Joe Quirk

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 Earths CO2 and climate history.

A glacier respires: Quantifying the distribution and respiration CO2 flux of cryoconite across an entire Arctic supraglacial ecosystem

Hodson, A., Anesio, A. M., Ng, F., Watson, R., Quirk, J., Irvine-fynn, T., Dye, A., Clark, C., McCloy, P., Kohler, J., Sattler, B. (2007). A glacier respires: Quantifying the distribution and respiration Co2 flux of cryoconite across an entire Arctic supraglacial ecosystem. Journal of Geophysical Research, 112 (G4).

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering

Forested ecosystems diversified more than 350 Ma to become major engines of continental silicate weathering, regulating the Earths atmospheric carbon dioxide concentration by driving calcium export into ocean carbonates. Our field experiments with mature trees demonstrate intensification of this weathering engine as tree lineages diversified in concert with their symbiotic mycorrhizal fungi. Preferential hyphal colonization of the calcium silicate-bearing rock, basalt, progressively increased with advancement from arbuscular mycorrhizal (AM) to later, independently evolved ectomycorrhizal (EM) fungi, and from gymnosperm to angiosperm hosts with both fungal groups. This led to ‘trenching’ of silicate mineral surfaces by AM and EM fungi, with EM gymnosperms and angiosperms releasing calcium from basalt at twice the rate of AM gymnosperms. Our findings indicate mycorrhiza-driven weathering may have originated hundreds of millions of years earlier than previously recognized and subsequently intensified with the evolution of trees and mycorrhizas to affect the Earths long-term CO2 and climate history.

Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation

UNLABELLED PREMISE OF THE STUDY Climate-induced forest retreat has profound ecological and biogeochemical impacts, but the physiological mechanisms underlying past tree mortality are poorly understood, limiting prediction of vegetation shifts with climate variation. Climate, drought, fire, and grazing represent agents of tree mortality during the late Cenozoic, but the interaction between drought and declining atmospheric carbon dioxide ([CO2]a) from high to near-starvation levels ∼34 million years (Ma) ago has been overlooked. Here, this interaction frames our investigation of sapling mortality through the interdependence of hydraulic function, carbon limitation, and defense metabolism. • METHODS We recreated a changing Cenozoic [CO2]a regime by growing Sequoia sempervirens trees within climate-controlled growth chambers at 1500, 500, or 200 ppm [CO2]a, capturing the decline toward minimum concentrations from 34 Ma. After 7 months, we imposed drought conditions and measured key physiological components linking carbon utilization, hydraulics, and defense metabolism as hypothesized interdependent mechanisms of tree mortality. • KEY RESULTS Catastrophic failure of hydraulic conductivity, carbohydrate starvation, and tree death occurred at 200 ppm, but not 500 or 1500 ppm [CO2]a. Furthermore, declining [CO2]a reduced investment in carbon-rich foliar defense compounds that would diminish resistance to biotic attack, likely exacerbating mortality. • CONCLUSIONS Low-[CO2]a-driven tree mortality under drought is consistent with Pleistocene pollen records charting repeated Californian Sequoia forest contraction during glacial periods (180-200 ppm [CO2]a) and may even have contributed to forest retreat as grasslands expanded on multiple continents under low [CO2]a over the past 10 Ma. In this way, geologic intervals of low [CO2]a coupled with drought could impose a demographic bottleneck in tree recruitment, driving vegetation shifts through forest mortality.

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.

Ectomycorrhizal fungi and past high CO2 atmospheres enhance mineral weathering through increased below-ground carbon-energy fluxes

Field studies indicate an intensification of mineral weathering with advancement from arbuscular mycorrhizal (AM) to later-evolving ectomycorrhizal (EM) fungal partners of gymnosperm and angiosperm trees. We test the hypothesis that this intensification is driven by increasing photosynthate carbon allocation to mycorrhizal mycelial networks using 14CO2-tracer experiments with representative tree–fungus mycorrhizal partnerships. Trees were grown in either a simulated past CO2 atmosphere (1500 ppm)—under which EM fungi evolved—or near-current CO2 (450 ppm). We report a direct linkage between photosynthate-energy fluxes from trees to EM and AM mycorrhizal mycelium and rates of calcium silicate weathering. Calcium dissolution rates halved for both AM and EM trees as CO2 fell from 1500 to 450 ppm, but silicate weathering by AM trees at high CO2 approached rates for EM trees at near-current CO2. Our findings provide mechanistic insights into the involvement of EM-associating forest trees in strengthening biological feedbacks on the geochemical carbon cycle that regulate atmospheric CO2 over millions of years.

A dynamic hydro-mechanical and biochemical model of stomatal conductance for C4 photosynthesis

A mechanistic dynamic model predicts CO2 uptake, water release by C4 leaves, simulated stomatal responses and water use optimality in response to light fluctuations over 1 day. C4 plants are major grain (maize [Zea mays] and sorghum [Sorghum bicolor]), sugar (sugarcane [Saccharum officinarum]), and biofuel (Miscanthus spp.) producers and contribute ∼20% to global productivity. Plants lose water through stomatal pores in order to acquire CO2 (assimilation [A]) and control their carbon-for-water balance by regulating stomatal conductance (gS). The ability to mechanistically predict gS and A in response to atmospheric CO2, water availability, and time is critical for simulating stomatal control of plant-atmospheric carbon and water exchange under current, past, or future environmental conditions. Yet, dynamic mechanistic models for gS are lacking, especially for C4 photosynthesis. We developed and coupled a hydromechanical model of stomatal behavior with a biochemical model of C4 photosynthesis, calibrated using gas-exchange measurements in maize, and extended the coupled model with time-explicit functions to predict dynamic responses. We demonstrated the wider applicability of the model with three additional C4 grass species in which interspecific differences in stomatal behavior could be accounted for by fitting a single parameter. The model accurately predicted steady-state responses of gS to light, atmospheric CO2 and oxygen, soil drying, and evaporative demand as well as dynamic responses to light intensity. Further analyses suggest that the effect of variable leaf hydraulic conductance is negligible. Based on the model, we derived a set of equations suitable for incorporation in land surface models. Our model illuminates the processes underpinning stomatal control in C4 plants and suggests that the hydraulic benefits associated with fast stomatal responses of C4 grasses may have supported the evolution of C4 photosynthesis.

Stomatal and non-stomatal limitations in savanna trees and C4 grasses grown at low, ambient and high atmospheric CO2

By the end of the century, atmospheric CO2 concentration ([CO2]a) could reach 800 ppm, having risen from ∼200 ppm ∼24 Myr ago. Carbon dioxide enters plant leaves through stomata that limit CO2 diffusion and assimilation, imposing stomatal limitation (LS). Other factors limiting assimilation are collectively called non-stomatal limitations (LNS). C4 photosynthesis concentrates CO2 around Rubisco, typically reducing LS. C4-dominated savanna grasslands expanded under low [CO2]a and are metastable ecosystems where the response of trees and C4 grasses to rising [CO2]a will determine shifting vegetation patterns. How LS and LNS differ between savanna trees and C4 grasses under different [CO2]a will govern the responses of CO2 fixation and plant cover to [CO2]a - but quantitative comparisons are lacking. We measured assimilation, within soil wetting-drying cycles, of three C3 trees and three C4 grasses grown at 200, 400 or 800 ppm [CO2]a. Using assimilation-response curves, we resolved LS and LNS and show that rising [CO2]a alleviated LS, particularly for the C3 trees, but LNS was unaffected and remained substantially higher for the grasses across all [CO2]a treatments. Because LNS incurs higher metabolic costs and recovery compared with LS, our findings indicate that C4 grasses will be comparatively disadvantaged as [CO2]a rises.