Annals of Botany 91: 213±226, 2003
doi:10.1093/aob/mcf185, available online at www.aob.oupjournals.org
REVIEW
Paludi®cation and Forest Retreat in Northern Oceanic Environments
R . M . M . C R A W F O R D 1 , * , C . E . J E F F R E E 2 and W . G . R E E S 3
1Plant
Science Laboratory, Sir Harold Mitchell Building, St Andrews University, St Andrews KY1 6AJ, 2Edinburgh
University Institute of Cell and Molecular Biology, Daniel Rutherford Building, King's Buildings, May®eld Road,
Edinburgh EH9 3JH and 3Scott Polar Research Institute, Lens®eld Road, Cambridge CB2 1ER, UK
Received: 20 August 2001 Returned for revision: 14 November 2001 Accepted 19 April 2002
Examination of temperature variations over the past century for Europe and the Arctic from northern Norway to
Siberia suggests that variations in the North Atlantic Oscillation are associated with an increase in oceanicity in
certain maritime regions. A southward depression of the treeline in favour of wet heaths, bogs and wetland tundra communities is also observed in northern oceanic environments. The physiological basis for this change in
ecological succession from forest to bog is discussed in relation to the long-term effects of ¯ooding on tree survival. The heightened values currently detected in the North Atlantic Oscillation Index, together with rising winter temperatures, and increased rainfall in many areas in northern Europe, presents an increasing risk of
paludi®cation with adverse consequences for forest regeneration, particularly in areas with oceanic climates.
Climatic warming in oceanic areas may increase the area covered by bogs and, contrary to general expectations,
lead to a retreat rather than an advance in the northern limit of the boreal forest. High water-table levels are not
automatically detrimental to forest survival as can be seen in swamp, bottomland and mangrove forests.
Consequently, the inhibitory effects of ¯ooding on tree survival and regeneration in northern regions should not
be uncritically accepted as merely due to high water levels. Evidence is discussed which suggests that physiological and ecological factors may interact to inhibit forest regeneration in habitats where there is a risk of prolonged winter-¯ooding combined with warmer winters and cool moist summers.
ã 2003 Annals of Botany Company
Key words: Review, North Atlantic Oscillation, ¯ooding, boreal forest, treeline, tundra, climate-change, bog, oceanicity.
INTRODUCTION
Paludi®cation denotes the process of bog expansion resulting from rising water tables as a consequence of peat
growth. In many parts of the northern hemisphere and, in
particular, in northern Europe paludi®cation is usually
accompanied by the disappearance of forest. This is such a
common phenomenon that it is accepted, almost without
question, as a natural occurrence that needs no further
explanation. That trees do not like high water tables is a
common but somewhat super®cial generalization. It is true
that many trees do not like growing in bogs, their deeper
anchoring roots die, and the trees become unstable and
subject to premature wind-throw. However, high water
tables are not universally detrimental to forest survival as
can be seen in the forested wetlands that ¯ourish in the
swamps, marshes and bogs of tropical and warm-temperate
regions. The black-water (Igapo) and white-water (Varzea)
inundation forests of the central Amazonian basin experience annual water-level ¯uctuations of up to 14 m, ¯ooding
vast areas of forest for periods which can be as long as
270 days per year (Ferreira, 2000). The river swamp forests
of North America's south-eastern coastal plain are dominated by swamp cypress (Taxodium distichum) and swamp
tupelo (Nyssa sylvatica var. bi¯ora) and the Sunderban
marshes in the Bay of Bengal have at least 26 species of
mangrove that survive daily inundation with salt water, even
* For correspondence. E-mail [email protected]
although only nine of the species have pneumatophores
(Braendle and Crawford, 1999).
Forests are found on bogs in northern areas but these are
usually in regions where the soil is frozen to a considerable
depth throughout the winter period and root metabolic
activity will therefore be minimal during periods of oxygen
deprivation. The black spruce (Picea mariana) and
tamarack (Larix laricina) are examples of trees that are
notable for their ability to grow on wet peatlands in the
continental cold-winter regions of north America. When
spring does arrive there is a rapid transition from frozen
soils to a warm growing season. Consequently, during the
summer growing season the active layer of the soil horizon
will normally be aerated. However, when late spring
¯ooding occurs on these forested peatlands it can be
detrimental to growth for both P. mariana and L. laricina
(Roy et al., 1999; Girardin et al., 2001).
In maritime regions, as in sub-Arctic QueÂbec, the Picea
mariana forests have been in retreat since the inception of
active peat growth from about 6000 BP. Similarly, in the
western Siberian lowlands over the past 6000 years there has
been a 3±400 km retreat of forest which in some areas used
to extend almost to the shores of the Arctic Ocean
(Kremenetski et al., 1998). Figure 1 shows the northern
limit of the Boreal Forest proper with coloured lines
representing the approximate modern limits for the sporadic
occurrence of individual tree species north of the limit of
closed forest. The areas where Holocene macrofossils have
ã 2003 Annals of Botany Company
214
Crawford et al. Ð Paludi®cation and Forest Retreat
F I G . 1. Comparison of present and past northern limits for tree survival in northern Siberia. Present-day distribution of the Boreal forest (brown) is
based on the vegetation map produced by Grid Arendal and published by the World Wide Fund for Nature. Mid-Holocene limits to forest trees are
regional generalizations from locations of fossil remains (green, evergreenÐpine and/or spruce species; red, treeÐbirch; purple, larch) based on
Kremenetski et al. (1998). Modern limits for the northern survival of individual tree species (colours as above) are also taken from Kremenetski et al.
(1998) as drawn by Callaghan et al., 2002.
been located and carbon dated are indicated by coloured
zones to the north of the current treelines. A pronounced
southerly depression of the northern limit of the Boreal
forest in the region of the western Siberian lowlands is due
to the presence of enormous areas of bog which now cover
terrain that was once covered with forest (MacDonald et al.,
2000). The climate in this region of the western Siberian
lowlands is in¯uenced by the proximity of the Arctic Ocean,
which, after the mid-Holocene rise in sea level and the
general climatic cooling after the hypsithermal, brought
about a regime of wet cool summers, resulting in extensive
replacement of forest by bog. Given the success of the treeform in the wetlands of warmer regions the question arises
as to why the oceanic wetlands of some northern regions
and, particularly north-western Europe, generally lack
signi®cant tree cover. Possible explanations are presented
in the discussion as to why wetlands vary in their tree cover
and whether or not certain temperature regimes make trees
less tolerant of ¯ooding.
C L I M A T I C L I M I T S O F TH E B O R E A L F O R E S T
Throughout North America and Eurasia trees eventually
reach a northern distribution limit which can be compared
with a number of thermal indicators. However, this does not
mean that in all areas the same natural processes are limiting
the northern limits of boreal forests. In the past, the northern
boundary of the boreal forest (the continental Arctic
treeline) has tended to be considered as a purely thermal
phenomenon. In North America this can be related to the
median July position of the polar front which matches
approximately the 10 °C July isotherm (Bryson, 1966).
However, a growing season mean temperature of 6±7 °C
now tends to replace this older KoÈppen's rule where the
limit to tree growth was considered as coinciding with the
10 °C isotherm of the warmest month of the year (KoÈrner,
1999). This modi®cation from a measurement indicating
maximum warmth to a temperature mean for the entire
growing season re¯ects a realization that the latitudinal and
altitudinal limits to tree growth are not directly related to the
ability to make a net carbon gain. Instead, the treeline is
more likely to be related to the length of growing season that
is needed for the production and development of new tissues
(KoÈrner, 1999). However, in any discussion between cause
and effect it is necessary to remember that mean temperatures, either of warmest months or entire growing seasons,
do not exist in nature and therefore should be considered
only as indicators and not causal factors (Holtmeier, 2000).
Despite attempts to ®nd a common causal basis for
the position of the treeline in North America and
Europe a generalized solution has proved elusive. This
is not surprising given that treelines are frequently only
approximate limits to the altitudinal or latitudinal
distribution
of
scattered
but
upright
trees
(SveinbjoÈrnsson, 2000). The degree of scatter can vary
and, in parts of Russia, the development of a mosaic of
vegetation at the tundra±taiga interface is particularly
noticeable, causing many Russian ecologists to doubt if
Crawford et al. Ð Paludi®cation and Forest Retreat
215
F I G . 2. Northern limits to the North American Boreal Forest: (A) proximity of oceanic in¯uences from the Hudson Bay and Labrador Sea; (B)
Normalized Difference Vegetation Index (NDVI) image recorded in May 1998 (8 km resolution) (colour scale: blue, 0; dark-green, 0´48±0´64;
yellow±orange, 0´76±0´88). Part A was generated from a Royalty Free Program `Mountain High Maps' published by Digital Wisdom, Cambridge; part
B from the 8-km resolution Path®nder data set.
there is even an approximate treeline that can be
mapped with any degree of precision. The basis of the
dif®culty that forest ecologists have in agreeing on the
position of a treeline can be seen in satellite images for
North America and Siberia recording the distribution of
evergreen vegetation by the Normalized Difference
Vegetation Index (NDVI) as seen in May (Figs 2 and
3).
The NDVI is a simple, unit-less index that is calculated
from satellite-measured re¯ectance in the red and nearinfrared regions of the electromagnetic spectrum (Tucker,
1979). It is based on the fact that mature, healthy greenleafed vegetation exhibits strong re¯ectance in the infrared
region and strong absorption in the red region. The NDVI
ranges between values of ±1 and +1, in the sense that it is
mathematically impossible for it to have a value outside this
range. Normally there is a strong correlation between the
green leaf area index (LAI) and the NDVI, but this is not to
imply that when the green LAI is zero the NDVI must also
be zero. The value obtained when the LAI is zero is
dependent upon the optical properties of the soil and,
although it is usually close to zero, it can be negative. Snow
216
Crawford et al. Ð Paludi®cation and Forest Retreat
Crawford et al. Ð Paludi®cation and Forest Retreat
and ice give NDVI values close to zero, while water bodies
can give negative values (see Tucker et al., 1975; Holben
et al., 1980).
In the 8-km resolution images images recorded in May
(Figs 2 and 3) there is a clear discontinuity between the blue
area (NDVI = 0) which represents the tundra still covered in
snow and ice with the already photosynthetically active
evergreen forest which is shown in dark and bright green
(NDVI > 0´25). This boundary is particularly clear in NDVI
images recorded at the start of the growing season before
deciduous vegetation has come into leaf. In North America a
southern displacement of the evergreen coniferous forest
can be observed in the oceanic regions, which are east and
west of the Hudson Bay as well as in Labrador (Fig. 2).
Similarly, in the western Siberian lowlands there is a
marked southward displacement of the Boreal Forest
between the rivers Ob¢ and Lena due to the in¯uence of
the Arctic Ocean (Fig. 3A±C). The NDVI images also help
to illustrate the scepticism with which many Russian
ecologists view the concept of a northern boreal forest
treeline. As shown in Fig. 1, the northern limit for boreal
forest proper deviates to the south of the treeline for
individual stands of trees. This extensive transition zone
(forest ecotone) between intact forest and completely
treeless tundra is particularly noticeable in the western
Siberian lowlands (Fig. 1). A high resolution NDVI image
from this transition zone is shown in Fig. 3C and reveals the
mosaic of tree and bog cover that is characteristic of the
forest ecotone that extends at this location north±south for
approx. 600 km from the south-eastern shore of Obskaya
Guba to the east±west ¯owing section of the River Ob¢. This
mosaic is considered by Russian ecologists to be a selfrenewing cyclic process taking place over hundreds of
years. Cryoperturbation causes the soil surface in localized
areas to rise above the general level of the bog (Chernov and
Matveyeva, 1997). In some areas this permits the active
layer to dry out suf®ciently to allow the re-establishment of
trees for a period until they shade the ground and cause the
permafrost to rise and favour once again the growth of
mosses as opposed to trees.
In addition to the problems caused by the cartographic
impossibility of tracing a line through the forest ecotone,
determining the possible movements of tree limits in
relation to climatic oscillations on a continental basis is
even more problematical. Even with the dramatic changes in
vegetation that take place at the tundra±taiga interface it is
dif®cult to make pan-Arctic generalizations as to the
probable extent of treeline movement at present, or in the
foreseeable future, as the climatic history of the different
217
regions in relation to trees is highly varied (Skre et al.,
2002). In Alaska, the treeline is currently at its most
northerly Holocene extent, while in north-western Canada
(Edwards and Barker, 1994) and northern QueÂbec (Payette
and Gagnon, 1985) as well as Siberia (Blyakharchuk and
Sulerzhitsky, 1999) there has been a retreat since the midHolocene. Where recent advances in treeline have been
observed it is frequently in areas where the dominant tree
species is already present in the phenotypically reduced
Krummholz form and climatic warming has resulted in the
emergence of vertical trees. [Note: genetically ®xed
Krummholz forms will have to be replaced by other
populations to show a change in form; see Holtmeier,
2000.] A recent change in Krummholz growth form has
been noticed both in sub-Arctic QueÂbec (Lavoie and
Payette, 1994) and on the western shore of Hudson Bay.
In this latter site, the Picea mariana treeline runs north±
south, parallel to the shore and has advanced eastwards by
12 km since the late 1800s due to the development of
vertical trees within already established Krummholz
(Lescop-Sinclair and Payette, 1995).
H I S T O R Y O F PA L U D I F I C A T I O N
The early Holocene warm period, usually referred to as the
hypsithermal or `climatic optimum', facilitated the advance
of forests in the northern hemisphere several 100 km to the
north of the present position of the tundra±taiga interface.
The duration of this early Holocene hypsithermal interval
differs from one region to another in the boreal zone as well
as between the northern and southern hemispheres. In southwestern Saskatchewan there was a warm-dry hypsithermal
period between 6400 and 4500 BP (Porter et al., 1999), while
in north-west Montana there was a warm dry period that
lasted from 10 850 to 4750 BP (Gerloff et al., 1995). In
western Norway the hypsithermal is dated to between 8000
and 6000 BP (Nesje and Kvamme, 1991) when hazel
(Corylus avellana) extended as far as the North Cape. In
Russia the early Holocene saw a spread of spruce, larch,
pine and tree birch to more northern latitudes than they now
inhabit (Fig. 1). In Siberia, Picea obovata was farther north
than at present between 8000 and 4500/4300 BP and Larix
spp. were further north between 10 000 and 5000/4500 BP.
Tree birches (Betula pubescens) reached the present-day
shoreline of the Barents Sea in the Bolshezemelskaya
Tundra (68°N) and in the Taimyr Peninsula (72°N) between
8000 and 9000 BP. In the Yamal Peninsula the tree birch
limit was near 70°N by 8000 BP (Kremenetski et al., 1998).
F I G . 3. Northern limits to the Eurasian Boreal Forest: (A) proximity of oceanic in¯uences from the Arctic Ocean; (B) Normalized Difference
Vegetation Index (NDVI) image recorded in May 1998 (8 km resolution) (colour scale: blue, 0; dark green, 0´48±0´64; yellow±green, 0´76±0´88); (C)
detail of the transition zone between forest and tundra as seen in the Normalized Vegetation Index recorded in May 1998 (1 km resolution) (colour
scale: blue, 0; blue±green, 0´11±0´25; dark-green, 0´26±0´40; bright green, 0´41±0´64). It is considered (see text) that this mosaic represents a selfrenewing cyclic process taking place over hundreds of years as patches of forest develop on land that dries out after being raised by frost-heave and
then reverts again to bog as tree-cover cools the underlying ground. Part A was generated from a Royalty Free Program `Mountain High Maps'
published by Digital Wisdom, Cambridge; part B from the 8-km resolution Path®nder data set; part C from the 1-km AVHRR global land data set
distributed by the EROS Data Center, Distributed Active Archive Center (EDC DAAC), at the US Geological Survey's EROS Data Center in Sioux
Falls, South Dakota.
218
Crawford et al. Ð Paludi®cation and Forest Retreat
In Scotland recent research has shown that in the
Hebrides and northern Isles (Orkney and Shetland) large
areas that are now treeless, hyper-oceanic bogs, once had an
extensive cover of birch woodland with Corylus avellana,
Salix spp., Populus spp. and Sorbus aucuparia extending to
their coastal fringes, while more central and eastern areas
may have had stands with more warmth-demanding species
(Tipping, 1994).
The ecological consequences of forest retreat are not
uniform and suggest that the causes of forest disappearance
may differ from one region to another. In the more
continental areas forest gives way to tundra. However, this
is not a universal situation. In many areas the treeline is now
at latitudes where thermal conditions are adequate for tree
growth but regeneration is prevented by the growth of peat.
The development of oceanic conditions in these northern
areas appears to have taken place as sea levels rose in the
Arctic Ocean and the Hudson Bay. This early to midHolocene expansion of Arctic waters altered the delicate
balance between temperature and air humidity so that both
in Arctic and sub-Arctic regions bogs began to replace
forest over a wide area both in northern QueÂbec (Payette,
1984) and in the Siberian lowlands (Kremenetski et al.,
1998). A marked climatic deterioration (KlitgaardKristensen et al., 1998), commonly termed `the 8200 BP
event' (probably due to freshwater ¯uxes in the ®nal deglaciation of the Laurentide ice sheet), appears to have been
accompanied by a reduction in tree cover throughout
Europe. In the Outer Hebrides (Scotland) blanket peat
began its appearance between 9000 and 8000 BP (Fossitt,
1996) and in western Lewis there was a progressive
replacement of trees by blanket peat which began about
7900 BP and continued with a further decline between 5200
and 4000 BP. A trend to more oceanic conditions with cool
moist summers appears to have continued in many areas
probably as a result of these early Holocene rises in sea
level. The Arctic Ocean and the Hudson Bay would
therefore have begun to exert a greater maritime in¯uence
on climate in northern Siberia and QueÂbec, respectively. By
approx. 5000/4500 BP the northern limit of tree birch in
Russia was similar to its present limit and this was mirrored
in the southward retreat of other tree species.
The late Holocene retreat of the Eurasian treeline
coincides also with declining summer insolation. This,
together with the cooling of Arctic waters, would have
created at northern latitudes a more oceanic climate with
cool moist summers which would allow permafrost levels to
rise and facilitate the development of bogs. The considerable antiquity of the peat in the upper layers of bogs in the
Pur-Taz region of western Siberia (for location see Fig. 3C)
has been taken to suggest that much of the peat growth took
place at an early date (Peteet et al., 1998). However,
comparison of methane emissions from the Holocene
Optimum (5500±6000 years BP) with modern levels from
forests of northern Eurasia, suggests that the area of tundra
and the proportion of wetlands within the boreal forest zone
is probably greater now than at any time in the past
(Velichko et al., 1998). Examination of the recent growth of
bogs suggests that bogs appear to engulf the forest both in
the maritime regions of Canada and northern Siberia as well
as in other locations, particularly near the present tundra±
taiga interface. The situation is complex, however, as at this
interface between forest and bog there is a cyclical
alternation between tree cover and wetland vegetation (see
below).
In Russia there has been a lengthy debate among
ecologists as to whether climatic warming will cause an
advance or retreat of the treeline (Kriuchkov, 1971). Those
who assume that climatic warming causes an advance of the
treeline northwards subscribe to the eventual overriding
in¯uence of climatic factors. There is, however, a powerful
argument, held by those who believe that the presence or
absence of trees is controlled by edaphic factors in¯uenced
by the proximity of the Arctic Ocean and the long-term
persistence of permafrost, that climatic warming in the
North Siberian lowlands can cause a retreat of the treeline
due to peat growth. Examination of the history of methane
emissions from boreal regions would suggest that if the
present trend to warmer, wetter conditions continues with
longer growing seasons, then bog expansion and paludi®cation are likely to increase (Peteet et al., 1998).
In North America recent studies have questioned whether
or not temperature alone is the main controlling factor for
the northern limit of forest, and suggest that the risk of
natural ®res may be particularly acute at the tundra±taiga
interface. The frequency of forest ®res makes it essential
that trees retain a capacity for subsequent regeneration
(Payette et al., 2000). The removal of trees, whether by ®re
or any other agency, will lead to rising water tables. Fire can
also aid bog formation as particles of ash and carbon
deposited into the soil pro®le can reduce drainage and
therefore initiate peat growth (Mallik et al., 1984). Trees
can colonize peatlands in cold climates but remain nevertheless highly susceptible to deteriorating environmental
conditions (Arseneault and Payette, 1997). In a study
covering the little ice-age periods in northern QueÂbec, it was
found by these authors that black spruce continued to
colonize the peatlands as long as the adjacent well-drained
sites were occupied by seed-producing forest. This need for
neighbouring forest is two-fold. In addition to the need for a
seed source there is also a requirement for shelter to reduce
the damaging effects of winter snow-drifting conditions.
When neighbouring areas succumb to periodic ®res then
both the seed source and shelter are removed. Under these
conditions the surviving trees suffer die-back of supranival
stems. The trees then ®nally succumb to drowning in
permafrost-induced ponds. The post-®re degradation and
disappearance of the conifer stands from the peatlands
represent the ultimate stage of a positive feedback process
triggered by a modi®cation of the snow regime at the
landscape scale. In this connection it is relevant to note that
recent research in Siberia has shown that along the tundra±
taiga boundary there is a high frequency of thunder storms
suggesting an increased ®re probability due to the warmer
conditions of the forest increasing evapo-transpiration from
the bog (Valentini et al., 2000).
One of the most dramatic examples of boreal landscape
changes from forest to bog is the deforestation of northern
Scotland that took place at the beginning of the Neolithic
period. As noted above, during the hypsithermal period,
Crawford et al. Ð Paludi®cation and Forest Retreat
forest cover in Scotland extended from the mainland to the
Hebrides and the northern Isles of Orkney and Shetland.
Some replacement of trees by blanket bog took place before
the period of Neolithic settlement (Fossitt, 1996). However,
the advent of Neolithic farming in oceanic areas such as
Orkney and Shetland (Bennett et al., 1992; Bunting, 1996),
western Norway (Kaland, 1986) and the Hebrides (Tipping,
1994) was marked by the rapid and extensive replacement
of trees by heathlands and peat bog to an extent that did not
take place in more continental areas. The reasons for this
apparent sudden deforestation and ultra-sensitivity to
human disturbance in oceanic areas need further examination. It may be that the grazing activities of Neolithic
settlers opened up the tree canopy suf®ciently in the
maritime environment to allow the water table to rise and
®nally accomplish the paludi®cation process and treeremoval which had begun with the post-hypsithermal onset
of oceanic conditions.
M O N I T O R I N G C L I M A T I C C H A N G E S IN
O C E A N I C EN V I R O N M E N T S
If mild, wet winters present a threat to tree survival in the
more oceanic regions of northern Europe, then current
climatic trends need to be examined to determine the future
viability of northern forests and whether they are likely to be
negatively affected by increased paludi®cation. It is now
apparent that in relation to the growth of wetlands there is a
cyclic behaviour in the climatic record of northern Europe.
Ten periods of increased effective precipitation have been
detected in changes in bog vegetation in northern England
since 760 BC (Mauquoy and Barber, 1999). It is also possible
to relate the intensity of maritime conditions with the
periodic behaviour of the North Atlantic Oscillation (NAO).
The NAO has emerged as the dominant varying atmospheric
phenomenon in the northern hemisphere and the only
atmospheric teleconnection pattern with a periodic behaviour that matches the 700-year stable isotope record of the
Greenland GISP2 ice core (White et al., 1997). In the past
century there have been three periods with prolonged and
signi®cant increases in the winter (January to March) NAO
index. Anomalies caused by these changes include dry
winter-time conditions over southern Europe and the
Mediterranean and wetter-than-normal conditions over
northern Europe (Hurrell, 1995; Hurrell and VanLoon,
1997). Warmer and wetter winters have also had noticeable
effects on agriculture, interfering with potato harvest and
the sowing of winter cereals in the autumn as well as
delaying ®eld operations in spring.
Some of the changes in climatic pattern which may result
from variation of the NAO index can be integrated by
examining the degree to which maritime conditions (or the
converse continentality) may be changing over an extensive
geographical area. One such integration is obtained with
Conrad's Index of Continentality (Conrad, 1946) where
variation in temperature range is combined with a correction
for latitude:
CI = [1´7A/sin (ù + 10)] ± 14
219
where CI is Conrad's Index of Continentality; A the average
annual temperature range (°C); and ù is degrees latitude.
The scale provides values approximating to nearly zero for
Thorshavn (Faroe: 62°2¢N, 6°4¢W) and almost 100 for
Verkoyansk (Russia: 67°33¢E, 133°24¢E).
The ecological hazards of oceanicity for some types of
vegetation have previously been reviewed and related to
values of Conrad's Index averaged over the period 1961±
1990 (Crawford, 2000). This present paper extends the
study to cover the past century using the 0´5° gridded
monthly temperature data for the years 1901±1998 (New
et al., 1999, 2000) and covering Europe and the Arctic from
northern Norway to Siberia. Amounts of change differ
between one decade and another, and a substantial part of
what appears to be two major cyclical periods with about 60
years duration is evident in the decadal means for northern
regions (Fig. 4A±D). They also correlate broadly with the
changes in the NAO (Fig. 5A and B; Table 1). During the
warmer periods in these cycles, Conrad's Index in northern
Siberia is reduced (more oceanic), and during the colder
periods Conrad's Index is increased (more continental). The
warm period from 1991 to 1998 (the most recent data
available at the time of writing) has been more oceanic than
any other decade in the past century. Two examples of the
spatial distribution of the changing pattern of inter-decadal
oceanicity are shown in Fig. 6. The oceanic areas of Norway
and Britain show low-amplitude decadal changes in
oceanicity but nevertheless, within these lower values,
there is greater year-to-year variation than in the more
continental regions as measured by the coef®cient of
variation (Fig. 6D).
Examination of precipitation in Europe over the period
1986±1995 (Fig. 7A) shows the expected pattern of a
decrease in moving from west to east. The corresponding
precipitation anomaly map (Fig. 7B) indicates that there has
been a tendency for a northward movement of the rain belts
with a signi®cant reduction in rainfall amounts in parts of
the Mediterranean, western Iberian peninsula, the Balkans
and Turkey. When the number of rain-days in the year is
examined (Fig. 7C) it can be seen that the highest totals are
as expected in the hyper-oceanic regions of Ireland,
Scotland and western Norway. However, it is also notable
that the oceanic regions of western Siberia have 210±240
rain days per annum (Fig. 7C) and that the ratio of summer
to winter precipitation (Fig. 7D) shows that more rain falls
in summer than winter. In these regions, both the number of
rain days per annum and the amount of precipitation have
increased since about 1950 compared with the earlier half of
the century. The region has been showing a positive
anomaly of the order of one rain-day per month and a
precipitation anomaly of about 0´1 mm per day since 1980,
but this trend cannot always be extended as a generalization
to other parts of Europe, which show considerable individuality in the patterns of climate change during the
century (Table 1).
Given these observations it would appear that there is a
suf®cient corpus of information to suggest that the meteorological conditions which created the extensive bogs that
have developed over the past 6000 years in western Europe
and in the western Siberian lowlands have not diminished
220
Crawford et al. Ð Paludi®cation and Forest Retreat
F I G . 4. Changes of annual mean temperature, Conrad's Index and annual temperature range in the Siberian Arctic (lat 60±85°N, long 10±180°E) and
of annual mean temperature in the northern hemisphere temperature compared with the 1961±1990 meansÐall curves Lowess smoothed. (A) Decadal
changes of annual mean temperature; (B) decadal changes of Conrad's Index anomaly; (C) decadal changes of annual temperature range; (D) annual
mean temperature anomalies from the 1961±1990 means for the northern hemisphere, 1901±1998. Temperature data from the Climatic Research Unit
0´5° gridded 1901±1995 Global Climate Dataset (New et al., 1999, 2000).
and in some areas are clearly increasing. Given that climate
warming in Europe and the Eurasian Arctic is correlated
with increasing oceanicity, there are therefore grounds for
considering that paludi®cation is likely to increase and be a
dominant feature controlling natural plant succession both
on the Atlantic seaboard and at the tundra±taiga interface in
the Siberian lowlands.
P H Y S I O L O G IC A L H A Z A R D S F O R F L O O D E D
T R E ES
Adaptations to ¯ooding in plants are usually considered as
either avoidance mechanisms or else tolerance adaptations.
In the former, aerenchyma facilitates aeration of the
inundated root. In the latter, metabolic adaptations have
been found which allow some plants to endure anaerobic
conditions for a length of time suf®cient to overcome the
period of oxygen deprivation caused by ¯ooding. Both these
aspects of ¯ooding have been extensively discussed
(Armstrong et al., 1994; Braendle and Crawford, 1999)
and are by no means mutually exclusive as there are
examples of ¯ood-tolerant species which employ both types
of adaptations. Spartina anglica can survive total anoxia for
more than 28 days (Crawford, 1989) and is also capable of
allowing aeration of roots when growing in the lower parts
of salt marshes without developing particularly large root
diameters (Bouma et al., 2001). Similarly, when ¯ooded,
the common osier (Salix viminalis) is able to aerate upper
Crawford et al. Ð Paludi®cation and Forest Retreat
221
F I G . 5. North Atlantic Oscillation (NAO) anomalies for 1900±2000 (grey columns with superimposed lowess line in black: data from Hurrell, 1995)
compared with anomalies of annual mean temperature (°C) (green) and annual temperature range (°C) (red) for (A) a restricted part of the western
Siberian lowlands (lat 62´5±67´5°N, long. 62´5±67´5°E, showing a signi®cant relationship between NAO and the annual mean temperature. The
temperature range anomaly is typically of opposite sign to the mean anomaly. (B) Spain (lat 36±44°) showing weak relationships between NAO index
and mean temperature but a stronger relationship between NAO and annual temperature range.
adventitious roots, while deeper roots (200±300 mm) rely on
anoxia-tolerance for their survival (Jackson and Attwood,
1996). However, in most trees, particularly as they grow in
size, aeration of the deeper anchoring roots is not a facility
that is readily available. Trees with large trunks and deep
anchoring roots represent the ultimate challenge in withstanding oxygen-deprivation in wetland habitats.
Outside the tropics most of these ultra-¯ood-tolerant
swamp forests usually have either a relatively short winter
or no winter, and trees do not have the stress of preserving
an extensive root system in anaerobic conditions throughout
long, non-productive periods. In the cold and cool-temperate regions of the world, ¯ooding is generally unfavourable
for tree survival unless the ground is frozen during the
period of potential inundation. The few woody species that
survive in the wetlands at high latitudes are generally bushes
and scrub of a limited number of genera in which Salix spp.
and Alnus spp. are probably the most successful. In dry
habitats alders will grow as pole trees, but when ¯ooded, the
basal buds are stimulated to develop and the bush form
predominates (Crawford, 1989). The greater area of stem
surface that this produces close to the ground facilitates
222
Crawford et al. Ð Paludi®cation and Forest Retreat
TA B L E 1. Matrix of Pearson correlations, r (n = 98), between anomalies of the NAO index and of the northern hemisphere
annual mean temperature with annual mean temperature and annual temperature range of four European regionsÐSiberian
lowlands (lat 60±70°, long 65±85°), British Isles (lat 49±61°, long ±10° to ±3°), Turkey (lat 36±44°, long 27±32°) and Spain
(lat 36±44°, long ±9° to 4°)
Siberia
Mean temperature anomaly
Temperature range anomaly
British Isles
Mean temperature anomaly
Temperature range anomaly
Turkey
Mean temperature anomaly
Temperature range anomaly
Spain
Mean temperature anomaly
Temperature range anomaly
r
P
r
P
r
P
r
P
r
P
r
P
r
P
r
P
NAO index
anomaly
Northern
hemisphere mean
temperature anomaly
0´384
0´000096
±0´277
0´0057
±0´290
0´0038
0´482
0´00000049
±0´198
0´051 (n.s.)
0´170
0´095 (n.s.)
0´167
0´10 (n.s.)
0´0629
0´54 (n.s.)
0´543
0´0000000074
±0´321
0´0013
0´0799
0´43 (n.s.)
0´413
0´000024
0´192
0´058 (n.s.)
±0´0177
0´86 (n.s.)
0´571
0´00000000083
0´0827
0´42 (n.s.)
F I G . 6. Decadal variations in Conrad's Continentality Index (CI) in Europe (lat 11±66°N, long 34±72°E). (A) Distribution of CI for 1991±1998.
(B±D) CI anomalies with respect to the 1961±1990 mean: (B) CI anomaly for 1941±1950; (C) CI anomaly for 1991±1998; (D) distribution of
coef®cients of variation (CV) of Conrad's Index during the 9-year period 1990±1998. Colour scale intervals chosen to maximize contrasts.
Crawford et al. Ð Paludi®cation and Forest Retreat
223
F I G . 7. Distribution of precipitation amount, frequency and seasonality in Europe: (A) total annual precipitation (mm) during 1986±1995; (B) annual
precipitation anomaly 1986±1995 with respect to the 1961±1990 30-year mean; (C) rain-days, 1986±1995; (D) the ratio of summer (April±September)
to winter (October±March) precipitation. Temperature and precipitation data from the CRU 1901 to 1995 Global Climate Dataset (New et al., 1999,
2000).
aeration. The bush or polycormic form is therefore possibly
adapted better, in terms of aeration potential, as the area of
lenticel-containing bark in the basal region of the stems is
greater. These stem adaptations combined with the presence
of adventitious roots as in willow, and negatively geotropic
roots in nitrogen-®xing alders, facilitate the supply of
oxygen in waterlogged soils.
In any discussion of the physiology of oxygen deprivation
in perennial plants it is important to distinguish between
short-term and long-term tolerance. Species that are only
tolerant of short periods of anoxia frequently accelerate
glycolysis and thus overcome temporary energy shortages.
By contrast, species that are able to endure long-term anoxia
of oxygen deprivation have been shown to down-regulate
their metabolism (SchluÈter and Crawford, 2001). Similarly,
the common osier Salix viminalis has been found to respond
to decreasing oxygen supply during the growing season by
reducing both shoot and root growth. When rooted cuttings
were waterlogged for 4 weeks in a glasshouse, soil redox
potentials quickly decreased to below zero. At depths of
100±200 mm and 200±300 mm, extension by existing root
axes was halted by soil ¯ooding, while adventitious roots
from above failed to penetrate these deeper zones. After
4 weeks waterlogging, all arrested root tips recommenced
elongation when the soil was drained; their extension rates
exceeding those of roots that were well drained throughout
the experiment (Jackson and Attwood, 1996).
Trees appear to be most at risk from ¯ooding in oceanic
climates where winters are long, wet and not particularly
cold. Further north, in some of the coldest regions of the
boreal forest, Picea mariana and Larix dahurica can grow
on bog surfaces even when permafrost is not far below the
surface. However, as noted above, in all these situations the
soils are frozen for most of the winter, the roots are
relatively shallow and oxygen demand is lower and supply
less impeded (Crawford, 1992). An entirely different winter
situation is found in northern oceanic regions such as the
British Isles and parts of western Norway. Tree roots stay
metabolically active and continue growing after shoot
growth has ceased, and only become dormant after the
onset of low temperatures (Coutts and Philipson, 1987).
Actively growing root tips of Picea sitchensis are highly
susceptible to damage if waterlogged but develop some
tolerance after they stop growing (Nicoll and Coutts, 1998).
224
Crawford et al. Ð Paludi®cation and Forest Retreat
Experimental studies of over-wintering trees of P. sitchensis
have shown that ¯ooding under milder winter conditions,
while the roots are still growing, causes a marked decrease
in root carbohydrate reserves. This does not lead to the
immediate death of the root, but when carbohydratedepleted roots are exposed once again to air, when the
water table is lowered, there is extensive die back of the root
system presumably due to post-anoxic injury (Crawford and
Braendle, 1996). Death of the whole tree will not be
immediate, but reduced root development will make the
larger trees unstable and therefore prone to wind-blow.
Trees which have an active sap ¯ow in early spring have a
need for adequate over-wintering supplies of carbohydrate.
In birches, the active upward movement of xylem sap in
spring carries with it substantial quantities of soluble
carbohydrates, ethanol, organic and amino acids
(Crawford, 1996). This ¯ow has been suggested as the
means whereby roots of some woody plants compensate for
the lack of oxygen in the soil atmosphere by exporting
hydrogen to the shoot and thus maintaining the redox
balance of the inundated root system (Crawford, 1996). The
upward movement of hydrogen in reduced compounds as a
constituent of the xylem ¯ow is a more ef®cient means of
exporting the oxygen debt of submerged organs than the
slow downward diffusion of gaseous oxygen through more
than 1 m of woody tissue. This replacement of oxygen
import by hydrogen export does, however, have a metabolic
cost, namely the provision of a high carbohydrate store in
the over-wintering root. In the bottomland trees of the USA
it has been shown that high pre-¯ood root starch concentrations are associated in those species that can tolerate
prolonged inundation. The bottomland Fraxinus pennsylvanica (green ash) and ¯ood-tolerant Nyssa aquatica (water
tupelo) store more carbohydrate in their roots and retain less
in their leaves than the less ¯ood-tolerant Quercus alba
(Gravatt and Kirby, 1998). Regeneration of bottomland
forests is dependent on the trees having the facility to pursue
their natural amphibious life style. The trees of bottomland
forests in North America are highly dependent on intermittent periods of low water levels for regeneration. In the past
it was suf®cient for this to take place once every 20±30
years. However, improved river-level regulation has
removed even this amount of occasional draw-down and
now seriously threatens the regeneration of these forests in
several areas such as the Mississippi Basin and the swamp
forests of Louisiana. Even the recruitment of such ¯oodtolerant trees as the swamp cypress (Taxodium distichum)
and the swamp tupelo (Nyssa sylvatica) is prevented when
there is no relief from constant ¯ooding (Conner et al.,
1981). Similarly, it is predicted that higher ¯ood levels on
the Rhine will reduce the establishment of hardwood trees
species in the low-lying sites in this river's ¯ood-plain
forests (Siebel et al., 1998). The Amazonian tidal swamp
forest (Varzea) provides another example of the variation in
response between species in response to wet and dry
seasons. A study of carbohydrate levels at the end of the dry
season showed that most species had high levels of starch.
The exceptions were the palms and the most aquatic of the
other woody species, for which the dry season was the stress
period and the wet season the period when they accumulated
carbohydrate reserves (Scarano et al., 1994).
In all the ¯ood-tolerant forests so far examined it would
appear that possession of adequate carbohydrate reserves is
a prerequisite for ¯ooding tolerance. It therefore follows
that the risk of carbohydrate starvation is likely to be greater
if winters are warmer and wetter. First, warmer winters will
delay the onset of root dormancy and, secondly, wetter
winters will be likely to cause non-dormant roots to
accelerate their carbohydrate draw-down due to the
hypoxia-induced increased glycolytic activity that normally
affects plants not adapted to long-term anoxia-tolerance
(Braendle and Crawford, 1999). Carbohydrate starvation
will not only deprive plants of energy reserves and create a
so-called `energy crisis', but will also reduce the ability of
the tree to synthesize compounds such as ascorbic acid,
which together with other anti-oxidants are necessary for
preventing tissue damage when ¯ood-waters subside,
exposing plants to the risk of post-anoxic injury.
Carbohydrate metabolism is intimately linked with ascorbate production (Smirnoff and Wheeler, 2000) and starved
roots are likely to be less able to defend themselves against
post-anoxic injury.
CONCLUSIONS
Holocene paludi®cation and extensive forest retreat in
northern and oceanic regions has taken place over the last
6000 years from northern QueÂbec through Newfoundland
and Scandinavia to Arctic Siberia. This has also been a
period over which the climate has become more oceanic in
these areas. It is evident from the results presented here that
a notable effect of episodes of climatic warming during the
last century as a whole has been to increase oceanicity in
northern maritime areas. Climatic warming beyond that
which has occurred during the last two decades is therefore
likely to result in additional increases in precipitation, and
rainfall frequency and further reduction in temperature
range in northern maritime regions. Such changes can be
expected to increase bog growth. Peat accumulation raises
the water table (paludi®cation) and, although there may be
periodic episodes of drying out and forest re-advance, the
underlying peat will remain and can be expected to respond
with renewed growth to further periods of oceanicity. The
northward advance of forest that took place during the early
Holocene as a response to climatic warming will therefore
be unlikely to be repeated as in many areas bogs that have
formed in the intervening period will hinder forest expansion. There may even be a retreat south of the tundra±taiga
interface as more forest in engulfed by further bog
expansion.
ACKNOWLEDGEMENTS
This research has been supported by an Emeritus Fellowship
from the Leverhulme Foundation (R.M.M.C.) which is
gratefully acknowledged. Research on the tundra±taiga
interface has been supported by the Royal Swedish
Academy of Sciences and the International Arctic Science
Committee. Figure 1 was drawn with assistance from Dr B.
Crawford et al. Ð Paludi®cation and Forest Retreat
R. Werkman. The authors thank the Distributed Active
Archive Centre (Code 902.2) at the Goddard Space Flight
Center, Greenbelt, MD 20771, USA for producing and
distributing the Path®nder data in their present form. The
original data products were produced under the NOAA/
NASA Path®nder Program, by a processing team headed by
Ms Mary James of the Goddard Global Change Data Center
and the science algorithms were established by the AVHRR
Land Science Working Group, chaired by Dr John
Townshend of the University of Maryland. Goddard's
contributions to these activities were sponsored by
NASA's Mission to Planet Earth Program.
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