated subaerial weathering fluxes. The resulting increase in nutrient fluxes stimulated marine productivity in the short term but led to a negative feedback on productivity in the longer term as the OMZ of the Nanpanjiang Basin expanded, putting both phytoplankton and zooplankton communities under severe stress. Radiolarians exhibit large declines in diversity and abundance well before the global mass extinction horizon, demonstrating the diachroneity of the marine biotic crisis. The latest Permian crisis, which was probably triggered by the Siberian Traps flood basalts, intensified the destructive effects of the earlier local eruptions on terrestrial and marine ecosystems of the South China craton.     

Did the evolution of the phytoplankton fuel the diversification of the marine biosphere?

We discuss the possible links between the fossil record of marine biodiversity, nutrient availability and primary productivity. The parallelism of the fossil records of marine phytoplankton and faunal biodiversity implicates the quantity (primary productivity) and quality (stoichiometry) of phytoplankton as being critical to the diversification of the marine biosphere through the Phanerozoic. The relatively subdued marine biodiversity of the Palaeozoic corresponds to a time of relatively low macronutrient availability and poor food quality of the phytoplankton as opposed to the diversification of the Modern Fauna through the Mesozoic–Cenozoic. Increasing nutrient runoff to the oceans through the Phanerozoic resulted from orogeny, the emplacement of Large Igneous Provinces (LIPs), the evolution of deep-rooting forests and the appearance of more easily decomposable terrestrial organic matter that enhanced weathering. Positive feedback by bioturbation of an expanding benthos played a critical role in evolving biogeochemical cycles by linking the oxidation of dead organic matter and the recycling of nutrients back to the water column where they could be re-utilized. We assess our conclusions against a recently published biogeochemical model for geological time-scales. Major peaks of marine diversity often occur near rising or peak fluxes of silica, phosphorus and dissolved reactive oceanic phosphorus; either major or minor ⁸⁷Sr/⁸⁶Sr peaks; and frequently in the vicinity of major (Circum-Atlantic Magmatic Province) and minor volcanic events, some of which are associated with Oceanic Anoxic Events. These processes appear to be scale-dependent in that they lie on a continuum between biodiversification on macroevolutionary scales of geological time and mass extinction.     

The effects of natural and anthropogenic environmental changes on ecosystem processes at the catchment scale

The catchment is the smallest natural unit of the landscape that combines linked terrestrial and aquatic ecosystems. The fluxes of water and elements through the catchment link the various components of the system; biotic and abiotic, terrestrial and aquatic, plants and soils, atmosphere and vegetation, soils and waters. A large amount of empirical evidence now demonstrates that the impacts of natural and anthropogenic changes on the various components of catchment ecosystems are tightly connected.     

Changes in terrestrial biota before the Permian-Triassic ecological crisis

The period around the Permian-Triassic boundary was marked by one of the most important and interesting events in the evolution of life. The diversity of both marine and continental biotas decreased. The changes were global and led to the establishment of the new Mesozoic World. Transformations of the organic world constituted a single process with changes in the inorganic components of the biosphere. The preceding glacial period had ended and the “cool,” zonal, and markedly seasonal climate was replaced by a “warm,” “equable,” virtually non-seasonal and azonal climate. The new climatic organization remained on Earth for more than two hundred million years. The biotic crisis was global: it involved the sea, the land, and inland waters. The changes on land began earlier and more superficial. The principal events were in the Kazanian and Vyatkian, before the end of the Permian. The crisis was caused to a greater extent by biospheric processes than by momentary external influences, the latter at most triggering the crisis.     

Constraining the role of early land plants in Palaeozoic weathering and global cooling

How the colonization of terrestrial environments by early land plants over 400 Ma influenced rock weathering, the biogeochemical cycling of carbon and phosphorus, and climate in the Palaeozoic is uncertain. Here we show experimentally that mineral weathering by liverworts—an extant lineage of early land plants—partnering arbuscular mycorrhizal (AM) fungi, like those in 410 Ma-old early land plant fossils, amplified calcium weathering from basalt grains threefold to sevenfold, relative to plant-free controls. Phosphate weathering by mycorrhizal liverworts was amplified 9–13-fold over plant-free controls, compared with fivefold to sevenfold amplification by liverworts lacking fungal symbionts. Etching and trenching of phyllosilicate minerals increased with AM fungal network size and atmospheric CO₂ concentration. Integration of grain-scale weathering rates over the depths of liverwort rhizoids and mycelia (0.1 m), or tree roots and mycelia (0.75 m), indicate early land plants with shallow anchorage systems were probably at least 10-fold less effective at enhancing the total weathering flux than later-evolving trees. This work challenges the suggestion that early land plants significantly enhanced total weathering and land-to-ocean fluxes of calcium and phosphorus, which have been proposed as a trigger for transient dramatic atmospheric CO₂ sequestration and glaciations in the Ordovician.     

Biogenic Enhancement of Weathering and the Stability of the Ecosphere

A dynamic model of the global carbon cycle is used to determine the influence of biotic amplification of weathering on the overall stability of the biosphere. It takes into account the most important processes for the long-term evolution of the Earth. The model is solved under the condition of slow changing luminosity, volcanic activity, and continental area. We find that for large enough amplification factors the system has two stable states, the abiotic and biotic solution. Furthermore, this leads to an extension of the life span of the biosphere by 0.7 Gyr compared to previous studies underestimating the effect of biogenic enhancement of weathering. It can be shown that the biosphere is resilient to random perturbation of the global carbon cycle for the next 0.5-1.0 Gyr.     

Ecological effects of El Niño in terrestrial ecosystems of western South America

I make a summary review of how El Niño/Southern Oscillation (ENSO) determines peculiar atmospheric and oceanographic conditions in western South America, thus affecting precipitation patterns in adjacent land masses, with cascading effects on marine and terrestrial plants, on sea and land birds, and on marine and terrestrial mammals. With regard to terrestrial ecosystems, I discuss the following biotic responses to El Niño-driven precipitation: 1) aboveground vegetation flushes immediately among herbs but not among shrubs. 2) The seed bank is quickly replenished of ephemeral seeds, but perennial seeds recover one year later. 3) Small rodents Irrupt within months of El Niño arrival, but larger ones take a full year to increase. 4) Predator numbers lag one year behind their mammal prey, with smaller predators responding more quickly. Considering these responses, I offer a simplified model of El Niño-driven bottom-up control in terrestrial ecosystems of western South America. Apart from the direct links already described, there is a weak feedback loop between the plant compartments (vegetation and seeds) and their herbivores: primary productivy is the driving force, and is little affected by herbivory. Another weak feedbaek loop links herbivores and their predators: the latter seem to just "surf" over prey levels, skimming excess prey.     

Rise of the earliest tetrapods: an early Devonian origin from marine environment

Tetrapod fossil tracks are known from the Middle Devonian (Eifelian at ca. 397 million years ago--MYA), and their earliest bony remains from the Upper Devonian (Frasnian at 375-385 MYA). Tetrapods are now generally considered to have colonized land during the Carboniferous (i.e., after 359 MYA), which is considered to be one of the major events in the history of life. Our analysis on tetrapod evolution was performed using molecular data consisting of 13 proteins from 17 species and different paleontological data. The analysis on the molecular data was performed with the program TreeSAAP and the results were analyzed to see if they had implications on the paleontological data collected. The results have shown that tetrapods evolved from marine environments during times of higher oxygen levels. The change in environmental conditions played a major role in their evolution. According to our analysis this evolution occurred at about 397-416 MYA during the Early Devonian unlike previously thought. This idea is supported by various environmental factors such as sea levels and oxygen rate, and biotic factors such as biodiversity of arthropods and coral reefs. The molecular data also strongly supports lungfish as tetrapod's closest living relative.     

A comparison of the colonization of the planktic realm and the land

Metazoans evolved in the sea and quickly invaded benthic niches. It was from these niches that other large ecosystems were colonized through the later Precambrian and the Phanerozoic. Entering these new environments, the colonists encountered new sets of macroevolutionary controls. Narratives of each colonization are important for historical ecology, while comparison of different events can throw light on these underlying controls. Recent narrative work on the evolution of plankton has suggested that this series of events was unique in respect of its duration and method. Animals have been migrating into the plankton since the Proterozoic, and all the main planktic groups have a benthic origin. Migration was usually by single species acting independently of their native community. A comparison with the other major Phanerozoic colonization, that of the land, highlights these unusual features. Colonization of the land began in the Ordovician and seems to have occurred sporadically. Several of the major groups of terrestrial animals originated on land. The invasion of land is usually related to the evolution of land plants and is perhaps best regarded as migration at the level of the community. The major differences between the two colonizations may be attributable to the dominant control of the environment over plankton versus that of biotic interaction over land animals.     

Transpiration and assimilation of early Devonian land plants with axially symmetric telomes-simulations on the tissue level

Early terrestrial ancestors of the land flora are characterized by a simple, axially symmetric habit and evolved in an atmosphere with much higher CO(2)concentrations than today. In order to gain information about the ecophysiological interrelationships of these plants, a model dealing with their gaseous exchange, which is basic to transpiration and photosynthesis, is introduced. The model is based on gas diffusion inside a porous medium and on a well-established photosynthesis model and allows for the simulation of the local gas fluxes through the various tissue layers of a plant axis. Necessary parameters consist of kinetical properties of the assimilation process and other physiological parameters (which have to be taken from extant plants), as well as physical constants and anatomical parameters which can be obtained from well-preserved fossil specimens. The model system is applied to an Early Devonian land plant, Aglaophyton major. The results demonstrate that, under an Early Devonian CO(2)concentration, A. major shows an extremely low transpiration rate and a low, but probably sufficiently high assimilation rate. Variation of the atmospheric CO(2)concentration shows that the assimilation is fully saturated even if the CO(2)content is decreased to about one-third of the initial value. This result indicates that A. major was probably able to exist under a wide range of atmospheric CO(2)concentrations. Further applications of this model system to ecophysiological studies of early land plant evolution are discussed.     

Morphological evolution in land plants: new designs with old genes

The colonization and radiation of multicellular plants on land that started over 470 Ma was one of the defining events in the history of this planet. For the first time, large amounts of primary productivity occurred on the continental surface, paving the way for the evolution of complex terrestrial ecosystems and altering global biogeochemical cycles; increased weathering of continental silicates and organic carbon burial resulted in a 90 per cent reduction in atmospheric carbon dioxide levels. The evolution of plants on land was itself characterized by a series of radical transformations of their body plans that included the formation of three-dimensional tissues, de novo evolution of a multicellular diploid sporophyte generation, evolution of multicellular meristems, and the development of specialized tissues and organ systems such as vasculature, roots, leaves, seeds and flowers. In this review, we discuss the evolution of the genes and developmental mechanisms that drove the explosion of plant morphologies on land. Recent studies indicate that many of the gene families which control development in extant plants were already present in the earliest land plants. This suggests that the evolution of novel morphologies was to a large degree driven by the reassembly and reuse of pre-existing genetic mechanisms.     

A cross-ecosystem comparison of the strength of trophic cascades

Although trophic cascades (indirect effects of predators on plants via herbivores) occur in a wide variety of food webs, the magnitudes of their effects are often quite variable. We compared the responses of herbivore and plant communities to predator manipulations in 102 field experiments in six different ecosystems: lentic (lake and pond), marine, and stream benthos, lentic and marine plankton, and terrestrial (grasslands and agricultural fields). Predator effects varied considerably among systems and were strongest in lentic and marine benthos and weakest in marine plankton and terrestrial food webs. Predator effects on herbivores were generally larger and more variable than on plants, suggesting that cascades often become attenuated at the plant–herbivore interface. Top‐down control of plant biomass was stronger in water than on land; however, the differences among the five aquatic food webs were as great as those between wet and dry systems.     

Origin and evolution of green plants in the light of key evolutionary events

Green plants (Viridiplantae) are ancient photosynthetic organisms that thrive both in aquatic and terrestrial ecosystems, greatly contributing to the changes in global climates and ecosystems. Significant progress has been made toward understanding the origin and evolution of green plants, and plant biologists have arrived at the consensus that green plants first originated in marine deep-water environments and later colonized fresh water and dry land. The origin of green plants, colonization of land by plants and rapid radiation of angiosperms are three key evolutionary events during the long history of green plants. However, the comprehensive understanding of evolutionary features and molecular innovations that enabled green plants to adapt to complex and changeable environments are still limited. Here, we review current knowledge of phylogenetic relationships and divergence times of green plants, and discuss key morphological innovations and distinct drivers in the evolution of green plants. Ultimately, we highlight fundamental questions to advance our understanding of the phenotypic novelty, environmental adaptation, and domestication of green plants.     

Leaf evolution: gases, genes and geochemistry

AIMS: This Botanical Briefing reviews how the integration of palaeontology, geochemistry and developmental biology is providing a new mechanistic framework for interpreting the 40- to 50-million-year gap between the origination of vascular land plants and the advent of large (megaphyll) leaves, a long-standing puzzle in evolutionary biology. SCOPE: Molecular genetics indicates that the developmental mechanisms required for leaf production in vascular plants were recruited long before the advent of large megaphylls. According to theory, this morphogenetic potential was only realized as the concentration of atmospheric CO2 declined during the late Palaeozoic. Surprisingly, plants effectively policed their own evolution since the decrease in CO2 was brought about as terrestrial floras evolved accelerating the rate of silicate rock weathering and enhancing sedimentary organic carbon burial, both of which are long-term sinks for CO2. CONCLUSIONS: The recognition that plant evolution responds to and influences CO(2) over millions of years reveals the existence of an intricate web of vegetation feedbacks regulating the long-term carbon cycle. Several of these feedbacks destabilized CO2 and climate during the late Palaeozoic but appear to have quickened the pace of terrestrial plant and animal evolution at that time.     

The role of land plants,phosphorus weathering and fire in the rise and regulation of atmospheric oxygen

The evolution of vascular plants and their spread across the land surface, beginning ～420 Ma, progressively increased the rate of weathering of phosphorus from rocks. This phosphorus supply promoted terrestrial and marine productivity and the burial of organic carbon, which has been the major source of O₂ over geological timescales. Hence, it is predicted that the rise of plants led to an increase in the O₂ content of the atmosphere from ～12 vol %, 570–400 Ma to its present level of ～21 vol % by ～340 Ma. Previous modelling studies suggest that O₂ then rose to ～35 vol % ～300 Ma. Such high concentrations are difficult to reconcile with the known persistence of forests, because rising O₂ increases the frequency and intensity of vegetation fires, tending to decrease biomass and cause ecological shifts toward faster regenerating ecosystems. Rising O₂ also directly inhibits C3 photosynthetic carbon assimilation and increases the production of toxic reactive oxygen species in cells. These effects suppress plant‐induced phosphorus weathering and hence organic carbon burial, providing a sensitive negative feedback on O₂. A revised model predicts that this mechanism could have regulated atmospheric O₂ within the range 15–25 vol % for the last 350 million years.     

Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm

The dramatic decline in atmospheric CO₂ evidenced by proxy data during the Devonian (416.0–359.2 Ma) and the gradual decline from the Cretaceous (145.5–65.5 Ma) onwards have been linked to the spread of deeply rooted trees and the rise of angiosperms, respectively. But this paradigm overlooks the coevolution of roots with the major groups of symbiotic fungal partners that have dominated terrestrial ecosystems throughout Earth history. The colonization of land by plants was coincident with the rise of arbuscular mycorrhizal fungi (AMF), while the Cenozoic (c. 65.5–0 Ma) witnessed the rise of ectomycorrhizal fungi (EMF) that associate with both gymnosperm and angiosperm tree roots. Here, we critically review evidence for the influence of AMF and EMF on mineral weathering processes. We show that the key weathering processes underpinning the current paradigm and ascribed to plants are actually driven by the combined activities of roots and mycorrhizal fungi. Fuelled by substantial amounts of recent photosynthate transported from shoots to roots, these fungi form extensive mycelial networks which extend into soil actively foraging for nutrients by altering minerals through the acidification of the immediate root environment. EMF aggressively weather minerals through the additional mechanism of releasing low molecular weight organic chelators. Rates of biotic weathering might therefore be more usefully conceptualized as being fundamentally controlled by the biomass, surface area of contact, and capacity of roots and their mycorrhizal fungal partners to interact physically and chemically with minerals. All of these activities are ultimately controlled by rates of carbon‐energy supply from photosynthetic organisms. The weathering functions in leading carbon cycle models require experiments and field studies of evolutionary grades of plants with appropriate mycorrhizal associations. Representation of the coevolution of roots and fungi in geochemical carbon cycle models is required to further our understanding of the role of the biota in Earth's CO₂ and climate history.     

Twelve testable hypotheses on the geobiology of weathering

Critical Zone (CZ) research investigates the chemical, physical, and biological processes that modulate the Earth's surface. Here, we advance 12 hypotheses that must be tested to improve our understanding of the CZ: (1) Solar-to-chemical conversion of energy by plants regulates flows of carbon, water, and nutrients through plant-microbe soil networks, thereby controlling the location and extent of biological weathering. (2) Biological stoichiometry drives changes in mineral stoichiometry and distribution through weathering. (3) On landscapes experiencing little erosion, biology drives weathering during initial succession, whereas weathering drives biology over the long term. (4) In eroding landscapes, weathering-front advance at depth is coupled to surface denudation via biotic processes. (5) Biology shapes the topography of the Critical Zone. (6) The impact of climate forcing on denudation rates in natural systems can be predicted from models incorporating biogeochemical reaction rates and geomorphological transport laws. (7) Rising global temperatures will increase carbon losses from the Critical Zone. (8) Rising atmospheric P(CO2) will increase rates and extents of mineral weathering in soils. (9) Riverine solute fluxes will respond to changes in climate primarily due to changes in water fluxes and secondarily through changes in biologically mediated weathering. (10) Land use change will impact Critical Zone processes and exports more than climate change. (11) In many severely altered settings, restoration of hydrological processes is possible in decades or less, whereas restoration of biodiversity and biogeochemical processes requires longer timescales. (12) Biogeochemical properties impart thresholds or tipping points beyond which rapid and irreversible losses of ecosystem health, function, and services can occur.     

Investigating Devonian trees as geo‐engineers of past climates: linking palaeosols to palaeobotany and experimental geobiology

We present the rationale for a cross‐disciplinary investigation addressing the ‘Devonian plant hypothesis’ which proposes that the evolutionary appearance of trees with deep, complex rooting systems represents one of the major biotic feedbacks on geochemical carbon cycling during the Phanerozoic. According to this hypothesis, trees have dramatically enhanced mineral weathering driving an increased flux of Ca²⁺ to the oceans and, ultimately, a 90% decline in atmospheric CO₂ levels through the Palaeozoic. Furthermore, experimental studies indicate a key role for arbuscular mycorrhizal fungi in soil–plant processes and especially in unlocking the limiting nutrient phosphorus in soil via Ca‐phosphate dissolution mineral weathering. This suggests co‐evolution of roots and symbiotic fungi since the Early Devonian could well have triggered positive feedbacks on weathering rates whereby root–fungal P release supports higher biomass forested ecosystems. Long‐standing areas of uncertainty in this paradigm include the following: (1) limited fossil record documenting the origin and timeline of the evolution of tree‐sized plants through the Devonian; and (2) the effects of the evolutionary advance of trees and their in situ rooting structures on palaeosol geochemistry. We are addressing these issues by integrating palaeobotanical studies with geochemical and mineralogical analyses of palaeosol sequences at selected sites across eastern North America with a particular focus on drill cores from Middle Devonian forests in Greene County, New York State.     

Anthropogenic transformation of the biomes, 1700 to 2000

Aim To map and characterize anthropogenic transformation of the terrestrial biosphere before and during the Industrial Revolution, from 1700 to 2000. Location Global. Methods Anthropogenic biomes (anthromes) were mapped for 1700, 1800, 1900 and 2000 using a rule‐based anthrome classification model applied to gridded global data for human population density and land use. Anthropogenic transformation of terrestrial biomes was then characterized by map comparisons at century intervals. Results In 1700, nearly half of the terrestrial biosphere was wild, without human settlements or substantial land use. Most of the remainder was in a seminatural state (45%) having only minor use for agriculture and settlements. By 2000, the opposite was true, with the majority of the biosphere in agricultural and settled anthromes, less than 20% seminatural and only a quarter left wild. Anthropogenic transformation of the biosphere during the Industrial Revolution resulted about equally from land‐use expansion into wildlands and intensification of land use within seminatural anthromes. Transformation pathways differed strongly between biomes and regions, with some remaining mostly wild but with the majority almost completely transformed into rangelands, croplands and villages. In the process of transforming almost 39% of earth's total ice‐free surface into agricultural land and settlements, an additional 37% of global land without such use has become embedded within agricultural and settled anthromes. Main conclusions Between 1700 and 2000, the terrestrial biosphere made the critical transition from mostly wild to mostly anthropogenic, passing the 50% mark early in the 20th century. At present, and ever more in the future, the form and process of terrestrial ecosystems in most biomes will be predominantly anthropogenic, the product of land use and other direct human interactions with ecosystems. Ecological research and conservation efforts in all but a few biomes would benefit from a primary focus on the novel remnant, recovering and managed ecosystems embedded within used lands.