Dole Effect Research Articles

Determination of respiration and photosynthesis fractionation factors for atmospheric dioxygen inferred from a vegetation–soil–atmosphere analogue of the terrestrial biosphere in closed chambers

Abstract. The isotopic composition of dioxygen in the atmosphere is a global tracer which depends on the biosphere flux of dioxygen toward and from the atmosphere (photosynthesis and respiration) as well as exchanges with the stratosphere. When measured in fossil air trapped in ice cores, the relative concentration of 16O, 17O, and 18O of O2 can be used for several applications such as ice core dating and past global productivity reconstruction. However, there are still uncertainties about the accuracy of these tracers as they depend on the integrated isotopic discrimination of different biological processes of dioxygen production and uptake, for which we currently have very few independent estimates. Here we determined the respiration and photosynthesis fractionation factors for atmospheric dioxygen from experiments carried out in a replicated vegetation–soil–atmosphere analogue of the terrestrial biosphere in closed chambers with growing Festuca arundinacea. The values for 18O discrimination during soil respiration and dark respiration in leaves are equal to -12.3±1.7 ‰ and -19.1±2.4 ‰, respectively. In these closed biological chambers, we also found a value attributed to terrestrial photosynthetic isotopic discrimination equal to +3.7±1.3 ‰. This last estimate suggests that the contribution of terrestrial productivity in the Dole effect may have been underestimated in previous studies.

Dole effect as a measurement of the low-latitude hydrological cycle over the past 800 ka.

The quest of geological proxies to evaluate low-latitude hydrological changes at a planetary scale remains an ongoing issue. The Dole effect is such a potential proxy owing to its global character. We propose a new approach to recalculate the fluctuation of the Dole effect (∆DE*) over the past 800 thousand years (ka). The ∆DE* calculated this way is dominated by precession cycles alone, with lesser variance in the obliquity bands and almost no variance in the eccentricity bands. Moreover, the ∆DE* is notably correlated with Chinese stalagmite δ18O record over the past 640 ka; simulated terrestrial rainfall changes between 30°N and 30°S over the past 300 ka. Our findings highlight the predominant role of the low-latitude hydroclimate in governing the ∆DE* on orbital time scales, while high-latitude climate impacts are negligible. In turn, we argue that the ∆DE* can be used to indicate low-latitude hydrological changes at a global extent.

A 14 ka high-resolution δ18O lake record reveals a paradigm shift for the process-based reconstruction of hydroclimate on the northern Tibetan Plateau

The influence of the mid-latitude westerlies (MLW) competing with the Asian summer monsoons (ASM) over the Tibetan Plateau (TP) remains a matter of discussion on how and to which extent both atmospheric systems have been controlling hydro-climate during the Holocene. Depleted oxygen isotopes in lake deposits were commonly interpreted in terms of enhanced summer monsoon moisture supply, implying a migration of the ASM deep into the interior of the plateau during Holocene periods. In order to test this relationship we used a high resolution oxygen isotope record (mean 20 yr resolution) in combination with carbonates and mineral phases, titanium flux, grain size and ostracod abundances derived from a 6.84 m long sediment core in the endorheic Kuhai Lake basin, north-eastern TP. The results confirm 1) continuous positive co-variance between enriched δ18Ocarb and total carbonates during the last 14 ka, indicative of dominant seasonal influence on multi-decadal to centennial scale isotopic signatures in lake water and respective carbonate precipitation, 2) negative co-variance between allochthonous sediment flux and δ18Ocarb (and carbonates) attributed to relative increase of flux rates during non-summer seasons, 3) correspondence of lake level variations with carbonate mineral phases and the occurrence/disappearance of ostracod assemblages, and 4) inverse relationships between isotopic signatures in ASM-dominated and MLW-controlled lake records across the TP. Enriched δ18Ocarb in Kuhai Lake sediments was primarily a result of high evaporation during the summer seasons, while ASM-related rainfall amount did not play an important role, likely counterbalanced by isotopic signatures from different water sources. Conversely, depleted δ18Ocarb was mainly attributed to water supply during non-summer seasons of colder temperatures and generally light isotopic signatures from MLW-derived sources. This finding may lead to a paradigm shift in such way that depleted δ18O in carbonates is primarily not the result from ASM-related rainfall as previously assumed. The reconstructed hydro-climatic history of Kuhai Lake indicates the dominance of westerly-derived climate during the Younger Dryas interval (12.8–11.5 ka) under very shallow pond-like conditions. Despite climate amelioration during the early Holocene (11.5–7.5 ka) hydrological conditions remained unstable with frequent alternations between dominance of summer and winter seasons. During the middle Holocene (7.5–5.5 ka) the lake experienced highest lake levels dominated by summer monsoon-related water supply, assigned to the Holocene hydro-climatic optimum. Frequent high-amplitude fluctuations afterwards (5.1–2.9 ka) refer to cooling/drying events under enhanced MLW influence accompanied by a strong lake level decline. The late Holocene (2.9 ka- Present) period experienced moderate isotopic variations and fluctuating lake levels in response to variable influence of summer- or winter-related hydro-climatic conditions.This seesaw-like pattern with amplitudes of >10‰ in δ18Ocarb resembles fluctuations in cave records and variations between air and seawater (Dole effect). High correspondence with cooling events derived from North Atlantic drift ice and meltwater discharge indicate close ties to northern hemispheric climate transmitted by the MLW across the TP.

Discrimination in Tree Stems O2 Uptake and the Dole Effect

AbstractThe difference in δ18O between the atmospheric O2 and seawater is named the Dole effect (DE). Interpretation of past DE variations, a proxy for monsoonal intensity, is based on current understanding of global O2 fluxes. One such O2 flux that was poorly studied is the discrimination in O2 uptake by tree stems (Dstem). Stems differ from leaves in their lower gas permeability, which reduces the internal [O2] and poses diffusion limitations to local respiration. Diffusion limitations are expected to lower the effective discrimination below enzymatic values (17–30‰). Given fixed permeability, the lowest internal [O2] and thus the greatest diffusional effect are expected in high O2 influx. Dstem and O2 influx values were obtained by measurements of stem‐chamber air and a numerical model that resolves the gas exchange in the chamber. According to 101 results of temperate, Mediterranean, and tropical trees, the global Dstem is 19.2‰. Assuming basal O2 diffusion limitation in the stems, the results indicate involvement of the alternative oxidase respiration, with enzymatic discrimination factor of above 20‰. Small seasonal variations in Dstem were uncoupled from the O2 influx rates that tracked the temperature changes. This indicates a possible adjustment between the aeration capability of the stems and O2 uptake rate, which helps to maintain sufficient O2 supply. The mean Dstem value agrees with the assumed discrimination for leaf respiration, thus supporting current DE understanding. The small Dstem seasonal variations give an indication that climate variations on millennial and interglacial scales did not have a strong effect on Dstem values.

Attaining a productive structure for technology: The Bayh–Dole effect on university–industry–government relations in developing economy

This paper attempts to provide a systematic assessment of the ‘Bayh–Dole’ effect on the university–industry–government structures of Malaysia, a developing economy, from a quantitative dimension, in order to provide policy-makers with the central aspects of structural change. This paper takes account of those studies which question the significance of university patenting from the perspective of quality and utility. We observe widespread endogenization of university patenting and co-patenting processes in indigenous technology development cycles after the passage of Bayh–Dole-type legislation. The basic research supports and subsequent provisions of Bayh–Dole-type legislation provide us with the implications of strategic policy in attaining a productive network structure for technological innovations. We consider the importance of Bayh–Dole-type legislation in routinizing university research with regard to potential commercial values or applications. Thus, we break new ground in considering what the passage of such legislation actually achieves in a developing economy.

On the Δ17O budget of atmospheric O2

We modeled the Δ17O of atmospheric O2 using 27 ordinary differential equations comprising a box model composed of the stratosphere, troposphere, geosphere, hydrosphere and biosphere. Results show that 57% of the deficit in 17O in O2 relative to a reference water fractionation line is the result of kinetic isotope fractionation attending the Dole effect, 33% balances the positive Δ17O of O(1D) in the stratosphere, and 10% is from evapotranspiration. The predicted Δ′17O O2 relative to waters is −0.410‰ as measured at the δ18O of air. The value for Δ′17O O2 varies at fixed δ18O with the concentration of atmospheric CO2, gross primary production, and net primary production as well as with reaction rates in the stratosphere. Our model prediction is consistent with our measurements of the oxygen isotopic composition of air O2 compared with rocks if rocks define a fractionation line with an intercept in δ′17O=103ln(δ17O/103+1) vs. δ′18O=103ln(δ18O/103+1) space less than SMOW but more positive than some recent measurements imply. The predicted Δ17O is less negative than that obtained from recent measurements of O2 directly against SMOW. Underestimation of Δ′17O O2 can only be ameliorated if the integrated (bulk) Δ′17O for stratospheric CO2 is significantly greater than measurements currently allow. Our results underscore the need for high-precision comparisons of the 17O/16O and 18O/16O ratios of atmospheric O2, VSMOW, and rocks.

A reply to Etzkowitz’ comments to Leydesdorff and Martin (2010): technology transfer and the end of the Bayh–Dole effect

Three periods can be distinguished in university patenting at the U.S. Patent and Trade Office (USPTO) since the Bayh---Dole Act of 1980: (1) a first period of exponential increase in university patenting till 1995 (filing date) or 1999 (issuing date); (2) a period of relative decline since 1999; and (3) in most recent years--since 2008--a linear increase in university patenting. We argue that this last period is driven by specific non-US universities (e.g., Tokyo University and Chinese University) patenting increasingly in the USA as the most competitive market for high-tech patents.

The contribution of respiration in tree stems to the Dole Effect

Abstract. Understanding the variability and the current value of the Dole Effect, which has been used to infer past changes in biospheric productivity, requires accurate information on the isotopic discrimination associated with respiratory oxygen consumption in each of the biosphere components. Respiration in tree stems is an important component of the land carbon cycle. Here we measured, for the first time, the discrimination associated with tree stem oxygen uptake. The measurements included tropical forest trees, which are major contributors to the global fluxes of carbon and oxygen. We found discrimination in the range of 12.6–21.5‰, indicating both diffusion limitation, resulting in O2 discrimination values below 20‰, and alternative oxidase respiration, which resulted in discrimination values greater than 20‰. Discrimination varied seasonally, between and within tree species. Calculations based on these results show that variability in woody plants discrimination can result in significant variations in the global Dole Effect.

High alternative oxidase activity in cold soils and its implication to the Dole Effect

Variations in the Dole Effect, which have been used to infer past changes in biospheric productivity, are strongly affected by isotopic discrimination in soil respiration. Respiration through the alternative oxidase (AOX) pathway is associated with a higher discrimination than the one associated with the “normal” dark respiration pathway (the cytochrome pathway, COX). However, observations of O2 discrimination and AOX activity in undisturbed natural environments are scarce. In the current study we measured the O2 concentration and stable isotopes in the root zone of tundra, boreal forest and alpine forest soils. To estimate the discrimination from this data, we have performed O2diffusion experiments in gamma‐sterilized soil columns, with varying soil clay content. The discrimination found in the diffusion experiments was independent of clay content, and the value found, 14 ± 2‰, is the same as the one for binary diffusion of O2 in N2, indicating no interaction between the O2 and clay particles. Based on the field and laboratory results, the respiratory discrimination in the soils studied is 15–31‰, with the higher values associated with colder soils. The high discrimination found for cold (<6°C) soils indicates that AOX is a major respiratory pathway in these soils. This relationship between soil temperature and discrimination can be used in future interpretations of Dole Effect variations.

Oxygen isotope fractionation in the ocean surface and18O/16O of atmospheric O2

[1] We have recently published a new evaluation of Earth's Dole effect, which was based, in part, on measurements of δO2/Ar, δ17O and δ18O of dissolved argon and oxygen in the ocean surface. In calculations of the oxygen isotope effect due to photosynthesis and respiration (ɛup), gross O2 production (G) was an important factor. However, our estimates of G were based on an approximate equation, and in a recent publication it has been suggested that G obtained with this equation could be underestimated by about 33%. If true, such underestimation of G might lead to different ɛup values. To test this possibility, we have used a new rigorous equation with relevant information on isotopic composition of photosynthetic O2 and recalculated ɛup. Given the uncertainties, the new values do not differ from the previous ones, and therefore, the implications of the strong fractionation in the upper ocean (∼25‰) to the global Dole effect remain as in our original publication.

The isotopic composition of atmospheric oxygen

[1] Atmospheric O2 is almost 24‰ more enriched in 18O than seawater, and this enrichment is known as the Dole effect. For a long time it has been accepted that there is no oxygen isotope fractionation in photosynthesis, and thus the Dole effect should be the result of preferential terrestrial and marine respiratory consumption of 16O over 18O, and also several permil enrichment of leaf water from which terrestrial photosynthesis produces 18O enriched O2. This concept has led to the understanding that the record of past Dole effect variations was strongly affected by changes in the ratio of photosynthetic production between land and sea. However, recent studies in our lab have led to two major new observations: (1) O2 produced by certain marine phytoplankton, representing important groups of primary producers, is significantly enriched (up to 6‰) in 18O with respect to the substrate seawater and (2) effective oxygen isotope fractionation in soil respiration is considerably smaller than the intrinsic respiratory fractionation. Here we take these two observations into account and show that the magnitudes of the terrestrial and marine components of the Dole effect are close, and both are close to the measured Dole effect. As a result, the magnitude of the global Dole effect should not be sensitive to past changes in the ratio of land-to-sea photosynthetic rates. Instead of the land-sea control, variations in low-latitude hydrology, and possibly changes of fractionations in the marine biosphere, are more important in regulating the magnitude of the Dole effect and its past variations.

Enrichment of oxygen heavy isotopes during photosynthesis in phytoplankton

Some of the oxygen produced during oxygenic photosynthesis is consumed but little is known about the extent of the processes involved. We measured the (17)O/(16)O and (18)O/(16)O ratios in O(2) produced by certain marine and freshwater phytoplankton representing important groups of primary producers. When the cells were performing photosynthesis under very low dissolved oxygen concentrations (< 3 μM), we observed significant enrichment in both (18)O and (17)O with respect to the substrate water. The difference in δ(18)O between O(2) and water was about 4.5, 3, 5.5, and 7‱ in the diatom Phaeodactylum tricornutum, Nannochloropsis sp. (Eustigmatophyceae), the coccolithophore Emiliania huxleyi and the green alga Chlamydomonas reinhardtii, respectively. The difference in δ(17)O was about 0.52 that of δ(18)O. As explained, the observed enrichments most probably stem from considerable oxygen consumption during photosynthesis even when major O(2)-consuming reactions such as photorespiration were minimized. These enrichments increased linearly with rising O(2) levels but with different δ(17)O/δ(18)O slopes for the various organisms, suggesting engagements of different O(2)-consuming reactions with rising O(2) levels. Consumption of O(2) may be important for energy dissipation during photosynthesis. The isotope enrichment observed here, not accounted for in earlier assessments, closes an important gap in our understanding of the difference between the isotopic compositions of atmospheric oxygen and that of seawater, i.e., the Dole effect.

What drives the millennial and orbital variations of δ18O atm?

The isotopic composition of atmospheric oxygen ( δ 18O atm) is a complex marker that integrates changes in global sea-level, water cycle, and biosphere productivity. A strong signature of orbital precession has been identified leading to the use of low-resolution measurements of δ 18O atm to date ice core records. However, the drivers of these δ 18O atm variations are still poorly known. Here, we combine records of millennial and orbital scale variations on the NorthGRIP, Vostok, and EPICA Dome C (EDC) ice cores to explore the origin of δ 18O atm variations. We show that, superimposed on the dominant precession signal, millennial δ 18O atm variations record systematic decreases during warm phases of the Dansgaard–Oeschger events and systematic increases during the cold phases. We show that at both timescales δ 18O atm is strongly related to the monsoon activity itself influenced by precessional and millennial shifts in InterTropical Convergence Zone (ITCZ). Then, we show that despite its simplicity, the Dole effect defined as the difference between δ 18O atm and δ 18O of global sea-level enables one to remove the obliquity signal within the δ 18O atm record and is a good indicator of hydrological cycle and biosphere productivity. Finally, we compare the δ 18O atm records to past changes in atmospheric composition recorded in ice cores and conclude that δ 18O atm responds much more than CH 4 to precession signal, in contrast with earlier views. Similarities observed at orbital timescales between CO 2 and δ 18O atm reveal a stronger coupling than previously thought between the carbon and the oxygen cycles.

The decline of university patenting and the end of the Bayh–Dole effect

University patenting has been heralded as a symbol of changing relations between universities and their social environments. The Bayh–Dole Act of 1980 in the USA was eagerly promoted by the OECD as a recipe for the commercialization of university research, and the law was imitated by a number of national governments. However, since the 2000s university patenting in the most advanced economies has been on the decline both as a percentage and in absolute terms. In addition to possible saturation effects and institutional learning, we suggest that the institutional incentives for university patenting have disappeared with the new regime of university ranking. Patents and spin-offs are not counted in university rankings. In the new arrangements of university–industry–government relations, universities have become very responsive to changes in their relevant environments.

A model of the Earth's Dole effect

The Earth's Dole effect describes the isotopic 18O/16O‐enrichment of atmospheric oxygen with respect to ocean water, amounting under today's conditions to 23.5‰. We have developed a model of the Earth's Dole effect by combining the results of three‐dimensional models of the oceanic and terrestrial carbon and oxygen cycles with results of atmospheric general circulation models (AGCMs) with built‐in water isotope diagnostics. We obtain a range from 22.4‰ to 23.3‰ for the isotopic enrichment of atmospheric oxygen. We estimate a stronger contribution to the global Dole effect by the terrestrial relative to the marine biosphere in contrast to previous studies. This is primarily caused by a modeled high leaf water enrichment of 5–6‰. Leaf water enrichment rises by ∼1‰ to 6–7‰ when we use it to fit the observed 23.5‰ of the global Dole effect. The present model is designed to be utilized in forthcoming paleo studies allowing a quantitative analysis of long‐term observations from polar ice cores.

Contribution of soil respiration in tropical, temperate, and boreal forests to the 18O enrichment of atmospheric O2

The 18O content of atmospheric O2 is an important tracer for past changes in the biosphere. Its quantitative use depends on knowledge of the discrimination against 18O associated with the various O2 consumption processes. Here we evaluated, for the first time, the in situ 18O discrimination associated with soil respiration in natural ecosystems. The discrimination was estimated from the measured [O2] and δ18O of O2 in the soil‐air. The discriminations that were found are 10.1 ± 1.5‰, 17.8 ± 1.0‰, and 22.5 ± 3.6‰, for tropical, temperate, and boreal forests, respectively, 17.9 ± 2.5‰ for Mediterranean woodland, and 15.4 ± 1.6‰ for tropical shrub land. Current understanding of the isotopic composition of atmospheric O2 is based on the assumption that the magnitude of the fractionation in soil respiration is identical to that of dark respiration through the cytochrome pathway alone (∼18‰). The discrimination we found in the tropical sites is significantly lower, and is explained by slow diffusion in soil aggregates and root tissues that limits the O2 concentration in the consumption sites. The high discrimination in the boreal sites may be the result of high engagement of the alternative oxidase pathway (AOX), which has high discrimination associated with it (∼27‰). The intermediate discrimination (∼18‰) in the temperate and Mediterranean sites can be explained by the opposing effects of AOX and diffusion limitation that cancel out. Since soil respiration is a major component of the global oxygen uptake, the contribution of large variations in the discrimination, observed here, to the global Dole Effect should be considered in global scale studies.

Microbial respiration and diffusive transport of O2, 16O2, and 18O15O in unsaturated soils and geologic sediments.

Molecular oxygen (O2) in unsaturated geologic sediments plays an important role in soil respiration, biodegradation of organic contaminants, metal oxidation, and global oxygen and carbon cycling, yet little is known about oxygen isotope fractionation during the consumption and transport of O2 in unsaturated zones. We used a laboratory kinetic cell technique to quantify isotope fractionation due to respiration and a numerical model to quantify both consumptive and diffusive fractionation of O2 isotopes at a field site comprised of unsaturated lacustrine sandy materials. The combined use of laboratory-based kinetic cell experiments and field-based isotope transport modeling provided an effective tool to characterize microbial respiration in unsaturated media. Based on results from the closed-system kinetic cells, O2 consumption and isotope fractionation were attributed to the alternative cyanide-resistant respiration pathway. At the field site, the modeled depth profiles for O2 and delta18O matched the measured in situ data and confirmed that the consumption of O2 was via the alternative respiration pathway. If the cyanide-resistant respiration pathway is indeed widespread in soils, its high oxygen isotope enrichment factor could help to explain the discrepancy between the predicted present-day Dole effect (+20.8/1000) and the observed Dole effect (+23.5/1000). Thus, further soil O2 isotope studies are needed to better characterize and model the fractionation of oxygen isotopes during subsurface respiration and the potential impact on the isotopic content of atmospheric O2.

Effects of photorespiration, the cytochrome pathway, and the alternative pathway on the triple isotopic composition of atmospheric O2

The triple isotopic composition of atmospheric O2 is a new tracer used to estimate changes in global productivity. To estimate such changes, knowledge of the relationship between the discrimination against 17O and the discrimination against 18O is needed. This relationship is presented as θ = ln(17α)/ln(18α). Here, the value of theta was evaluated for the most important processes that affect the isotopic composition of oxygen. Similar values were found for dark respiration through the cytochrome pathway (0.516 ± 0.001) and the alternative pathway (0.514 ± 0.001), and slightly higher value was found for diffusion in air (0.521 ± 0.001). The combined effect of diffusion and respiration on the atmosphere was shown to be close to that of dark respiration. The value we found for photorespiration (0.506 ± 0.005) is considerably lower than that of dark respiration. Our results clearly show that the triple isotopic composition of the atmosphere is affected by the relative rates of photorespiration and dark respiration. Also, we show that closing the current global isotopic balance will enable the estimation of the current global rate of photorespiration. Using the Last Glacial Maximum as a case study, we show that variations in global rate of photorespiration affected the triple isotopic composition in the past. Strong fractionations measured in illuminated plants indicated that the alternative pathway is activated in the same conditions that favor high rate of photorespiration. This activation suggests that the global rate of the alternative pathway is higher than believed thus far, and may help to close the gap between the calculated and measured Dole Effect.

Occurrence of an exceptional carbonate dissolution episode during early glacial isotope stage 6 in the Southeastern Atlantic

Concentration and mass accumulation rate profiles from Southeastern Atlantic sediment cores located off Namibia show that an exceptional episode in benthic carbonate dissolution occurred during early glacial isotope stage 6 (substages 6.6 and 6.5) between about 186 000 and 170 000 yr BP. Although this episode is restricted to or is more pronounced in this region than in other areas of the Atlantic Ocean, its exceptional character with respect to older and younger climatic episodes at the same site cannot be fully explained by local factors alone, but requires a combination of local and global influences. The onset of the carbonate dissolution episode is related to a more efficient transfer of organic matter from surface eutrophic areas to the lower and is due to low sea level, while its termination relates to a change in either global ocean alkalinity or bottom water circulation. An evaluation of the magnitude of this local carbonate dissolution episode suggests that its contribution to a global alkalinity change may have been significant. Carbonate dissolution was probably amplified by stronger upwelling activity of the Benguela System linked to an exceptional northern excursion of the boreal summer ITCZ during early glacial isotope stage 6. This low latitude global linkage may explain how this carbonate dissolution event as well as other ‘anomalies’ observed for early stage 6, like an important Dole effect minimum or a ‘cold’ Mediterranean sapropel, are related.

Atmospheric oxygen 18 and sea-level changes

Past isotopic composition of atmospheric oxygen (δ 18O atm) can be inferred from the analysis of air bubbles trapped in ice caps. The longest record covers the last 420 ka (thousand of years) at the Vostok site in East Antarctica. It shows a strong modulation by the precession and striking similarities, but also noticeable differences, with the deep-sea core oxygen 18 record from which changes in the oxygen content of sea-water (δ 18O sw) and in sea-level can be derived. Indeed, δ 18O atm is driven by complex fractionation processes occuring during respiration and photosynthesis. Both δ 18O atm and its difference with respect to δ 18O sw (the Dole effect) are influenced by factors such as the ratio of oceanic and terrestrial productivities which may have significantly changed between different climates. Also, the response time of δ 18O atm to oceanic changes should be taken in consideration but this parameter itself depends on biospheric activity. We review the various aspects of the link between the δ 18O atm and the δ 18O sw signals. We also examine the approach followed by Shackleton (Science (2000)) for deriving sea-level change from the δ 18O atm Vostok record, assuming that the phase between this record and insolation changes is constant and that the Dole effect is a fraction of the precessional component of the δ 18O atm signal. Glaciological constraints on the Vostok chronology and the complexity of the Dole effect show that those two assumptions are quite probably too simplistic.