!The Woods Hole Research Center; 13 Church Street, P.O. Box 296, Woods Hole, MA 02543, U.S.A.
2 University of Hawaii, Department of Oceanography, 1000 Pope Rd., MSB525, Honolulu,
Hl96822, U.S.A.
3 Northern Foresty Center; 5320-122 Street, Edmonton, Alberta T6H 355, Canada
4100 Ecology Building, University of Minnesota, 1987 Upper Buford Circle, St. Paul, MN 55108,
Abstract. A positive correlation exists between temperature and atmospheric concentrations of carbon dioxide and methane over the last 220,000 years of glacial history, including two glacial and three
interglacial periods. A similar correlation exists for the Little Ice Age and for contemporary data.
Although the dominant processes responsible may be different over the three time periods, a warming
trend, once established, appears to be consistently reinforced through the further accumulation of
heat-trapping gases in the atmosphere; a cooling trend is reinforced by a reduction in the release of
heat-trapping gases. Over relatively short periods of years to decades, the correspondence between
temperature and greenhouse gas concentrations may be due largely to changes in the metabolism
of terrestrial ecosystems, whose respiration, including microbial respiration in soils, responds more
sensitively, and with a greater total effect, to changes in temperature than does gross photosynthesis.
Despite the importance of positive feedbacks and the recent rise in surface temperatures, terrestrial ecosystems seem to have been accumulating carbon over the last decades. The mechanisms
responsible are thought to include increased nitrogen mobilization as a result of human activities,
and two negative feedbacks: C02 fertilization and the warming of the earth, itself, which is thought
to lead to an accumulation of carbon on land through increased mineralization of nutrients and,
as a result, increased plant growth. The relative importance of these mechanisms is unknown, but
collectively they appear to have been more important over the last century than a positive feedback
through warming-enhanced respiration. The recent rate of increase in temperature, however, leads
to concern that we are entering a new phase in climate, one in which the enhanced greenhouse
effect is emerging as the dominant influence on the temperature of the earth. Two observations
support this concern. One is the negative correlation between temperature and global uptake of
carbon by terrestrial ecosystems. The second is the positive correlation between temperature and
the heat-trapping gas content of the atmosphere. While C02 fertilization or nitrogen mobilization
(either directly or through a warming-enhanced mineralization) may partially counter the effects of a
warming-enhanced respiration, the effect of temperature on the metabolism of terrestrial ecosystems
suggests that these processes will not entirely compensate for emissions of carbon resulting directly
from industrial and land-use practices and indirectly from the warming itself. The magnitude of the
positive feedback, releasing additional C02, CH4, and N20, is potentially large enough to affect the
rate of warming significantly.
Climatic Change 40: 495-518, 1998.
© 1998 Kluwer Academic Publishers. Printed in the Netherlam:fs.
1. Introduction
The global climatic system involves primary and secondary causes that influence
global temperature and other climatic factors. The secondary effects are considered 'feedbacks' insofar as they influence the primary effect. In the case of the
warming of the earth, feedbacks are 'positive' if they tend to enhance a warming trend, 'negative' if they diminish the warming. Kellogg (1983) and Lashof
(1989) have explored this topic in detail. Physical feedbacks, including water vapor,
clouds, polar ice, the heat storage of the ocean, and other processes, are usually
included in general circulation models (GCM's). These processes determine how
the earth's physical climate responds to changes in radiative forcing, such as those
caused by variation in solar radiation and concentrations of greenhouse gases (J. T.
Houghton et aI., 1990, 1992, 1996). The wide range of climate sensitivities reported
by different models results from uncertainties in measurement of these physical
In addition to the feedbacks that determine how climate responds to changes in
radiative forcing are feedbacks that modify the radiative forcing itself. For example,
biotic exchanges of greenhouse gases are sensitive to changes in temperature, moisture, and radiation. Such feedbacks are not generally included in GCM's, probably
because GCM's are generally driven by prescribed concentrations of CO2 rather
than by prescribed emissions, and because of the uncertainty regarding the link
between temperature change and terrestrial carbon storage. The biotic feedbacks
are complicated but potentially large. Terrestrial ecosystems exchange more than
100 PgC with the atmosphere annually, about 117 of the total amount of carbon in
the atmosphere. Biotic feedbacks to radiative forcing have the possibility for either
dampening or accelerating a global warming, once begun. Recent reviews of the
topic include the IPCC chapter on terrestrial feedbacks (Melillo et aI., 1996) and
the proceedings of a symposium (Woodwell and Mackenzie, 1995).
The most widely recognized biotic feedback is the enhancement of photosynthesis by elevated levels of CO 2 in air, the so-called carbon dioxide fertilization
effect. It has been incorporated for many years into carbon cycle models on the
assumption that the increased photosynthesis results in increased carbon storage on
land (Keeling, 1973; Keeling et aI., 1989; Allen and Amthor, 1995; Wullschleger et
al., 1995). The issue is complicated by the fact that carbon storage (net ecosystem
production or NEP) is determined by the balance between photosynthesis (gross
production) and total respiration of the ecosystem, including plant, animal, and microbial respiration (Woodwell and Whittaker, 1968; WoodwellI995). Many factors
apart from carbon dioxide affect rates of photosynthesis. Similarly, many factors
influence the respiration of plants, and also affect rates of decay of organic matter,
and hence its storage, in sbils. NEP is determined not only by net primary production (NPP)_but also by rates of respiration of the organisms that feed on plants
and the organisms of decay in soils. The environmental factors affecting rates of
metabolism include the availability of water, nitrogen and other nutrient elements,
sunlight, temperature, the successional status of ecosystems, and disturbances such
as fire, disease, toxins and storms. Over large areas NEP is generally close to zero,
but a greater proportion of plant communities will exhibit slightly positive NEP as
they recover from past disturbances, and a smaller proportion will exhibit negative
NEP immediately following disturbance.
Any of the factors mentioned above may have influences on NEP that are as
great as or greater than the direct effects from changes in the concentration of
carbon dioxide in the atmosphere (Woodwell, 1983, 1989; Houghton, 1995; Wullschleger et al., 1995). In the absence of other changes, a stimulation of photosynthesis due to the increase in carbon dioxide in the atmosphere would be expected
to increase the storage of carbon on land because of the lag between growth and
decay. However, with increasing temperatures this first order relationship may no
longer apply. The major reason is the sensitivity of respiration to temperature: a
warming increases the rate of respiration, including the rate of decay of organic
matter in soils (Woodwell, 1983; Jenkinson et al., 1991; Raich and Schlesinger,
1992; Townsend et al., 1992; Schimel et al., 1994). In addition, the loss of carbon
through enhanced respiration due to disturbance is commonly much more rapid
than the accumulation of carbon through regrowth of the plant populations of
disturbed ecosystems (Kurz et al., 1995; Houghton et aI., 1983). In the case of
a warming, there is a possibility that the warming itself may cause a series of disturbances in terrestrial ecosystems that will speed the warming. If so, what are the
mechanisms involved and how seriously might our current appraisals of the speed
and severity of the warming be in error? Will the warming speed the warming? If
so, for how long and by how much? Insights into these questions may be obtained
from observations of the concentrations of greenhouse gases in the atmosphere and
surface temperature over three time scales: the last glacial cycle, the Little Ice Age,
and the contemporary record.
2. Recent Glacial History: The Record from Ice
The glacial record over the past 220,000 years shows that throughout that period
atmospheric carbon dioxide and methane concentrations have been correlated with
temperature (Bamola et aI., 1987; Lorius et aI., 1988; Raynaud et aI., 1993; Jouzel
et aI., 1993) (Figure 1).
As temperature has risen, so have carbon dioxide and methane concentrations;
as temperature has dropped, carbon dioxide and methane concentrations have also
dropped. Nitrous oxide, for the shorter period for which there are data, has followed
the same pattern (Khalil and Rasmussen, 1989; Leuenberger and Siegenthaler,
1992). Although the trends in -temperature have been reversed several times and
the causes of the reversals are not clear, the pattern is consistent with a positive
feedback once the warming or cooling has begun. Temperature does not discernibly
lead the changes in concentrations of greenhouse gases during warming periods
Figure 1. C02, ClL;, and temperature in the Vostok core (from louzel et aI., 1993).
although it does during the cooling periods. The record for the Vostok core suggests
that a change of 1°C in this period was equivalent to a change of 10-15 ppmvof
carbon dioxide or about 2;PgC in the atmosphere (Table I).
Variations in methane concentrations in the glacial record are similar to those
for carbon dioxide concentrations (Raynaud et al., 1993). Because methane has
very low solubility in seawater, its atmospheric variation is thought to reflect
The relationship between changes in temperature and changes in the carbon dioxide concentration
in the atmosphere over several different periods. Uncertainties in this table are most heavily
focused on the temperature changes in that there is little basis for knowing whether the changes
in temperature associated here with the changes in carbon dioxide concentrations were in fact
global means or local. If the temperature changes recorded in ice cores were local, and if higher
latitudes experience temperature changes greater than the global mean, the estimates of feedback
(PgC/yr) calculated here are conservative
Glacial age
220,000 years
change in
change in
Bamola et al., 1987
Lorius et al., 1988
Raynaud et al., 1993
to present
Jouzel et aI., 1993
Little Ice Age
Etheridge et aI., 1996
Mackenzie and Mackenzie, 1995
Houghton, 1995
Keeling et aI., 1989
a In Houghton's analysis (1995) annual deviation in global temperature was correlated with
annual carbon flux rather than with C02 concentration. The flux varied by 1.5 PgC/yr between
1940 and 1990. The changes in terrestrial carbon per °C were calculated from regressions.
changes in terrestrial metabolism (Woodwell, 1989; Blunier et aI., 1995); and the
observation that the long-term variations in methane and carbon dioxide are similar is one reason why terrestrial ecosystems are implicated as a major cause for
changes in carbon dioxide. Methane is produced principally through anaerobic
decay in wetlands. Production and emission are heavily influenced by the moisture content of soils and peats (Nisbet and Ingham, 1995; Gorham, 1995). Large
quantities of methane also occur as clathrates in coastal oceans. Although this form
of methane is not under biotic control, it is vulnerable to release through warming,
may have been a large source of carbon for the atmosphere in the past, and may be
for the future (MacDonald, 1990).
Raynaud et ai. (1993) have suggested that about 50% of the variation in temperature was controlled by the concentration of trace gases, and that little is known
of the factors determining the trace gas concentrations. Changes in the carbon
content of terrestrial ecosystems might have affected past concentrations of C02,
but reconstructions of the terrestrial distribution of carbon in past climates yield
widely different results (Prentice and Fung, 1990; Adams et aI., 1990; Friedlingstein et aI., 1992; Van Campo et aI., 1993; Prentice et aI., 1993). Estimates show
that terrestrial carbon was lower during the Last Glacial Maximum (LGM) , but
estimates vary between no difference from the present and 1350 PgC less than
the current inventory. This high value seems unlikely because it represents more
than 60% of the total amount of organic carbon held in the soils, detritus, and
vegetation of the earth today (Schimel et aI., 1995). Recent analyses by Bird et aI.
(1994 a,b) based on the I3C content of the pre-industrial and LGM biota, ~uggest
that the range was more reasonably between 310-550 PgC less than at present or,
if the I3C of oceanic carbon at the LGM is not well constrained, 270-720 Pg. A
similar range was given by Sundquist (1993). Crowley (1995), based on new data
on pollen from COHMAP, estimates the change to have ranged between 750 and
1050 PgC less than at present, and notes that the results are generally not consistent
with the marine l3C record. Thus the magnitude of terrestrial carbon in the past
seems poorly known. Nevertheless, no study suggests that carbon was lost from
land during deglaciation. The I3C record suggests that the warming following the
LGM led to an accumulation of carbon on land. The change in quasi-steady-state
conditions between the LGM and the Holocene suggests that over this time frame
of centuries to millennia terrestrial ecosystems provided a negative feedback on
the carbon dioxide-temperature relationship as carbon moved from the atmosphere
into the plants and soils (including peat) of the successional tundra, forests, and
wetlands that developed as the ice retreated from northern lands. The increase in
atmospheric carbon during this period requires that the oceans be a source of at
least 170 PgC, and perhaps as much as 1350 PgC (170 plus the maximum estimate
of the deviation from the current inventory on land). The oceans appear to have
been a major positive feedback on this time scale.
The Vostok and Byrd ice cores from Antarctica record what may have been near
equilibrium conditions, achieved over centuries to millennia. Ice cores from Greenland bring the resolution down to a few decades and show that changes in climate
(Alley et aI., 1993), CH 4 (Blunier et al., 1995), and CO2 (Figge and White, 1995)
were often abrupt, more abrupt than oceanic models can reproduce. The changes
in climate are thought to result from shifts in the thermo-haline circulation of the
Atlantic (Rind et al., 1986; Broecker et al., 1988, 1990; Lehman and Keigwin,
1992; Hughen et al., 1996), but the causes of the shifts are unclear. It is possible
that terrestrial ecosystems played a role in the rapid changes.
3. Temperature and Atmospheric Trace Gases During the Last Few
Hundred Years: 1750-1940
Since the late 1700s atmospheric carbon dioxide levels have increased by nearly
30%, from about 280 to about 360 ppmv (in 1995). If we estimate the total enhanced effect of all heat-trapping gases (except water vapor) as though it were
due to carbon dioxide, the CO2-equivalent levels have risen 40%, from 310 ppmv
one hundred years ago to 430 ppmv in 1992. With this increase in heat-trapping
capacity, the general circulation models predict an average warming of 0.7 to
1.3°C, more than the amount of warming observed (J. T. Houghton et aI., 1996).
When aerosols are added to the models, however, the range of modelled warming
overlaps with and is lower than the warming observed (Houghton et aI., 1996). The
aerosols are formed from S02 released into the troposphere from human activity.
They cool the earth by stimulating the formation of brighter clouds that reflect
solar radiation back to space, and by particulate backscattering of incoming solar
radiation. Clearly, climate is not regulated by the concentration of heat-trapping
gases alone. Another indication is that much of the warming took place prior to the
1940s, before the most substantial increase in atmospheric trace gas concentrations.
One interpretation of the changes in temperature since the late 1800s is that the
early part of the record still represents in part a recovery from the Little Ice Age
of the 15th through mid-19th centuries or later. It should be recalled that recovery
from the last stage of the Wisconsin glaciation has not been continuous and unidirectional. The recovery has involved a series of temperature fluctuations, including
the cool periods of the Younger Dryas and Little Ice Age and the warm intervals
of the Holocene Climatic Optimum and the Medieval Warm Period. Of special
interest here is the observation that during the Little Ice Age, when temperatures
fell, atmospheric carbon dioxide levels also appear to have fallen (Etheridge et aI.,
1996) (Figure 2) (Table I).
It appears that the decline in temperature may have preceded the decline in atmospheric carbon dioxide. The observation is consistent with the data of the Vostok
ice core (Figure 1) which show that during cooling phases, changes in atmospheric
CO2 and Cf4 concentrations lagged changes in temperature. The recovery from the
Little Ice Age, whatever its cause, extended into the latter part of the 19th century
and perhaps into part of the 20th.
4. Contemporary Observations of Temperature and Trace Gases: 1941-1995
Between 1940 and the mid- to late-1970s the observational record shows a small
decrease in temperature (Jones, 1994). This trend has been followed by increasing global temperatures with ten of the warmest years on record in the 1980s
and 1990s. In contrast to most model calculations, the Southern Hemisphere has
warmed more than the Northern Hemisphere, particularly since 1950 (Jones, 1994).
The observations suggest that changes in the temperature of the earth over the
past century and more have been influenced heavily, possibly controlled, by factors other than the accumulation of heat-trapping gases in the atmosphere. Strong
evidence suggests that sulfate aerosols have cooled the northern hemisphere differentially and were the cause of the global cooling from the Mount Pinatubo eruption
(Dutton and Christy, 1992).
> 290
• ••••
~:I HO'' ' ':", EPO,'"
,---+-- _+__ , __~
Figure 2. C02 and temperature during the Little Ice Age (from Etheridge et aI., 1996, Mackenzie
and Mackenzie, 1995).
The cause of the global cooling of about 0.1 °C, beginning in 1940 and extending through the mid-1970's, is uncertain. Several mechanisms have been suggested
including decreased solar activity, increased stratospheric volcanic dust and sulfate
aerosol in the high atmosphere and, most recently, increased tropospheric sulfate
aerosol, particularly in the Northern Hemisphere, derived from anthropogenic S02
emissions (Charlson, 1995). Whatever the actual mechanism, the effect of greenhouse gases on temperature was largely masked by other factors for the period
1940 to the mid-1970's. Except for the brief period 1935-1945 heat-trapping gases
continued to accumulate in the atmosphere (Etheridge et al., 1996). The coincidence between the cooling and the brief stabilization of concentration around 1940
is, perhaps, significant.
Contemporary data over the last 35 years or so (Keeling et aI., 1989; Kuo et
aI., 1990; Marston et al., 1991) show a positive correlation between temperature
and CO2 concentrations, with temperature generally leading changes in the C02
concentrations by 6 months"to a year (Figure 3).
The data of Keeling et al. (1989) suggest that a change of approximately 3
ppmv in carbon dioxide concentration occurs per °C change in temperature, equal
to about 6 PgC in the atmosphere (Table I). The pattern is consistent with a release
o .,
Figure 3. Residual concentrations of C02 (fossil fuel, mean oceanic uptake, and seasonal variations
removed) and annual deviations in mean global surface temperature (from Keeling et a!., 1989 and
supplemental data from Keeling and Whorf).
(or reduced absorption) of carbon dioxide by surface water of the ocean in response
to warming, with a release from land through increased rates of respiration of
plants and increased rates of decay of organic matter in soils with warming, and
with changes in net ecosystem production (NEP) on land in response to moisture
availability related to temperature (Keeling et al., 1989, 1996).
Mean global warming over two decades, 1970-1990, was about 0.2 °C/decade
before the eruption of Mount Pinatubo in June and July 1991 resulted in a brief
period of surface cooling. The volcanic dust and sulfur aerosols reduced the temperature of the earth by approximately 0.5°C, and the rate of accumulation of
carbon dioxide in the atmosphere declined abruptly as well. As the atmosphere
has cleared, the warming trend of the 80's appears to have been re-established in
the period 1993 to 1997.
The growth rates of C~ also decreased dramatically after the Mount Pinatubo
eruption from an average rate of growth of 10.6 ppb yc 1 over the period 19831993, to 5.0 and 3.6 ppb yr- 1 in 1992 and 1993, respectively (Bakwin et al., 1994).
Similarly the growth rate of N 20 decreased from about 1 ppb yr- 1 in 1991 to 0.5
ppb yc 1 in the years 1992 and 1993 (Thompson et aI., 1994). Year-to-year changes
in interhemispheric transport and in equatorial upwelling linked to ENSO events
may have contributed to the changes in growth rates (Bakwin et al., 1994), but the
patterns are consistent with the premise that the production of these biogenic gases
is temperature sensitive (see also Bekki and Law, 1997).
Braswell et al. (1997) recently reported a lagged negative correlation between
global monthly temperature and growth rate in atmospheric C02, the reverse of
the correlation presented here between temperature and C02 concentrations (Figure 3). Their analysis pertainedio years 1982~1991; for temperature data they used
temperature anomalies from the satellite-borne Microwave Sounding Unit (MSU)
(Spencer et al., 1990). These temperature data pertain to the lower troposphere
rather than to the surface and may contain spurious trends (Hurrell and Trenberth,
1997), but assuming they are a reasonable surrogate for surface temperature, the
analysis found that warm years were followed 2 years later with reduced rates of
growth in atmospheric CO2 . That is, warm years apparently led to an increased
terrestrial uptake. Interestingly, their analysis also showed increased rates of CO2
growth (reduced terrestrial uptake) 1-6 months and 6-8 years after anomalously
warm months (their Figure la). These positive correlations are similar to those
reported here (Figure 3 with a 6-month lag and Figure 4 with a 7-year lag, respectively). Braswell et al. addressed only the 2-yr lagged negative correlation. Had
they considered the shorter- or longer-term responses, they might have come to
conclusions similar to those advanced here.
5. The 'Missing Carbon' Problem
The well known difficulties in predicting climatic warming are confounded by
uncertainties in defining the global carbon budget. In the analyses outlined here we
emphasize the potential of terrestrial ecosystems for releasing significant additional
carbon into the atmosphere in response to a rapid warming. At present, however,
the major difficulty in defining the global budget appears to lie in finding, not new
sources of carbon for the atmosphere, but new sinks, regions that are absorbing the
carbon already known to be being released to the atmosphere. Analyses based on
oceanic models and data over the decade of the 1980s suggest that net terrestrial
uptake averaged close to 2 PgC/yr (northern forests + residual sink in Equation (1»
(from Schimel et aI., 1995)
(1 )
The emissions of carbon from combustion of fossil fuels (and production of
cement) are thought to have averaged about 5.5(±0.5) PgC/yr during the 1980s.
The net release from deforestation, reforestation, and other changes in land use,
globally, is estimated to have averaged about 1.6(±0.7)/yr (Houghton, 1995). This
estimate does not include a stimulation of carbon storage on land caused by CO2 or
nitrogen fertilization. It is based only on changes in land use (clearing, cultivation,
and abandonment of agricultural lands and harvest of wood). Rates of natural disturbance were assumed to have remained unchanged, and ecosystems undisturbed
by human activity were assumed to be balanced with respect to carbon (NEP = 0).
The net release of 1.6 PgC/yr was comprised of a net release of 1.6(±0.5) PgC/yr
from the tropics and a net-llux of 0(±0.5) PgC/yr from the temperate and boreal
zones (Houghton, 1995). In contrast, direct measurements of forest growth based
on data from forest inventories in northern temperate and boreal zones (Kauppi
et al., 1992; Birdsey et al., 1993; Kolchugina and Vinson, 1993; Apps and Kurz,
1994; Turner et aI., 1995; Shvidenko and Nilsson, 1997) show a net accumulation
of 0.6 PgC/yr in those regions (Houghton, in press). Slightly higher sinks (0.8 and
0.9 PgC/yr) were calculated earlier by Dixon et al. (1994) and Houghton (1996b),
respectively, from earlier inventories. This accumulation of carbon in northern midlatitude forests is in excess of the accumulation calculated from regrowth of forests
following earlier harvests (land-use change) (0.0 PgC/yr). The additional uptake of
0.6 PgC/yr may be the result of earlier disturbances such as fires in the last century
or the stimulation of plant growth due to CO 2 or N fertilization not considered in
the analyses based on land-use change. The accumulations are consistent with the
uptake of CO2 observed in the Harvard forest in central Massachusetts (Wofsy et
aI., 1993; Goulden et aI., 1996).
If a similar sink of approximately 0.6 PgC/yr, or more, were to exist in tropical
forests as it apparently does in temperate zone forests, the global carbon equation
might be balanced. Unfortunately, few forest inventories have been carried out in
tropical forests, so an uptake there is difficult to determine directly. However, measurement of CO2 flux over 55 days in both dry and wet seasons in an Amazonian
forest showed a net uptake of 1.0 MgC/ha/yr (Grace et al., 1995), equivalent to
0.56 PgC/yr if the uptake is assumed to apply to the entire Amazonian region.
The total average release of carbon to the atmosphere in the 1980's was thus
thought to include 5.5 PgC/yr from fossil fuels and 1.0 PgC/yr from terrestrial
ecosystems (1.6 PgC/yr from land-use change and -0.6 PgC/yr in northern midlatitude forests, causes unknown). Some of the carbon released into the atmosphere
accumulates there. Between 1980 and 1991 the accumulation ranged between
about 5 and 2 PgC annually and averaged about 3.2 PgC. The difference between
the 6.5 Pg released, plus any further release from the warming itself, and the
amount accumulating in the atmosphere, would be expected to be the amount
absorbed into the oceans, more than 3.3 Pgc. The difficulty is that the amount
accumulating in the oceans, as estimated by several techniques, seems to be limited
to about 2.0 ± 0.8 Pg (Schimel et al., 1995). The difference, 1.3(±1.1) PgC/yr, has
been called 'missing carbon'.
The possibilities for explaining the imbalance are limited. In fact, several analyses based on atmospheric data and models rather than on models of oceanic uptake appear to require an even larger terrestrial sink. Tans et ai. (1990) used rates
of emission of carbon from fossil fuels, the observed latitudinal gradient in atmospheric CO2, the differences in CO2 partial pressure between the ocean and the
atmosphere, and a model of atmospheric transport to estimate the role of terrestrial
ecosystems in net carbon exchange. Their conclusion was that lands in the northern
middle latitudes may have been taking up as much as 3.4 PgC/yr during the interval
1981 to 1987. The magnitude of northern uptake was dependent on the magnitude
of a tropical source. More recently Ciais et al. (1995), on the basis of isotopic
variations in atmospheric C02, have shown that northern lands were taking up as
much as 3.5 PgC in 1992. The greater terrestrial uptake found by these atmospheric
deconvolutions, in comparison to oceanic analyses, is largely explained by the
fact that the atmospheric analyses determine the flux of carbon to or from the
atmosphere, while the oceanic analyses determine the net change in carbon storage.
If one considers that there is a non-atmospheric (riverine) flux that has transported
carbon from land to the sea since preindustrial times, the two approaches are reconciled (Sarmiento and Sundquist, 1992; Tans et aI., 1995). The overall appraisal
of oceanic absorption and transport of carbon seems reasonably well established,
although not at all beyond the need for continued analyses. Besides the analyses already discussed, analyses of variations in atmospheric oxygen (Battle et aI.,
1996; Bender et al., 1996; R. F. Keeling et al., 1996) and in oceanic l3C (Quay et
al., 1992; Tans et al., 1993; Heimann and Maier-Reimer, 1996) are consistent in
defining a significant terrestrial sink for carbon. Although the absorption of carbon
by the ocean varies significantly year by year in response to temperature and other
factors (Francey et al., 1995; Keeling et al., 1995), all of these analyses based
on atmospheric and oceanic data point to terrestrial ecosystems as accumulating
An additional flux from the land into the coastal oceans has not been considered in these analyses. Land-use practices over the past century have increased the
transport of fixed carbon through streams into the coastal oceans. This increase in
the flux may approach 0.4 PgC/yr according to Wollast and Mackenzie (1989). Its
importance depends on the extent to which any such flux results in the long-term
burial of carbon in sediments. A substantial fraction of the riverine carbon flux is
probably oxidized directly and released to the atmosphere.
Three other mechanisms are advanced as having the potential for 'explaining'
the current imbalance in the global carbon cycle: the fertilization effect of increased
carbon dioxide in the atmosphere (Wullschleger et aI., 1995), nitrogen mobilization
(Garrels et aI., 1975, Galloway et aI., 1995), and variations in temperature and
moisture (Dai and Fung, 1993). Schindler and Bayley (1993) and Galloway et ai.
(1995) have presented analyses that suggest that enough nitrogen is being mobilized by human activities in the northern hemisphere to account on a stoichiometric
basis for an additional carbon storage of 1-2 Pg annually in the mid-latitudes. This
possibility, taken with the conclusions of physiological ecologists (Wullschleger
et al., 1995) and other modelling efforts such as those of Post et ai. (1985, 1992),
provides a basis for a significant increase in carbon storage on land but does not
reverse or negate the overall correlation between carbon dioxide and temperature.
Moreover, other fates of mineral nitrogen, such as immobilization by microbial
biomass and loss via leaching and denitrification, or other limiting factors may
prevent realization of the full potential of the increased carbon storage in plant
biomass from the enhanced mineralization of nitrogen (Davidson, 1995).
The historic pattern of the missing carbon sink offers clues about the relative
importance of the processe$ responsible, in particular the net effect of temperature.
The missing sink is the difference between the net flux of carbon from terrestrial
ecosystems (obtained by inverse calculations with ocean models) (Siegenthaler
and Oeschger, 1987; Keeling et al., 1989; Sarmiento et al., 1992) and the flux
attributable to land-use change (Houghton, 1995) (Figure 4).
The difference (missing sink) was approximately zero before 1920, suggesting
that changes in land use accounted for the net flux of carbon to the atmosphere. After 1920, however, the difference between the net flux and the flux due to changes in
land use has generally increased, indicating an annually increasing sink for carbon
on land. In the mid- to late 1970s the sink diminished.
This analysis suggests that the warming of the 1980's coincided with a reduced
uptake (or an enhanced release) of carbon on land, while the earlier, more gradual
warming before 1940 did not. Before 1940 temperature had no apparent relationship to interannual variation in terrestrial carbon storage. Since 1940, however, the
accumulation of carbon in terrestrial ecosystems seems to have been negatively
correlated with global temperature; that is, a warming has accompanied a release
of carbon from land. The correlation results largely from the cooling trend between
1940 and 1975 and the warming from 1975 to 1990. The changes in temperature
precede the terrestrial flux by about 7 years. The correlation shows a 3.4 to 6.4
PgC release (or reduced uptake) per °C (Houghton, 1995) (see Table I). Although
temperature seems to account for much of the variability in the missing carbon
since 1940 (Houghton, 1995), temperature does not account for the background
sink that has prevailed since 1920 or so, or for the apparent lack of change in
terrestrial carbon storage as the earth warmed between about 1890 and 1940. Several mechanisms have obviously been working together. The net effect to date
appears to have been an annual accumulation of carbon on land, a missing sink.
The danger is that increased rates of warming will alter the relative importance
of the processes. The current sink appears to be diminishing and may ultimately
become an unanticipated further source. The correlation between temperature and
terrestrial carbon emissions is growing in strength as the heat-trapping gas content
of the atmosphere increases.
The problem of the 'missing' carbon remains. The possibilities are: analyses
of changes in land-cover overestimate the release of carbon, measurements of
carbon accumulation in forests and soils are incomplete or systematically low,
the terrestrial sink is distributed widely over the earth in plants and soils and is
undetectable, or only a portion of the missing sink is on land. While detection
of a 2 PgC/yr increase in the carbon content of the vegetation of the earth (700
PgC) (Woodwell et aI., 1995) would be difficult, the cumulative imbalance since
1920 represents 50-70% of the current forest biomass in temperate zone forests.
Such a large accumulation in temperate zone forests should be observed, and the
implication is that much of the residual terrestrial sink (Equation (1» must be in
tropical ecosystems (Enting et aI., 1995; Grace et aI., 1995; R. F. Keeling et aI.,
1996), or in soil as well as biol]l<lsS (Bird et al., 1996).
Resolution of the global carbon balance is important because some of the mechanisms for carbon accumulation on land can be expected to continue to be effective
while others may not. If CO 2 fertilization has been responsible for an accumula-
·300.0 (')
- - - Deviation in global mean air temperature (0C)
Residual flux of carbon (PgC/yr)
• • • Atmospheric CO2 concentration (reverse scale) (ppmv)
Figure 4. The residual, or 'missing', flux of carbon (net terrestrial flux minus flux from changes in land use) between terrestrial ecosystems and the
atmosphere (revised from Houghton, 1995) (negative values indicate an accumulation of carbon on land); annual deviations in mean global surface
temperature; and atmospheric concentrations of C02 (inverse scale).
tion of carbon on land, for example, the process may be expected to continue,
even to increase, the annual storage of carbon in proportion to increases in atmospheric CO2 concentrations. Alternatively, if today's carbon cycle is balanced
by some temporarily favorable combination of precipitation and temperature (Dai
and Fung, 1993), or the fertilization effect is reduced in the future, concentrations
of atmospheric CO 2 will be higher than projected by a model that assumes current
and future terrestrial storage to be linked to atmospheric CO 2 .
6. How Large a Biotic Feedback?
The recent rate of increase in temperature leads to concern that we are entering a
new phase in climate, one in which the enhanced greenhouse effect is emerging as
the dominant influence on the temperature of the earth. The question of the amount
of carbon that might be mobilized as carbon dioxide and methane is the key to the
scale of the net feedback. The contemporary correlation between temperature and
CO2 concentrations includes both oceanic (largely abiotic) and terrestrial (largely
biotic) feedbacks. The accumulation of dissolved CO2 in the surface of the oceans
reduces its further capacity for absorbing carbon. Similarly, warming the surface
waters also reduces its retention of CO 2 • Both processes tend to accentuate the
accumulation of CO2 in the atmosphere as the earth warms. Consideration of terrestrial metabolic processes also suggests a positive feedback between the temperature
and atmospheric carbon through increased respiration. Assuming, conservatively,
that terrestrial processes account for half of the year-to-year variation (Francey et
aI., 1995, Keeling et aI., 1995), biotic feedbacks might release 3 PgC per 1°C rise
in temperature. A similarly conservative value is obtained from the analysis by
Houghton (1995).
A comparison of the correlations between temperature and either CO 2 concentrations or terrestrial carbon flux (Table I) suggests that the greatest feedback
(PgCrC) occurs over centuries, the smallest over years, and feedbacks of intermediate magnitudes over millennia. This comparison raises the issue of the time scale
over which sensitivities of feedbacks to temperature can be applied. For example,
over what time period or for how long might a metabolic release (or reduced uptake) of 3-6 PgC/oC occur? Time is not included in the units, and it is difficult
to extrapolate the relationship to the 2°C (range 1 °c to 3.5 0C) warming of mean
global surface air temperature projected to occur by 2100 by the most recent IPCC
assessment (Houghton et al., 1996). If a single year were, hypothetically, to be
2°C warmer than the years surrounding it, a release of 6-12 PgC from terrestrial
ecosystems might be expected. What if the 2°C higher temperature lasted not 1
year, but 100 years? Would an ilhnual release of 6-12 PgC continue for 100 years,
releasing 600-1200 PgC (current stocks of terrestrial carbon are estimated to be
1500 to 2000 PgC)? Would the annual release decline as the labile portion of soil
organic matter was lost? Or would the total release be only 6-12 PgC, limited to
the first few years of the higher temperature? The same questions apply to the more
gradual, but long-term warming projected by the IPCe. The correlations between
temperature and atmospheric CO 2 or between temperature and terrestrial carbon
flux do not offer an answer to the length of time or the total amount of carbon that
might be released with a long-term warming. The correlation between CO 2 and
temperature for the Little Ice Age suggests that a 2°C warming might result in a
total release of 80 PgC over decades (Table J). The range of possibilities is large.
At the longest scale of centuries to millennia, new equilibria can be expected.
Models of change in vegetation in response to a warming of the earth often, but not
uniformly, predict increased carbon storage in terrestrial ecosystems under future,
warmer climates (Prentice and Fung, 1990; Prentice and Sykes, 1995). The predictions generally assume a new equilibrium climate; the increased storage of carbon
results from an increased area of forest, especially in the far north. These changes
are consistent with the negative terrestrial feedbacks thought to have occurred over
the timeframe of centuries to millennia during the transition from the LGM to the
Will the transition to a new equilibrium occur over years to decades, the time of
human interest? Probably not. First, climate is unlikely to stabilize until well after
emissions of greenhouse gases have been reduced. Furthermore, a change in the
distribution of forests requires that existing forests, adapted to present conditions,
must disappear and be replaced in toto by new forests, complete with stocks of
soil carbon and nutrients and with trees from other regions selected for a climate
and photoperiodic regime that is novel for them. Even if increased storage of carbon can be anticipated in such forests in a new 'equilibrium', it is unlikely that
the pathways by which the earth reaches this state will be marked by significant
negative feedbacks on climate in the next 100 years. Rates of forest development
are too slow to accommodate a change in mean temperature of the earth of a tenth
of a °/decade. Such a change would be equivalent to a change in the climatic zones
of the middle latitudes amounting to 10-15 km/decade, possibly more.
Thus at the intermediate scale of decades to a few centuries, the changes in climate associated with a greenhouse warming may not take place gradually through
mortality and recruitment, but, rather, abruptly and catastrophically, such as with
drought, fire, and disease. The intermediate-scale relationship between temperature
and CO 2 concentrations suggests that large and rapid changes have occurred in the
past (Dansgaard et aI., 1993, Stager and Mayewski, 1997), linked to changes in
oceanic mixing and to terrestrial changes as well. A warming of tenths of a °C
per decade can be expected to outrun the capacity of forest trees to respond in
very few decades (Woodwell, 1983, 1989; Davis and Zabinski, 1992; Solomon and
Cramer, 1993). The effect is a transition from forest to shrublands, grasslands, or
to more severe impoverisJ;unent (Woodwell, 1990). Some of the most conspicuous
examples of impoverishment are to be seen at the forest-steppe, forest-prairie, or
forest-cerrado borders around the world. Such transitions in the structure and pattern of vegetation will be accelerated by increased frequency and intensity of fires
and droughts as warming progresses, by the spread of diseases and pests into new
ranges, as well as by the increased frequency of human disturbance. The transitions
in climate are not transitions to a new stability, but to continuous instability marked
by a progressive, open-ended global warming.
7. Conclusions
The role of terrestrial ecosystems, especially forests, in modulating the atmospheric
• content of heat-trapping gases, including carbon dioxide, methane and nitrous oxide, is obviously large and important in the short term of days to years. During the
1980's and first half of the 1990's the annual increase in atmospheric carbon dioxide varied between 1 PgC and about 5 PgC (Conway et aI., 1994). The modulating
factors are obviously inconstant, the variability is high, and the range is significant
in the context of anthropogenic releases that appear to be 6-8 PgC/yr.
The combination of the glacial record and the contemporary data appears to
set limits on the patterns of responses possible. There is little basis for the assumption that the changes inherent in a greenhouse-gas driven warming will stop
the warming through accelerated storage of carbon in forests and other terrestrial
ecosystems. Despite the negative feedback of C02 fertilization, the effect of N
mobilization, and recovery from past land-use, all of which may be causing an
accumulation of C on land at present, CO2 in the atmosphere is still increasing.
Evidence provided by the Antarctic and Greenland ice cores suggests that the increase in atmospheric CO2 will act as a positive feedback on climate. The data seem
to limit the overall response of temperature and trace gases to a positive feedback
in which a warming, however caused, results in the further accumulation of carbon
dioxide and methane (and probably nitrous oxide) in the atmosphere. The net effect
must be a further contribution to the warming.
Support for this concern comes from the record of temperature and carbon
dioxide anomalies following the Mt. Pinatubo eruption in June and July, 1991.
Such triggering events as the Mt. Pinatubo eruption may have caused the abrupt
reversals of climatic trends observed in records such as those of the Vostok and
Greenland cores. We believe that the concentrations of the heat-trapping gases,
including especially carbon dioxide, have reached the point where their influence,
despite the feedback effect of the drop in temperature due to Pinatubo, will remain large as the atmosphere clears, and that temperature globally will return to
its upward trend. The temperature and carbon dioxide anomaly records for 1993
through 1997 already show evidence for a return to the pre-Pinatubo trends. The
emerging dominance of the heat-trapping gases is especially important because of
the positive feedback now recognized as characteristic of the climatic changes of
the past. The feedback has always existed, but when the effect of temperature was
dominated by other factors, such as dust in the upper atmosphere, the influence
of the heat-trapping gases was not strong enough to dominate in modulating tem-
perature globally. Now, if these gases are emerging as the dominant influence, the
importance of the feedback will become conspicuous and the potential exists for a
far more rapid and significant excursion of global temperature.
The most serious questions have to do with the potential for surprises (Broecker,
1987), especially surprises that lead to positive feedbacks. If, for instance, warming
causes a sufficient decline in the water-table of northern peatlands, particularly
toward their southern boundary, subterranean fires could speed the oxidation of
the peat in the vast, remote peatlands of Canada and Russia (Gorham, 1995). Alternatively, if water tables remain high, for instance through permafrost melting
at high latitudes as temperature increases (Halsey et al., 1995; Zoltai, 1993), the
peatlands might shift toward the production of methane at high rates. The issue is
the more serious because the positive feedbacks are coupled directly to some of
the most difficult human problems, such as the growth of the human population
and the expansion of demands for food, fiber, land and energy. These needs are
filled through use of fossil fuel and through changes in land use that involve deforestation. Deforestation not only releases carbon to the atmosphere; it also reduces
those negative feedbacks dependent on terrestrial carbon accumulation. Urgency is
attached to efforts to reduce the risks. The biotic feedback issue, critical as it is, has
been commonly assumed to reduce the accumulation of heat trapping gases in the
atmosphere, not to amplify the trend. The assumption is serious in that the margin
of safety in allowing a warming to proceed may be substantially less than has been
widely believed.
This paper benefited from ideas discussed at an IPCC-sponsored workshop in
Woods Hole, October 1992. The authors acknowledge the contributions of the
participants. Earlier versions of the manuscript were improved with suggestions offered by Colin Prentice, Richard Birdsey, and several anonymous reviewers whose
efforts are much appreciated.
The authors are pleased to have had support from various sources over several
years for work leading to this paper. Support has included grants from the A. W.
Mellon Foundation, the Jessie Smith Noyes Foundation, the W. Alton Jones Foundation, and various grants from the National Science Foundation, the Department
of Energy, the National Aeronautics and Space Administration, and the Environmental Protection Agency. The work has been supported as well by the Woods
Hole Research Center.
The University of Hawaii, School of Ocean and Earth Science and Technology,
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(Received 5 December, 1996; in revised form 9 February, 1998)

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