Journal of Experimental Botany, Vol. 52, No. 357, pp. 801-809,
April 15, 2001
© 2001 Oxford University Press
Original Papers |
The high oxygen atmosphere toward the end-Cretaceous; a possible contributing factor to the K/T boundary extinctions and to the emergence of C4 species
1 Department of Plant Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel
2 Blaustein Institute for Desert Research, Ben Gurion University of the Negev, 84990, Israel
Received 22 June 2000; Accepted 20 October 2000
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
Angiosperm plants were grown under either the present day 21 kPa O2 atmosphere or 28 kPa, as estimated for the end-Cretaceous (100–65 MyBP). CO2 was held at different levels, within the 24–60 Pa range, as also estimated for the same period. In C3 Xanthium strumarium and Atriplex prostrata, leaf area and net photosynthesis per unit leaf area, were reduced by the high O2, while the whole-plant respiration/photosynthesis ratio increased. The high O2 effects were strongest under 24 Pa, but still significant under 60 Pa CO2. Growth was reduced by high O2 in these C3 species, but not in Flaveria sp., whether C3, C4, or intermediary grown under light intensities <350 µmol m-2 s-1 PPF. Photosynthesis of C3 Flaveria sp. was reduced by high O2, but only at light intensities >350 µmol m-2 s-1 PPF. It is concluded that the high O2 atmosphere at the end-Cretaceous would have reduced growth of at least some of the vegetation, thus adversely affecting dependent fauna. The weakened biota would have been predisposed to the consequences of volcanism and the K/T boundary bolide impact. Conversely, photosynthesis and growth of C4 Zea mays and Atriplex halimus were little affected by high, 28 kPa, O2. This suggests an environmental driver for the evolution of C4 physiology.
Key words: K/T boundary, extinctions, paleo-atmosphere, oxygen, C4 emergence.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
High ambient oxygen and the K/T boundary extinctions
65 million years ago (MyBP) mass disappearances of some 70% of all biotic species, delineated the Cretaceous-Tertiary (K/T) boundary (Hallam and Wignall, 1997
). Alvarez et al. proposed that the causal agent was a climatic cataclysm, resulting from the impact of a bolide (Alvarez et al., 1980). This has now been widely accepted (Macleod and Keller, 1996). However, one conundrum remains: the decline of certain flora and fauna species which commenced some ten million years before the K/T event (Sloan et al., 1986; Johnson and Hickey, 1990; Sweet et al., 1990; Johnson, 1993; Macleod et al., 1997). These and other findings have suggested more gradually developing biosphere degrading factors, such as extreme volcanism (Hallam, 1987; Venkatesen et al., 1993; Courtillot, 1999).
Models of the paleo-atmosphere indicate that there have been periods of comparatively high oxygen such as the 40 kPa event in the Carboniferous (Berner and Canfield, 1989; Berner et al., 2000). High levels of CO2, such as were prevalent in most of Phanerozoic eon, tend to counteract the photorespiration-inducing, photosynthesis- reducing effect of high O2, although decreased activation of other stromal enzymes has also been reported (Leegood and Walker, 1982). Oxygen reduced net photosynthesis is significant even at the present atmospheric level of 21 kPa O2 (von Caemmerer and Farquhar, 1981). At the end-Cretaceous, oxygen is estimated to have reached 
28 kPa, while CO2 was comparatively low, with estimates ranging from 23 Pa (Lasaga et al., 1985) to the more recent 30–90 Pa (Berner, 1997). It is suggested that the high oxygen atmosphere at the K/T boundary may also have been involved in the pre-K/T boundary decline of both flora and dependent fauna.
Beerling (Beerling, 1994) calculated rates of leaf photosynthesis for the O2/CO2 atmospheric composition and temperatures of the late Cretaceous to the present time, using the Farquhar et al. and von Caemmerer and Farquhar leaf biochemistry models (Farquhar et al., 1980; von Caemmerer and Farquhar, 1981). His calculations showed a strong effect of high O2. Interpolating in Beerling's Fig. 6, for the late Cretaceous, the calculated rate of photosynthesis is seen to decline from 100 to 60 MyBP by 40–60%. However, these models do not take into account possible changes in leaf area (see below) and gas conductance (Rachmilevitch et al., 1999) in response to elevated O2. The effect on plants of the very high (35 kPa) O2 event calculated for the Carboniferous period (345–280 MyBP) has been studied (Beerling et al., 1998). After 6 weeks growth under 35 Pa CO2 and either high or present-day O2, photosynthesis per unit leaf area was reduced 29% by the high O2.
|
High ambient oxygen and the evolution of C4 plants
13C/12C isotope evidence has been reported for the presence of C4 plants from strata dated to 15 MyBP (Cerling et al., 1994
, 1998; Kingston et al., 1994). Isotope evidence for C4 plants from the Cenomanian/Turanian (C/T) boundary period (100 MyBP) has been reported (Kuypers et al., 1999). However, these findings may be confounded by CAM species, which could produce similar 13C/12C values.
Most discussions of environmental conditions which encouraged the evolution of C4 from C3 physiology emphasize the effects of low atmospheric CO2, high temperatures and water stress to which C4 species are relatively well adapted (Ehleringer et al., 1997; Ehleringer and Monson, 1993; Cerling et al., 1998; Collatz et al., 1998). The present study relates to the potential advantage of C4 plants under relatively high ambient O2.
The following hypothesise were tested: (a) that the primary production of C3 angiosperms would have been adversely affected by the high oxygen composition of the late-Cretaceous, and (b) that the same high ambient oxygen would not affect C4 plants and may therefore have provided an environmental driver for their evolutionary emergence.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
Plant species
Two C3 species, Xanthium strumarium L., and Atriplex prostrata D.C. and two C4 species, Zea mays L. and Atriplex halimus L. were studied. Initial growth studies and some photosynthesis measurements were also carried out on Flaveria pringlei Gandoger (C3), F. trinervia C.Mohr (C4) and the C3–C4 intermediates F. floridana J.R. Johnston and F. sonorensis A.M. Powell. All species studied were forage angiosperms. Angiosperms are thought to have emerged and diversified in the early Cretaceous (Crane et al., 1995
). Fast growing species were chosen in order that plant parts used for physiological measurements would have developed under the atmospheric composition being studied and in order that significant growth response could be measured in relatively short periods (weeks). All observations were limited to vegetative growth.
Growth conditions
The growth chamber system for control of ambient O2 and CO2 partial pressures was as described previously (Rachmilevitch et al., 1999). Plant growth and physiological parameters were studied under six atmospheric compositions shown in Table 1.
|
CO2 was controlled to ±3 Pa and O2 to ±0.5 kPa. Light intensity was 380±20 µmol m-2 s-1 PPF at the plant tops for 12 h d-1, obtained from a mixture of fluorescent and incandescent lamps. Air temperatures were 24 and 19±0.5 °C in the day and night periods, respectively. Air humidity was above 70% RH at all times, but below the dew point.
Gas exchange measurements
Carbon dioxide exchange of whole young plants (roots and shoots) each about 20 cm tall, was measured, over periods of days, in mini-chambers (Reuveni and Gale, 1985). Environmental conditions, including light, temperature, humidity, and atmospheric composition were the same as in the growth chambers. The ratio of net daily respiration/gross-photosynthesis (R/P) was calculated assuming that respiration in the light was 30% of the average dark period values (a reasonable but arbitrary value, see Kromer, 1995). Gas exchange parameters of single, fully developed, attached leaves were determined with an ADC (UK) Model LCA-2 system. For these measurements, different mixtures of oxygen, nitrogen and carbon dioxide were obtained with two cascaded Wosthoff Co (Germany) gas-mixing pumps (Model 2G-18–2F). Gas exchange was measured and exchange parameters were calculated by standard procedures (von Caemmerer and Farquhar, 1981). CO2 assimilation/internal leaf CO2 partial pressure (A/Ci) curves were derived from gas exchange measurements made under 900 µmol m-2 s-1 photosynthetic photon flux (PPF). Data curves for the A/Ci and A/PPF data were smoothed with right-angle hyperbolae regressions. When measuring the rapid effect of high O2 on leaf photosynthesis, O2 pressure was switched between 21 and 28 kPa at different levels of PPF, and photosynthesis was measured after 14–16 min.
Growth rates
Relative growth rate (RGR) was calculated as (ln F–ln I)/t, where F is the final dry wt in grams, I the initial dry wt, estimated from the initial fresh weights and the fresh wt/dry wt ratio of parallel samples, and t, the elapsed time in days.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
Response of C3 plants to the high (28 kPa) O2 composition of the end-Cretaceous period, when grown under low-end CO2 estimates (24 or 35 Pa) for the same period
In the C3 species X. strumarium and A. prostrata, grown under a medium level estimate of CO2 (35 Pa) photosynthesis per unit leaf area was much reduced by high O2, albeit to different degrees in the two species. As shown in Fig. 1
, photosynthesis as expressed in the A/Ci curve of X. strumarium was much suppressed in plants grown and measured under 28 versus 21 kPa O2. This is evident both in the initial slope (an indication of Rubisco activity) and in the maximum rate of assimilation— considered an indication of a limitation in ribulose bisphosphate regeneration. However, in A. prostrata only the maximum rate of photosynthesis was reduced under high O2.
|
An example of the effect of ambient oxygen (28 or 21 kPa) on whole plant CO2 exchange of A. prostrata and X. strumarium, grown under a low level estimate of CO2 (24 Pa), over a 4 d period, is shown in Fig. 2
.
|
As seen in Fig. 2
, high, 28, versus low, 21 kPa O2, reduced CO2 uptake of both these C3 species by 25–40% when grown under 24 Pa CO2. However, night-time CO2 efflux was not proportionally reduced, as could be expected (Amthor, 1989). This resulted in an increased respiration/gross-photosynthesis (R/P) (Table 2). A similar result was obtained for plants grown under 35 Pa CO2. Plant carbon gain is determined by leaf area, by photosynthesis per unit leaf area and by the overall R/P ratio. As shown in Table 2, leaf area was also reduced by 28 versus 21 kPa O2 under both 24 and 35 Pa CO2, in both species. Leaf number per plant (data not shown) was not affected.
|
As shown above (Figs 1
, 2; Table 2) at low and medium level estimates of the ambient end-Cretaceous CO2 there was a strong effect of elevated O2 on photosynthesis, leaf area and R/P ratio of the C3 species X. strumarium and A. prostrata. This was expressed in overall growth (RGR). Data for RGR are given below, in Fig. 5, together and for comparison with those of the C4 species. Contrary to these C3 species, the four Flaveria species studied (including C3, C4 and intermediary C3–C4 species (see ‘Materials and methods’) showed no RGR effect of ambient oxygen, when grown under 24 Pa CO2 and either 28 or 21 kPa O2 (data not shown). This was unexpected, especially for the C3 species, as high O2 greatly increased the leaf gas conductance of all the Flaveria species (Rachmilevitch et al., 1999). This anomaly was resolved when photosynthesis of Flaveria was measured as a function of light intensity. An example of such an A/PPF function is given for the C3 Flaveria pringlei (Fig. 3).
|
|
As seen in Fig. 3
, 28 versus 21 kPa O2 significantly reduced the photosynthesis of leaves of F. pringlei, only at PPF>350 µmol m-2 s-1. The 12 h daytime light intensity in the chambers in which the plants were grown, was only 380 µmol m-2 s-1 PPF, at the plant tops, and considerably less within the canopy.
Response of C3 plants to the high ambient O2 (28 kPa) of the end-Cretaceous, when grown under a high-end estimate for CO2 (60 Pa) for the same period
As noted above, recent estimates of the atmospheric CO2 partial pressure toward the end-Cretaceous, suggest a level of about double the pre-industrial 27 Pa, although confidence limits are very wide (Berner, 1994, 1997). As relatively high CO2 counteracts at least one negative effect of high O2 on C3 plants, namely competition with CO2 for the Rubisco enzyme (von Caemmerer and Farquhar, 1981), the response of the C3 species X. strumarium and A. prostrata to high (28 kPa) O2 when grown under 60 Pa CO2 was studied (Fig. 4).
|
As seen in Fig. 4
, in A. prostrata plants grown under 60 Pa CO2, high, 28 kPa O2, had a smaller effect on photosynthesis than in plants grown under 24 Pa CO2 (Fig. 1). However, for X. strumarium the effect was essentially the same.
As noted above, there was a significant depression of RGR in the two C3 species, when grown under 28 versus 21 kPa O2 (Fig. 5). This depression was larger in plants grown under the lower levels of CO2 (24 or 35 Pa), but still present in plants grown at 60 Pa CO2. (Also shown in Fig. 5, for comparison, are similar RGR data for two C4 species—see below.)
Response of C4 species to the high (28 kPa) O2 atmosphere of the end-Cretaceous
Leaf area and photosynthesis (the latter as expressed by A/Ci and A/PPF functions) of the C4 species Atriplex halimus and Zea mays showed no response to elevated O2 (28 versus 21 kPa) when plants were grown under either low (24) or high end (60 Pa) CO2 (data not shown). Daily carbon exchange and R/P values for C4 plants (as in Fig. 2 and Table 2) also failed to show any response to growth under 28 versus 21 kPa O2 (data not shown). Consequently and as could be expected from these results, there was no effect of 28 versus 21 kPa O2 on the growth (RGR) of the two C4 species, when ambient CO2 was held at 24, 35, or 60 Pa (Fig. 5). This is in contrast to the deleterious effect of high (28 kPa) ambient O2 on the growth of the C3 species.
Leaf diffusion conductance of C3 and C4 species, grown under the atmospheric composition of the end-Cretaceous
A study of the response of leaf water vapour diffusion conductance (gs) to the oxygen level prevailing during the K/T boundary period has been reported previously (Rachmilevitch et al., 1999). In these experiments ambient CO2 had been held at the lower estimates of 24 or 35 Pa. Growth under 28 versus 21 kPa O2 resulted in much higher values of gs. This was found for the C3 species Atriplex prostrata, Xanthium strumarium and Flaveria pringlei, the C3–C4 intermediate F. sonorensis, and the C4 species F. trinervia. Only the C3-C4 intermediate F. floridana showed just a small increase in gs, in response to the elevated O2. In view of the above noted recent higher estimate for the end-Cretaceous atmospheric CO2, the study was extended to include gs response to 28 kPa O2 under 60 Pa CO2. To this were added gs measurements of the two C4 species Atriplex halimus and Zea mays. Results are presented in Fig. 6. For comparison some of the previous data for gs of X. strumarium and A. prostrata grown under the lower estimates for atmospheric CO2 (Rachmilevitch et al., 1999) have been included.
In the two C3 species grown under the lower ambient levels of CO2 (24 and 35 Pa) high 28 versus low, 21 kPa O2 much increased gs (Fig. 6). This effect was particularly pronounced in A. prostrata. However, when grown under 60 Pa CO2, gs of plants grown under 21 kPa O2 unexpectedly increased in both species, as compared to that of plants grown under 35 Pa CO2. Under 60 Pa CO2 there was no further significant effect (P>0.05) of oxygen level (28 versus 21 kPa) on gs in either of these C3 species. In the two C4 species A. halimus and Zea mays, stomatal conductance, gs, generally showed no significant response to high O2. An exception was for A. halimus grown under 24 Pa CO2 in which gs was some 50% higher when plants were grown under 28 versus 21 kPa O2 (P<0.01).
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
Crucial factors of this study are the actual partial pressures of carbon dioxide and oxygen prevalent at the end-Cretaceous. All estimates have wide confidence limits (cf. Berner and Canfield, 1989
; Berner et al., 2000). Just one high-end estimate for O2, namely 28 kPa, has been used, and a range of carbon dioxide values between 24 and 60 Pa (Lasaga et al., 1985; Berner, 1997).
Care is needed when projecting the characteristics of ancient plants from the response of their extant representatives. There is an inherent assumption that physiological responses to environmental parameters have not changed significantly with time, in this case the last 150 million years. Moreover, modern, highly bred plants, such as the Z. mays studied here, have almost certainly had their photosynthesis/growth characteristics modified. However, Rubisco, the main enzyme involved in the response of C3 plants to ambient CO2 and O2 has been highly conserved. Such changes as have been found, such as subunit composition or O2/CO2 specificity, are for species originating in periods separated by hundreds of millions of years (Jordan and Ogren, 1981; Badger and Andrews, 1987). Theoretical models of the response of leaf photosynthesis to ambient O2 and CO2 are based on known biochemical properties of Rubisco (Farquhar et al., 1980; Beerling, 1994). Responses found here were generally as could be expected from these models. However, hitherto unreported effects have also been found of high O2 on leaf area, leaf diffusion–conductivity, and the respiration/photosynthesis (R/P) ratio.
Response of C3 plants to the simulated end-Cretaceous atmosphere
An early paper on soybean (Glycine max) reports the effect of medium levels of O2 (30 kPa) at low CO2 (<35 Pa) on plant photosynthesis (Forrester et al., 1966). Data from their Fig. 7 indicate a 45% drop in the rate of photosynthesis per unit leaf area, when going from (present day) 36 Pa CO2 and 21 kPa O2 to the low end CO2 estimate for the end-Cretaceous of 24 Pa and the high end O2 estimate of 28 kPa. This is similar to what was obtained for the C3 species studied here and is in general accord with the report of Beerling et al. (Beerling et al., 1998) working with a simulated Carboniferous atmosphere of 35 kPa O2 and 35 Pa CO2. As in this study, the expected reduction in photosynthesis (see Introduction) was found and it was reported that there was no adaptation of plants to the high O2 atmosphere.
As shown in Fig. 1, in C3 plants grown under a medium level estimate for CO2 (35 Pa) photosynthesis was reduced by ambient 28 versus 21 kPa O2. However, respiration was not reduced proportionally (Fig. 2), as could be expected (Amthor, 1989). This may have been a result of a relative increase in the rate of respiration in response to high O2 (Gale, 1974). Consequently the ratio of daily respiration to gross photosynthesis (R/P) increased very significantly (Table 2). Leaf area was reduced by about 25% in the high O2-grown plants, irrespective of whether the plants were grown under low or medium CO2 (24 or 35 Pa) (Table 2). There was, therefore, a combination of at least three factors; all of which tend to reduce primary productivity: reduced leaf area, reduced photosynthesis per unit leaf area and higher R/P ratio.
Under low and medium level estimates of CO2 for the end-Cretaceous (24 and 35 Pa), high O2 was detrimental to factors affecting primary productivity of the C3 species X. strumarium and A. prostrata. The same effects were also present, but to a lesser degree, when they were grown under the higher (60 Pa) CO2 estimate. As before, the two species differed in degree of response. This can be seen in the leaf A/Ci curves of plants grown under 60 Pa CO2 and either 21 or 28 Pa O2 (Fig. 4). Whereas in A. prostrata the high O2 effect was smaller than when the plants had been grown under low ambient CO2 (Fig. 1), in X. strumarium the O2 response was just as large.
The above effects of high O2 translated into a large reduction of RGR in the C3 plants grown under 28 versus 21 kPa O2 at the lower (24 and 35 Pa) ambient CO2 levels (Fig. 5). In plants grown under 60 Pa CO2 RGR reduction was much smaller, but still significant. It should be borne in mind that vegetative growth is essentially exponential. Consequently, over extended periods, even a small drop in RGR becomes a large percentage reduction in primary productivity. As could be expected from the variability in physiological responses, there was considerable species variability in growth response (as shown in Fig. 5 and discussed below, for C4 species). Of special significance in respect to C3 species variability was the lack of growth response of the C3 and C3–C4 intermediate Flaveria species to high (28 kPa) O2 (data not shown). This was found when they were grown under relatively low (24 Pa) ambient CO2 and a maximum daytime light intensity of 380 µmol m-2 s-1 PPF, at the plant tops. This lack of growth response was found despite the large increase in gs of all the Flaveria species studied (C3, C4 or C3–C4 intermediates) when grown under high O2 (Rachmilevitch et al., 1999). However, as shown in Fig. 3, at high PPF (>350 µmol m-2 s-1) leaves of the C3 Flaveria species showed a clear, rapid (within minutes) 20% reduction in photosynthesis in response to high O2 (28 versus 21 kPa). This suggests that there may have been reduced growth of Flaveria species in geographic regions of high solar insolation. However, it should be noted that plants growing under high solar radiation and not, as here, in a growth cabinet, may adapt, ontogenetically.
In the present study, plant response to the putative end-Cretaceous atmosphere was compared to that of today. However, in most of the Cretaceous period, CO2 levels were much higher than today and dropped to a low at the K/T boundary (Berner, 1994). Consequently, the percentage reduction in primary productivity, in the tens of millions of years preceding the K/T boundary, may have been even more significant than found here.
Response of C4 plants to the simulated end-Cretaceous atmosphere
Photosynthesis and growth of the C4 species studied here (Z. mays, A. halimus and F. trinervia) did not respond to high 28, versus low, 21 kPa O2. This was the case even when they were grown under 24 Pa CO2, the low-end estimate for the end-Cretaceous period. Apart from A. halimus grown under low (24 Pa) CO2, there appeared to be no gs response to high O2 in Z. mays and A. halimus (Fig. 6). This differs from what was found for the C4 species F. trinervia in which gs much increased in high O2, low CO2-grown plants (Rachmilevitch et al., 1999). High gs sensitizes plants to water stress. The reduction in leaf area in response to elevated O2 in C3 plants (Table 2) may have been a result of high gs-induced water stress. However, this was not measured, or expected, as air humidity was very high in the growth chambers (see Materials and methods). If increased gs in response to high O2 were indeed more common in C3 than in C4 plants, this would be a further factor favouring the evolution of C4 physiology. However, the variance found here among the few species studied, requires a further survey of C3 and C4 species gs response to O2, before conclusions can be drawn.
Lack of evidence of C4 plants in a given stratum does not necessarily mean that they had not yet emerged, only that they were not widespread. Until recently the earliest indication of the presence of C4 plants was reported for strata dated to 15 MyBP (Kingston et al., 1994) with earlier indications for 100 MyBP (Kuypers et al., 1999). Today, C4 species contribute only 18% to world plant productivity mainly, but with exceptions (see Sage and Monson, 1998) in regions of high solar insolation (Ehleringer et al., 1997; Collatz et al., 1998). It is possible that the relatively low ambient O2 of today (21 kPa) is one reason for the lack of more widespread distribution of extant C4 species.
|
Conclusions |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
The paleo-atmosphere and the K/T boundary extinctions
The C3 species studied here are considered to be representative of important angiosperm forage plants of the late Cretaceous period. However only a few species were tested and the degree of their reactions varied. Even so the results obtained strongly suggest that for some millions of years prior to the bolide impact of 65 MyBP, primary production of many plant species would have been severely diminished. Reduced plant production would have adversely affected the sustenance of dependent herbivores (insect and animal) with the effect amplified in carnivores and along the ecological food chain. This, together with other factors of biosphere degradation at the end-Cretaceous period (see Introduction) may explain the decline in many biota species which occurred prior to the 65 MyBP K/T boundary catastrophe. As ventured by Hallam and Wignall, the bolide impact may have been ‘only the final coup de grace’ (Hallam and Wignall, 1997
). It is intriguing to note that according to the models of Berner and Canfield and Berner et al. (Berner and Canfield, 1989; Berner et al., 2000), the end-Permian, the greatest of all the mass extinctions (Courtillot, 1999) was preceded (albeit by some tens of millions of years) by the highest ever O2 event (40 kPa), with concomitant low, 25 Pa, CO2 (Berner, 1994).
The paleo-atmosphere and the emergence of C4 plants
Contrary to the response of the C3 species, the primary productivity of the C4 species was unaffected by the (assumed) 28 kPa O2 of the end-Cretaceous, even at the lowest estimate for CO2 (24 Pa) for that period, which was tested. This suggests that high O2 may have constituted a strong driver for the evolution of C4 from C3 plants, at least as far back as about 100 MyBP, the earliest date for which evidence has been found suggesting their presence (Kuypers et al., 1999). This is in addition to other C4 evolution-inducing environmental factors, such as low CO2, high temperatures and water stress (Ehleringer and Monson, 1993; Cerling et al., 1994, 1998).
|
Acknowledgments |
|---|
This project was carried out under a grant from the Bi-National, US Israel Research Fund (BSF). Partial support was received from the Aaron Beare Foundation, South Africa. Special thanks are due to Professor Robert Pearcy for his co-operation and for extending the use of facilities at UC Davis, CA, to JG, for the Flaveria studies.
|
Notes |
|---|
3 To whom correspondence should be addressed. Fax: +972 2 579 0252. E-mail: galej{at}vms.huji.ac.il
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
|---|
Alvarez LW, Alvarez W, Asaro F, Michel HV.1980. Extraterrestrial cause for the Cretaceous-Tertiary Extinction. Science 208, 1095–1108.
Amthor JS.1989. Respiration and plant productivity. New York: Springer-Verlag.
Badger MR, Andrews TJ.1987. Co-evolution of Rubisco and CO2 concentrating mechanisms. Progress in Photosynthesis Research 3, 601–609.
Beerling DJ.1994. Modeling palaeophotosynthesis: late Cretaceous to present. Philosophical Transactions of the Royal Society of London Series B 346, 421–432.
Beerling DJ, Woodward FI, Lomas MR, Wills MA, Quick WP, Valdes PJ.1998. The influence of Carboniferous palaeoatmospheres on plant function: an experimental and modelling assessment. Philosophical Transactions of the Royal Society of London Series B 353, 131–139.
Berner RA.1994. A revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science 294, 56–91.
Berner RA.1997. Paleoclimate—the rise of plants and their effect on weathering and atmospheric CO2. Science 276, 544–546.
Berner RA, Canfield DE.1989. A new model of atmospheric oxygen over Phanerozoic time. American Journal of Science 289, 331–361.
Berner RA, Petsch ST, Lake JA, Beerling DJ, Popp BN, Lane RS, Laws EA, Westley MB, Cassar N, Woodward FI, Quick WP.2000. Isotope fractionation and atmospheric oxygen: implications for phanerozoic O2 evolution. Science 287, 1630–1633.
Caemmerer von S, Farquhar GD.1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.[ISI]
Cerling TE, Ehleringer JR, Harris JM.1998. Carbon dioxide starvation, the development of C4 ecosystems and mammalian evolution. Philosophical Transactions of the Royal Society of London Series B 353, 159–171.
Cerling TE, Wang Y, Quade J.1994. Expansion and emergence of C4 plants. Nature 371, 112–113.
Collatz GJ, Berry JA, Clark JS.1998. Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past and future. Oecologia 114, 441–454.[ISI]
Courtillot V.1999. Evolutionary catastrophes. The science of mass extinction. Cambridge University Press.
Crane PR, Friis EM, Pedersen KR.1995. The origin and early diversification of angiosperms. Nature 374, 27–33.
Ehleringer JR, Monson RK.1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review Ecological Systems 24, 411–439.[ISI]
Ehleringer JR, Cerling TE, Helliker BR.1997. C4 Photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285–299.[ISI]
Farquhar GD, Caemmerer von S, Berry JA.1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.[ISI]
Forrester ML, Krotkov G, Nelson CD.1966. Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. 1. Soybean. Plant Physiology 41, 421–427.
Gale J.1974. Oxygen control of reproductive growth. Possible mediation via dark respiration. Journal Experimental Botany 25, 987–989.
Hallam A.1987. End-Cretaceous mass extinction event: argument for terrestrial causation. Science 238, 1237–1242.
Hallam A, Wignall PB.1997. Mass extinctions and their aftermath. Oxford UK: Oxford University Press.
Johnson KR.1993. Extinction at antipodes. Nature 366, 511–512.
Johnson KR, Hickey LJ.1990. Mega floral change across the Cretaceous/Tertiary boundary in the northern Great Plains and Rocky mountains, USA. Geological Society of America 247, 433–444.
Jordan DB, Ogren WL.1981. Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature 291, 513–515.
Kingston JD, Marino BD, Hill A.1994. Isotopic evidence for neogene hominid paleoenvironments in the Kenya Rift Valley. Science 264, 955–959.
Kromer S.1995. Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46, 45–70.[ISI]
Kuypers MMM, Pancost RD, Damste JSS.1999. A large and abrupt fall in atmospheric CO2 concentration during Cretaceous times. Nature 399, 342–345.
Lasaga AC, Berner RA, Garrells RM.1985. An improved geochemical model of atmospheric CO2 fluctuations over the past 100 million years. Geophysical Monographs 32, 397–411.
Leegood RC, Walker DA.1982. Regulation of fructose-1– 6-biphosphate activity in leaves. Planta 156, 449–456.
Macleod N, Keller G (eds).1996. Cretaceous-Tertiary mass extinctions. Norton U.K.
Macleod N, Rawson PF, Forey PL et al.1997. The Cretaceous-Tertiary biotic transition. Journal of the Geological Society, London 154, 265–292.
Rachmilevitch S, Reuveni J, Pearcy RW, Gale J.1999. A high level of atmospheric oxygen, as occurred toward the end of the Cretaceous period, increases leaf diffusion conductance. Journal of Experimental Botany 50, 869–872.
Reuveni J, Gale J.1985. The effect of high levels of carbon-dioxide on the dark respiration and growth of Medicago sativum. Plant, Cell and Environment 8, 623–628.
Sage RW, Monson RK (eds).1998. C4 plant biology. Academic Press.
Sloan RE, Rigby Jr JK, Van Valen LM, Gabriel D.1986. Gradual dinosaur extinction and simultaneous ungulate radiation in the Hill Creek formation. Science 232, 629–633.
Sweet AR, Braman DR, Lerbekmo JF.1999. Palynofloral response to K/T boundary events: a transitory interruption within a dynamic system. Geological Society of America Special Paper 247, 457–469.
Venkatesen TR, Pande K, Gopolan K.1993. Did Decan Volcanism predate the K/T transition? Earth and Planetary Science Letters 119, 181–189.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||