Productivity of forests in the Eurosiberian boreal region and their potential to act as a carbon sink -- a synthesis

Productivity of forests in the Eurosiberian borealregion and their potential to act as a carbonsink Ð a synthesis

E . - D . S C H U L Z E , * J . L L O Y D , * F . M . K E L L I H E R , ² C . W I R T H , * C . R E B M A N N , *

B . L UÈ H K E R , * M . M U N D , * A . K N O H L , * I . M . M I L Y U K O V A , ³ W . S C H U L Z E , §

W . Z I E G L E R , ¶ A . B . V A R L A G I N , ³ A . F . S O G A C H E V , ³ R . V A L E N T I N I , * *

S . D O R E , * * S . G R I G O R I E V , ² ² O . K O L L E , * M . I . P A N F Y O R O V , ³

N . T C H E B A K O V A , ³ ³ and N N V Y G O D S K A Y A ³

*Max-Planck Institute for Biogeochemistry, PO Box 100164, 07701 Jena, Germany, ²Manaaki Whenua, Landcare Research,

PO Box 69, Lincoln, New Zealand, ³Institute of Evolution and Ecology, Russian Academy of Sciences, Leninsky Prospect 33,

117071 Moscow, Russia, §Botanisches Institut, University TuÈbingen, Auf der Morgenstelle 1, 72076 TuÈbingen, Germany,

¶Department of Biophysics and chemical Physics, Comenius University, Mlynska Dolina F1, 84215 Bratislava, Slovakia,

**Dept of Forest Science and Environment, University of Tuscia, 01100 Viterbo, Italy, ²²Ecological Travel Centre, Scienti®c

Park, Korp.1, r.127, Moscow State University, 119899 Moscow, Russia, ³³Forest Institute, Siberian branch of the Russian

Academy of Sciences, Akademgorodok, Krasnoyarsk, 660036 Russia

Abstract

Based on review and original data, this synthesis investigates carbon pools and ¯uxes

of Siberian and European forests (600 and 300 million ha, respectively). We examine

the productivity of ecosystems, expressed as positive rate when the amount of carbon

in the ecosystem increases, while (following micrometeorological convention) down-

ward ¯uxes from the atmosphere to the vegetation (NEE = Net Ecosystem Exchange)

are expressed as negative numbers. Productivity parameters are Net Primary Produc-

tivity (NPP=whole plant growth), Net Ecosystem Productivity (NEP = CO2 assimilation

minus ecosystem respiration), and Net Biome Productivity (NBP = NEP minus carbon

losses through disturbances bypassing respiration, e.g. by ®re and logging). Based on

chronosequence studies and national forestry statistics we estimate a low average NPP

for boreal forests in Siberia: 123 gC m±2 y±1. This contrasts with a similar calculation

for Europe which suggests a much higher average NPP of 460 gC m±2 y±1 for the for-

ests there. Despite a smaller area, European forests have a higher total NPP than Si-

beria (1.2±1.6 vs. 0.6±0.9 3 1015 gC region±1 y±1). This arises as a consequence of

differences in growing season length, climate and nutrition.

For a chronosequence of Pinus sylvestris stands studied in central Siberia during

summer, NEE was most negative in a 67-y old stand regenerating after ®re (± 192 mmol

m±2 d±1) which is close to NEE in a cultivated forest of Germany (± 210 mmol m±2 d±1).

Considerable net ecosystem CO2-uptake was also measured in Siberia in 200- and

215-y old stands (NEE:174 and ± 63 mmol m±2 d±1) while NEP of 7- and 13-y old logging

areas were close to the ecosystem compensation point. Two Siberian bogs and a bog in

European Russia were also signi®cant carbon sinks (± 102 to ± 104 mmol m±2 d±1). Inte-

grated over a growing season (June to September) we measured a total growing season

NEE of ± 14 mol m±2 summer±1 (± 168 gC m±2 summer±1) in a 200-y Siberian pine stand

and ± 5 mol m±2 summer±1 (± 60 gC m±2 summer±1) in Siberian and European Russian

bogs. By contrast, over the same period, a spruce forest in European Russia was a car-

bon source to the atmosphere of (NEE: + 7 mol m±2 summer±1 = + 84 gC m±2 summer±1).

Two years after a windthrow in European Russia, with all trees being uplifted and few

successional species, lost 16 mol C m±2 to the atmosphere over a 3-month in summer,

R

Correspondence: E.-D. schulze, fax +49/ 3641 643701, e-mail

[email protected]

Global Change Biology (1999) 5, 703±722

# 1999 Blackwell Science Ltd. 703

compared to the cumulative NEE over a growing season in a German forest of

± 15.5 mol m±2 summer±1 (± 186 gC m±2 summer±1; European ¯ux network annual aver-

aged ± 205 gC m±2 y±1).

Differences in CO2-exchange rates coincided with differences in the Bowen ratio,

with logging areas partitioning most incoming radiation into sensible heat whereas

bogs partitioned most into evaporation (latent heat). Effects of these different surface

energy exchanges on local climate (convective storms and ®res) and comparisons with

the Canadian BOREAS experiment are discussed.

Following a classi®cation of disturbances and their effects on ecosystem carbon

balances, ®re and logging are discussed as the main processes causing carbon losses

that bypass heterotrophic respiration in Siberia. Following two approaches, NBP was

estimated to be only about 13±16 mmol m±2 y±1 for Siberia. It may reach 67 mmol m±2 y±1

in North America, and about 140±400 mmol m±2 y±1 in Scandinavia.

We conclude that ®re speeds up the carbon cycle, but that it results also in long-term

carbon sequestration by charcoal formation. For at least 14 years after logging, regrowth

forests remain net sources of CO2 to the atmosphere. This has important implications

regarding the effects of Siberian forest management on atmospheric concentrations. For

many years after logging has taken place, regrowth forests remain weaker sinks for

atmospheric CO2 than are nearby old-growth forests.

Keywords: boreal forest, Europe, net biome productivity, net ecosystem productivity, net

primary productivity, Siberia

Received 21 July 1998; resubmitted 10 December and accepted 29 December 1998

Introduction

Global carbon mass balance calculations suggest that

about one third of the anthropogenic CO2 emissions are

incorporated into the terrestrial biosphere every year

(Keeling et al. 1996). One widely held view is that a major

terrestrial carbon sink is located in the northern hemi-

sphere (Tans et al. 1990; Ciais et al. 1995), but another

recent model-experiment suggests that continental USA

is a major region for carbon sequestration (Fan et al.

1998). In addition to the temperate region, the boreal

forest is the most widespread vegetation type in the

northern hemisphere. As a consequence of its vast area it

might also contribute signi®cantly to this sink (Melillo

et al. 1995). The total area of Russian Siberia is 13 million

km2 (Shvidenko & Nilsson 1994) which is about 30%

greater than Europe (10 million km2 area including

European Russia, Stanners & Bourdeau 1995) and 12%

greater than boreal North America (11.5 million km2 of

Canada and Alaska). However, with 600 vs. 300 million

ha of forest, Siberia is much more extensively forested

than Europe or boreal North America (500 million ha).

Nevertheless, model predictions are controversial as to

what extent the boreal region could contribute to the

global carbon sink (Ciais et al. 1995, Fan et al. 1998;

Rayner et al. 1999).

Although the boreal region is the largest contiguous

forested area of the world, estimates of its productivity

vary widely. For example, Melillo et al. (1993) estimated

that the global boreal forest has an average net primary

production (NPP) of 228 gC m±2 y±1 (19 mol C m±2 y±1)

which scales across the boreal forest biome to an NPP of

2.9 3 1015 gC y±1. Including the temperate coniferous

forests and boreal woodlands of the northern hemisphere

this number would increase to about 5.1x 1015 gC y±1

which is about 10% of global NPP. However, considering

the large fraction of NPP that returns to the atmosphere

by respiration, logging and ®res (Schimel et al. 1996), it

seems unlikely that the extra-tropical region can be a net

carbon sink of order 2±4 3 1015gC y±1 as suggested by

some authors (Ciais et al. 1995). Moreover, a much

smaller sink there would con®rm the predictions of Fan

et al. (1998) and Rayner et al. (1999).

To more precisely understand the productivity of

representative Siberian forest stands, and to evaluate the

proposed role of these forests as a CO2 sink, three

growing season expeditions into the Siberian region have

been undertaken to date. In addition, long-term mea-

surements were commenced at selected sites in 1998. We

measured NPP and net ecosystem productivity (NEP)

which describes the balance between NPP and hetero-

trophic respiration, and the associated above- and below-

ground carbon pool sizes. The newer concept of net

biome productivity (NBP), including larger scale carbon

losses that bypass heterotrophic respiration such as

harvest or ®re (Schulze & Heimann 1998) is also utilized

in the following analysis. Similar measurements made in

Germany allow for comparisons and quanti®cation of

Eurosiberian forest carbon exchange rates. The following

L704 E . - D . S C H U L Z E et al.

# 1999 Blackwell Science Ltd., Global Change Biology, 5, 703±722

synthesis is based on published material, re-evaluation of

existing data, and previously unpublished data.

Materials and methods

Experimental sites in Siberia and Germany were mono-

typic forest stands and bogs representative of the

regional vegetation (Table 1).

1 Larix gmelinii forest of eastern Siberia near Yakutsk

(60°51¢N, 128°16¢E): Deciduous larch covers about 54% of

the forested area in Siberia (Shvidenko & Nilsson 1994)

growing mainly on loamy soils east of the Yenisey river.

The NEE measurements were made above a 125-y old

stand 160 km south of the city Yakutsk. Biomass and

growth were measured in a chronosequence of 49±380-y

old stands growing on loamy permafrost soil (Schulze

et al. 1995). This site was selected because it is at the

centre of this species distribution outside the range of

forest management. It was described by forest authorities

in Yakutsk as the largest pristine region of Larix forest.

2 Pinus sylvestris forest of Central Siberia near Zotino

(60°44¢N, 89°09¢E): Pine covers 12% of the forest area in

Siberia (Shvidenko & Nilsson 1994), mostly to the west of

the Yenisey river. NEE measurements were carried out in

a range of habitats, including 7- and 13-y old logging

areas, 53- and 215-y old natural regenerations after ®re

and an area dominated by lichens. Biomass and growth

of pine were studied in a chronosequence of stands

ranging from 28- to 450-y on sandy soil without

permafrost (Pergelic Cryochrept, Wirth et al. 1999). This

region was indicated by the Krasnoyarsk Institute of

Forest Research to be typical of pine forests growing on

alluvial sands and, interspaced with bogs. This vegeta-

tion type dominates a region extending from the Ural

Mountains to the Yenisey River. The sites were chosen to

be at the margin between managed and nonmanaged

areas. Long-term ¯ux measurements started in 1998 close

to the site of the FIRESCAN experiment (ManoÈ &

Andreae 1994) at `Bor Island'.

3 Picea abies in the `Central Reserve' at Fyedorovskoye

near Nelidovo, about 300 km NW of Moscow (56°27¢N,

32°55¢E): The 35 000 ha forest reserve is one of the few

closed forests remaining in that region and has therefore

been used for ecosystem studies since the 1960s (see

Karpov 1973; Gravenhorst et al. 1998). In the same forest,

¯ux measurements were carried out not only in a mature

forest growing on peat over clay soil but also over a 2-y

old windthrow area where all trees had been broken or

roots uplifted, and regeneration of early successional

broad-leaved species had begun.

4 Sphagnum bogs of European Russia and west Siberia:

European Russia and west Siberia are characterized by

large Sphagnum bog areas. To provide a comparison to the

forest studies at Fyedorovskoye and Zotino, microme-

teorological ¯ux measurements were made above Sphag-

num bogs close to the forest sites. At Fyedorovskoye,

¯uxes were measured in the centre of a 5-km2 large raised

bog. At Zotino, short-term measurements were carried

out in 1996 on a 2-km2 bog, and long-term ¯uxes were

measured in the centre of a 10-km2 Aapa-type bog.

5 Picea abies of West Europe in a managed forest at the

Waldstein Mountains near Bayreuth, Germany (50°09¢N,

11°52¢E): NEE was measured above a 43-y old stand.

Biomass and growth were measured in a chronose-

quence of 28- to 140-y old stands on loamy soil (Mund

1996). The region has been a central study site for

ecosystem research over many years (Schulze et al. 1989a)

and it is presently contributing to the EUROFLUX and

the CANIF project of the EEC. Both projects indicate that

this site is representative of central European coniferous

forest (Bauer et al. 1996; see also Stanners & Bourdeau

1995). Based on 1996/97 carbon exchange data, this site is

close to the average of all European forest measurement

sites (Euro¯ux Report 1997, Contract ENV4-CT95-0078,

EEC DGXII-D2, Brussels, Belgium).

The eddy covariance technique was used to measure

NEE and the partitioning of available energy into

evaporation and sensible heat ¯uxes (Kelliher et al.

1997, 1998, 1999; Hollinger et al. 1998). Biomass and

R

Table 1 Climate and habitat parameters characterizing the experimental sites

Av. temp. Precipitation

Max tree

Annual July Annual May±Sept. Days height Soil Perma

Site (°C) (°C) (mm) (mm) > 5 °C (m) type frost

Yakutsk ± 10 19 213 150 126 23 silt loam yes

Zotino ± 3.3 18 663 349 147 20 sand no

Fyedorovskoye + 3.6 14 714 320 165 24 peat/clay no

Waldstein + 5.8 15 1100 550 210 28 loam no

P R O D U C T I V I T Y O F F O R E S T S I N T H E E U R O S I B E R I A N B O R E A L R E G I O N 705


growth was determined from selective harvesting of

trees in stands of different age (Schulze et al. 1995; Wirth

et al. 1999) and from tree ring analysis (Mund 1996; Wirth

1996). The soil carbon content was quanti®ed in the same

stands. The content of black carbon was determined by

LuÈ hker (1997) using a modi®ed method of Kuhlbusch &

Crutzen (1995).

We are aware of the problems involved in extrapola-

tions from plot data to regions (see Moore 1996). The

regional estimates of NPP in this study are based on

published forest inventories for Europe (Stanners &

Bourdeau 1995) and Siberia (Shvidenko & Nilsson 1994)

using a wood density of 300 kgdw m±3wood +bark for

Siberia, as measured by Schulze et al. (1995) and Wirth

et al. (1999). This density is lower than the wood density

of 479 kgdw m±3wood used by Shvidenko & Nilsson (1999).

In the regional comparison of NPP, a wood density of 400

kgdw m±3wood was used for European conifers. For

European hardwoods, 500 kg dw m±3wood was used

(KoÈrner et al. 1993). Additional plot level NPP and

biomass data were collected at all study sites, and the

contribution of NPP losses by self-thinning was esti-

mated from this plot level information (Schulze et al.

1995; Mund 1996; Wirth et al. 1999). Our NPP data were

compared with regional estimates by Shvidenko &

Nilsson (1994) to ascertain its representativeness. Root

biomass and ®ne root turnover rate were estimated

following Jackson et al. (1997) and Steele et al. (1997) as

well as Vogt et al. (1996). We considered as many Russian

publications as possible, especially concerning biomass

and productivity measurements (Isaev 1991).

Forest biomass and net primary productivity(NPP)

Pinus sylvestris and Larix spp. cover 68% of the Siberian

forested area (Shvidenko & Nilsson 1994), and Picea and

Pinus spp. 51% of the European forest area (Stanners &

Burdeau 1995). Figure 1 summarizes our biomass mea-

surements for these dominant species (Schulze et al. 1995;

Mund 1996; Vygodskaya et al. 1998; Wirth et al. 1999) and

gives regional estimates for North America (Botkin &

Simpson 1990), west Europe (Stanners & Burdeau 1995),

European Russia and Siberia (Shvidenko & Nilsson

1999).

On mesic sites, Siberian Pinus and Larix accumulate

stemwood biomass at less than half the rate of west

European Picea (Fig. 1), the latter being representative of

a broad range of European tree species (Kramer 1988).

While Picea in Europe obtains an above-ground biomass

of about 21 kgdw m±2 in 100 years, Pinus and Larix of

Siberia reached only 7.5 kgdw m±2 at the same age. Thus,

a 380-y old Pinus stand in Siberia has about the same

biomass as a 50-y old Picea plantation in Europe. In

European Russia, the biomass of Picea and Pinus is

intermediate between that of West Europe and Siberia

(Smirnov 1967; Smirnov & Semenova 1970; Vygodskaya

et al. 1998). On favourable sites Siberian Larix (and Pinus,

unpublished) may accumulate biomass at rates compar-

able to European Russia (Utkin 1965) but stands

deteriorate beyond a certain optimum age. This does

not happen under less favourable conditions where

biomass remains constant or may even increase at a

very low rate irrespective of age. For Pinus sylvestris,

variation in the data expresses the range of habitats

under which this species grows in European Russia: low

productivity Sphagnum bogs to highly productive sites

with a herbaceous understorey.

NPP includes growth above- and below-ground.

However, since growth of tree roots is dif®cult to

measure (due to rapid turnover, soil depth and mycor-

rhizal interaction), above-ground-NPP (ANPP) is fre-

quently the only measurement. From forest inventories it

is possible to approximate ANPP from the volume

L

Fig. 1 Living above-ground biomass in

Siberian Pinus (Wirth et al. 1999) and Larix

(Utkin 1965; Schulze et al. 1995) stands as

compared to West European Picea abies

(Mund 1996) and Russian European Picea

obovata (Vygodskaya et al. 1998) and Pinus

sylvestris (Alekseev 1975). Average levels

of biomass in Europe (Stanners &

Bourdeau 1995), of Siberia (Shvidenko &

Nilsson 1999) and North Ameriaca (Botkin

& Simpson 1990) are also shown.

706 E . - D . S C H U L Z E et al.


growth of stem wood (usually termed as net annual

increment) given in yield tables. However, forest

inventories include only the standing crop of intensively

managed forests, neglecting tree death as a component of

NPP in natural unmanaged forests (Schulze 1982; Lloyd

1999; Shvidenko & Nilsson 1999). As stands develop, tree

death by self-thinning can completely offset growth

under nonmanaged conditions. In managed forests,

natural self-thinning is avoided by harvest and this

wood being exported from the forest is included in the

European inventories (Pretzsch 1996). By contrast, in

unmanaged forests dead trees decompose on site and so

are not included in an inventory (Shvidenko & Nilsson

1999). ANPP thus cannot always be approximated by

dividing standing biomass by stand age.

According to our Siberian plot studies, the amount of

wood lost by self-thinning is slightly more than the wood

increment (Fig. 2). Shvidenko & Nilsson (1999) estimate

that Russian tree mortality (913 3 106 m3 y±1) occurs at

about the same rate as stem-wood growth of the standing

crop (966 3 106 m3 y±1). ANPP for Russia can then be

approximated as the sum of these two rates (1879 3 106

m3 y±1 = 2.5 m3 ha±1 y±1). These data agree well with our

plot studies where ANPP of stem wood (accounting for

concurrent growth and tree mortality) averaged

2.7 m3 ha±2 y±1 (or 41 gC m±2 y±1). Our estimate of ANPP

(wood and litter) of 84 gC m±2 y±1 was very close to the

estimates for Larix in Central Siberia by Kajimoto et al.

(1998: 90 gC m±2 y±1). They are in the range of North

American northern boreal forest stands (124 gC m±2 y±1

in Picea mariana and 110 vs. 51 gC m±2 y±1 in old vs.

young Pinus banksiana; Gower et al. 1997). As suggested

in Fig. 1, the range of ANPP depends on site conditions,

so it is expected to be large in the boreal zone. Clearly,

regional differences in ANPP exist, but the available data

are too sparse for calculation of the associated probable

errors. Despite this uncertainty, ANPP seems to be

higher in (Western and Russian) Europe than in Siberia

by a factor of about 3 (Fig. 2). Due to the differences in

forest area, the difference in growth rate between Europe

and Siberia diminishes to factor < 2 at a regional scale.

The growth of coarse roots can be estimated with

reasonable accuracy from ANPP. Coarse root biomass

has been variously estimated as 40% of above-ground

biomass in Siberian stands (Monserud et al. 1996) down

to 30% in Europe (Jackson et al. 1997) and 22±34% in

European Russia (Karpov 1973). These estimates were

included in Fig. 2 but they do not dramatically change

the NPP comparison between Siberia and Europe.

An estimate of NPP is not complete without ®ne root

growth. Jackson et al. (1997) assume that ®ne roots

turnover occurs once per year, contributing on average

33% to NPP of boreal forests. This agrees well with the

estimates of Steele et al. (1997) for the BOREAS sites in

R

Fig. 2 Comparison of carbon pools and ¯uxes of European and Siberian forests. Wood, wood increment in Siberia calculated with

400 kgdw m±3wood, average of Schulze et al. (1995), Wirth et al. (1999) and Shvidenko & Nilsson (1999); Wrus, Wood increment in Rus-

sia; Wwest, Wood increment in West Europe, calculated with 400 kg dw m±3wood average for conifers (E, N, W-Europe) and 500 kgdw

m±3wood for hardwood in S-Europe (KoÈrner et al. 1993); leaves, based on the measured ratios of needle to wood growth (needle

growth (g m±2 y±1) = 0.11 + 1.08 3 wood growth, r = 0.9). Wood growth includes standing crop+self thinning (Mund 1996; Wirth et al.

1999). Th, thinning and self-thinning calculated from average biomass and loss of stems for Siberia (Wirth et al. 1998). For Europe,

losses by self thinning are assumed to take place only in European Russia. In West European forest, this increment would be har-

vested by thinning and thus part of the wood increment. CR, Coarse roots=0.4 3 wood biomass for Siberia (Monserud et al. 1996),

and 0.3 3 wood biomass for Europe (Jackson et al. 1997). Forest area=597.3 3 106 ha for Siberia (Shvidenko & Nilsson 1999) and

303 3 106 ha for Europe including European Russia (Stanners & Bourdeau 1995).



Canada and of Axelsson & Brackenhielm (1980) for

Sweden. By contrast, a survey of published data (Vogt

et al. 1996) suggests below-ground growth on comparable

soil types is on average 17.5% of NPP in boreal forest and

23.7% of NPP in cold temperate forest (range 13±38% of

NPP). Vogt et al. also warn that ®ne root production may

only weakly be correlated to NPP, because litter nutrient

content is a more important determining variable. Fine

root production following Jackson et al. was 49 and 172

gC m±2 y±1 in Siberia and Europe which would exceed

stem-wood growth by a factor of 2±3. This appears high

since ®ne roots may live longer than 1 years in boreal

zone (Kajimoto et al. 1998). On the other hand, the

estimate of Vogt et al. results in a ®ne root growth of

only 2±55 gC m±2 y±1 for Siberia and Europe which seems

to be too low considering nutrient limitations in Siberia.

A ®ne root biomass (< 1 mm in diameter) of 26 gC m±2

was actually measured at the Waldstein site, 27 to 57 gC

m±2 y±1 in European Russia (Karpov 1973), which would

represent growth assuming a turnover of 1 years (H.

Persson, CANIF project, unpubl.). Thus, depending on

the assumptions made for ®ne root growth, NPP ranges

between 102 and 149 gC m±2 y±1 for Siberia and 401 and

518 gC m±2 y±1 in Europe.

The estimates of NPP for boreal forests are less than

earlier values (Table 2). For the North American boreal

forest, NPP estimates have decreased by around a factor

of 2±3 over time of publication (Moore 1996). In contrast

to our relative low Siberian NPP estimate, our temperate

zone estimate is larger than the previous values. This is

supported by recent growth trends and inventory data

for European forests. Spieker et al. (1996) showed that

NPP of European forests was lower in the past.

While comparing regional NPP of Europe and Siberia

one should be aware that regional estimates contain

other major uncertainties, one of which is forest area. For

instance, the West European forest area (excluding

European Russia) was estimated to be 136.7 million ha

by the European Environmental Agency (Stanners &

Bourdeau 1995), as used in this study, which is close to

149.3 million ha of the FAO forest resource assessment of

1990 (FAO 1990), but 30% lower than the area under

investigation for forest decline (197 million ha: EC-UN/

ECE 1996). Similar uncertainties exist for Siberia, where

the `Forest Fund' (973.2 million ha) includes land which

has been converted into other landuse, and the `Forest

Land' (710 million ha) includes sparse forests, unregen-

erated areas, wetlands and lakes. Only the `Forest Area'

refers to forest in a strict sense. This was estimated to be

605 million ha in 1994 and 597 million ha in 1998

(Shvidenko & Nilsson 1994, 1999).

Climatic and edaphic reasons for the differencesin NPP between Siberia and Europe

There are several reasons for larger NPP in Europe than

in Siberia despite a smaller forest area. The most striking

difference between the two regions is length of the

growing season (MuÈ ller 1982). Siberia typically has only

120±150 days per year with average temperatures greater

than 5 °C. This compares with about 210 days in

Germany (Table 1).

Relative to the European and the North American

boreal forest region, Siberia is colder especially in winter

(mean January temperatures are ± 31 °C vs. ± 21 °C in

North America and ±15 °C in Europe). It is also drier

due to the long distance from temperate oceans and the

rainfall barrier of the Ural Mountains (Miachkova 1983).

The average annual rainfall decreases from west to east

by more than 80% in Siberia (Table 3), which signi®cantly

L

Forest Net Primary Productivity (gC m±2 y±1)

Temperate Boreal

Conifer Deciduous Conifer Deciduous

Total NPP

Melillo et al. (1993) 465 620 238

Potter et al. (1993) 226 315 226 153

Warnant et al. (1994) 419 659 419

Woodward et al. (1995) 300 300 250 200

Ruimy et al. (1996) 331 417 331 417

Denning et al. (1996) 400 300

Lloyd (1999) 336 504 180 228

This study 459 123 123

Stem growth NPP (and thinning)

Shvidenko & Nilsson (1999) 95 36

This study 93 18

Table 2 Estimates of Net Primary

Productivity (NPP) in temperate and

boreal forests

708 E . - D . S C H U L Z E et al.


affects the forest water balance. For the German forest,

tree canopy evaporation typically uses less than half the

summer rainfall but this fraction increases to 70±80% in

European Russia and West Siberia and it actually exceeds

summer rainfall in East Siberia. In East Siberia trees

effectively `mine' soil-water which is provided by the

previous winter's recharge and by thawing of the

permafrost. Drainage to surface-waters occurs mainly

during snow melt (Kelliher et al. 1997). At the central

Siberian site, with no permafrost, the water-holding

capacity of sand is very low (4 mm/0.1 m depth; Kelliher

et al. 1998) but in some cases roots may reach > 3 m soil

depth and thus be adequately supplied with water

despite water de®cits in the surface soil (Zimmermann

et al. 1999).

One to two week long drought periods are a

characteristic feature of the Siberian growing climate

(Kelliher et al. 1997, 1998). For upland soils, this can

quickly lead to water de®cits that detrimentally affect

surface conductance, Gs (Fig. 3a) and evaporation, E

(Fig. 3b) but CO2 assimilation, A, can be less effected

(Fig. 3c). Indeed the latter appeared to even increase

during the early phase of a drying cycle, despite

decreasing Gs. This response of A may be due to a slow

recovery from drought that occurred prior to the rain-

event and later in this drying cycle. Assimilation was

later observed to decrease in a manner similar to E. Since

Siberian light coniferous forests typically have relatively

open canopies (projected crown area/total ground

area = 60±70% for pine, Wirth et al. 1999) and signi®cant

penetration of solar radiation to the ground, high rates of

understorey evaporation can occur. Understorey eva-

poration rates (which may depend on whether ground-

vegetation is present) are linearly related to the available

energy and may even exceed tree canopy transpiration

on ®ne summer days (Fig. 3d,e).

The effect of soil water de®cit is enhanced by

extreme conditions of low air humidity during the

day. In Siberian forests the air saturation de®cit, D,

can be as high as 3 kPa (Kelliher et al. 1997, 1998;

Vygodskaya et al. 1997) or similar to conditions in the

Negev desert (Schulze & Hall 1982) and in great

contrast to Germany (Dmax = 1.6 kPa). Even though

stomata close with increasing D during the day

(Fig. 3f), forest evaporation is less affected (Fig. 3g).

There is thus only limited stomatal control over the

ecosystem evaporation rate, i.e. there is a tendency for

stomata to maintain constant evaporation at high air

saturation de®cits but the contribution of understorey

evaporation offsets the tree canopy response evident

in sap ¯ow measurements (Arneth et al. 1996;

Zimmermann et al. 1999). Under comparable condi-

tions, evaporation rates are 30% lower from Larix

stands than for pine forest which would make the

former better adjusted to the conditions of East Siberia

where rainfall is evidently limiting. The effect of

R

Table 3 The hydrological balance of East Siberia (Kelliher et al. 1997), Central Siberia (Kelliher et al. 1998), European Russia

(Molchanov 1968) and European spruce forest (Schulze et al. 1989a). All data are expressed in mm. Precipitation is taken as a

positive ¯ux into the ecosystem (as indicated by +). In contrast evaporation as a water loss from the system is indicated by (±). Since

soil water depletion supports transpiration of the vegetation in summer it is indicated by (+) while soil water recharge uses rain

water and it is indicated by (±)

Evaporation

Soil Seepage

Location Season Precipitation Wet Dry Water & runoff

East Siberia June±Aug. +112 ±22 ±161 +71 0

Yakutsk Sept.±May +101 0 0 ±71 ±30

Total +213 ±22 ±147 0 ±30

Central Siberia May±Sept. +297 ±60 ±205 ±32

Zotino Oct.±April +300 0 ±40 ±260

Total +597 ±60 ±245 ±292

European Russia Total +525 ±121 ±204 ±200

Northern Taiga Total +550 ±123 ±341 ±86

Mixed boreal forest Total +521 ±136 ±291 ±94

Southern forest steppe April±Sept. +652 ±156 ±287 ±209

Europe Oct.±March +516 ±78 ±5 ±433

Waldstein Total +1168 ±234 ±292 ±643



stomatal closure at high D on CO2 assimilation

(Fig. 3h) is less obvious at the canopy level than the

leaf level (Vygodskaya et al. 1997). This analogy of

increasing scale leading to a lesser apparent effect of

D on H2O and CO2 exchange is striking and it points

to the possibility of similar compensating factors.

In addition to the extreme hydrological conditions,

forest growth in Siberia is constrained by the availability

of nitrogen and other nutrients. This is evident from an

examination of the self-thinning process (Westoby 1984).

For fully stocked pristine Siberian forests, the relation-

ship between stand biomass and tree density does not

follow the general self-thinning line characterized by a

slope of ±0.5 in a double logarithmic plot, and the

measured slopes are substantially lower than the species-

speci®c thinning lines for above-ground competition for

light of most conifers. This deviation can be explained by

strong below-ground competition altering the allometric

growth pattern of trees which determine the slope

(Osawa & Allen 1993; Wirth et al. 1999). It is suggested,

that an overall negative self-thinning slope of ±0.5

characterizes forest ecosystems in which low site quality

limits productivity. The attainable biomass at a certain

stand density can additionally be lowered by ®re

induced mortality, which mainly occur during an early

stage of stand development when trees have not yet

developed a ®re resistant bark (Wirth et al. 1999). In

young stands, ®re reduces stand density without

proportional effects on biomass. Following ®re, the

surviving trees develop towards closing the canopy

again, but due to nutrient and water limitations there is

not suf®cient time to reach the self-thinning line before

the next ®re occurrence. This effectively accelerates the

thinning process at a lower level of biomass than would

be expected from the available light. At a later stage of

development when ®re mortality decreases due to the

L

Fig. 3 Surface conductance (a), evaporation (b) and net CO2 assimilation (c) of Larix gmelinii stands (canopy plus ground cover)

during a period of dry weather, following a 20-mm rainfall. Understorey evaporation of Vaccinium (d) and lichens (e) as related to

available energy at the forest ¯oor. Ecosystem evaporation (f), conductance (g), and CO2 assimilation of Larix gmelinii as related to

the saturation de®cit of the air (h) (from Kelliher et al. 1997, 1998 and previously unpubl. data).

710 E . - D . S C H U L Z E et al.


®re-resistant bark, below-ground competition deter-

mines the spacing of trees.

The effect of competition for nutrients is dif®cult to

quantify in the ®eld. Symptoms of nutrient de®ciency

(yellowing of needles or other nutrient related types of

damage) have not been observed in our Siberia plots

although nitrogen concentrations are extremely low (0.4±

0.6 mmolN gdw±1 in Pinus and 1.1 mmolN gdw

±1 in Larix).

The effect of nitrogen (N) competition becomes more

obvious from the needles of seed-trees left without

competition of neighbouring trees after logging. In such

trees the N concentration in 1-y old needles was

0.94 mmol gdw±1 (n = 9) as opposed to 0.54 mmol gdw

±1

for trees growing in a nearby close canopy that had not

been logged (n = 30). Similarly over 14 years, the radial

stem-wood increment was about 2.5 mm y±1 for the seed

trees but only 0.5 mm y±1 in the unlogged stand.

Surprisingly, the European managed spruce forest

shows a very similar thinning response to the Siberian

forests studied, albeit at a much higher biomass

(Fig. 4). In this case it is because forest management

effectively avoids competition for light by a common

silvicultural practice to cultivate a low density of trees

with special dimensions as construction wood. The

overall effect is that management can act in a very

similar way as ®re on the tree population in a natural

forest.

In contrast to Siberia, N deposition has changed the

recent growth rates of many forests in Europe (Spieker

et al. 1996). Indeed, at present, the volume increment

of German forests is twice as high as in reference

yield tables (Pretzsch 1996). The magnitude of the

effect can be demonstrated by an analysis of ring

growth for individual trees. Taking the German

Waldstein site as an example, Fig. 6a shows that trees

currently 140-y old grew at a much lower rate when

they were young, compared to today's trees from

younger stands. Also, 140-y old trees do not now

show a reduced growth rate as would be expected for

old growth stands (Kramer 1988). They are now

growing at a rate considered typical of young stands.

Although the change in growth has been mainly

related to nitrogen deposition (Schulze 1994a), an

associated interaction with increasing CO2 concentra-

tions is probable (Lloyd 1999).

The stem volume growth rates of Pinus sylvestris

trees in Siberia are lower by a factor of six compared

to Picea abies trees in Germany (note the difference in

y-axis scales in Fig. 6). In contrast to Europe, initial

growth rates of young stands in Siberia has hardly

changed since 1800 although there is a small and

signi®cant trend to increased regeneration-phase

growth for Siberian pine (Wirth 1996). Large effects

of ®re on subsequent tree growth are also evident.

The increased availability of nutrients after ®re

accounts for the initial rapid growth spurt which later

levels off. In the later stages of stand development,

smaller forest ¯oor ®res occur every 20±50 years which

do not destroy the stand, but burn the ground cover,

litter and part of the upper humus layer, and weak or

small trees. These ground-®res result in a 10±20-year

growth depression of the surviving trees due to ®re

damage followed by 10±15 years of accelerated growth

under the reduced competition and higher nutrient

supply. In 1995 the surviving trees in this stand were

in a stage of rapid growth following a major ®re in

the year 1965. The accelerated growth after ®re is an

additional indicator that water and nutrient supply are

major limiting factors, although in some cases the low

microbial activity may ultimately be limited by water

alone.

Net Ecosystem Exchange of CO2 (NEE), watervapour and heat

Net primary productivity supplies organic carbon as

an energy source for heterotrophic organisms, which

in turn recycle nutrients by decomposing the litter to

R

Fig. 4 Self-thinning of Larix gmelinii and

Pinus sylvestris stands in Siberia (Schulze

et al. 1995; Wirth et al. 1999), and Picea abies

in West Europe (Mund 1996).



support plant growth. Thus, a large fraction of carbon

returns to the atmosphere due to microbial respiration

during litter decomposition (Townsend et al. 1995).

Litter mass and quality in combination with site

conditions (e.g. soil moisture) determine the microbial

activity in boreal soils (Ross et al. 1998). Because of the

very close interaction between tree roots, their

ectomycorrhizal fungal sheath and soil microbes, it is

not possible to separate these sources of respiratory

CO2 without major disturbance in forests. The net

ecosystem balance of assimilatory and respiratory

processes can however, be measured by the eddy

covariance technique. The BOREAS study showed how

Net Ecosystem Exchange (NEE) depends strongly on

the vegetation type (Baldocchi & Vogel 1997; Jarvis

et al. 1997; La¯eur et al. 1997) and exhibits strong year-

to-year variation (Goulden et al. 1997) in the boreal

zone.

The range of NEE in Central Siberia is given in Fig. 7

for different Pinus stands and a Sphagnum bog. Data

represent mean (6 SE) values over the same 5±10-day

period in mid-July 1996. Here we use the normal

micrometeorological convention in which downward

¯uxes from the atmosphere (i.e. net photosynthesis) are

denoted as negative. Daytime NEE reached ± 11 mmol

m±2s±1 in a 53-y old regenerating forest supplied with

ground water as well as rainfall. This level of CO2 uptake

was higher than in a 215-y old stand, while

7±13 y-old stands after logging had a daytime NEE close

to the ecosystem compensation point where assimilation

balances respiration (i.e. NEE = 0). During summer the

bog had a daytime NEE similar to the 215-y old forest

stand.

Compared to daytime net assimilation, night-time net

respiration was highest in the fast growing 67-y old

stand, followed by the logging areas. Lowest rates were

in the bog, where waterlogging probably inhibited

decomposition (Fig. 7). Eighty percent of respiration in

the 215-y old stand emanated from the ground (Kelliher

et al. 1999).

Table 4 summarizes the main components of carbon

and energy ¯uxes in Siberia and Europe. Energy

exchange was dominated mostly by sensible heat ¯ux

in forest stands [daily average Bowen ratios (H/LE) > 1]

in Siberia and Europe. This was also observed in

BOREAS (e.g. Baldocchi et al. 1997; Jarvis et al. 1997). At

a Bowen ratio of 2, 67% of incoming net radiation is

dissipated as sensible heat. This was 83% in logging areas

(Bowen Ratio 3±5) but only 38% for the bog (Bowen ratio:

0.6). In the bog the Bowen ratio was still higher than the

equilibrium value due to partial drying of the surface in a

largely rain-free measurement period (see Fig. 3). The

differences in energy dissipation between bogs and

forests in Siberia are important because return of water

vapour to the atmosphere is the major source of water for

precipitation. The delivery of vapor to the atmosphere by

logging areas is 30% lower than that of the bog (Fig. 7b).

The nonevaporated water from the logging areas is lost

to ground and surface waters which are in turn

regionally connected to the bog, at least in part. Reducing

inputs of water vapor to the atmosphere through

evaporation as a consequence of large scale logging in

west Siberia could affect the hydrological balance not

only in situ but also to the east of the continent unless

runoff contributes to increased wetland formation at sites

close to groundwater. In a patchy landscape the genera-

tion of heat from logging areas and the generation of

water vapor from bogs may promote convective storms

and this could in turn affect the ®re cycle. Effects of local

land-use practice on regional climate and stream ¯ow

have been demonstrated elsewhere (Stohlgren et al. 1998).

NEE-¯uxes exhibit even larger site-to-site variability

than the evaporation rates. NEE was most negative in

Europe, closely followed in Siberia by the well-watered

67-y old pine regeneration and a 200-y pristine old

growth forest, and by the bog. The differences in daytime

net assimilation are accentuated by variations in night-

time net respiration. Most strikingly, compared to all

other sites the 150-y old spruce forest near Moscow, the

Fyedorovskoye site, exhibited the most negative (max-

imum) NEE during the day, but this was compensated

by high night respiration to an extent that this stand was

usually a C-source on a 24-h basis. The same effect was

observed in the windthrow area. The 7-and 13-y old

logging areas were carbon sources on a 24-h basis, even

though they are covered by relatively fast growing trees

which were up to 5 m tall. The 24-h NEE of Pinus

sylvestris is similar to those of Pinus banksiana and Picea

mariana during the BOREAS project (Table 4)

Clearly, long-term ¯ux measurements are needed in

Siberia before further conclusions can be drawn. Such

measurements started in 1998. Figure 8 shows cumu-

lative seasonal NEE at the German site Waldstein,

above spruce forest and a bog in European Russia, the

Fyedorovskoye site, and above a 200-y old pine forest

in Central Siberia near Zotino, site at Bor Island. The

Bor Island site in Siberia is not identical to the

location for which data are shown in Fig. 7. It had

similar age to the 215-y old stand but a higher LAI

(1.9). The Sphagnum bog covered a larger area than the

bog whose data are shown in Fig. 7. Measurements

started after snow melt in April for Germany, and in

June for Russia.

From April to September 1998, the German forest net

CO2 uptake accumulated steadily during the growing

season. In September, however, respiration exceeded

assimilation which decreased the cumulative C-assimi-

lated from 19 to 15.5 mol m±2. Measurements started later



in the year near Moscow, Fyedorovskoye site, where the

forest was a C-sink only in June. Later, it changed to a C-

source cumulatively delivering 7 mol m±2 to the atmos-

phere by early October. This contrasts with the Siberian

pine forest that exhibited on average a higher rate of daily

C-assimilation than the German forest. It reached a

cumulative net C-uptake of ± 14 mol m±2 by the end of

the growing season. The C-assimilation characteristics of

bogs seem similar in European Russia and Siberia. In both

cases assimilation started later than in nearby forest due to

frozen ground in the wetter bogs and net assimilation

there reached a cumulative level of 7 mol m±2 by the end of

the growing season. The high rate of net C-assimilation for

the Siberian forest compared to the German and European

Russian forest is surprising given the harsh climatic

conditions in Siberia and low NPP. Most unexpected was

the response of the pristine 200-y old spruce forest near

Moscow. Initially this forest had net assimilation in spring

that was lower than at all other sites although daytime

NEE reached the most negative rates. However, respira-

tion there was very high probably due to the 0.5 m deep

peat soil. The response of this forest is very similar to that

of a spruce forest in central Sweden (NOPEX site,

Lindroth et al. 1998). The NOPEX forest changed to an

even stronger C-source than the Fyedorovskoye forest

after 1±2 months of assimilation delivering 9±10 mol m±2

to the atmosphere. Seasonal NEE is thus not simply

related to the NPP, and it can vary greatly from the

photosynthetic capacity (measured as maximum daytime

ecosystem exchange). NEE also depends strongly on

respiration of the organic layer, and this carbon pool

accumulated over decades to centuries. Decomposition

takes place not only in recent litter but also in older layers

(Townsend et al. 1995), and it thus acts as a `ecosystem

R

Table 4 Bowen ratios and daily mid summer ecosystem ¯uxes of water (mm d±1) and carbon dioxide (mmol m±2 d±1), averages of 5±

20 days of measurement in July 1996. n.d. not determined. For comparison the lower part of the table contains data for different

study sites of the BOREAS experiment: (1) Baldocchi et al. 1997; (2) McCaughey et al. 1997; (3) Pattey et al. (1997); (4) Jarvis et al. 1997;

(5) Goulden et al. 1997; (6) La¯eur et al. 1997; (7) Suyker et al. 1997

Ecosystem C-¯ux in July

(mmol m±2s±1)

Av.daily Daily (mmol m±2 d±1) Leaf area

Bowen evaporation day night daily sum index

Location Ratio (mm d±1) max. average in summer (m2 m±2)

Germany

Waldstein

43-y Picea 2.0 1.3 ±15 3.1 ±210 8.1

European Russia

Fyedorovskoye

110-y Picea 1.6 1.9 ±19 6.3 +44 8.0 long-term site

Sphagnum bog 0.7 1.6 ±6 2.1 ±62 n.d. long-term site

Windthrow 1.1 1.3 ±6 4.4 +164 < 1

Siberia

140-y Larix 1.4 1.6 ±7 2.1 ±63 1.4

200-y Pinus 2.1 1.7 ±11 1.5 ±174 1.9 long-term site

215-y Pinus 2.6 1.4 ±9 1.5 ±61 0.6

Lichen woodland 2.0 1.3 ±6 2.0 ±30 0.1

67-y Pinus 0.9 2.6 ±11 1.1 ±192 1.9

7-y logging 5.2 0.8 ±7 1.8 +14 0.2

13-y logging 2.9 1.2 ±4 1.5 +8 0.2

Sphagnum Bog 1 0.6 2.6 ±7 0.7 ±104 n.d.

Sphagnum Bog 2 0.5 3.0 ±6 1.1 ±102 n.d. long-term site

Canada (BOREAS)

Pinus banksiana old 1±2 < 2.5 ±17 n.d. n.d. 1.9±2.2 (1)

Pinus banksiana yg 1±4 2±3 ±6 1.1 ±158 1.1 (2)

Picea mariana 54°N 1±2 1±3 ±8 2.0 ±188 3.7±4.0 (3)

Picea mariana 54°N 1±3 2 ±9 6 ±66 4.5 (4)

Picea mariana 56°N 2 0.6 ±10 5 0 n.d. (5)

Fen 0.1±0.2 1±2 ±10 n.d. +6 n.d. (6)

Fen n.d. n.d. ±13 n.d. ±52 n.d. (7)



memory' which may compensate C-assimilation under

certain conditions (Fyedorovskoye site). Also, Fig. 8

shows, that high NEE is possible at high and low NPP

sites, which was suggested in marine studies (Williams

1998).

The seasonally, integrated NEE over summer also

varied greatly during BOREAS (± 8 to ± 18 molC per

summer season; Jarvis et al. 1997; McCaughey et al.

1997a). However, including winter respiration, the

Picea mariana forest of Goulden et al. (1997) was at or

slightly above its compensation point. This demon-

strates possible signi®cance of winter respiration

(Zimov et al. 1993; Winston et al. 1997). These data

are not yet available for Siberia, but the German forest

was at the compensation point all winter (Rebmann,

unpubl.). Therefore the annual carbon balance was not

affected signi®cantly by the relatively mild European

winter where assimilation continued to balance

respiration. Wetlands also showed a great variability

during BOREAS ranging between an annual carbon

source (+ 0.05 molC m±2: McCaughey et al. 1997b) and

a carbon sink (± 7 molC m±2: Suyker & Verma 1997).

Both Russian Sphagnum bogs were larger C-sinks than

those studied in Canada.

The effects of disturbances on the carbonbalance

In theory, NEE measured by eddy covariance should

represent the long-term ecosystem carbon balance, as

de®ned by NEP. On average, for the years 1996 and 1997

NEE was ± 272 gC m±2 y±1 in a total of 8 ¯ux studies in

temperate coniferous and broad-leaved forests of

Europe, and ± 46 gC m±2 y±1 in 4 boreal coniferous forests

of the EUROFLUX network (Euro¯ux report 1997,

Contract ENV4-CT95±0078, EEC-DGXII D2, Brussels,

Belgium). This rate seems high considering an average

NPP of 459 gC m±2 y±1 across Europe (Fig. 2).

Obviously, NEE over 1-y periods is unlikely to

include disturbances. In Siberia, even continuous

measurements over 2 years have a < 10% chance of

including a ®re in the study. The long-term rate of

carbon sequestration includes periodic but rare dis-

turbances. At present the effect can only be quanti®ed

by inventory data of above and below-ground carbon

pools. Shvidenko & Nilsson (1999) thus estimate a net

carbon ¯ux from the atmosphere into the soil of

± 0.8 mol m±2 y±1 (10.1 gC m±2 y±1) during the period of

1961±83 in Russia. However, in the following 10 years,

Russia changed from a net sink to a net source for

carbon (+ 0.6 mol m±2 y±1 = 7.1 gC m±2 y±1) due to

anthropogenic and natural disturbances. These larger

scale and longer term rates are much lower than the

annual NEE measurements in Siberia, North American

and European temperate and boreal forests (EURO-

FLUX report 1997; BOREAS, special issue J. Geophys

Res. 102D; Fig. 8 of this study). In a regional

assessment of carbon exchange by forests of the

Paci®c north-west of Canada which included anthro-

pogenic disturbances by logging, Cohen et al. (1996)

demonstrated that over time this region is a C-source

with an annual net carbon ef¯ux to the atmosphere as

large as 9 mol CO2 m±2 y±1 despite reafforestation.

Thus, forest inventory data point to much lower

carbon exchange rates than NEE measurements which

needs further examination. We suggest that episodic

disturbances, which change NEE, have not been

included in monitoring programs. This may lead to

erroneous conclusions about longer term carbon

exchange rates. An example of the effect of ecosystem

disturbance is presented in Fig. 8, where a 2-y old

windthrow lost 16 molC m±2 over a 3-month period in

summer, which is more than the rate of assimilation

of the 43-y old spruce forest in Germany. Based on

the decay rate of wood, we estimate that windthrough

may affect the forest carbon balance as long as

30 years (A. Knohl, unpubl.).

Figure 9 classi®es disturbances in terms of the fate of

carbon in ecosystems. There are disturbances that act as

continuous forcing on ecosystems, such as daily, seaso-

nal, or long-term changes in temperature, CO2 concen-

tration and net radiation. The effects of these

environmental ¯uctuations on NEE can be determined

when eddy covariance measurements are conducted

over a period of several years or if these are included

in the resultant carbon models. However, there are also

periodic or rare events which disrupt the ecosystem

exchange, such as uprooting of trees by strong winds or

insect outbreak or ¯ooding. These events may turn

ecosystems temporarily or permanently into different

types of communities, until forest regeneration takes

place. Plant debris from the forest may remain in the

community, but there may also be an increase in soil

respiration by microbial decomposition. Thus even if net

carbon uptake occurred over a decade, it is possible that

this carbon could be lost by severe disturbance in the

following decade. There are also different disturbances,

like logging, grazing and ®re, which export carbon and

nitrogen from an ecosystem bypassing heterotrophic

respiration. In the Russian forests, 87 3 1012 gC y±1 are

harvested, of which 27% remains on site as slash, with

77% removed from harvest site, 16% exported for local

fuel and 57% for industrial products such as paper and

other wood products (Shvidenko & Nilsson 1998). In the

west European forests 180 3 1012 gC y±1 were exported

from the ecosystem by harvesting in 1990 (Stanners &

Bourdeau 1995).



Fire is a natural disturbance factor which occurs

regularly in the boreal forest of Siberia with the average

area affected being about 3.5 million ha y±1 (0.6% of the

forest area, Shvidenko & Nilsson 1999). In central Siberia,

we estimate from ®re scares in stem-wood cross sections,

that ground ®res may occur at a relatively higher

frequency (50% probability of a 30-y return period) than

do crown ®res (every 100±200 y). During ground ®res,

the litter and surface organic layer are burnt. Most ®re

frequency models assume a Poisson probability distribu-

tion of occurrence (Johnson & Gutsell 1994). This implies

that ®res are dependent on climate and independent of

fuel load, which is debatable for forests. Figure 6

indicates from the growth depression that occurred in

all age classes that sometimes all stands burn in the same

region irrespective of age and fuel load.

Fire has several consequences at the ecosystem level.

One dramatic effect is that if two crown ®res occur in

close succession or if crown ®res occur over large areas,

the forest may not be able to regenerate due to a lack of

seed trees and sites for germination. In the Siberian pine

forest region, such patches of vegetation dominated by

lichens are frequently encountered. Here pine seems not

able to regenerate unless another ground ®re occurs.

Since the fuel load of lichens is sparse, these patches

usually remain and may become stable lichen woodlands

(see Table 4).

Fire returns the above-ground litter and upper soil

carbon to the atmosphere at a much faster rate than

natural decomposition. Thus, ®re can be simply seen as

accelerating the carbon cycle, decreasing the average

standing biomass and contributing to the observation

that boreal forest stands typically operate below the

theoretical self-thinning line (Fig. 5). However, besides

the conversion of organic matter into CO2, ®re also

immobilizes carbon as charcoal or black carbon (see

below).

Table 5 (upper part) summarizes the carbon stores of

soils at a burnt and an unburnt site on Bor Island, close to

Zotino, and where a large-scale ®re experiment was

undertaken in 1993 (Goldammer & Furyaev 1996). The

unburnt site had an ecosystem carbon density of about

766 molC m±2 with 54% in the above-ground biomass,

37% in the organic layer including dead trees and 9% as

soil organic matter. Trees were not consumed by the

intensive crown ®re but they subsequently died, increas-

ing greatly the `fresh' litter pool. Due to the mobilization

of organic carbon after the ®re, the amount of organic

matter in the soil E-horizon had increased at the time of

sampling which was 3 years after ®re. Overall, ®re

reduced the ecosystem carbon pool by only 23%

although the organic layer (including dead trees) pool

almost doubled.

The effect of ground ®res is not as dramatic (Table 5

lower part). Even though repeated forest ¯oor ®res

apparently occurred in our Siberian chronosequence (see

Fig. 6), carbon density in the litter and O3 + A-layer

increased with stand age.

Shvidenko & Nilsson (1999) estimate that 150 3 1012 gC

(2.1 mol C m±2 y±1) are lost by direct (58 3 1012 gC y±1) and

indirect (92 3 1012 gC y±1) effects of ®re in Russia. The

latter includes post®re respiratory losses.

Black carbon

Black carbon is the fraction of soil carbon considered to

be in a semistable form (Kuhlbusch 1998). It may

originate from microbial activity during decomposition

as well as from charcoal formation due to the incomplete

combustion of biomass during ®res (Haumaier & Zech

1995; Kuhlbusch & Crutzen 1995). Black carbon in soils

can be identi®ed by its level of condensation which may

be measured by the Hydrogen/C or Oxygen/C ratio

(Haumaier & Zech 1995).

R

Fig. 5 Annual growth of tree volume (m3 tree±1 y±1) as derived from tree ring analysis for (a) Picea abies in West Europe (Mund 1996)

and (b) Pinus sylvestris in central Siberia (Wirth 1996).



In the 215-y-old Siberian pine stand (Fig. 10) the

H/Cratio of untreated organic (bulk) material de-

creased from about 1.5 in the litter layer to < 1 in the

soil A and AE horizon (LuÈ hker 1997). However, it

increased again in the soil B-horizon. The organic

material from each horizon contains decomposing

matter as well as charcoal and ®ne, dust-like particles.

The fraction of black carbon in this mixture of

compounds can be quanti®ed after solvent extraction

and a thermal treatment at 340 °C in pure oxygen

(Kuhlbusch 1995). In litter, the H/C-ratio of treated

material was 75% lower than in untreated material,

but in the A-and AE-horizon, nearly the same H/C

ratio was obtained in treated and untreated material,

indicating a large fraction of black carbon.

Table 6 shows the black carbon content by soil horizon

taking into account the loss of weight during combus-

tion. The black carbon content is very low in the litter and

O2-layer (mainly dust-like particles), but it increases in

the lower humus and E-horizons, reaching a maximum

in the EB-horizon (charcoal and dust like particles). Tree

roots were observed to grow as a solid mat in a charcoal

layer of the O3-horizon. On average, we ®nd about 65±70

molC m±2 as black carbon in the organic layer and

mineral soil including the B-horizon. This represents

20±24% of the total soil carbon. The C-horizon contains

an additional 20 mol C m±2 black carbon which is 13% of

the total soil C there.

Net Biome Productivity (NBP)

Schulze & Heimann (1998) advocate that the concept of

NEP needs to be extended to account for disturbances

that lead to carbon losses which bypass heterotrophic

respiration, such as ®re and harvest. The carbon

exchange rate that includes these processes has been

termed `Net Biome Productivity', NBP. We know of no

previous attempts to measure NBP and compare it with

NPP and NEP.

As an example, we shall try to quantify the long-term

effect of ®re. First and following Shvidenko & Nilsson

(1999), assuming that 2.6% of the carbon which was

directly released by ®re (58.1 3 1012 g y±1) was converted

to charcoal (IPPC-Guidelines 1997), on average 16

mmolC m±2 y±1 would enter the soil in this form in

Russia. Obviously, this rate is much smaller than the net

change in Russian carbon stocks of 800 mmol m±2 y±1 for

Russia for 1961±83 (Shvidenko & Nilsson 1999). Follow-

ing Table 6, the soil pro®le in central Siberian pine forest

contained a total of 65±72 mol black C m±2 to the depth of

0.75 m (B-horizon). Assuming 16 mmol C m±2 y±1 charcoal

production, this suggests that the region has been

exposed to ®res for the last 4063 years. This estimate

can be cross-checked by radio-carbon dating. The age of

L

Tab

le5

Th

eco

mp

artm

enta

liza

tio

no

fec

osy

stem

carb

on

(mo

lC/

m2)

ina

Sib

eria

nP

ine

fore

st(0

±0.5

mso

ild

epth

).D

ata

rep

rese

nt

aver

ages

of

3±5

sam

ple

sp

ersi

tew

hic

hw

ere

tak

en

inth

em

idd

leb

etw

een

tree

s,w

hic

hw

asin

mo

stca

ses

ou

tsid

eth

ecr

ow

np

roje

ctio

n

Ab

ov

e-g

rou

nd

liv

eb

iom

ass

So

ilca

rbo

n/

ho

rizo

n

Sta

nd

No

.of

age

tree

sm

±2

Wo

od

Nee

dle

Lic

hen

To

tal

Lit

ter

Dea

dtr

ees

O3

+A

A/

EE

BT

ota

l

bu

rnt

Bo

r0

00

00

1749

20

3124

2294

un

bu

rnt

Bo

r0.

1434

019

5441

325

155

102

3010

3119

8

280.

9565

105

8029

9525

616

1490

660.

2829

928

633

329

230

3222

356

124

139

0.11

403

167

426

4121

819

2011

1110

2

202

0.08

435

195

459

4963

5027

3013

169

215

0.03

274

13n

.d.

287

5136

5041

5161

254

383

0.05

594

237

624

5983

4231

446

182

av.2

8±38

334

518

637

843

120

3624

3118

152

716 E . - D . S C H U L Z E et al.


the Siberian black carbon at the base of where it

accumulates was 5250 years and 4910 years in two

independent soil samples (AMS 14C-analysis laboratory

Kiel, Germany). If the 65 mol black C m±2 accumulated in

about 5000 years, the accumulation rate would be

13 mmol m±2 y±1.

Schlesinger (1990) derived a long-term C-accumulation

rate of 67 mmol m±2 y±1 for North American boreal forest

by an indirect approach of measuring organic carbon

content in an age sequence of soils. Extrapolating from

accumulations of soil nitrogen (and accounting for the

nonlinearity of C-immobilization: Schlesinger 1990), it is

possible that NBP may reach the order of 140±400 mmol

m±2 y±1 in Scandinavia (Schulze et al. 1989b). In all cases

NBP is less than 1 ½ of NPP, but that carbon is

immobilized in a long-term carbon sink.

The Role of intermediate carbon pools as carbon sinks

The differences between NPP, NEP and NBP result

from different time constants for carbon turnover and

these can be associated with or result in intermediate

carbon pools. The importance of these intermediate

pools as global carbon stores has been discussed by

Melillo et al. (1996) with respect to the effects of

elevated CO2. They estimated a lag period of 30 years

for NPP to preceed heterotrophic respiration during

CO2 forcing. When taking into account the disturbance

cycle of ®re and harvest, intermediate pools are

probably turned over faster with management, i.e

the lag would decrease below 30 years. Buying time,

with respect to reduction of carbon emissions, may

thus become more dif®cult if forests are managed

R

Fig. 6 Average daily courses of ecosystem

CO2 exchange of (a) Siberian pristine pine

forest and natural regeneration after ®re,

(b) Regrowth after logging, and (c) a bog

all located near Zotino, Central Yenisey

River, July 1996.



using conventional plantation forestry techniques

(WBGU 1998).

According to the Kyoto protocol to the UN Framework

Convention on Climate Change, the biological sinks of

reforestation and afforestation minus deforestation can

be used to balance anthropogenic emissions of carbon

from fossil fuels (Steffen et al. 1998). In this context it is

important to estimate the net biome effect, because it is

not at all clear if the balance of deforestation and

reforestation will create sources or sinks for carbon

dioxide (WBGU 1998). Firstly, for Siberia, our 200-y old

forests were larger C-sinks during summer (as measured

by NEE) than two younger regenerating forests and

reached a cumulative rate close to a managed spruce

forest in Germany. Secondly, inspecting all biomass

compartments and carbon ¯uxes it emerges that main-

taining old growth pristine forest with a 30-yr ground

®re cycle contributes more to the global carbon budget

(in terms of reducing atmopsheric carbon dioxide

concentrations) than logging pristine forest and estab-

lishing new forest on mineral soil. This is because of the

large amounts of carbon in biomass and in the organic

layer which is lost during logging. Based on our forest

growth curves, it takes > 200 years to replace the living

biomass removed when old-growth forests are logged,

and it will take even longer to replace the soil carbon lost

due to the mechanical disturbance.

Conclusions

Siberian forest productivity is low compared to Eur-

opean forests. On average, NPP is 10.2 mol m±2 y±1 in

Siberia vs. 38 mol m±2 y±1 in Europe (positive sign for

productivity). In summer, NEE (negative sign for ¯uxes

from the atmosphere) is ± 30 to ± 192 mmol m±2 d±1 or ±5

to ± 14 mol m±2 summer±1 in natural systems of Siberia,

but + 11 mol m±2 d±1 in logging areas, as compared to

±210 mol m±2d±1 (± 15.5 mol m±2summer±1) in Germany. A

mature spruce forest in European Russia was a C-source

(+ 7 mol m±2summer±1). NBP (positive sign for product-

ivity) is 13 to 16 mmol m±2 y±1 in Siberia but may reach

> 140 mmol m±2 y±1 in Europe.

L

Fig. 7. Cumulative carbon ¯uxes for

Picea abies in West Europe, Picea abies in

European Russia and Pinus sylvestris in

Central Siberia, as well as of Sphagnum

bogs in European Russia and Central

Siberia. The cumulative carbon losses of a

2-y windthrow area in European Russia

are also shown.

Table 6 Content of total carbon and black carbon (molC/m2)

in different soil layers of a 215-y old stand (av 6 SD). The

samples were taken near the stem (n = 4), in the middle of the

projected crown (n = 3) and the edge of the crown projection

(n = 3), and in the middle between trees (n = 1, see also

Table 5). The C-horizon was sampled only outside the crown

Horizon Total soil C Black C % of total C

Crown centre

L-O2 91.4 6 11 0.51 6 0.06 0.6

03-E 136.1 6 7 19.47 6 1.33 14.3

EB 77.3 6 15 33.41 6 6.70 43.2

B1 25±50 39.6 6 3 15.60 6 2.09 39.4

B2 50±75 20.4 6 2 2.55 6 0.27 12.5

Subtotal 365 72 20

Outside crown

L-O2 50.6 6 8 0.28 6 0.05 0.6

03-E 90.6 6 5 11.65 6 2.29 12.9

EB 51.3 6 7 22.60 6 2.91 44.1

B1 25±50 61.5 6 12 26.32 6 5.66 42.8

B2 50±75 20.1 6 2 3.79 6 1.11 18.9

Subtotal 274 65 24

C 75±300 151.0 6 27 19.55 6 4.63 12.9

718 E . - D . S C H U L Z E et al.


The Bowen ratio is typically high in boreal forests,

especially in logging areas. This results in the generation

of sensible heat, which may affect climate. The interac-

tion of bogs with Bowen ratios < 1 and forest with Bowen

ratios > 1 may enhance convective storms which affect

runoff and the ®re cycle.

Disturbances signi®cantly affect the carbon balance.

Logging areas exhibit an NEE close to zero for up to

13 years despite high NPP in the regenerating stand.

Windthrow also leads to massive C-losses. The C-loss of

the spruce forest in European Russia seems to be related

to an activation of soil organic carbon rather than to a

loss in assimilation capacity. Fire speeds up the carbon

cycle and reduces standing biomass, but adds to the soil

black carbon pool by the production of charcoal.

Old forest stands of Siberia can be signi®cant carbon

sinks and reach a cumulative annual carbon ¯ux that is

close to that in Germany despite a much lower NPP. The

high NEP of Siberian forest is however, at high risk to be

lost by disturbance through ®re. In contrast, forests with

high rates of C-assimilation may be a C-source if high

rates of decomposition of organic carbon in the soil leads

to high ecosystem respiration rate as in the case of the

spruce forest in European Russia where the soil organic

matter is an old peat layer. Thus relations between NPP

and NEP are more complex than previously thought and

they seem to be strongly dependent on processes in the

soil, where C-pools may accumulate or disintegrate over

very long time periods and act as a `ecosystem memory'.

In Siberia, maintaining old growth pristine forest

contributes more to the global net carbon sink than

reforestation after logging.

Acknowledgements

This research began in 1993 with support of the German

Bundesminister fuÈ r ErnaÈhrung, Landwirtschaft und Forsten,

the Humboldt foundation (Max-Planck Forschungspreis), the

New Zealand Foundation for Research, Science and Technol-

ogy, and the New Zealand/German Agreement for Scienti®c

and Technological Co-Operation. The ¯ux measurements in

1996 through 1998 were funded by the Volkswagen Founda-

tion (I/71 846) and later by the EEC (EUROFLUX network at

the Waldstein site and EUROSIBERIAN CARBON FLUX

project at the Fyedorovskoye and the Zotino site). The long-

term measurements were instrumented by the MPI for

Biogeochemistry.

R

Fig. 9. Molar C/H ratios of litter and humus material before

and after combustion at 340 °C in oxygen.

Fig. 8. Classi®cation of ecosystem

disturbances with respect to effects on the

carbon and nitrogen cycle.



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Documents

Productivity of forests in the Eurosiberian boreal region and their potential to act as a carbon sink -- a synthesis