Contributions of Quaternary botany to modern ecology and biogeography

Figures & data

Table 1. Selected reviews on Quaternary floristic and vegetational history of different geographical areas. See Birks HJB and Berglund (2018) for further examples.

Region	References
Global	Huntley and Webb (1988); Tallis (1991)
Equatorial	Flenley (1979); Bush et al. (2011)
Canada	Ritchie (1984, 2008)
Eastern North America	Webb T et al. (1983a); Davis MB (1983b); Webb T (1988a); Grimm EC and Jacobson (2004)
South America	Urrego et al. (2009)
Europe	Huntley (1988)
Central Europe	Firbas (1949); Lang (1992, 1994)
Czech Republic	Kuneš and Abraham (2017)
Denmark	Iversen (1967, 1973)
Britain and Ireland	Godwin (1975)
Scotland	Edwards KJ et al. (2018)

Table 2. Selected reviews of contributions of Quaternary botany to modern ecology or biogeography.

General – dynamics, no-analogue assemblages, drivers of change, etc.	West RG (1964); Walker (1982a, 1990); Birks HJB (1986, 1993a); Bennett (1988b); Davis MB (1989c); Foster et al. (1990); Delcourt HR and Delcourt (1991); Ritchie (1991, 1995); Schoonmaker and Foster (1991); Huntley (1996); Mitchell FJG (2011); Luouys et al. (2012); Reitalu et al. (2014); Jackson and Blois (2015); Nogués-Bravo et al. (2018)
Resilience, diversity and stability	Walker (1982b, 1989)
Equilibrium–disequilibrium concepts	Davis MB (1986a)
Vegetation dynamics	Walker and Chen (1987); Prentice (1988a)
Interface between Quaternary botany and evolution	Bennett (1997)

Figure 1. (a) Mid-elevation belt of Pinus contorta, P. ponderosa, Picea engelmannii, Betula papyrifera, and Populus tremuloides between lowland xeric Artemisia tridentata sagebrush-steppe and high-elevation snow and dry open alpine vegetation, Borah Peak, Idaho, USA. This is a possible modern analogue for a'classical' macrorefugium for trees in the mountains of southern Europe during the last glacial maximum (LGM). Photograph: HJB Birks. (b) Local stands of Picea crassifolia along water seepages at 3600 m on the south-eastern Tibetan Plateau, Sichuan, China. This is a possible modern analogue for a 'microrefugium' for trees in Europe during the LGM. Modern pollen percentages of Picea at this site are less than 3%. Photograph: HJB Birks.

Figure 2. The glacial–interglacial cycle for north-west Europe showing the broad changes in biomass (above-ground productivity), soil status, and temperature that take place during a glacial stage (cryocratic – blue) and its associated interglacial stage (protocratic, mesocratic, oligocratic and telocratic – orange). The largest changes in temperature occur at the glacial–interglacial transitions; that is at the beginning and end of the cryocratic phase, particularly at the cryocratic–protocratic transition. There are also fine-scale climatic changes within an interglacial stage and a glacial stage. Based on Iversen (1958), Andersen ST (1994), and Birks HJB and Birks (2004). In the Holocene (present interglacial), the Homo sapiens phase (Birks HJB 1986) replaces the oligocratic and telocratic phases at sites with fertile soils (Birks HJB 1986).

Figure 3. Summary pollen diagram of the composite long pollen sequence from the Velay Plateau in the south-eastern part of the French Massif Central. The interglacial stages are shaded in pale brown and the corresponding marine isotope stages (MIS) are shown. Note the change between interglacial stages with dominant temperate trees and cold, dry glacial stages with dominant Poaceae and steppe taxa. The Holocene is MIS 1, the Ribains interglacial is MIS 5e (= Eemian), the Bouchet I interglacial is MIS 7c, the Landos interglacial is MIS 9e, and the Praclaux interglacial is MIS 11e (= Holsteinian). Redrawn and modified from de Beaulieu et al. (2001).

Figure 4. Comparison of interglacial tree pollen stratigraphies in five interglacial stages in the composite long pollen sequence from the Velay Plateau in the south-eastern part of the French Massif Central (Figure 3). Major tree pollen taxa are coloured identically between interglacials. The approximate age of the onset of each interglacial is also shown along with the correlations with marine isotope stages (MIS). Redrawn and modified from de Beaulieu et al. (2006).

Figure 5. Schematic diagram summarising the main stages and associated pedological changes (1–4) occurring in the transition from a podsol supporting coniferous forest in the late-glacial (stages 1 and 2) to a brown-earth soil with deciduous forest in the early-mid Holocene (stage 4) at Kis-Mohos Tó (NE Hungary) via an intermediate phase of a podsolic brown-earth with deciduous trees in the early Holocene (stage 3). The chemical record in the lake sediment at Kis-Mohos Tó is summarised. Redrawn from Willis et al. (1997).

Figure 6. Gerzensee, a kettle-hole lake on the Swiss Plateau at 603 m elevation (46.83°N, 7.55°E). This site has been the focus of detailed studies on rapid warming and associated biotic changes in the late-glacial and early Holocene (Ammann and Oldfield 2000; Ammann et al. 2013a, 2013b, 2013c), for example the study summarised in Figure 7. The Bernese Alps are in the background. Photograph: AF Lotter.

Figure 7. Vegetation and soil development around Termination A (Oldest Dryas/Bølling transition) about 14,665 calibrated years ago at Gerzensee, Switzerland (see Figure 6). Changes in stable oxygen-isotope ratios (δ¹⁸O‰) of bulk carbonate in the lake sediments (A) provide a climate proxy independent of the pollen stratigraphy. The physiognomy of the past vegetation (B) and vegetation type (C) are inferred from pollen (D) and plant-macrofossil data (the nitrogen-fixing shrub Hippophaë rhamnoides is shown in orange in B). Pollen-accumulation rates (grains cm^–2 yr^–1) (D) reflect vegetation cover and biomass, whereas rates of palynological change (per 70 yr) (E) highlight times of marked change shown by a small or big * that are 50% or 75% greater than the mean rate of change, respectively. Palynological richness (α-diversity) (F) is estimated as number of taxa cm^–2 yr^–1 to allow for the changes in pollen-accumulation rates (D). The inferred soils (G) are summarised in terms of the extent of the active layer, amount of nitrogen-fixation based on the abundance of nitrogen-fixing plants in the pollen and plant-macrofossil stratigraphies, and general soil types. Inferred changes in the potential nitrogen and phosphorus resources during the vegetation development are also shown (H). All the stratigraphical data are smoothed with a running mean over five samples. Redrawn and modified from Ammann et al. (2013b) and Birks HJB et al. (2016b).

Table 3. Possible dominant mycorrhizal types and nitrogen fixers in a north-west European glacial–interglacial cycle and suggested levels of above-ground productivity, available soil phosphorus levels, and amount of nitrogen fixation. This scheme is based on many sources including Harley and Harley (1987), Read (1993a, 1993b), Cázares et al. (2005), Kuneš et al. (2011), and Dickie et al. (2013).

Stage Phase	Glacial Cryocratic	Protocratic	Interglacial Mesocratic	Oligocratic + Telocratic
Above-ground productivity	+	++	+++	++
Available P	+	+++	++	+
N fixation	+	+++	++	+
Vegetation	Herbs and open ground	Grassland, open scrub and woodland	Forest	Open forest, heaths, bogs
N-fixers	Dryas, legumes*	Dryas, legumes*	?
Mycorrhizal types
Arbuscular mycorrhiza	Salix, grasses	Juniperus, Salix, grasses	(P-scavengers) Ulmus, Fraxinus, Alnus, Taxus
Ectomycorrhiza	Dryas, Salix	Dryas, Betula, Salix, Populus	Quercus, Corylus	(P-miners) Pinus, Picea, Fagus
Ericoid mycorrhiza		Empetrum		Vaccinium, Empetrum
Non-mycorrhizal	Herbs	Herbs		Herbs

+ = low; ++ = medium; +++ = high

* Including Astragalus alpinus, Lotus corniculatus, Anthyllis vulneraria, Hedysarum spp., Oxytropis spp., and Trifolium spp., which have been found in cryocratic and protocratic pollen assemblages (e.g. Iversen 1954; Andersen ST 1961; Birks HJB 1973)

Figure 8. The series of pollen diagrams presented by Lennart von Post in his 1916 lecture in Kristiania along a south-west to north-east transect from Zealand (site F), through Skåne and Småland (sites 1–8) and into Västergötland, Östergötland, and Närke on the borders of the north and central Swedish uplands (sites 9–12). The southern limit of Picea abies lies between sites 3 and 4, and the northern limit of Fagus sylvatica is near site 6. The EK-Blandskog + Corylus curve is the combined values of Quercus, Ulmus, Tilia, and Corylus (‘Quercetum Mixtum’). The colours are those that von Post used in his original lecture-chart. As on all his diagrams, von Post has signed it in the bottom right-hand corner. Based on a diagram in Fries M (1967) but extensively modified. This series of pollen diagrams was subsequently published in very different formats by von Post (1924, 1926a).

Figure 9. Picea pollen percentages (expressed as percentages of total tree pollen) at over 250 sites in southern Sweden in the (1) Sub-Boreal, (2) early Sub-Atlantic, (3) middle Sub-Atlantic, and (4) recent times. The native southern range limit (in 1924) is indicated as a solid line on the map for recent times (4). Modified from von Post (1924).

Figure 10. Maps of Quercus (deciduous) pollen percentages across Europe for 12,000, 10,000, 8000, 6000, 4000, and 2000 radiocarbon years before present (BP) drawn as isopollen contours representing different percentage values (modified from Huntley and Birks 1983), and for 14,000, 11,500, 9000, 7000, 4500, and 2000 calibrated years BP drawn as different sized solid circles representing different pollen percentage values (modified from Brewer et al. 2017). The blue shading on the dot maps for 14,000 and 11,500 yr BP shows the likely extent of glacial ice in Fennoscandia. The two sets of maps have been approximately correlated in time using the IntCal13 radiocarbon calibration curve and CalPal (www.calpal-online.de) as the isopollen maps are in radiocarbon years BP and the dot maps are in calibrated years BP.

Table 4. Selected examples of Holocene isochrone maps for different geographical areas.

Area	References
Eastern North America	Moran (1973); Davis MB (1976, 1978, 1983a, 1983b, 1986a); Bernabo and Webb (1977); Jacobson GL (1979); Webb T (1981); Webb T et al. (1983a, 1983b); Björck (1985); Davis RB and Jacobson (1985); Gaudreau and Webb (1985); Davis MB et al. (1986)
Britain and Ireland	Birks HJB (1989)
Fennoscandia	Donner (1963); Aario (1965); Aartolahti (1966, 1967); Moe (1970); Persson (1975); Tolonen and Ruuhijärvi (1976); Høeg (1978); Tolonen (1983)
Russia	Serebryanny (1971, 1973)

Figure 11. Isochrones (in radiocarbon years BP) for Quercus pollen in Britain and Ireland. Modified from Birks HJB (1989).

Table 5. Estimated rates of spread (m yr^–1) of trees during the Holocene in Britain and Ireland (Birks 1989) and on the European mainland based on Huntley and Birks (1983), Feurdean et al. (2013), Brewer et al. (2017), and Giesecke and Brewer (2018).2017

	Britain and Ireland (Birks 1989)	Europe (Huntley and Birks 1983)	Europe – S (Feurdean et al. 2013)	Europe – N (Feurdean et al. 2013)	Europe (Brewer et al. 2017)	Europe (Giesecke and Brewer 2018)
Abies	-	40–300	205	170	200	250
Alnus	500–600	50–2000	225	100	200–500	600
Betula	250	>2000	540	260	?	800
Carpinus	-	50–1000	115	60	400	500
Corylus	500	1500	na	na	1000	1000
Fagus	100–200	200–300	130	90	300	400
Fraxinus	50–200	200–500	na	na	200	-
Picea	-	80–500	385	70	250	500
Pinus	<100–700	1500	360	195	?	600
Quercus	50–500	150–500	220	165	500	500
Tilia	50–500	300–500	na	na	500	500
Ulmus	100–550	500–1000	na	na	1000	1000

S = assuming spreading from southern macrorefugia only; N = spreading from northern microrefugia; ? = not estimable; na = not available

Figure 12. Possible scenarios for tree spreading across a large area in an interglacial stage. 1. The moving-front or continuous wave hypothesis where trees 'march' across the landscape. 2. Rare far-distance dispersal events form small outlying populations. 3. Populations expand from the outlying populations into locally favourable sites or enclaves. 4. Merging of large and small populations. Small scattered populations expand (as in 3) and are a source for dispersal events, as are the large populations. Scenarios 2, 3, and 4 combined are likely to be most important. Based, in part, on Davis MB (1987) and Giesecke (2013).

Table 6. Selected examples of range expansions or contractions of taxa that appear to show a ‘stop’ or ‘go’ behaviour during the Holocene.

Taxon/Taxa	Area	Reference
Abies alba and Fagus sylvatica	Central Europe	Tinner and Lotter (2006)
Betula alleghaniensis	Great Lakes region	Jackson and Booth (2002)
Conifers (mixed)	Yellowstone	Krause and Whitlock (2017)
Fagus grandifolia, Tsuga canadensis, and other trees	NE USA and Great Lakes region	Davis MB (1987); Woods and Davis (1989); Parshall (2002); Booth et al. (2004); Minckley et al. (2011); Clifford and Booth (2015)
Juniperus osteosperma	Rockies	Lyford et al. (2003)
Larix laricina	NW Quebec	Peñalba and Payette (1997)
Pinus contorta var. latifolia	Yukon	Edwards ME et al. (2015)
Pinus edulis	Utah	Gray et al. (2006)
Tsuga mertensiana	South-central Alaska	Anderson RS et al. (2017)

Figure 13. The changing relative abundance expressed as a percentage of the maximum attained values of tree taxa through time in Britain and Ireland. The top panel (1) shows how relative abundance changes through time in the absence of any detectable dispersal limitation or expansion limitation, as shown by the Holocene behaviour of Corylus, Populus, Salix, or Ulmus. The middle panel (2) shows relative abundance changes for taxa that experience dispersal limitation but little or no expansion limitation (e.g. Betula, Pinus). The bottom panel (3) shows relative abundance changes for taxa that may experience not only dispersal limitation but also prolonged expansion limitation (e.g. Alnus, Carpinus, Fagus) that may extend for 2000–3000 years. Of these, Alnus is the most extreme in its expansion limitation due to the rarity of its 'island-like' wet habitats. There are not enough detailed data to assess the long-term behaviour of Fraxinus, Quercus, or Tilia.

DL = Dispersal limitation; EL = Expansion limitation; EP = Expansion phase.

Figure 14. Suggested location of refugial areas for Fagus sylvatica during the last glacial maximum (blue circles) and the major spread into Europe during the Holocene (blue arrows). The green shaded areas are the present native range of F. sylvatica. Modified from Magri et al. (2006).

Table 7. Numbers of total and species partial extinctions and exterminations of taxa in recently studied Late Pliocene sequences in Belarus and Early or Middle Pleistocene interglacials in Poland along with their assumed correlations with Marine Isotope Stages (MIS) and interglacial stages in western Europe (Lindner et al. 2013). (Based on Stachowicz-Rybka 2015a and data from Mamakowa and Velichkevich 1993a; Velichkevich and Granoszewski 1996; Velichkevich and Lesiak 1996; Velichkevich and Mamakowa 2003; Velichkevich and Zastawniak 2003; Velichkevich et al. 2004; Stachowicz-Rybka 2011, 2015a, 2015b, 2015c; Drzymulska 2018).

	Estimated age (kyr)	MIS	Western Europe stage	Polish stage	Total extinctions	Species extinctions	Exterminations	Number of taxa identified
Middle Pleistocene	370–425	11	Holsteinian	Mazovian	1	5	4	198
	480–620	13–15	Cromerian IV	Ferdynandovian 2	0	17	4	174
Early Pleistocene	710–760	17	Cromerian III	Domuratovian and Ferdynandovian I (Podlasian p.p.)	0	12	3	155
	790–815	19/20	Cromerian II/Glacial A1	Augustovian (Podlasian p.p.)	0	13	3	147
	865–1000	21	Cromerian I	Podlasian p.p.	0	18	4	162
Late Pliocene				Kholmech	1	78	24	170

p.p. = in part

Table 8. Comparison of modern climatic requirements of cool-temperate tree genera that grew in Europe in the Neogene but had been exterminated by the early Pliocene, that were present in Europe in the Neogene but have relictual disjunct distributions today, and that were present in the Neogene and are widespread in Europe today (based on Svenning 2003). Minimum growing degree days and the moisture index (actual evapotranspiration/potential evapotranspiration) are only available for genera in North America.

	Regionally extinct in Europe	Relictual in Europe	Widespread in Europe
Cool-temperate tree genera	38	9	26
Mean temperature of the coldest month (°C)	−7.98 ± 6.39	−12.0 ± 5.76	−23.4 ± 9.14
Mean annual temperature (°C)	6.26 ± 4.00	4.26 ± 2.88	−4.47 ± 2.28
Mean annual precipitation (mm yr^–1)	547 ± 322	273 ± 206	274 ± 215
Growing degree days (°C)	1.4 ± 0.64	1.3 ± 0.41	0.37 ± 0.45
Moisture index (AET/PET)	0.54 ± 0.26	0.29 ± 0.23	0.28 ± 0.22

Table 9. Selected genera or species other than trees that were exterminated from north-west Europe during the Neogene or Pleistocene. See Tralau (1959, 1963a), van der Hammen et al. (1971), Huckerby and Oldfield (1976), Watts (1988), Lang (1994), Mai (1995), Drzymulska (2018), and Góis-Marques et al. (2019) for details.

Shrubs	Ferns
Clethra	Osmunda cinnamonea
Coriaria	O. claytonia
Corylopsis	Wetland shrubs or herbs
Eleagnus	Chamaecyparis thyoides
Fothergilla	Decodon verticillatus
Parthenocissus	Dulichium arundinaceum
Rhus	Aquatic plants
Staphylea	Azolla filiculoides
Styrax	Brasenia schreberi
Vines	Euryale ferox
Epipremnum	Nymphoides aquatica
Schizandra	Proserpinaca cf. palustris

Table 10. Selected examples of publications on the role of persistence, evolutionary adaptation, and of phenotypic plasticity in influencing biodiversity patterns today and in the future.

Holt (1990)	Nicotra et al. (2010)	Merilä and Hendry (2014)
Davis MB and Shaw (2001)	Sussman (2010)	Etterson et al. (2016)
Etterson and Shaw (2001)	Dawson TP et al. (2011)	Graae et al. (2018)
Davis MB et al. (2005)	Hill JK et al. (2011)	Henn et al. (2018)
Jump and Peñuelas (2005)	Hoffmann and Sgrò (2011)	Lallensack (2018)
Parmesan (2006)	Shaw RG and Etterson (2012)	Nogués-Bravo et al. (2018)
Aitken et al. (2008)	Alberto et al. (2013)
de Witte and Stöcklin (2010)	Franks et al. (2014)

Figure 15. (1) Fundamental, potential, and realised niches of a species in response to two environmental variables. The realised niche is where populations of the species actually occur and is a subset of the potential niche constrained by biotic, abiotic, and other factors. The potential niche is where the fundamental niche intersects with the realised environmental space at a particular time. (2) A schematic representation of how changes in the realised environmental space between time 1 and time 2 can affect species co-occurrences. At time 1, the potential niches of species 1 and species 2 overlap and the species can potentially co-occur at sites within the intersection. At time 2, the potential niches of the two species do not overlap and hence they will not co-occur in the realised world. (3) The four modes of population response of five species (a-e) to environmental change. Species a mode 1: persistence. Species b modes 1 and 2: shift within local habitat conditions. Species c modes 1, 2, and 3: spread to distant newly-suitable sites and disappear from some former sites. Species d modes 1 and 4: widespread extirpation without colonisation of new areas, thereby changing from being a widespread species to a local or rare species. Species e is the inverse of species d where a formerly rare species colonises extensive new areas. Redrawn from Jackson and Overpeck (2000).

Table 11. The frequency of the four modes of response in species populations and species combinations (‘associations’) within Europe and North America during the late-Quaternary.

Mode	Population	Associations
1. Persistence	Rare	Rare
2. Local shifts	Occasional – frequent	Occasional
3. Spreading, colonisation, and expansion	Common	? Rare
4. Local or regional extermination	Frequent	Common

Table 12. Suggested drivers within the realised environment space (RES) resulting in no-analogue pollen assemblages and possible no-analogue vegetation types during different stages in the late-Quaternary in north-west Europe and eastern North America.

Stages	Potential drivers within RES	References
Interglacials	Climate and seasonality ?Herbivores ?Lags in spreading and population expansion	Watts (1988); Bartlein et al. (1998); Sandom et al. (2014b); Past Interglacials Working Group of PAGES (2016)
LGM	Climate ?Herbivores ?Soils Low CO2	Iversen (1967, 1973); Godwin (1975); Lang (1994); Jackson et al. (2000b); Jackson and Williams (2004)
Late-glacial	Climate, especially seasonality induced by insolation change Herbivores Fire Soils	Iversen (1954, 1967, 1973); Cushing (1963); Birks HH (2003); Jackson and Williams (2004); Gill et al. (2009, 2012); Jones RA et al. (2017)
Early Holocene	Climate, especially seasonality induced by insolation change Lags in spreading or population expansion	Webb T (1981, 1987); Prentice (1983); COHMAP Members (1988); Wright et al. (1993); Birks HJB (2008)

Figure 16. The three major hypotheses (H1–H3) and processes for changes in pollen-assemblage composition and abundance: environmental forcing (H1), biotic interactions (H2), and neutral processes (H3) that can cause ecological drift (Jackson and Blois 2015). These processes may interact in the real world. Exogenous environmental change (e.g. climate change) may be a major driver of assemblage properties both directly and indirectly by influencing interactions between taxa and initiating neutral processes. Climate varies continuously and may influence processes within all three hypotheses to modify assemblage properties (Jackson and Blois 2015). The three underlying hypotheses H1, H2, and H3 correspond to the hypotheses discussed in the text. Modified from Jackson and Blois (2015).

Table 13. Estimates of tree-population doubling times (t_d = log_n(2/r); rounded to nearest 5 years) derived from pollen-stratigraphical data (PAR) from North America (Tsukada and Sugita 1982; Tsukada 1982c, 1982d; Bennett 1986, 1988a; MacDonald and Cwynar 1991; MacDonald 1993a; Fuller 1998; Edwards ME et al. 2015), England (Bennett 1983, 1988b), Central Europe (Giesecke et al. 2007; Bradshaw RHW et al. 2010), Italy (Magri 1989), north-east Australia (Walker and Chen 1987; Chen 1988), and Japan (Tsukada 1981, 1982a, 1982b, 1982c; Tsukada and Sugita 1982; Kito and Takimoto 1999). Modified from MacDonald (1993a).

Region		Taxon	Doubling time (years)
North America		Abies	410
		Alnus rubra	110–180
		Fagus grandifolia	240–445
		Picea	35–180
		Pinus contorta ssp. contorta	110–175
		Pinus contorta ssp. latifolia	80–1100
		Pseudotsuga menziesii	50–365
		Tsuga mertensiana	30–460
		Tsuga plicata	225–240
England		Alnus glutinosa	175–270
		Betula	60
		Corylus avellana	45
		Pinus sylvestris	75
		Quercus	80–140
		Tilia cordata	100
		Ulmus	30–68
Central Europe		Fagus sylvatica	200–430
Italy		Abies	1120
		Carpinus	370–1360
		Corylus	440
		Fagus	370–810
		Juniperus	1175
		Olea	620
		Pinus	1130
		Quercus (deciduous)	665–1290
		Tilia	720
		Ulmus	665
		Zelkova	715
Australia	Gymnosperm canopy trees	Agathis	200
		Podocarpus	240–355
	Angiosperm canopy trees	Balnops	170
		Blepharocarya	150
		Cunoniaceae	65–120
		Elaeocarpus	105–165
		Eugia	185
		Rapanea	150
	Secondary trees	Macaranga/Mallotus	90–105
		Moraceae/Urticaceae	80–110
		Trema	80–110
Japan		Cryptomeria japonica	265–1085
		Fagus	125–435
		Pinus	55

Table 14. Estimates of tree-population halving times (t_h = log_e(2/r); rounded to nearest 5 years) derived from pollen-stratigraphical data (PAR) from North America (Tsukada and Sugita 1982), England (Peglar 1993a; Peglar and Birks 1993), and Japan (Tsukada 1983).

Region	Taxon	Halving time (years)
North America	Castanea dentata	5–15
	Tsuga canadensis	35
England	Ulmus	5
Japan	Picea	200–580

Table 15. Estimates of tree-population doubling times (t_d = log_e(2/r); rounded to nearest 5 years) derived from pollen-stratigraphical data (PAR) from two sites in southern Ontario after the marked decline of Tsuga canadensis pollen at about 5400 years ago (calculated from data in Fuller 1998).

Region	Taxon	Doubling time (years)
Ontario, Canada	Acer saccharum	350–695
	Betula	350–695
	Fagus gradifolia	230–695
	Pinus banksiana/resinosa	350–695
	Pinus strobus	695
	Quercus	350
	Thuja/Juniperus	230–695
	Tsugao canadensis	760–1000

Table 16. Estimates of tree-population doubling times (t_d = log_e(2/r); rounded to nearest 5 years) calculated from the eigenvalue (λ) of the transition matrix where log_eλ = r (see Piñero et al. 1984). Data from various sources compiled and documented by Bennett (1986).

Taxon	Doubling time (years)
Araucaria cunninghamii	35
Araucaria hunsteinii	10–15
Astrocaryon mexicanum	20
Nothofagus fusca	25
Pentaclethra macroloba	350
Podocarpus barteri	55
Sequoia sempervirens	165

Figure 17. Generalised pollen-stratigraphical patterns and inferred population processes suggested by Watts (1973) in the establishment and expansion of a tree in the mesocratic phase within an interglacial stage. The very approximate durations of the establishment and expansion intervals are also shown. Modified from Birks HJB and Tinner (2016a).

Figure 18. Hypothetical pollen-stratigraphical reflections of the same climate oscillation in different regions along an imaginary transect from south to north. In the far north, locality A, the climatic oscillation results in a retreat of tundra and expansion of ice. Locality B records the classical Allerød–Younger Dryas–early Holocene pattern of Betula woodland–tundra–Betula woodland. Farther south, the climatic oscillation is recorded by other vegetational and hence pollen-stratigraphical changes. Note that at localities D and F no major pollen-stratigraphical changes are observed as no ecotones are crossed. Based on Fægri and Iversen (1950).

Figure 19. Contrasts between an abrupt extrinsically forced ecological change (left panels) with an abrupt intrinsically forced change (right panels). In the extrinsically forced change, a large widespread change in temperature (a), e.g. the Younger Dryas–Holocene transition, causes abrupt ecological changes that are synchronous with or slightly lag behind the climate change at sites 1, 2, and 3 (c), resulting in a strong temporal coherence of change (e). With intrinsically forced change, a long-term progressive trend such as droughts and megadroughts (b) are mediated by site-specific (1–6) thresholds (d). These site-specific thresholds cause abrupt changes across the drought period (f). Clusters of site-level abrupt changes may result from extreme events which may impact many sites simultaneously (f). Modified from Williams et al. (2011a).

Figure 20. (a) The ecological thresholds for the establishment of prairie, oak (Quercus) woodland, and mixed deciduous forest (Bigwoods) in central Minnesota plotted along a climatic gradient (e.g. precipitation) that influences fire frequency. Redrawn from Grimm EC (1983). (b) Schematic representation of ecological thresholds for the establishment of prairie and woodland in central Minnesota. The horizontal axis is time; the vertical axis is a climatic gradient (e.g. mean annual precipitation). In the upper right quadrant (woodland only) above the woodland threshold for annual precipitation (Pw), only woodland will persist as a stable state once it is established. Either of two potentially stable states – woodland or prairie – can persist in areas with climate delimited by the thresholds for woodland (Pw) and prairie (Pp), while only prairie will persist as a stable state below the critical threshold for annual precipitation (Pp) and for increased fire recurrence (lower right quadrant: prairie only). Tw represents the minimum time required for woodland to invade prairie. The vegetation outcomes and pathways are summarised in the right-hand column. Redrawn from Grimm EC (1983) and Delcourt HR and Delcourt (1991).

Table 17. Selected examples of detailed fire histories reconstructed from charcoal in Quaternary botanical sequences with emphasis on interactions of fire with other variables, and rapid state shifts and system dynamics.

Interaction of fire, climate, vegetation, biomass and fuel-load, land use, and fauna	Rapid state shifts, alternative stable states, alternative transient states, abrupt changes (‘tipping points’) and system dynamics
Camill et al. (2003)	Walker (1982b)
Szeicz et al. (2003)	Tausch et al. (1993)
Craine and McLauchlan (2004)	Franklin SB and Tolonen (2000)
Umbanhowar (2004)	Lytle (2005)
Lynch et al. (2006, 2014)	Fukami and Nakajima (2011)
Umbanhowar et al. (2006)	Minckley et al. (2012)
Hotchkiss SC et al. (2007)	Fletcher et al. (2014b)
Shuman et al. (2009)	Calder and Shuman (2017, 2019)
Frégeau et al. (2015)	Crausbay et al. (2017)
Brussel et al. (2018)	Jeppesen et al. (2018)
Carter VA et al. (2018a)	Ratajczak et al. (2018)
Finsinger et al. (2018)	Stevens-Rumann et al. (2018)
Mariani et al. (2019)	Calder et al. (2019)

Table 18. Selected examples of recent theoretical and Quaternary studies on ecosystem dynamics, in particular regime shifts.

Theoretical studies
Scheffer et al. (2001, 2012, 2015) Andersen T et al. (2009) Contamin and Ellison (2009) Brock and Carpenter (2010)	Drake JM and Griffen (2010) Scheffer (2010) Carstensen and Weydmann (2012) Dakos et al. (2015)	Burthe et al. (2016) Ratajczak et al. (2018) Taranu et al. (2018)
Quaternary botanical studies on detecting regime shifts, thresholds, and tipping points
de Boer et al. (2013b) Davies (2016b)	Morris et al. (2019)	Stegner et al. (2019)
Palaeolimnological studies on detecting regime shifts, early-warning signals of a critical transition, thresholds, and tipping points
Randsalu-Wendrup et al. (2012, 2014, 2016) Wang R et al (2012) but see Carstensen et al. (2013)	Seddon et al. (2014b) Bunting L et al. (2016)	Ramstack Hobbs et al. (2016) Beck et al. (2018) Taranu et al. (2018)

Table 19. Approximate age of modern British woodland assemblages inferred from pollen-analytical stratigraphies and macrofossil data. The assemblages are based on the dominant tree taxa as indicated from pollen and/or plant macrofossil taxa. To aid vegetation reconstruction, fossil tree-pollen values have been transformed by Andersen’s (1970) general pollen representation factors as modified for British taxa (Edwards ME 1986). The antecedent pollen assemblage or vegetation type are based on available dated pollen data from Britain (Birks HJB 1989; Bennett and Birks 1990; Fyfe et al. 2010, 2013; Brewer et al. 2017). For details of the NVC types, see Rodwell et al. (1991).

Assemblage	NVC type	Estimated age of assembly (cal kyr BP)	Antecedent assemblage or vegetation type
Modern assemblages
Salix spp. woodland	W1 – 3	13.5	Late-glacial tall herb vegetation
Betula spp. woodland	W4	12.9	Juniperus and Salix scrub, herbs
Alnus glutinosa woodland	W5, W6	6.3–7.8	Salix woodland
Alnus glutinosa–Fraxinus excelsior woodland	W7	6.8	Mixed woodlands with abundant Ulmus
Fraxinus excelsior woodland	W8, W9	3.2	Mixed Quercus and Fagus woodlands
Quercus spp. woodland	W10, W11, W16, W17	9.5	Betula–Pinus woodland
Fagus sylvatica woodland	W12, W14, W15	4.5	Mixed Quercus and Tilia woodlands
Taxus baccata woodland	W13	4.0	Mixed Quercus woodland
Pinus sylvestris woodland	W18	8.8	Betula woodland and Juniperus scrub
No obvious modern counterparts
Betula–Corylus woodland		10.9	Salix scrub and grassland
Betula–Corylus–Pinus woodland		10.1	Betula–Corylus woodland
Corylus–Quercus–Ulmus woodland		10.1	Betula-Corylus woodland
Tilia cordata woodland		8.8	Betula–Corylus–Quercus–Ulmus woodland

NVC = National Vegetation Classification; W = Woodland; cal kyr BP = thousands of calibrated years before present

Table 20. Selected examples of prehistoric human activities in the Amazon basin, lowland Congo basin, and Indo-Malaya region detected by palynological and associated palaeoecological studies with the approximate age of the activities and relevant references.

Region	Activity	References
Amazon Basin
Lowland Amazonia	Prehistoric burning and agriculture from about 500 BCE to create fertile Terra Preta de Indio (Indian dark earth) soils through addition of organic waste, excrement, and bones	Glaser (2007); Junqueira et al. (2010); Willis and Bhagwat (2010)
Upper Xingu region, Brazil	Transformation of forest to agricultural land and parkland 1250–1600 CE; catastrophic depopulation 1600–1700 CE	Heckenberger et al. (2003, 2007); Willis and Bhagwat (2010)
Western Amazonia	Localised agriculture and burning 3000–1000 BCE, palm use	McMichael et al. (2015); Bush et al. (2016, 2017); van der Sande et al. (2019)
Central and western Amazonia, Peru, and Brazil	Forest clearance, burning, cultivation of Zea mays and possibly Manihot esculenta 5000–1000 BCE, and cultivation of Oryza 2000 BCE	Bush et al. (1989, 2007a, 2007b); Browne Ribeiro (2017); Hilbert et al. (2017)
Bolivian Amazonia	Plant cultivation (Zea mays, Annonaceae, Cucurbitaceae), forest disturbance and fires 6000–600 BCE	Whitney et al. (2013); Maezumi et al. (2018a, 2018b)
Ecuadorian Amazonia	Zea mays cultivation 500 BCE–1200 CE	Bush and Colinvaux (1988)
Northern Peruvian aseasonal Amazonia	Local-scale forest clearances since 450 BCE indicating persistent localised impacts by pre-Columbian indigenous people	Kelly TJ et al. (2018)
Colombia Amazonia	Increased abundance of palm trees	Balée (1988); Behling (1996); Behling et al. (1999)
Lowland Congo Basin
Gabon	Extensive habitation, clearance, and cultivation of Pennisetum glaucum, iron-working furnaces 1000–650 BCE	Mbida et al. (2000); Oslisly (2001); White LJT (2001); Willis et al. (2004); Oslisly et al. (2013)
Republic of Congo	Localised forest burning 1000 CE–today	Brncic et al. (2007); Tovar et al. (2014)
Indo-Malaya
Thailand	Human occupation and management of lowland rainforests, possibly increasing tree richness	Kealhofer and Penny (1998); Kealhofer (2003); White JC et al. (2004); Willis et al. (2004)
Sumatra	Slash-and-burn clearance and agriculture 5000 BCE, permanent clearings early CE	Maloney (1980, 1985); Morley (1982); Flenley (1988); Flenley and Butler (2001)
Sarawak, Malaysian Borneo	Decline of coastal peat swamp forests by burning and human activity 1500 CE	Cole LES et al. (2015)
Irian Jaya, Indonesia	Forest destruction by fire 8000 BCE	Flenley (1988); Haberle et al. (1991)
Papua New Guinea	Forest clearance in highlands from 3000 BCE or earlier, swamp disturbances from 7000 BCE possibly for Colocasia cultivation, burning from 8000 BCE, agriculture and banana cultivation 7000 BCE	Walker and Flenley (1979); Flenley (1988); Denham et al. (2003); Willis et al. (2004); Boyd et al. (2005); Summerhayes et al. (2017)
New Guinea highlands	Forest exploitation 4900–3600 BCE, forest disturbance, introduction of Ipomoea batatas, forest ‘gardening’ 800–1000 CE and 1700–1800 CE	Oldfield et al. (1980); Worsley and Oldfield (1988); Summerhayes et al. (2010, 2017)
Solomon Islands	Forest clearance by people of New Georgia in 1800 CE with a population twice that of today with settlements of up to 7000 people, subsequent population decline and migration, secondary forest regeneration	Bayliss-Smith et al. (2003); Willis et al. (2004)

Table 21. Selected examples of publications on the potential contribution of Quaternary or ‘Deep-time’ palaeobiological studies to conservation by providing a historical perspective.

General
Hunter et al. (1988) Dietl and Flessa (2009, 2011, 2017) Rick and Lockwood (2012) Davies et al. (2014) Dietl et al. (2015)	Davies (2016a) Dietl (2016b) Rull et al. (2016) Boyer et al. (2017)	Gillson et al. (2017) Kosnik (2018)
Climate change and reserve design
Graham RW (1988)
Ecosystem management and applications to conservation
Gillson and Marchant (2014)
Historical ecology and conservation
Szabó and Hédl (2011)
Deep-time perspectives
Yasuhara et al. (2016)

Table 22. Further examples of Quaternary palaeobiological studies that link directly to conservation and management that are not discussed in the text.

General
Willis et al. (2007a, 2007b) Davies and Bunting (2010)	Gill et al. (2015) Gillson (2015)	Rull et al. (2017b) Whitlock et al. (2018)
Forest conservation
Delcourt HR (2002)	Vegas-Vilarrúbia et al. (2011)
Wetland conservation
Gell P (2017)
Biodiversity and management
Hanley et al. (2008, 2009a)
Resource management
Jackson et al. (2009a)	Colombaroli et al. (2017)
Archaeology and historical ecology
Hayashida (2005)	Ekblom and Gillson (2017)
Future climate change
Willis et al. (2010b)

Table 23. Selected examples of detailed local- or regional-scale palynological studies on the history of specific vegetation types in Europe, Asia, and United States.

Czech Republic	Jamrichová et al. (2012); Bobek et al. (2018)
Ireland	Mitchell FJG (1988)
Italy	Hofstetter et al. (2006); Tinner et al. (2013)
Kyrgyzstan	Beer et al. (2008)
North-east United States	Foster et al. (1996); Motzkin and Foster (2002); Foster and Motzkin (2003)
Norway	Bjune et al. (2013)
Romania	Feurdean and Willis (2008)
Slovakia	Juřičková et al. (2018)
Spain	Morales-Molino et al. (2017); Ezquerra et al. (2019)
Sweden	Lindbladh and Foster (2010)
Switzerland	Valsecchi et al. (2010); Tinner et al. (2013)

Table 24. Selected examples of palaeoecological studies that contribute to establishing baseline or reference conditions at a particular site or vegetation type.

General approach and rationale
Davis MB (1989c) Willis et al. (2005)	Froyd and Willis (2008)	Birks HJB (2012a)
Lakes and wetlands
Battarbee (1999) Ayres et al. (2008) Renberg et al. (2009)	Gell P. (2010) Bennion and Simpson (2011) Battarbee et al. (2012)	Sayer et al. (2012) Wiik et al. (2015)
Peatlands
Geary and Fyfe (2016)
Heathlands
Forbes et al. (2018)
Grasslands and steppe
Pokorný et al. (2015)	Novenko et al. (2016)
Deciduous forests
Lindbladh et al. (2007)
Conifer forests
Stephenson (1999) Swetnam et al. (1999)	Gavin et al. (2009) Bjorkman and Vellend (2010)	Carter VA et al. (2018b)

Figure 21. Vegetation responses at two sites on eastern Madagascar (Fossa and Bassin) to an environmental perturbation (sea-level rise and subsequent drought) about 1000 years ago. Pollen assemblages at Fossa (left) recover towards the previous stable state (high ecological resilience) whereas at Bassin (right) the pollen assemblages continue to diversify (low ecological resilience). Each period shows a time-series of relative pollen proportions (vertical axis) (P continuous line) and a smoothed version (dashed line) based on a robust locally weighted polynomial model (span = 0.25). Heathland is Erica, Asteraceae, and Poaceae pollen, 'Forest' is the sum of pollen of littoral forest tree taxa at Fossa and the sum of pollen of open Uapaca forest tree taxa at Bassin. Recovery refers to a return to forest conditions (see Virah-Sawmy et al. 2009a, 2010 for details). The small inset panels in each large panel show a phase plot for the smoothed pollen data where the relative pollen abundance (P) is plotted against the local rate-of-change gradient (horizontal axis) (ΔP/Δt). The smoothed data were interpolated and resampled at uniform time intervals for the same number of points as in the original data-sets. The proximity of these points on the phase plots indicate the rate of change in system state, with arrows showing the direction of time from old to young. The dashed ovals enclose the stable forest state prior to the perturbation. The system appears to be moving towards full recovery at Fossa (high ecological resilience) whereas there are no signs of recovery at Bassin (low ecological resilience). Redrawn from Willis et al. (2010a).

Figure 22. A schematic representation of the glacial legacy or ‘ecological memory’ on interglacial vegetation models of Herzschuh et al. (2016). During interglacials following mild glacial stages (left), NE Asia was colonised by evergreen trees (e.g. Picea, Pinus) from nearby glacial-stage refugia. In contrast, during interglacials following cold glacial stages (right) Larix spp. and deciduous shrubs were dominant in response to the combined effects of permafrost persistence and distant glacial-stage refugia of evergreen trees, and fire. This model implies that vegetation–climate disequilibrium can last for many millennia. Modified from Herzschuh et al. (2016).

Table 25. Comparison of ‘proximate’ and ‘ultimate’ diversity and stability on oceanic islands and continental mainlands (modified from Cronk 1997).

	Oceanic islands	Continental mainlands
Diversity
Proximate (richness)	Low	High
Ultimate (uniqueness)	High	Low
Stability
Proximate (ecological time 1–100 years)	Low	High
Ultimate (geological time 10^3–10^6 years)	High*	Low

*Oceanic islands are unstable over longer time periods (>~10x10⁶ yrs) as they can sink below the sea and become sea-mounts – the general dynamic of oceanic island biogeography (see Whittaker RJ et al. 2008, 2017; Fernández Palacios 2016; Weigelt et al. 2016; Borregaard et al. 2017)

Table 26. Selected examples of islands or island groups in different oceans where pollen-analytical studies show compositional stability prior to the onset of human impact and ecosystem modification. The approximate duration of the periods with stable pollen composition is given, along with the age for the onset of human activities and an indication of plant extinctions or exterminations of all types on each island. The duration of the stable phases are minimal as the pollen assemblages in some of the sequences may commence within the stable phase.

Island or island group	Approx. duration of stable pollen composition (cal. yrs)	Onset of human impact	Extinctions or exterminations (all types)	References
Atlantic Ocean
Iceland	6000	870 CE	-	Caseldine et al. (2003); Lawson et al. (2007)
Færoe Islands	9000	700 CE	+	Jóhansen (1968, 1985, 1989); Hannon and Bradshaw (2000); Hannon et al. (2001, 2005, 2010); Lawson et al. (2005, 2008); Vickers et al. (2005)
Shetland Isles	6000	2500 BCE	+	Jóhansen (1975); Bennett et al. (1992)
Outer Hebrides	8000	500 CE	+	Bennett et al. (1990)
Azores	5500	1450 CE	+	Connor et al. (2012); Rull et al. (2017a)
Canary Isles	7000	100 CE	+	de Nascimento et al. (2009, 2016); Nogué et al. (2013)
Santo Antâo Island, Cabo Verde	~1700	450 CE		Castilla-Beltrán et al. (2019)
Bermuda	8000	1600 CE	-	Watts and Hansen (1986); Rueger and von Wallmenich (1996)
Haiti	6000	3000 BCE	+	Higuera-Gundy et al. (1999)
Tristan da Cunha	5000	1550 CE	-	Hafsten (1960); Ljung (2007); Ljung and Björck (2011)
Inaccessible Island	8000	?	-	Preece et al. (1986)
Nightingale Island	~8000	1700 CE	-	Hafsten (1951)
Gough Island	~4000	1700 CE	-	Hafsten (1960)
Falkland Islands	7000	?	-	Barrow (1978)
South Georgia	6000	?	-	Barrow (1978, 1983a, 1983b); Barrow and Lewis (1983); Clapperton et al. (1989)
South Shetland Islands	300	?	-	van der Knaap and van Leeuwen (1993)
Mediterranean
Balearic Islands	4000	4000 BCE	-	Yll et al. (1994, 1997); Pérez-Obiol and Sadori (2007)
Corsica	4000	2000 BCE	-	Reille (1975)
Sicily	6000	750 BCE	-	Pérez-Obiol and Sadori (2007); Noti et al. (2009); Tinner et al. (2009)
Malta	3000	7500 BCE	-	Carroll et al. (2012)
Crete	3000	6000 BCE	-	Bottema (1980); Bottema and Sarpaki (2003)
Indian Ocean
Madagascar	3000–6000	0–30 CE	+	Burney (1987a, 1993); Virah-Sawmy et al. (2010)
Mauritius	7500	1600 CE	+	de Boer et al. (2013a, 2013b); Gosling et al. (2017)
Marion Island	6000	?	-	Scott (1985)
Pacific Ocean
Carlisle Island, Alaska	7300	?	-	Kuzmicheva et al. (2019)
St Paul Island, Alaska	14,000	?	-	Graham RW et al. (2016); Wang Y et al. (2017); Wooller et al. (2018)
Hawaiian Islands	6000	1000 CE	+	Selling (1948); Burney et al. (1995); Hotchkiss S and Juvik (1999); Hotchkiss S (2003)
Galápagos	9000	500 CE	-	Colinvaux and Schofield (1976); Restrepo et al. (2012); Astudillo (2018)
Marquesas Islands, French Polynesia	1000	1500 CE	-	Allen MS et al. (2011)
Mo’orea, French Polynesia	2000	1000 CE	-	Stevenson et al. (2017)
Tahiti, French Polynesia	>6000	1700 CE	-	Prebble et al. (2016)
Rimatara, French Polynesia	800	1100 CE	+	Prebble and Wilmshurst (2009)
Rapa Nui (Easter Island)	22,000	1200 CE	+	Flenley et al. (1991); Dumont et al. (1998); Hunt TL and Lipo (2006); Mann DG et al. (2008)
Selkirk Island (Chile)	7000	1500 CE	-	Haberle (2003)
Southern Ocean
North Island, New Zealand	2000	1100 CE	-	Prebble and Wilmshurst (2009)
South Island, New Zealand	3000	400 CE	-	Prebble and Wilmshurst (2009)
Tasmania	8000	1400 BCE	-	Fletcher and Thomas (2010); Fletcher et al. (2014a); Stahle et al. (2016); Jones PJ et al. (2017)

- = no evidence of extinctions/exterminations; + = evidence of extinctions/exterminations; ? = unknown or not clear, cal = calibrated

Figure 23. Summary percentage pollen diagram from Ewing Island (sub-Antarctic Auckland Islands) with selected taxa plotted against depth with a calibrated age scale in years CE. Grey zone shows the time of earliest sealing activity in the region. Redrawn from Wilmshurst et al. (2015).

Figure 24. Mount Roraima, a spectacular tepui in Venezuela. Photograph MM from Switzerland (Wikimedia Commons).

Figure 25. Near the summit area of the Eruoda tepui, north-east of the Chimautá massif, Guyana Highlands where Nogué et al. (2009) prepared a pollen sequence covering the last 13,000 years. Photo: Sandra Nogué-Bosch.

Figure 26. Summary pollen and Sporormiella-type (Sporor.) spore stratigraphies (expressed as percentages of upland pollen sum) and charcoal concentrations at Appleman Lake, Indiana between 16,700 and 9000 years ago. The shaded part indicates when the pollen assemblage has no modern pollen analogue. The Sporormiella-type spore record is used as a proxy for megafaunal abundance. Modified from Gill et al. (2009).

Figure 27. Conceptual model of top-down drivers of Late Quaternary vegetation dynamics mediated by biotic interaction. Arrow thickness reflects the hypothesised relative importance of each link. Dashed arrows represent poorly understood or studied relationships. Modified from Gill (2014).

Table 27. Recent contributions to the debate about the causes of Late Pleistocene and early-Holocene megafaunal extinctions.

Barnosky et al. (2004a, 2004b, 2015)	Sandom et al. (2014a)	Westaway et al. (2017)
Koch PL and Barnosky (2006)	Cooper et al. (2015)	Galetti et al. (2018)
Hansen and Galetti (2009)	Grayson and Meltzer (2015)	Price et al. (2018)
Lorenzen et al. (2011)	Graham RW et al. (2016)	Mann DH et al. (2019)
MacDonald et al. (2012)	Saltré et al. (2016)	Smith FA et al. (2019)
	Di Febbraro et al. (2017)

Figure 28. Schematic summaries of the general major trends in the four types of diversity proposed by McGill et al. (2015) at the meta-community scale of organisation (sensu McGill et al. 2015) within the protocratic, mesocratic, Homo sapiens, and oligocratic phases of the Holocene and the last 200 years ('Anthropocene' and 'Great acceleration') based on terrestrial palynological data from northern and central Europe. The vertical axis for all four diversity types runs from low (L) to high (H). The horizontal axis for the four phases and the last 200 years reflects time from oldest (left) to youngest (right). The trends are schematic trajectories of diversity change with the arrows representing the end-point in the different phases. Redrawn from Birks HJB et al. (2016a).

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