H. John B. Birks1,2,4 & Katherine J. Willis1,3,4

1University of Bergen, 2University College London, 3University of Oxford, and 4Jesus College Oxford

ALPINES, TREES, AND REFUGIA

Introduction

Definitions

Last Glacial Maximum

Alpines in LGM

Trees in LGM

Southern and Mediterranean refugia

Central, eastern, and northern refugia

Current models based on available fossil evidence

Is tree-growth in the LGM of central Europe possible?

Holocene

Cryptic refugia for alpines

Conclusions

INTRODUCTION

The Quaternary period is the past 2.8 million years (Myr) of Earth’s history. A time of very marked climatic and environmental changes

Large terrestrial ice-caps started to form in the Northern Hemisphere about 2.75 Myr, resulting in multiple glacial-interglacial cycles driven by variations in orbital insolation on Milankovitch time-scales of 400, 100, 41, and 19-23 thousand year (kyr) intervals

Glacial conditions account for up to 80% of the Quaternary

Remaining 20% consist of shorter interglacial periods during which conditions were similar to, or warmer than, present day

Glacial conditions:

1. Large terrestrial ice-sheets

2. Widespread permafrost

3. Temperatures 10-25C lower than present at high-mid latitudes

4. High aridity and temperatures 2-5C lower than present at low latitudes

5. Global atmospheric CO2 concentrations as low as 180 ppmv rising to pre-industrial levels of 280 ppmv in intervening interglacials

6. Steep climatic gradient across Europe and Asia during the Last Glacial Maximum (LGM)

Major climate forcing for the last 450 kyr calculated at 60N. Global ice volume (f) plotted as sea-level, so low values reflect high ice volumes.

Jackson & Overpeck 2000

Present day

21,000 cal. year BP

General circulation model (GCM) simulations of 21 kyr Last Glacial Maximum

Pollard & Thompson, 1997; Peltier, 1994

Ice-sheets

Permafrost

Relict soils

Approximate extent of ice and of assumed continuous permafrost in Europe during LGM Willis 1996

Emphasis on EuropeLGMCurrent interglacial – the Holocene‘Alpines’TreesRefugiaPalaeobotanical evidence (macrofossils, microfossils)

“…direct evidence can come only from fossils, indicating the existence, location, and duration of refugia, and their biotic composition in comparison with surrounding areas. Thus, palaeontology and genetics can operate synergistically, each suggesting fruitful geographical sampling areas for the other.”

Stewart & Lister 2001What do we know about the ranges of trees and alpines during the LGM?

What do we know about ‘alpines’ during the current Holocene interglacial?

DEFINITIONS

‘Alpines’ - plants that today have their main occurrences above the altitudinal tree-line or beyond the latitudinal tree-line. Includes alpines sensu stricto and arctic plants

Last Glacial Maximum (LGM) – about 18000-25000 years ago, coldest period of the last (Weichselian) glacial stage

Holocene – last 11500 years (~10000 radiocarbon years) of Earth’s history, so-called ‘post-glacial’ period or current interglacial

Refugia – areas for the growth and survival of species during adverse or unfavourable environmental conditions. Sources for subsequent recolonisations when environmental conditions become more favourable

- areas of survival for species during glacial episodes when temperate species survived in micro-environmentally favourable locations south of the continental ice-sheets and alpine species survived above or below the region of mountain glaciation and near the continental ice-sheets

- refugia for other types of species also existed in areas far removed from glaciation (e.g. tropical rain-forest refugia)

Cryptic refugia – restricted refugia in northern Europe; areas of sheltered topography with buffered, stable local microclimates (Stewart & Lister 2001). Possibly not detectable by pollen analysis

Iversen 1973

Vegetation 20 kyr ago

Widespread ice, tundra, and steppe in north and east; park-tundra in south and east, and forest confined to Mediterranean basin

LAST GLACIAL MAXIMUM

Older Dryas (ca. 14 kyr) landscape in Denmark

Iversen 1973

Abundant alpines along with species of steppe habitats (e.g. Helianthemum, Hippophae, Ephedra)

Possible LGM landscape in central Europe

Open steppe with abundant Artemisia and Chenopodiaceae, and extensive loess deposition

Alpines In LGM

Besides familiar arctic-alpines found commonly as fossils such as

also find fossils of plants not growing in central European mountains, only in northern Europe today

Dryas octopetala Lychnis alpina

Salix herbacea Saxifraga oppositifolia

Salix reticulata Oxyria digyna

Betula nana Bistorta vivipara

Saxifraga cespitosa Silene acaulis

Ranunculus hyperboreus Campanula uniflora

Salix polaris Koenigia islandica

Silene uralensis Pedicularis hirsuta

Lang 1994

Koenigia islandica

Other northern plants found as fossils in central Europe in LGM

Silene uralensis

Salix polaris

Pedicularis hirsuta

Ranunculus hyperboreus

Common alpines in LGM throughout northern and central Europe

Lychnis alpina

Dryas octopetalaSilene acaulis

Bistorta vivipara

Betula nanaSaxifraga oppositifolia

Interglacial

LGM

S N

Traditional refugium model – narrow belt in southern mountains

van der Hammen et al. 1971

Trees in the LGM southern and Mediterranean refugia

Location of Ioannina basin in Pindus Mountains, NW Greece

Tzedakis et al. 2002

Tzedakis et al. 2002

LGM

Pinus

Quercus

Fagus

Ulmus

Corylus

Alnus

Pistacia

Tilia

Betula

Abies

Bennett et al., 1991; Birks & Line, 1992

Pollen evidence for traditional southern European LGM refugial model

Taxa that have reliable macrofossil or pollen evidence for LGM presence in south European refugia

Carpinus betulus Quercus pubescens

Carpinus orientalis Quercus pyrenaica

Castanea sativa Quercus robur

Fraxinus ornus Quercus macrantha

Olea europaea Quercus petraea

Abies Phillyrea

Acer Picea

Alnus Pistacia

Betula Pinus

Corylus Tilia

Fagus Ulmus

Fraxinus

What about trees in central, eastern, and northern Europe during the LGM?

Detection difficult

1. Low pollen values – do these result from long-distance pollen transport or from small, scattered but nearby populations?

Classic problem in pollen analysis since Hesselman’s question to Lennart von Post in 1916. No satisfactory answer.

2. Few continuous sites of LGM age

3. Pollen productivity related to temperature and some trees cease producing pollen under cold conditions

4. Pollen productivity may also be reduced by low atmospheric CO2 concentrations

5. Other sources of fossil evidence critically important – macrofossils, macroscopic charcoal, and conifer stomata

Fossil evidence for trees and shrubs in LGM in northerly locations: pollen & macrofossil evidence

• e.g. Palaeoecological results from Bulhary, South Moravia

• Buried peat dated to 25,000 yr BP

• Pollen record indicates existence of park-forest vegetation (Pinus sylvestris, Pinus cembra, Larix, Picea abies, Juniperus communis)

• Excellent macrofossil assemblage including Betula pubescens and Salix sp.

E. Rybnícová & K. Rybníček, 1991. In: Palaeoevegetational Developments in Europe, Proceedings of the Pan-European Palaeobotanical Conference, 1991, Vienna Museum of Natural History, pp 73-79.

Fossil evidence for LGM refugia in northerly locations: pollen evidence from six sites in Romania

Feurdean et al. 2007

PinusPiceaBetulaSalixJuniperus

Greatest diversity during the LGM found in mid-altitude sites – 800-1300m asl – in Romania

Feurdean et al. 2007

Fossil evidence for trees in central and eastern Europe during the LGM: macroscopic charcoal evidence

Willis & van Andel 2004

Scanning electron microscope images of wood charcoal

Willis & van Andel 2004

SloCro

Aus

Svk

Hun

CzR PolUkr

Rom

SerB&H

CzR – Czech Republic; Aus – Austria; Slo – Slovenia; Cro – Croatia; Pol – Poland; Svk – Slovakia; Hun – Hungary; Ukr – Ukraine; Rom – Romania; Ser – Serbia; B&H – Bosnia & Herzegovina

Willis & van Andel 2004

Tree taxa that have reliable macrofossil evidence for LGM presence in central, eastern, or northern European refugia

Abies alba Pinus cembra

Alnus glutinosa Pinus mugo

Betula pendula Pinus sylvestris

Betula pubescens Populus tremula

Corylus Quercus

Carpinus betulus Rhamnus cathartica

Fagus sylvatica Salix aucuparia

Fraxinus excelsior Sorbus

Juniperus communis Taxus baccata

Picea abies Ulmus

Iberian, Italian, and Balkan peninsula LGM refugia – ‘classical’ model

Not complete

Southern + central + northern European LGM

refugia

Current model

Bhagwat & Willis 2007

MediterraneanLGM refugia

Northerly LGM refugia

Ice sheet

Willis et al. 2007 (in press)

Current model based on available fossil evidence

What was the LGM landscape like?In the lowlands north of the Alps, a mosaic of:

1. open-ground habitats on well-drained soils and exposed sites supporting a mixture of alpines, steppe, and ‘weed’ taxa

2. willow scrub on damper soils

3. tree populations on sheltered localities along river banks, in valleys, and in depressions where there was moisture and some shelter

In the mountains south of the Alps, a mosaic of:

1. low-altitude steppe or shrub steppe

2. belt of trees at mid-altitudes where there was adequate moisture and temperatures were not too cold

3. high-altitude open habitats with alpines and cold-tolerant steppe plants

North of the Alps

South of the Alps

Sichuan, China

Borah Peak, Idaho

Are there any ecological attributes characteristic of trees in southern LGM and northern LGM refugia?

Bhagwat & Willis (2007)

23 trees - southern refugia: large, animal-dispersed seeds

- northern refugia: wind-dispersed seeds

Could the trees identified in the macroscopic charcoal record have grown in the LGM environment of

central, eastern, and northern Europe?

Work in progress by Miguel Araújo, Shonil Bhagwat, and ourselves

Basic approach is to model present-day tree distributions in relation to contemporary climate using seven different species-climate modelling algorithms (climate-envelopes, bagging trees, random forests, etc.) to develop an ‘ensemble forecasting framework’ for analysing species-climate relationships (Araújo & New 2006)

Given modern tree-climate responses and LGM GCM model simulations from Paul Valdes, predict the LGM ranges for trees under LGM climates

LGM GCM models – UGAMP (UK), ECHAM3 (Germany)

predicted today predicted LGM & refugia

Corylus avellana

Fagus sylvatica

S,N

S,N

predicted today predicted LGM & refugia

Alnus glutinosa

Taxus baccata

Betula pendula

S,N

S,N

N

predicted today predicted LGM & refugia

Pinus sylvestris

Picea abies

Juniperus communis

S,N

S,N

N

Combined probabilities of occurrence (potential quantity of suitable habitat)

Today LGM

Abies alba 0.22 0.22 =

Alnus glutinosa 0.67 0.38 -

Betula pendula 0.63 0.36 -

Corylus avellana 0.62 0.31 -

Fagus sylvatica 0.41 0.31 -

Taxus baccata 0.26 0.23 -

Juniperus communis 0.64 0.70 +

Picea abies 0.38 0.45 +

Picea omorika 0.09 0.26 +

Pinus cembra 0.08 0.24 +

Pinus mugo 0.13 0.20 +

Pinus sylvestris 0.48 0.64 +

Some trees may have had more potential habitat in LGM than today

Pinus

Quercus

Fagus

Ulmus

Corylus

Alnus

Pistacia

Tilia

Betula

Abies

Bennett et al. 1991

Early post-glacial migration rates in response to climate change based upon traditional refugial model

Tree-Spreading Rates

• Currently assume spreading from southerly refugia only

• These ‘rates’ of movement in early Holocene are then used in a number of climate envelope models to predict movement of plants in response to future climate change

• But what if plants are not only in ‘southerly refugia’?

• Similar study in USA found that some plants were much further north during the LGM than pollen evidence suggests (e.g. McLauchlan et al., 2005)

• Spreading rates demonstrated to be vastly over-estimated

• Significantly affects our predictions about how plants will respond to global warming

Genetic-diversity Hotspots

• Currently assumed that most plants (and animals) were located in southern refugia and therefore this is where genetic diversity will be greatest.

• Holocene migration from these refugial regions can be mapped through genetic patterns.

• Increasing evidence for certain groups of plants (and animals) that do not fit this ‘southerly refugial model’.

• In order to map and protect centres of genetic diversity properly, need to have proper understanding of where the plants (and animals) existed during the LGM.

• Major challenge to palaeoecologists. More data needed from unambiguous sources like macrofossils and macroscopic charcoal. Need to critically reassess LGM pollen data.

A. Hampe & R.J. Petit, 2005. Ecology Letters 8, 461-481; K.J. Willis & H.J.B. Birks, 2006. Science 314, 1261-1265

Understanding ‘hotspots’ of genetic diversity very important to long-term conservation

HOLOCENE

Cryptic Refugia for Alpines

Alpines widespread in LGM as shown by macrofossil evidence

Became more restricted to alpine and arctic habitats above or beyond the tree-line in early Holocene with major climate warming and competition

Some species also occur today in small, isolated ‘cryptic’ refugia within the potential forest zone

Such cryptic refugia include sea-cliffs, other coastal habitats, inland cliffs and screes, open river-gravels, rocky gorges, and shallow soils on steep limestone slopes (Pigott & Walters 1954)

Ramasaig Cliff, Skye

High Force, Teesdale

Cronkley Fell, TeesdaleInchnadamph, W Sutherland

Yew Cogar Scar, Yorkshire Mullaghmore, County Clare

Bettyhill, Sutherland Dryas octopetala, Sutherland

Cetry Bank, Teesdale

Scar Close, Yorkshire

Falcon Clints, Teesdale

Alpines in UK that descend to low-altitudes (<50m) or even to sea-level (*) include:

Alchemilla alpina* Cerastium arcticum Oxyria digyna*

Arctostaphylos uva-ursi* Draba incana* Polystichum lonchitis*

Arctostaphylos alpina Dryas octopetala* Salix herbacea*

Arenaria norvegica Empetrum nigrum ssp. hermaphroditum*

Salix myrsinites

Asplenium viride* Epilobium anagallidifolium

Saxifraga aizoides*

Betula nana Juniperus communis ssp. nana*

Saxifraga hypnoides*

Bistorta vivipara* Juncus trifidus Saxifraga oppositifolia*

Cardaminopsis petraea* Juncus triglumis Sedum rosea*

Carex bigelowii Loiseleuria procumbens

Silene acaulis*

Carex capillaris* Luzula spicata Thalictrum alpinum*

Carex rupestris* Minuartia sedoides* Tofieldia pusilla

Cerastium alpinum*

Holocene thermal maximum in NW Europe between about 6-8 kyr with summers about 2-2.5C and winters 1-1.5C warmer than today.

Presumably forest- and scrub-zones reached their highest levels at this time.

Close correlation in Scandinavia between geographical distribution limits of alpines in lowland stations and maximum summer temperature, with the critical temperature varying over a range of at least 7C for different species (Dahl 1951).

Lower limits for many alpines controlled directly or indirectly by summer warmth or its close correlates, including growth and competition from more vigorous, larger lowland species.

As several alpines can be successfully grown in lowland gardens, their lower limits are more likely to be controlled by competition rather than by temperature directly (e.g. Sedum rosea).

Holocene thermal maximum may have eliminated altogether some of the most warmth-sensitive or cold-demanding species of the LGM and late-glacial flora (e.g. Cassiope hypnoides, Papaver radicatum agg.)

Others may have only survived in scattered localities at high levels (e.g. Diapensia lapponica, Sagina intermedia, Saxifraga cernua, Gnaphalium norvegicum). Competition-sensitive and warmth-sensitive.

More warmth-tolerant species may have remained widespread and abundant over a greater altitudinal range (e.g. Dryas octopetala). Competition-sensitive only.

Between these extremes, there are all degrees of ‘relictness’.

Almost nothing is known from the fossil record about Holocene history of alpines.

In process of becoming relict, actual localities in which a particular species survives may depend a good deal on chance.

Extent of suitable habitat may also be important.

A relict calcicole species will have a greater chance of survival in an extensive area of calcareous rocks than in an area with a very limited occurrence of suitable substrata.

When conditions for growth of alpines become sub-optimal, plant disease, herbivory, and chance events (e.g. rock-falls) may be causes of decline or local extinction, giving relict distributions.

CONCLUSIONS1. Trees survived the Last Glacial Maximum in refugia in southern,

central, and eastern Europe.

2. Alpines appear to have grown commonly in the LGM in northern and central Europe.

3. Existence of tree refugia in central and eastern Europe means that estimated rates of 500-1000 m per year for tree spreading are vast over-estimates as they assume refugia only around the Mediterranean Basin.

4. Many alpines grow in ‘cryptic refugia’ below the altitudinal tree-line or inside the latitudinal tree-line in naturally open habitats.

5. Cryptic refugia were occupied by trees in the LGM north of the Alps and by alpines in the Holocene.

6. Important implications of cryptic refugia to understanding genetic diversity.

7. Need for further LGM plant fossil evidence, especially macrofossils (seeds, fruits, leaves, macro-charcoal, stomata, etc.) as this is the only real proof of former presence. Provides ‘the factual basis for phytogeography’ (Godwin 1956, 1975).

ACKNOWLEDGEMENTS

Kathy WillisOxford & Bergen

Co-author

ACKNOWLEDGEMENTS

Shonil Bhagwat (Oxford)

Miguel Araújo (Madrid)

Hilary Birks (Bergen)

Cathy Jenks (Bergen)

DEDICATION

Herbert E. Wright, Jr. on the occasion of his 90th birthday for stimulating our interest in LGM refugia in the USA, Iran, and south-eastern Europe.

… but this evidence is based on very few pollen sequences

Huntley & Allen, 2003

Region that has therefore typically been classified as having a full-glacial vegetation as ‘polar desert’ or ‘tree-less’ steppe

But why does it matter what vegetation existed in Eurasia during the last 21 kyr?

? ?

But why does it matter what vegetation existed in Eurasia during the last 21 kyr?

Key to understanding:

• Response rates of plants (and some animals) to climate change

• Genetic diversity of Eurasian plants animals• Accuracy of climate models (ME)

Genetic Diversity Hotspots

• Currently assumed that most plants and animals located in southern refugia and therefore this is where genetic diversity will be greatest

• Postglacial migration from these refugial regions can be mapped through genetic patterns

Pinus sylvestris [Scots pine]3

But increasing evidence of certain groups of plants and animas that do not fit this ‘southerly refugial model

Fraxinus excelsior [Ash]2

Alnus glutinosa [Black alder]1

Calluna vulgaris [Heather]4

In order to properly map and protect centres of genetic diversity, need to have proper understanding of where the plants (and animals) existed during the last full-glacial

Key Research Questions

• What plants grew in Eurasia during last full-glacial to present?

• Where were trees located on the landscape?

• How quickly did plants migrate/move in response to early postglacial warming?

• Where did they move to?

(Alfano et al. QR, 2003)

Inferred extent of permafrost in Europe and N Eurasia during LGM (MAAT = mean annual air temperature)