Biotic response to rapid climatic changes during the Late Glacial : high resolution biostratigraphies and biological processes

Biotic responses to rapid climatic changes during the Late Glacial. High-resolution biostratigraphies and biological processes Organisms can respond to rapid climatic changes in three ways: 1) adaptation by evolution, affecting physiologyand morphology), 2) migrationand population dynamics including biogeographical changes) and 3) extinction local or global). Here, the focus is on examples of the second type. Organisms, whether algae, trees,or animals, find theirecological niches in a multi-dimensional space of gradients such as temperature winter, summer, means or extremes), humid¬ ity soil or air), pH, various nutrients, light. Presence or absence of taxa species, genera, families) can be related to such gradients.With training sets based on current gradients, they can also be related to environmental changes of the past e.g. summer mean temperatures or pH). The relationships between the occurrence of taxa and environmental variables can also be used to examine the biotic response to changes based on other proxies, for example, changes in temperature inferred from oxygen-isotope ratios in carbonates or from the content in organic matter of lake sediments. The groups of organisms referred to here are plants pollen), insects chironomids) and other aquatic invertebrates. The three Late Glacial periods with veryhigh rates ofchange in temperature estimates are the transition from the Oldest Dryas to the Bölling from GS-2 to GI-1 in the Late Glacial, ca. 14 670 cal yr BP), and the beginning and the end of the Younger Dryas ca. 12 600 cal yr BP, 11 500 cal yr BP respectively). The «classical» hypothesis was that trees represented in pollen diagrams) respond more slowly to climatic change than invertebrates aquatic or terrestrial) because of differences in life cycles.But it is shownhere that terrestrial vegetation) and aquatic invertebrate) ecosystems may respond synchronously. Three major biological processes are involved in the responses to climatic change: 1) Migration – can be slow if, for example, a longliving tree migrated back from a southern refugium. 2) Build-up of populations – intermediate velocity, for the process needs time depending on the life cycles of the organisms. 3) Productivity – can change rapidly, within a year or a few years e.g. pollen productivity, tree rings). The first two of these processes occur on the organisational level of populations, the last one on the level of the individual.These processes develop also in various combinations.


Introduction
Understanding climatic changes in the NorthAtlantic/ European region during the LateGlacial is necessary in any attempt to assess effects offuture climaticchanges, because they were larger and more rapid than fluctuations measured during the meteorologically recorded period. To assess the Late Glacial and Holocene) climatic changes, especially changes in summer temperatures, biostratigraphies are interpreted by applying so-called transfer functions, which relate today's presence or absence of taxa species, genera) to modern environmental variables e.g. summer temperatures;

Birks 2003).
A different approach to climate reconstruction was used in the studies summarized here: if, and only if, an independent line of evidence for climatic change is available, then these same relationships between taxa and climate variables can be used to assess the biotic response to a climatic change. Presented here is one example from a set of sites studied on an altitudinal transect in the Swiss Alps covering the beginning and the end of the Younger Dryas Ammann 2000; Ammann et al. 2000;Brooks 2000;Schwander et al. 2000;Wick 2000).
On this altitudinal transect, two sources were used to estimate climatic change independent of the biostratigraphies: 1) oxygen-isotope ratios in carbonates at Gerzensee, 603 m asl, and Leysin, 1230 m asl) and if carbonateic sediments were not available for the measurement of oxygen isotopes -2) the amount of organic matter in the lake sediment as loss-on-ignition at 550ºC, at Regenmoos, 1260 masl,andZeneggen, 1510 m asl). At Gerzensee, the oxygen-isotope ratios measured on bulk sediment i.e. biogenically precipitated carbonates such as tubes around Chara sp.) were also checked by measurements on mono-specific ostracod samples Von Grafenstein et al. 2000). This showed high correlations between isotope values from bulk sediment and from ostracods, indicating that the record was not distorted by reworked material in the bulk carbonates.
Biotic response is estimated here from two biostratigraphies recording changes in groups of organisms that have very different life cycles: vegetation as recorded in pollen stratigraphy includes annuals, biennials and long-lived species, like trees and shrubs that are usually thought to respond slowly to climatic change. Chironomids non-biting midges, Diptera/insects) goat least under favorable conditionsthrough annual lifecycles and may therefore trace climatic changes with little or no time lag.
Time control is a crucial issue when estimating rates of environmental change from a sediment sequence. But because the period of the late Younger Dryas and its transitioninto the Holocene coincides with aplateauof constant age inthe radiocarbon calibration curves, 14Cdating does not help unless a great many samples are dated in order to perform wiggle-matching; e.g. Gulliksen et al. 1998). Assuming synchroneity of major climatic shifts, such as thebeginning and the end of the Younger Dryas in the northern hemisphere, Schwander et al. 2000) propose the correlation of changes of oxygen-isotopes in the NGRIP North Greenland Ice core Project) ice-core with changes found at Gerzensee and Leysin, thus enabling the application of the time scale from NGRIP to these two terrestrial sites i. e. in cal yr BP).

Material and methods
To illustrate the conclusions about possible biological processes drawn herein, the findings for the site at Leysin in the western part of the Central Swiss Alps 46º20'49.96"N, 7º01'18.20"E, 1230 m asl) are presented here. Leysin belongs to the sites investigated already by Eicher & Siegenthaler 1976) and Welten 1982). During those investigations, a clear parallelism between pollen and oxygen-isotope ratios around the Younger Dryas could be shown. On new cores taken in 1992 with a modified Livingstone piston corer, the sampling resolution for stable isotopes and pollen were increased by a factor of about 3, and a chironomid stratigraphy analysis was included.
Sampling for isotope and biostratigraphies was performed on the same core at identical levels. The methods used for the analyses of pollen and chironomids are given in Wick 2000) and Brooks 2000), respectively. The biotic changes across the more than 100 pollen taxa and 30 chironomid taxa are summarised in Figure 1 as the scores on the first axis of a principal component Isotopic zones Lib stand for «Leysin isotopes on bulk sediments» and show a rapid decline in zone Lib-4 leading into the Younger Dryas Lib-4), and a rapid increase during zone Lib-6 leading out of the Younger Dryas into the early Holocene PB for Preboreal, Lib-7). The values on the first PCA-axies for pollen and chironomids summarize the degree of change between adjacent samples for pollen and chironomids. Le début et la fin du Dryas récent à Leysin 1230 m au-dessus de la mer) sur l'échelle temporelle de NGRIP i.e. en cal yr BP) Beginn und Ende der Jüngeren Dryas in Leysin 1230 m ü.M.) auf dem linearen Zeitmassstab von NGRIP i.e.in cal yr BP) analysis PCA). This method was used here because in a preliminary detrended correspondence analysis DCA) the gradient lengths were smaller than two sigmas for details see Ammann et al. 2000). The two time windows of onset and end of Younger Dryas were treated separately see lower and upper half of Fig. 1). The diagrams have been kept separate because two different cores were used: Leysin core B above 350 cm and Leysin core A below 350 cm. Although their correlation is not certain, the emphasis here was on the two periods of very rapid change.
3 Results and discussion In Figure 1, the two rapid transitions at the beginning and at the end of the Younger Dryas YD) are shown by the oxygen-isotope ratios as measured in the bulk sediment lake marl).The three columns following to the rightindicate that contents of d13C, carbonates, and organic matter are quite stable across these two transitions; it may therefore be assumed that the changes in d18O are not a result of sedimentary changes but rather of temperature changes see also Von Grafenstein et al. 2000). The curves for scores on the first PCA-axes for pollen and chironomid-stratigraphies are parallel during isotopic zone Lib-4 i. e. the onset of YD). Also, during isotopic zone Lib-6 i.e. the end of YD), the differences between identical samples are very small the opposite direction does not mean a seemingly opposite ecology, because it is only a quantitative measure for the overall change between adjacent samples). Thus, it may be concluded that the changes in pollen assemblages do not lag behind the changes in chironomid assemblages, and both do not lag behind the onset of the changes in the oxygenisotope ratios.
This is more synchroneity than expected. It must therefore be asked which biological processes are responsible for such fast responses to rising summer temperatures as is recorded in the oxygen isotopes.
Since the classical discussions about Late Glacial and early Holocene stratigraphies of pollen and beetles in northern EnglandbyPennington 1977) and by Coope 1977), pollen was often said to be slow to respond to climatic change because of migrational lags. Insects, in contrast, having much shorter life cycles and greater mobility, were thought to trace climatic changes without delay. Here, in contrast, a high synchroneity of responses in plants and insects was found. It is therefore concluded that the biological processes involved in the examples of Windermere in northern England and Leysin are not the same.
Since these early studies, multidisciplinary analyses of biostratigraphies have been made at a number ofsites.
Themost comprehensive study including theYounger Dryas was probably completed at Kråkenes in western Norway by Birks et al. 2000) where, apart from pollen and chironomids, seven other biostratigraphies were analyzed. Because of the lack of carbonates due to the geological setting, the analysis of oxygen isotopes was not possible, but the degree of synchroneity among the biotic changes can be estimated because the biostratigraphies were also developed from a single master core. Besides the climate reconstructions, one of several major findings at Kråkenes was that «the reaction times to the sharp temperature changes at the start and end of the Younger Dryas were very rapid and occurred within a decade of the temperature change» Birks et al. 2000: 92).
Biotic changes during the early Holocene, in contrast, were more gradual and not synchronous in the different groups of organisms Birks et al. 2000).
In order to estimate the rapidity of the biotic responses, it was necessary to assess the sampling resolution. On the basic assumption of hemispheric synchroneity for the onset and end of the Younger Dryas, the chronology from NGRIP could be transferred to the sites of Leysin and Gerzensee Schwander et al. 2000).
Consequently, the sampling resolution was estimated to be 17-30 years at Leysin, and 8-15 years at Gerzensee for the relevant transitions.
The categories sometimes made among biological processes involved in response to climate change are the following: • Migration: The limits of biogeographical ranges may change during or after climatic shifts, e.g. restriction of thermophilous species to the south during a glacial period or to the north in the southern hemisphere) or spreading of thermophilous taxa northwards after an ice age or due to current global warming e.g. Parmesan 2006; Walther et al. 2002).
• Building up of a population: When a taxon has arrived in a new area, the population may at first be very small just a few individuals). The growth of the population may be slow at the beginning, but for some taxa exponential later, depending on the species and a number of environmental conditions. Population growth then usually declines after reaching a level defined by the «carrying capacity» of the system for that species.
• Productivity: In contrast to the other two types of process that work on the level of the population, the changes in productivity occur on the level of the individuals. The width of tree rings or pollen productivity are examples. Not included here are variables such as number of offspring or success of reproduction that would reflect more the process of population growth.
The potential velocity or the time periods required for the three types of process differ widely and are spe-ciesspecific): • Migration or biogeographical migration means shifts of the range limits; it is not to be confused with seasonal migrations, as seen with birds or butterflies. Biogeographical migrations are rather slow, depending on species and their life histories; the latter include parameters such as age at first reproduction, dispersal capacities. Long-lived and slowly reproducing groups, such as trees, are expected to be slower than annual and highly mobile species, such as most insects. If there are no lags to the isotopic change in both the vegetation as recorded by pollen) and the aquatic invertebrates here chironomids), the slowest of the three types of response processes can be excluded. This would be migration, or at least latitudinal migration as is usually understood, for example trees migrating back from Southern to Central Europe.
Even dominant trees such as pine and birch, which had arrived during the Late Glacial interstadial Bölling and Alleröd) did not show delays in their responses to the isotope shifts. From the study of plant macro-remains by Tobolski & Ammann 2000), it appears that during the Younger Dryas trees were probably locally absent from Leysin, but regionally present: their distance for re-immigration from the valley bottom was so short that it could not be evaluated here due to the sampling resolution of about 30 years. This is an example of an altitudinal but not a latitudinal migration.

Conclusions
The following four conclusions may be drawn: 1) Terrestrial and aquatic ecosystems may respond rapidly and synchronously because biological processes on several organisational levels are involved.
2) Time needed for response processes decreases in the following order: migration > population-growth > productivity-change of the individual. 3) If no migrational lags or only migrational lags shorter than the sampling resolution) are involved, the pollen signal in response to climatic changes can be very fast because the rapid mechanism of changing pollen productivity may be involved. And 4) these findings do not contradict the classical concepts of Iversen 1964), who argued that aquatic organisms including water plants) may be faster than terrestrial plants in responding to climatic changes because their propagules get transported by water fowl high mobility), and they do not need soil development. The findings here rather build on these concepts and add to their Abstract: Biotic responses to rapid climatic changes during the Late Glacial. High-resolution biostratigraphies and biological processes Organisms can respond to rapid climatic changes in three ways: 1) adaptation by evolution, affecting physiology and morphology), 2) migration and population dynamics including biogeographical changes) and 3) extinction local or global). Here, the focus is on examples of the second type. Organisms, whether algae, trees, or animals, find their ecological niches in a multi-dimensional space of gradients such as temperature winter, summer, means or extremes), humid¬ ity soil or air), pH, various nutrients, light. Presence or absence of taxa species, genera, families) can be related to such gradients. With training sets based on current gradients, they can also be related to environmental changes of the past e.g. summer mean temperatures or pH). The relationships between the occurrence of taxa and environmental variables can also be used to examine the biotic response to changes based on other proxies, for example, changes in temperature inferred from oxygen-isotope ratios in carbonates or from the content in organic matter of lake sediments. The groups of organisms referred to here are plants pollen), insects chironomids) and other aquatic invertebrates. The three Late Glacial periods with veryhigh rates of change in temperature estimates are the transition from the Oldest Dryas to the Bölling from GS-2 to GI-1 in the Late Glacial, ca. 14 670 cal yr BP), and the beginning and the end of the Younger Dryas ca. 12 600 cal yr BP, 11 500 cal yr BP respectively).
The «classical» hypothesis was that trees represented in pollen diagrams) respond more slowly to climatic change than invertebrates aquatic or terrestrial) because of differences in life cycles. Butit is shown here that terrestrial vegetation) and aquatic invertebrate) ecosystems may respond synchronously. Three major biological processes are involved in the responses to climatic change: 1) Migrationcan be slow if, for example, a longliving tree migrated back from a southern refugium.