root production and mortality under elevated atmospheric carbon dioxide

Plant and Soil 187: 299-306, 1996. 299 © 1996 KluwerAcademic Publishers. Printed in the Netherlands.

Root production and mortality under elevated atmospheric carbon dioxide

A.H. F i t t e r 1, G .K . S e l f I , J. W o l f e n d e n 2, M.M.I . van V u u ren 3, T.K. B r o w n l, L. W i l l i a m s o n 1,

J .D. G r a v e s I and D. R o b i n s o n 4 I Department of Biology, University of York, PO Box 373, York Y01 5YW,, UK, 21nstitute of Environmental and Biological Sciences, Lancaster University, Lancaster LA1 4YQ, UK, 3Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, UK and 4Scottish Crop Research Institute, lnvergowrie, Dundee DD2 5DA, UK

Received 29 November 1995. Accepted in revised form 10 May 1996

Key words: carbon cycle, carbon dioxide, minirhizotron, mortality, root demography, turnover

Abstract

An essential component of an understanding of carbon flux is the quantification of movement through the root carbon pool. Although estimates have been made using radiocarbon, the use of minirhizotrons provides a direct measurement of rates of root birth and death. We have measured root demographic parameters under a semi-natural grassland and for wheat. The grassland was studied along a natural altitudinal gradient in northern England, and similar turf from the site was grown in elevated CO2 in solardomes. Root biomass was enhanced under elevated CO2. Root birth and death rates were both increased to a similar extent in elevated CO2, so that the throughput of carbon was greater than in ambient CO2, but root half-lives were shorter under elevated CO2 only under a JuncuslNardus sward on a peaty gley soil, and not under a Festuca turf on a brown earth soil. In a separate experiment, wheat also responded to elevated CO2 by increased root production, and there was a marked shift towards surface rooting: root development at a depth of 80-85 cm was both reduced and delayed. In conjunction with published results for trees, these data suggest that the impact of elevated CO2 will be system-dependent, affecting the spatio-temporal pattern of root growth in some ecosystems and the rate of turnover in others. Turrnover is also sensitive to temperature, soil fertility and other environmental variables, all of which are likely to change in tandem with atmospheric CO2 concentrations. Differences in turnover and time and location of rhizodeposition may have a large effect on rates of carbon cycling.

Introduction

Globally, over half of net production is transferred below ground to root systems (Fogel, 1985), and assessments of the fate of the anthropogenic carbon released in recent years have concluded that the untraced component is almost certainly in soils (Gif- ford, 1994; Taylor and Lloyd, 1992). If soils are the "missing sink", then the route that carbon follows into it is likely to be dominated by transfer to roots. To predict the changes that may occur in the global carbon cycle as climate changes, therefore, it is essential that we can quantify the rates at which carbon moves to roots, essentially a problem of allocation, and from

roots to soil, which is a problem of the dynamics of root systems.

When plants are grown in elevated atmospheric carbon dioxide concentrations they normally grow faster and, except under conditions where nutrients or water are nonlimiting (Stulen and den Hertog, 1993), frequently allocate relatively more carbon to belowground structures (Rogers, 1996). Neither response is universal: for example, Ferris and Taylor (1994) found root fraction to be unaffected in four grassland herbs, whereas Hunt et al. (1995) recorded increases in four grasses. The details of this response have been the subject of much debate (e.g. Loehle, 1995), and Baxter et al. (1994) have pointed out that measurements of biomass can confound ontogeny with treat-

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ment effects: they showed that the allometric coefficient remained unchanged in two grass species that displayed a highly signifcant reduction in leaf fraction in response to elevated CO2: Allocation is, in any case, only one of the variables that determines the rate of carbon cycling. Equally critical is the rate at which carbon passes through the root pool and is released either directly as carbon dioxide by respiration or con- tributes to the soil organic matter pool. It is insufficient to measure the size of the root carbon pool; its inputs and outputs must also be quantified.

Even where growth in elevated CO2 results in increased belowground biomass, it cannot be assumed that this represents a continuing increase in input to the belowground carbon pools. In most experiments, plants are transferred directly from ambient to elevated CO2 concentrations or grown from seed at elevated concentrations. This may result in an ontogenetic shift, in which root fraction (root mass as a fraction of total plant mass) is adjusted; subsequent carbon allocation patterns may not differ between treatments and yet a difference in root fraction will be maintained through- out the experiment. The effect of such a step change on carbon cycling may be much less than if there is a continuing change in allocation.

Unfortunately, it is difficult to measure actual rates of carbon transfer in realistic conditions, although it can be estimated using 14C-labelled CO2. However, both pulse labelling and continuous labelling experiments are required to answer distinct types of question about carbon flow (Meharg, 1994), and the potential of stable isotopes as tracers of carbon movement has not yet been realized fully. Rouhier et al. (1994) grew Castanea sativa seedlings outdoors at 350 and 700 #L L - i CO2 and found that plants grown in elevated CO2 had faster photosynthetic rates and smaller nitrogen contents (not concentrations). However, the treatment had no effect on growth, root fraction or carbon distribution in the plant, suggesting that a real carbon loss had occurred, although this was not supported statisti- cally because of variability of the plant material; they concluded that the additional carbon fixed was large- ly lost through the root system, implying a marked increase in carbon flux through the root carbon pool. Tfieir data also show that 73% of the carbon fixed by 2-year-old trees in a 6-day period wen'. to the root system in a 12-day experiment, though only 60% of plant biomass was belowground. This again emphasises the importance of the belowground component in studies of carbon cycling.

Part of the explanation of the discrepancy between carbon flux and biomass observed by Rouhier et al. (1994) is that root systems have a fast turnover rate: the longevity of individual root members may be as little as 10 d (Garwood, 1957). In consequence, measurements of biomass will always underestimate rates of carbon movement into belowground carbon pools. Studies using the differences between closely-spaced measurements of biomass, especially in forest ecosystems, have suggested that root turnover rates can be as high as 2.0 yr -1 (Burke and Raynal, 1994). Biomass- based methods are, however, complicated by the fact that birth and death of roots are always simultaneous processes and measurements of biomass only record the balance of the two. An alternative approach to quantifying turnover is to measure the rates at which roots are produced and die. These have confirmed that root turnover is a significant component of the plant carbon budget, and several studies have confirmed Garwood's (1957) original observation that roots may be very short-lived (e.g. Krauss and Deacon, 1994; Kosola et al., 1995).

Methodology

The use of rhizotrons

A major inhibition to demographic studies of roots is the difficulty of seeing them in soil, which has been resolved by the use of rhizotrons (McMichael and Tay- lor, 1987), a grand term for a root observation laboratory. A rhizotron is typically a deep, covered trench (> 2 m depth) with glass or perspex sides through which soil and roots can be observed. Apart from the ever- present problem that roots may behave differently at observation windows than in the bulk soil, the disad- vantage of a rhizotron is its scale, lack of portability and consequent problems with replication; the advan- tage is that large numbers of roots can be seen and that the observer can move freely within the trench. Many workers have overcome this problem by using minirhizotrons, which are simply glass tubes inserted into the soil, usually at an angle, down which can be pushed a remote viewing device such as an endo- scope, borescope or video camera. Images of roots growing against the outside of the tube can be recorded on video and processed later in the laboratory. If the tube is appropriately marked, the same image can be repeatedly filmed and true demographic data obtained. The disadvantages of the minirhizotron are that a very

small field of view (often less than 1 cm) is seen and that numerous images are therefore required to obtain a secure sample.

Minirhizotron data comprise counts and/or lengths of roots seen in a frame on a sequence of recording occasions. They are generally ill-suited to the estima- tion of root length density, though numerous workers have developed empirical relationships between the two. Counts from minirhizotron tubes are, however, ideally suited to demographic approaches. A cohort of roots can be followed for a long period and over- all survival calculated, from which a half-life can be obtained, by the regression of log fraction of surviving roots on elapsed time. Periods of high root production and mortality can be identified, and the spatial and temporal distribution of these peaks determined. The statistical analysis of demographic data is well established. Further, roots can be classified in terms of colour and size, allowing estimates of size-specific mortality to be made. ,~

One area where methodologies differ between lab- oratories is the criteria for determining death. We have used root disappearance from the field of view as the criterion, rather than browning or blackening of the root; disappearance is most easily applied to the roots of non-woody plants. One of the striking features of demographic studies of roots is the speed with which roots do disappear. It is a frequent observation that a root that is present and apparently healthy may vanish a week later. As yet, there are few observations avail- able as to the actual cause of disappearance, which may be rapid fungal attack or actual consumption by soil animals. Rarely, a root may become obscured by soil movement, but this is not likely to be a common occurrence since such roots should also re-appear at approximately the same frequency that they disappear.

One method of calculating turnover is from sur- vivorship of cohorts; however, the large seasonal changes in half-life that were apparent from the field studies make it very difficult to achieve appropri- ate comparisons between treatments. An alternative expression, which integrates the annual pattern of production and mortality, is the ratio of the cumulative number of roots produced in the year to the maximum visible at one time; this is analogous to estimating the ratio of total production to peak standing crop.

Studies in grassland soils

We have studied root demography under two contrasting grassland types at the Moor House National Nature

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Reserve (NNR) in northern England, one of the two major study sites for the UK TIGER programme (Ter- restrial Initiative in Global Environmental Research), and the site of an intensive set of investigations cen- tred around the carbon cycle. There is a mosaic of soil types including acid brown earths covered by grassland dominated by Festuca ovina and peaty gleys support- ing Nardus stricta and Juncus squarrosus; we have sampled both these over an altitudinal gradient from 170 m to the summit of Great Dun Fell at 845 m.

Similar turf to that studied in situ was transplanted from Moor House NNR in large blocks (45 x 45 × 25 cm) and embedded in sand in four Solardomes at Lancaster University, where it was maintained for 2 years in climate-controlled conditions (see Wolfenden and Diggle, 1995 for details of the environmental con- trois). Two Solardomes were maintained at ambient CO2 and two at ambient plus 250 #L L - I CO2.

We used minirhizotron tubes 250 mm long × 22 mm external diameter, inserted at an angle of 60 ° to the horizontal. The upper 36 mm of each tube protruded from the tuff, and was painted black to prevent light penetration and sealed initially with a rubber bung and later with a foil cap. Video images of roots visible against the surface of the tube were recorded using an Olympus OES swing-prism borescope with fibre-optic light source, and a Sony PVS1 portable video system. At each sampling occasion, images were taken at 2 cm intervals along the upper surface of the tube. Each image was approximately 7 mm in diameter, with a depth of field into the soil varying from ,-~ 1 mm in the mineral soil layers to occasionally several mm in uncompacted, organic-rich layers.

Images from selected frames were captured as .TIF files onto a PC fitted with a frame grabbing card and linked to a time-base COl'rector. This enabled a series of images in a temporal sequence to be viewed simulta- neously. Roots were identified on screen with a unique code number. For each root, its colour and diameter were estimated (on 5 point scales) and the presence of root hairs and branching was recorded. Branches were given a code that identified the parent root, but branching was only rarely observed. Data on individual roots were recorded on a Paradox 5 database. For this analysis, data were gathered for frame 3 (6 cm depth) in the brown earth soil and frame 5 (10 cm depth) inthe peat soil. There were two tubes per monolith in the solardomes, but we extracted data from only one of these. Field data (not described here) were from sets of 12 tubes in each case.

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Table 1. Regression parameters for linear regressions of cumulative root births and deaths against days elapsed (d) for the limestone monolith data in Figure 2a. The probability values (p) are for a t-test for a difference between treatments within a variable (births or deaths). The F- and R 2 values are for the signifcance and goodness-of-fit of the regression

Regression equation se of b p Fi,20 R 2

Births Ambient 6.32 + 0.036 d 0.0023 < 0.10 245 0.921

Elevated 9.22 + 0.042 d 0.0024 302 0.935

Deaths Ambient 3.44 + 0.035 d 0.0014 < 0.05 619 0.967

Elevated 5.05 + 0.043 d 0.0020 472 0.957

Root turnover was calculated both as the difference in cumulative births and deaths, and from cohort analyses. For the latter, records of the survival of all roots that were first recorded on a given date were extracted from the database, and a regression of the log of the fraction surviving against time calculated. The half- life of the cohort is given by log(2)/b, where b is the regression coefficient.

Studies on wheat

We have examined root demography in wheat grown in controlled conditions at 350 and 700 #L L - l in 1 m long tubes that allow unrestricted root penetration. The tubes were held in a temperature-controlled system at the Scottish Crop Research Institute in Dundee, that maintains realistic root zone temperatures (Gordon et al., 1996). CO2 concentration was crossed with two levels of soil moisture in a factorial design. For the first 40 d of the experiment, soil was watered 4 times a week, but thereafter a "dry" treatment was achieved by bringing soil to field capacity only once a week, so that soil moisture concentration varied down to 15-17% at elevated CO2, and 13-16% under ambient CO2. There were 4 tubes for each moisture/CO2 combination, each with a single wheat plant (Triticum aestivum cv. Tonic).

At weekly intervals the face of the root tube was removed for watering and at this time the entire length was filmed using a standard VHS video recorder. These video films were captured using an Applied Imaging Magiscan image analysis system. Exact overlays of all visible roots were recorded manually, using an acetate attached to the screen, and total lengths of roots determined from these by image analysis. At final harvest, soil was carefully excavated to determine whether the small number of roots that had disappeared from view

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Figure/.Root biomass density (mg cm -3) in soil cores extracted from a species-rich Festuca turf transplanted from Moor House National Nature Reserve into Solantomes at Lancaster University and maintained for two years at ambient or ambient + 250 #L L - l CO2. Biomass is significantly increased by CO2 at depths of 10 and 15 crn.

during the filming were still present; in most cases they were found to have been covered by soil disturbed during watering. There was little or no root mortality.

Root demography under elevated atmospheric carbon dioxide and temperature

Grassland

The effects of elevated atmospheric concentrations of CO2 were studied in the transplanted soil monoliths in the solardomes. In both the brown earth (Festuca) and peaty (JuncuslNardus) monoliths, root biomass was increased after two years in elevated CO2 relative to the ambient controls (Figure 1), although there was no increase in above-ground production (Wolfenden and Diggle, 1995). This increase in root biomass was paralleled by a greater number of root births visible

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Figure 2. Cumulative numbers of root births and deaths per minirbizotron tube under (a) a species-rich Festuca ovina turf on a limestone (brown earth) soil and (b) a species-poor Nardus strictalJuncus squarrosus turf on a peaty gley soil, both transplanted from Moor House National Nature Reserve into Solardomes at Lancaster University and maintained for two years at ambient or ambient + 250 #L L - t CO2. Solid symbols represent births, open symbols deaths; diamonds represent ambient and triangles elevated CO2. "Excess in elevated" represents the difference between (births - deaths) in elevated and ambient CO2; positive values means that roots are accumulating under elevated CO2, and vice versa.

in minirhizotron tubes at all times (Figure 2). In both soils, births and deaths were maintained at higher rates in elevated than ambient CO2, and in the limestone (brown earth) soil the rate of root accumulation and loss can be approximated by linear regression on cumulative births and deaths against time (Table 1). These show that both rates are accelerated equally in elevated CO2; in other words, production increases but there is no net accumulation of roots because turnover increases to match. This effect can be shown by estimating the excess of births over deaths in elevated as compared to ambient CO2: in the limestone soil there is brief accumulation of roots in summer, but a return to equilibrium in the autumn, a pattern maintained over two years (Figure 2a). In the peat soil, a small excess is maintained in elevated CO2 at first, but by the second year there is a deficit (Figure 2b), because turnover increases relatively more in elevated than in ambient CO2, a point confirmed by cohort analyses (Fitter et al., unpubl, data).

Arable crops

As with the grassland, elevated CO2 resulted in an increase in root biomass, though only in the surface layers of the soil. This is a consistent finding with annual species (e.g. cotton: Prior et al., 1994) and probably reflects the ontogeny of the root system. Over the duration of the experiment (116 d) we observed almost

no root mortality in wheat, so that it is not possible to calculate half-lives or estimate survival or longevity. Gibbs and Reid (1992), using a rhizotron under field conditions, found earliest mortality at about 125 d from sowing; even allowing for the slower development that occurs under field conditions, it appears that wheat roots are generally long-lived, most surviving for much longer than those of forage and other wild grasses or of other annual crops, e.g. groundnut Arachis hypogea, in which modal root ages at death were 3-4 weeks (Krauss and Deacon, 1994).

Root production rates of wheat were, however, sensitive to atmospheric CO2 concentration. Between 5 and 8 weeks from germination, wheat grown in elevated CO2 and dry soil had very slow rates of root development at the base of the soil profile (80-85 cm) as compared to those in ambient CO2, while there was enhanced root growth in the surface layers (10-15 cm) between 3-5 weeks (Figure 3); these differences did not occur in wet soil. The reduction in growth at depth may be a consequence of the increased allocation to surface roots. Under realistic climate change scenar- ios, this failure to develop roots at depth could increase the risk of water stress at a critical stage in growth, and from a carbon cycle perspective it means that rhizodeposition will occur primarily in surface soils under elevated CO2, probably increasing the chances of rapid decomposition.

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Figure 3. Wheat Triticum aestivum cv. Tonic root development measured at four depths on plants grown at 350 or 700 #L L-1 CO2 at the Scottish Crop Research Institute, Dundee. Data are averages for four tubes from each treatment, and were obtained from video images of 25 cm 2 of the exposed surface of 1 m long growth tubes (see Gordon et al., 1995 for further details).

Forests

The individual roots of woody plants are much longer- lived than those described so far. Norby (1994) stated that "the mean residence time of live fine roots gen- eraUy is about 1 yea r . . . ", contrasting markedly with the very short half-lives seen under grassland. Howev- er, there are numerous records of short-lived roots on woody plants: median lifespan of summer-produced roots under apple (Malus domestica) was 14-21 days (Head, 1966) and under citrus (Citrus volkameriana and C. jambhiri) was from 16-51 days (Kosola et al., 1995). Pregitzer and co-workers have provided demographic data for tree roots both under elevated CO2 and in relation to a climatic gradient, allowing estimates of t 1/2 of between 107 and 268 d. Under the grassland we studied in the field, only cohorts of roots produced in autumn have half-lives comparable with these, and typical summer cohorts have t 1/2 between 10 and 30 d (Fitter et al., unpubl, data), consistent with earlier estimates by Garwood (1957), and Troughton (1981). Pregitzer et al. (1995) measured survival of roots of Populus x euramericana over a short time-period (41 d): at a low N supply rate, elevated CO2 increased mortality (t 1/2 162 d vs. 268 d under ambient CO2),

but at high N, it had no effect, although t 1/2 was much shorter (107 and 116 d respectively).

D i s c u s s i o n

If there is an increase in the amount of fixed carbon going below ground as atmospheric carbon dioxide concentrations increase, this may have profound effects on the rate of the carbon cycle (Van de Geijn and van Veen, 1993). Because of the uncertainty surround- ing rates of processes in the below-ground component of the carbon cycle, there has been an urgent need to discover whether root systems are simply bigger under elevated CO2 or whether they are qualitatively different. For example, there might be changes in root system architecture (Berntson and Woodward, 1992), in root morphology (Ferris and Taylor, 1994; Rogers et al., 1992), or in the phenology of root system development. The demographic approaches described here are the best way to tackle the last of these and to detect the spatial consequences of the others, though they give little clue to the underlying mechanisms, which are likely to be due to the developmental changes that affect architecture and morphology.

The evidence from the three studies reported here is that root longevity and turnover are affected by elevated atmospheric CO2 in different ways depending upon the system studied. Under Festuca grassland, the abso- lute amount of root is increased after two years exposure to elevated CO2, but turnover (expressed here as the difference in the excess of births over deaths in elevated as opposed to ambient CO2) increases to match that. This increase is only observed on a long- term basis: there is net accumulation of roots each spring because the increase in death rate lags behind the increase in birth rate (Figure 2a). The implication is that the increase in biomass measured at the end of the experiment was either brought about by small and hard- to-detect differences accumulating over a long period, or occurred very early, shortly after first exposure of the turf to the increased CO2 concentration, and that root production thereafter merely maintained this difference. This has important implications for the study of root behaviour under elevated CO2, since many of the observed responses may result from adjustment to a step change in CO2 concentration. This phenomenon can be seen by calculating the ratio of cumulative mortality to cumulative production in the Festuca turf: at equilibrium this ratio should approach 1, but for the first 6 months of the experiment the ratio was below 0.9 in both treatments, indicating that the system is still adjusting to transplantation.

In contrast, there is clear evidence that turnover is relatively faster under a Juncus sward on the peat soil grown at elevated CO2. Here, there is no excess of births over deaths in elevated CO2 after 2 years (Figure 2b). Even so, biomass was greater in this system under elevated CO2, again suggesting that effects may be step responses to the change in CO2 concentration, a point confirmed by the fact that differences in birth rate could be observed from the start of the experiment. Whether this difference reflects differences between the species, the soils or an interaction of these is unknown.

There is also evidence for reduced root longevity and hence increased turnover in Pregitzer et al.'s (1995) poplar experiment, although the effect is smaller than that due to adding nitrogen. Similarly, Festuca turf is much more responsive to temperature than to raised CO2. In some ecosystems, direct effects of CO2 on turnover may be masked by secondary effects of climate change, acting through changes in temperature and N availability.

The wheat study could not detect changes in turnover, since wheat has a quasi-annual root system, most mortality being synchronous towards the end of

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the life-cycle. It did, however, reveal a marked change in the spatial and temporal pattern of root development that could have marked effects on plant performance and on carbon cycling. As shown in other species, wheat root growth was much greater in surface layers, but the novel finding was that root growth was both lesser in quantity and later in time at depths approach- ing 1 m. These changes will alter the time and location of rhizodeposition, which has been suggested as a determinant of carbon storage ability of ecosystems. Nepstad et al. (1994) demonstrated that Amazonian forest soils contain more carbon at depths below 1 m than is present in the above-ground biomass, and Fisher et al. (1994) also found large amounts of organic carbon in deep soil layers (below 40 cm depth) in South American savannahs. In the forest, radiocarbon data suggested that about 10-15% of the carbon at 8 m depth was modern, implying continuous input from roots. If shallow root development is a common phenomenon in elevated CO2, this would increase the rate at which carbon is returned to the atmosphere.

The effects of elevated atmospheric CO2 concentrations on root turnover are, therefore, unsurprisingly complex and probably system-specific. Elevated CO2 on its own will probably increase the size ofthe root carbon pool, and our evidence indicates that there will be a greater carbon flux through root turnover. It is likely that this response will interact with the increased global temperatures that will accompany a CO2-rich atmosphere, which will themselves accelerate turnover. On the other hand, if soils are drier decomposition will be slowed and plant tissues grown under elevated CO2 (including Festuca roots in this study) may have higher C:N ratios and maybe therefore decompose more slowly (Cotrufo et al., 1994).

Both CO2 and temperature will also alter the spatio- temporal pattern of root growth. Evidence presented in this paper shows that wheat root growth occurs pre- dominantly at shallower depths, a phenomenon that has already been observed in other systems. Rhizodeposi- tion of carbon either earlier in the year, when microbial activity is higher and typically resource-limited (e.g. summer rather than autumn), or at shallower depths, is likely to result in a more rapid return of carbon to the atmosphere and reduce the potential for soils to act as a major carbon sink.

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Acknowledgements

The research described here was funded by the Natural Environment Research Council under its TIGER (Ter- restrial Initiative in Global Environmental Research) programme and the Biotechnology and Biological Sci- ences Research Council under the BAGEC (Biologi- cal Adaptations to Global Environmental Change) programme; we are grateful for their support.

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Section ediwr: H Lambers

root production and mortality under elevated atmospheric carbon dioxide

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