MAMMALIAN FOSSILS AND QUATERNARY

Quaternary Science Reviews, Vol. 11, pp. 329-344,1992. Printed in Great Britain. All rights reserved.

MAMMALIAN

0277-3791/92 $15.00 (~) 1992 Pergamon Press plc

FOSSILS AND QUATERNARY

BIOSTRATIGRAPHY

A . M . Lister Department of Zoology, University of Cambridge, Cambridge, CB2 3E J, U.K.

Mammalian fossils are important biostratigraphic indicators in terrestrial Quaternary sequences. Their use in dating and correlating deposits is based on two main attributes: (1) the presence or absence of particular species in fossil assemblages; (2) the 'evolutionary stage' of individual species shown by their anatomy. The changes through time in these features, on which biostratigraphic usage depends, are the result of complex biological phenomena, including speciation, adaptation, distributional shifts, and extinction. Contrary to common biostratigraphic assumptions, the pattern of change is rarely simple, and moreover, varies from one species to another. Evolutionary trends show fluctuations of rate and direction, and may vary in timing across the species' range. Constant remoulding of geographical distributions produces complex patterns of presence/absence. A proper understanding of these phenomena is essential for the valid use of mammals in biostratigraphy. The pattern of evolutionary and distributional change in each species must therefore first be established, based on independently dated samples over a sufficient geographical range, before it can be used in the dating or correlation of a 'new' sample.

INTRODUCTION Fossil mammals are increasingly being recognised as valuable biostratigraphic indicators in terrestrial Quaternary sequences. In comparison with other animal and plant groups, the features of mammalian lineages which make them particularly suitable for this purpose are first, their rapid turnover, by origination and extinction of species; and second, the significant morphological evolution, often quantifiable, displayed by many lineages. In addition, in common with other groups, Quaternary environmental changes produced major shifts in the geographical distributions of mammalian species, which can also have biostratigraphic value. Any biostratigraphic scheme essentially entails (1) demonstrating, by superposition or independent dating, a succession of faunal or floral change in a particular geographical region; (2) linking schemes in different areas by independent dating or biotic similarity; (3) using the scheme to deduce a relative or absolute age for other, isolated assemblages. For each of these stages, biostratigraphic information gleaned from particular assemblages usually comprises one or both of the following: (1) The presence or absence of particular species in the fossil assemblage. Although often not explicitly recognised, this is a resultant of two independent patterns: first, the overall time range between the origination and extinction of species; and second, within that time range, changes in the distribution of species resulting in movement in and out of the study area. (2) The 'evolutionary stage' within a particular species, i.e. the morphology of certain anatomical structures, in relation to their pattern of change through time. The processes of species origination and extinction,

distributional change, and evolution, are complex biological phenomena. It is my contention in this paper that meaningful biostratigraphic deductions based on mammalian fossils must take into account the complexities of these biological processes. Many attempts to use mammalian fossils for relative dating in the Quaternary are seriously flawed because they assume an unrealistically simplified view of the way mammalian species behave in space and time. In this review I hope to outline these biological phenomena and explain their bearing on biostratigraphy. PRESENCE AND ABSENCE OF SPECIES

The occurrence or non-occurrence of one or more species in a particular deposit is a fundamental datum in biostratigraphy. In formal zonation (Hedberg, 1976), this information allows the establishment of 'rangezones' (based on the local stratigraphic range of one or more taxa) and 'assemblage-zones' (based on the cooccurrence of a number of taxa). It is also central to correlations between the established scheme and 'new' localities.

Species Identification It is essential for biostratigraphic usage that taxa be identified in an assemblage only to the level clearly demonstrated by the morphology of available fossils, and not on the basis of a pre-conceived idea of the age of the deposit, lest circularity be introduced. For example, the European rhinoceros species Dicerorhinus etruscus (Lower to early Middle Pleistocene) and D. hemitoechus (late Middle to Upper Pleistocene) can be reliably separated only on the basis of skulls or teeth (Gu6rin, 1980). Indeterminate limb bone fragments of rhinoceros should not be listed as D. estruscus because the deposit is believed to be of Lower Pleistocene age, but as Dicerorhinus sp. Biostrati-

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graphers need to be particularly aware of this problem when using faunal lists published by other authors.

Sibling Species In general, related species are not separable on all parts of the skeleton, but only on diagnostic elements. The problem of 'sibling species' can be seen as an extreme case of this. Sibling species are recently diverged, reproductively isolated species which are morphologically apparently identical to each other. A well-known example (Auffray et al., 1990) concerns the European house mouse, formerly regarded as a single species, which on the basis of biochemistry was shown to comprise two distinct species, Mus musculus and M. spretus in southern France (Britton and Thaler, 1978). Subsequently, using biochemically screened animals, Darviche and Orsini (1982) discovered discriminative morphological character complexes between the two species. Thaler (1986) was then able to trace the separate history of the two lines in the fossil record. It is possible that some fossil 'species' may be a conflation of more than one taxon, especially for small mammals. In most cases, intensive studies such as that for the house mouse are not available, and the palaeontologist must be vigilant for any morphological bimodality, and aware of the biostratigraphic consequences of possible unrecognised sibling species (namely, morphologically indistinguishable fossils found at two localities, thereby taken to support biostratigraphic correlation, which in fact pertain to different species). An example has recently been provided by van Kolfschoten (1990a, pp. 260 and 271-272), who has detected two possible sibling species within the European Lower Pleistocene vole Mimomys pliocaenicus, based on bimodal scatters within two molar characters (height of the enamel-free area, and occurrence of the

"Mimomys-islet'). Absence Data: The Problem of Negative Evidence If biostratigraphic conclusions are based on the

absence of a species in a sample, negative evidence is being invoked, and as such is susceptible to errors of sampling. First, the faunal collection may not be large enough to show up the presence of a rare species. Second, the species in life may not have frequented habitats local to the catchment area of the depositional site; for example, Devensian red deer (Cervus elaphus) in Britain are rare in regions of low relief, but relatively common in hilly areas (Lister, 1984). Third, taphonomic conditions at a particular location may not have favoured a species' preservation; for example, a carnivore-accumulated assemblage will be strongly biased toward the prey species selected by the carnivore. For these reasons, absence data should be treated with caution. The biostratigraphic utility of species absences will increase if: (i) there is a large collection of fossils from the site, increasing the chance of showing up rare species. In the case of microfauna, sediment samples must be sieved to a suitably fine level; (ii)

absence of a species is noted at a number of sites rather than just one, especially if they represent a range of palaeoenvironmental and sedimentary environments; (iii) several species absences rather than just one all point to the same conclusion; (iv) sites lacking the species, and those possessing it, which are thereby believed to be of different ages, cover similar sedimentary contexts and palaeoenvironments.

Species" Origination and Extinction This delimits the total time of existence of the species. The lower boundary (origination) is often more difficult to define than the upper (extinction), since the evolution of a species from its ancestor is often gradual when viewed on a Quaternary timescale (cf. Woodburne, 1987a). The question of whether certain fossils represent a particular species or its ancestor may be difficult to resolve because of the possible complexity of the evolutionary transition (see later). More straightforward and potentially more powerful is extinction, used here in the sense of total (global) termination of the lineage. If the timing of extinction has been well-established on the basis of many sites over the species" range, then the presence of its remains in a deposit implies an age pre-dating the extinction. It should be borne in mind that the date of extinction is always subject to revision in the light of new dated finds. An example of the use of extinction in biostratigraphy is provided by the giant deer, Megaloceros giganteus, a European species which became extinct towards the end of the Last Cold Stage. This can be considered well-established, as none of the hundreds of post-glacial (Holocene) sites across Europe has ever produced remains of this species, The latest radiocarbon-dated occurrences are ca. 10,600 BP (Stuart, 1982 and 1991); allowing a margin of error we may say that any Megaloceros-bearing deposits predate 10,000 radiocarbon years BP. This may be considered sufficiently well-established that the occasional apparently much younger record can be treated with suspicion. For example, Bachofen-Echt (1937) illustrated bronze and gold Scythian engravings, dated to 600-500 B.C., from the northern coast of the Black Sea, which are accurate representations of M. giganteus antlers. Bachofen-Echt concluded that the species had survived until that time, and this was accepted by Kurt6n (1968). However, in view of the total lack of fossil evidence of the species for the preceding 8,000 years, a more likely explanation is that the illustrations were based on fossil antlers exhumed by the Scythian people. An important proviso to the biostratigraphic use of extinction is that a species may have disappeared at different times in different parts of its range, as its distribution gradually contracted prior to its final demise. For example, the mammoth Mammuthus primigenius appears on current evidence to have become extinct in Europe by 12 ka BP, in Eastern

Mammalian Fossils and Quaternary Biostratigraphy Siberia and North America by 11 ka BP, and to have survived in north central Siberia until about 10 ka BP (Lister, 1991; Stuart, 1991). Further back in the Quaternary, extinction dates are known with much less certainty, and should be used with care accordingly. For example, several species, such as the rhinoceros Dicerorhinus etruscus and the giant deer Megaloceros verticornis, became extinct some time between the Cromerian and Hoxnian (Holsteinian) interglacials in Europe (i.e. between ca. 500 and ca. 250 ka BP), but the date is not known more precisely because of poor sampling and dating of the intervening Anglian (Elsterian) Cold Stage.

Distributional Shifts In pre-Quaternary biostratigraphy, temporal patterns of taxonomic occurrence often reflect major events such as species originations, extinctions, and large evolutionary transitions. With irreversible events such as these, it is valid to regard species as 'marker fossils' for particular periods of time. Large-scale migrations, for example the first entry of a taxon into a continent, also fall into this category. On Quaternary timescales, however, where short-term range fluctuations can be picked up, the presence or absence of a species may be due merely to shifts in its distribution in and out of the study area. In this situation, a 'marker fossil' approach to presence/absence data, whereby the presence of a taxon is thought to characterise a unique period of time, may be inappropriate. A geographical perspective is essential, so that the pattern of occurrence in the study region can be seen in the wider context of overall species range. Studies of present-day species can help in understanding the factors influencing distributional changes, and the ease with which they can occur. First, faunal compositions can change dramatically over very short geographical distances, following vegetational and climatic boundaries. Mares and Willig (1989) show that at the boundary between tropical gallery forest and grassland in central Brazil, quite different faunas exist in areas only a few metres distant from one another. In the time dimension, shifting the position of the environmental boundary could clearly result in a very rapid change in the faunal content of each area. Less dramatic examples are common, such as the elk (Alces alces), which has faithfully followed shifts in the coniferous forest belt in Europe through the postglacial (Szymczyk, 1973). Not only direct climatic or vegetational effects, but also the loss or gain of other mammalian species bearing a predatory, prey or competitive relationship to a particular species, can affect the range of that species. In the Middle East, there has been a dramatic expansion of the range of gazelles (Gazella gazella) into a variety of novel habitats in recent years, corresponding to the decline in deer and oryx, and the spread of agriculture (Yom-Tov and Mendelssohn, 1988; E. Tchernov, pers. commun.). In the U.S.S.R., the range of the saiga antelope (Saiga tatarica) expanded rapidly within about 30 years of the

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mid-20th century, spreading westwards by ca. 500 km from small enclaves in the steppes of Kazahkstan. This was due to a combination of a ban on hunting and the virtual extermination of the wolf, and the exceptional fecundity and migrational ability of this species in good conditions (Bere, 1970). Most modern examples of this type are due to human activities, but there is no reason why naturally-caused vegetational, climatic or faunal changes might not have brought about analogous shifts in the past. In the most recent, finely-stratified part of the Pleistocene fossil record, rapid, naturally-caused changes can be perceived. For example, there was an expansion of the range of saiga antelope ca. 12,500 BP, bringing it west into Britain for perhaps 1000 years or less in the Late Glacial interstadial (Currant, 1987). Such rapid shifts must also have occurred earlier in the Pleistocene, but the speed of change is usually beyond our resolution. Second, although the species occurring at a given time and place interact to form an ecologically balanced community, they do not necessarily migrate or change en bloc when conditions change. Each species can be regarded as an independent agent whose range and abundance is controlled by a complex of causes unique to itself. It will settle into a new range, which although affected by other mammalian species, will not, except in rare cases, be tied to them so tightly that 'blocks' of species shift ranges in perfect congruence. Physiological tolerances, the constraints of geography, and conditions of climate, vegetation and other fauna, will re-sort the species into new combinations. As a simple example, the spotted hyena (Crocuta crocuta), wolf (Canis lupus), and lion (Panthera leo) were present in Britain in both the Last Interglacial and Last Cold Stage, but in the former the medium-sized deer providing their prey was fallow deer (Dama dama), while in the latter it was reindeer (Rangifer tarandus). Fossil assemblages of species which today live allopatrically have been termed 'disharmonious'; this term is perhaps unfortunate, as such assemblages reflect the fact that Pleistocene ecosystems were not just those of today shifted geographically (cf. Lundelius et al., 1987). These phenomena have several important consequences for Quaternary faunal and biostratigraphic studies: (i) It is important to look outside the region of immediate interest, to appreciate how species ranges are shifting overall. (ii) The ease and rapidity of range shifts means that species compositions of faunas could change in a geological instant. This widely appreciated point implies that the immigration or emigration of particular species are potentially valuable as biostratigraphic markers in particular areas (Woodburne, 1987a, p. 15; Savage and Russell, 1983, pp. 6--8). The most valid application is when a species first spreads into a previously unoccupied area, preferably by a defined geographical route. An example is the spread of Bison from Eurasia to North America across Beringia, which is taken to mark the beginning of the Rancholabrean

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Land Mammal Age (Lundelius et al., 1987, p. 223). Nonetheless, Savage and Russell (1983, p. 4) cautioned against the chronostratigraphic usage of such 'golden spikes' beyond their inherent resolution. The possibility of earlier occurrence of the species, either continuous with the later one or as an independent incursion, is always present. Lundelius et al. mention several records of Bison in assemblages which on other grounds appear to pre-date the Rancholabrean. The potential rapidity of distributional changes also means that the immigration or emigration of one or a few species could easily occur within the span of a conventional Quaternary chronostratigraphic or climatic stage if environmental conditions changed, and cannot be taken alone to suggest that two faunas belong in separate stages, as has sometimes been assumed. An example is provided by the Ipswichian Interglacial in Britain. Continuous pollen cores of the equivalent continental Eemian (e.g. Miiller, 1974) demonstrate that within this stage, there was a cycle of vegetational change passing from birch and pine forest to climax deciduous forest, thence to semi-open 'parkland', and finally to pine and birch woodland again. Stuart (1976) suggested that in Britain, pollen-dated assemblages containing hippopotamus (Hippopotamus amphibius ) and fallow deer (Dama dama), but lacking horse ( Equus caballus) and mammoth (Mammuthus primigenius) pertain to the central part of the stage (e.g. in the deposits at Trafalgar Square, central London). Other assemblages, containing horse and mammoth but lacking hippopotamus and fallow deer (e.g. from the brickearths at Ilford, north-east London), could pertain to the later part of the stage, corresponding to the cooling of climate and opening out of vegetation. From the perspective of present-day ecology, such a model is entirely plausible; a 10--15,000 year period with significant climatic and vegetational transitions would be expected to show concomitant change in the mammalian fauna. There is a growing belief that the Ilford deposits may pertain to a different chronostratigraphic stage from those at Trafalgar Square (Sutcliffe, 1976; Currant, 1989), but a supposed inflexibility of the mammalian fauna within individual stages could not be regarded as part of the evidence for this. (iii) A particular species or small combination of species could occur repeatedly in a given area, as ranges shift back and forth in response to similar environmental cues. For example, a simple combination such as horse and mammoth can have limited biostratigraphic significance in Upper Pleistocene Europe, because the two species could be expected in any of the repeated phases of cool, grassy conditions which occurred. If, however, there is a large combination of species which seems, based on independently dated deposits, to be peculiar to a given time period, their use together as a local or regional biostratigraphic marker is valid. An example is the British Middle Ipswichian fauna mentioned above, where an assemblage comprising hippopotamus (Hippopotamus amphibius), fallow deer (Dama dama), straight-tusked

elephant ( Palaeoloxodon antiquus), narrow-nosed rhinoceros (Dicerorhinus hemitoechus) and various others (see Stuart, 1976; Currant, 1989) is consistently found. At present, there is no indication from welldated sites that this assemblage occurred at any other time in the British Middle or Upper Pleistocene. This fauna thus approaches the status of an 'Assemblagezone' (Hedberg, 1976). The combination of geographical and environmental conditions, historical constraints and faunal interactions which leads to a particular large group of mammalian species coexisting is unlikely to be exactly repeated. In temperate latitudes, such indicators are most valid for interglacials, when a substantial diversity of mammalian species entered the area. For long periods in the cold stages, a more limited array of species, more similar between successive stages, appeared each time (Lister and Brandon, 1991), and so faunal combinations are of less use in biostratigraphy. (iv) Correlations based on migration events may be hampered because immigration is not simultaneous in different areas. This has caused problems, for example, in the subdivision of the Blancan Land Mammal Age across North America, using first and last appearances of key taxa (Lundelius et al., 1987, p. 218).

Palaeoenvironmental Indications The known environmental requirements of species may provide additional biostratigraphic information. For example, the occurrence of species limited to temperate, forested habitats would indicate, in northern latitudes, that the fauna was of interglacial age. Conversely, the presence of open-ground, coldadapted species would suggest a 'cold stage'. Although such deductions are limited in that they do not indicate which interglacial or cold stage is involved, the information may still be of biostratigraphic value. The details of palaeoenvironmental reconstruction per se are beyond the scope of this paper, but certain comments are relevant to their use in biostratigraphy. These relate primarily to the confidence with which we can deduce palaeoenvironments from mammalian species.

(i) Deductions based on modern species ranges Fossil occurrences of species still living today can provide more secure evidence than those of extinct ones, in that direct information on their habitat tolerances is often available. Where possible, it is important to look not just at the modern distribution, but also to understand the biological basis for its limitations. For example, the modern range of the European fallow deer, Dama dama, does not extend further east than the Black Sea or further north than southern Sweden. Attempts to introduce the species into Norway have failed, presumably because of the cold climate (Chapman and Chapman, 1975). Fossil occurrences of fallow deer can therefore confidently be taken to indicate temperate, oceanic conditions. Hippopotamuses are similarly good indicators of warm

Mammalian Fossils and Quaternary Biostratigraphy conditions; their exclusion from cold climates is due to the fact that they cannot maintain a positive energy balance in water below 18°C (Haltenorth and Diller, 1980). Taken by itself, a species' distribution may not illustrate the full range of conditions under which it is capable of living, either because of past geographical accidents, human influence, or competitive exclusion by other species. Lions (Panthera leo) are restricted to subsaharan Africa today, but their exclusion from the Middle East and Mediterranean zone is known to have been due to human influence in historical times (Haltenorth and Diller, 1980). Thus, an assumption that a fossil occurrence of lions reflected tropical conditions would be misleading. In some cases, the examination of a species across the whole of its modern range may be revealing. In Europe, red deer (Cervus elaphus) are largely restricted to woodland, so Quaternary occurrences of the species have been taken to indicate wooded conditions. Across the entire holarctic range of the species, however, there are several populations today which subsist on a largely treeless habitat. Moreover, a number of European Quaternary deposits with independent evidence of vegetation demonstrate the presence of the species under largely or wholly open conditions (Lister, 1984). In some cases, the presence of a species in a deposit might reflect a local pocket of suitable habitat, even though the regional environment was of a different overall type. Finally, note that combinations of climate and vegetation sometimes occurred in the Quaternary which have no precise modern equivalents, so that deductions of palaeoenvironment based on species' modern ranges need careful assessment. For example, the fauna of the 'steppe tundra' vegetation of the British Last Cold Stage included species currently living in tundra (e.g. lemmings) alongside those currently living in steppe (e.g. ground squirrels) (Stuart, 1974).

(ii) Possible changes of adaptation through time It is important to consider whether the habitat tolerances of a species may have changed through time, so that present-day limitations do not apply in the fossil record. By and large, if there is no discernible change in the adaptive morphology of the species, as seen in thorough studies of its fossil remains, it can be assumed that environmental tolerances were similar. This conclusion can be strengthened by collating occurrences of the species at sites with independent palaeoenvironmental information. In some taxa, adaptive morphology has clearly changed, and/or there may be a shift in the known palaeoenvironment in which it is found. Praeovibos priscus, the Middle Pleistocene precursor of the modern, arctic-adapted musk-ox Ovibos moschatus, appears to have tolerated milder conditions than its successor, to judge from its occurrence at sites such as Arago, S.W. France, in association with temperate and boreal species (Crrgut and Gu6rin, 1979). Alces latifrons, the precursor of the modern moose Alces

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alces, was adapted to more open conditions than its forest-dwelling successor, to judge both from its skull and antler structure, and from known palaeoenvironments in which it has been found (Lister, in press).

(iii) Extinct species With extinct species, assessment of palaeoenvironment must be based on two sources: first, the adaptations of the animal deduced from its anatomy; and second, occurrences of the species with associated independent palaeoenvironmental information. For example, the extinct woolly rhinoceros Coeiodonta antiquitatis appears to have been adapted to cold climates by its furry coat, and to a treeless, grassy diet by its cranial and dental morphology (Fortelius, 1983). In addition, virtually all fossil occurrences in known palaeoenvironments indicate a cold, open habitat. The mammoth (Mammuthus primigenius) was also essentially a species adapted to cold, open habitats, but while the bulk of fossil occurrences reflect this, the species did also sometimes live under temperate and/or partially-wooded conditions (West, 1969; Lister, 1991). The importance of considering the fauna as a whole is critical here. A combination of mammoth, woolly rhinoceros, red deer and reindeer (Rangifer tarandus) in the Quaternary of central Europe would very clearly indicate 'cold stage' conditions, although two of the species (mammoth and red deer) taken alone would be ambiguous, as described above.

EVOLUTION Many mammalian lineages in the Pleistocene underwent marked evolutionary transitions, and these are often observable as morphological changes in their fossilised bones, teeth, horns, and so on. Such trends are potentially of great biostratigraphic value. In formal biostratigraphic zonation, they form the basis for the erection of 'Lineage-zones', biostratigraphic zones based on a segment of the morphological trend in an evolving lineage (Hedberg, 1976). An 'ideal' evolutionary change from a biostratigraphic point of view would be one which is easily observable (and preferably quantifiable) on the fossil remains, which is genetically based (see below), and which conforms to one of the following two patterns: (1) a character changing gradually, unidirectionally, and synchronously over the geographic range of the species; (2) a new character appearing suddenly at a particular time, synchronously over the geographic range of the species. Biostratigraphic studies have often assumed, usually implicitly, that one or other of these patterns was followed in every case of evolutionary change. Biological evolution, however, is a complex process which rarely meets these criteria, and follows different patterns in different lineages. It is essential for correct biostratigraphic usage that this complexity be taken

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into account. The pattern of change must be independently established for each lineage before it can be utilised in biostratigraphy.

Choice of Morphological Characters" (1) Body size Easily quantifiable by measurements of almost any skeletal element, is the most ubiquitous type of change observed in Quaternary mammal lineages. It is also the least suitable as a biostratigraphic indicator. Biostratigraphy requires that a particular character state is unique to a particular period of time. Size, however, is far too labile to be reliable in this respect. Biologically, there are at least three reasons for this: (a) Body size is easily directly affected by climatic and vegetational conditions, which can cause substantial change in phenotype (body form), without genetic change, within the space of one or a few generations. An example of this was provided by the introduction of red deer (Cervus elaphus) from Scotland to the lush pastures of New Zealand, which caused an increase in mean body weight by a factor of two to three in the space of 15-20 years (Huxley, 1931). In a more detailed study, roe deer (Capreolus capreolus) in a forest in north-east France suffered a reduction in mean body weight of ca. 22% in ten years, due to increased population density and concomitant competition for food (Maillard et al., 1989). Such changes are with equal ease reversible. (b) Even where body-size differences and similarities between populations are genetically-based, they can be rapidly altered by natural selection. In addition, because body size is controlled by many different genes (i.e. it is polygenic: Mather, 1949), similar body size in two samples of a species is not a good indicator of relatedness or contemporaneity, because the same size may be the result of different gene combinations in the two samples. (c) Many different adaptive forces act on body size. Thus natural selection could produce similar body size in two populations for quite different reasons. An example serves to illustrate the inadequacy of body size as a biostratigraphic marker. It had been thought, based on samples from various sites (Eisenmann, 1980), that all populations of caballine horse (Equus caballus) in early Middle Pleistocene Europe were of large body size. At Little Oakley, Essex, however, Lister et al. (1990) found a caballine horse of small body size in an unequivocally early Middle Pleistocene context. A special case is the use of body size to deduce cold stage or interglacial conditions because of a supposed inverse correlation between body size and palaeotemperature. This is based on the idea that larger animals, with a smaller surface to volume ratio, are better at conserving heat in a cold environment. Some workers have even calculated precise palaeotemperatures on the basis of tooth size in certain mammalian species (Davis, 1981; Klein and Scott, 1989). These

ideas have their basis in Bergmann's Rule, the finding that among modern mammals, many species display a latitudinal cline, with smaller individuals closest the equator, and progressively larger sizes toward the north and/or south (Rensch, 1936). A well-documented example is the puma, Felis concolor (Kurt6n, 1973). Extended to the time dimension, analogous trends might be expected in the Quaternary, with larger individuals expected in cold stages, smaller ones in warm phases. This pattern has been documented in certain cases, such as the European brown bear (Ursus arctos) (Kurt6n, 1968), and the vole Microtus oeconomus in Britain (Stuart, 1982). Where well established for a particular species, such trends are of considerable palaeoecological interest, and may have some biostratigraphic value. It cannot be assumed, however, that this pattern is universal, or that where it does occur, the causal factor was always temperature. As mentioned above, body size is subject to many selective forces in addition to temperature regulation, and in the modern fauna, many species show trends contrary to Bergmann's Rule (McNab, 1971). An example is the American otter, Lutra canadensis, whose reduction in size toward the north is believed to be because holes in the ice become smaller in the arctic (Scholander, 1956). Such causal factors would be very difficult if not impossible to deduce in the fossil record. Even where Bergmann's Rule holds true, species may be following cues other than temperature. Several recent workers attribute Bergmannian trends to the fact that larger individuals can survive longer without food (Searcy, 1980). Langvatn and Albon (1986), studying size clines in red deer in Norway, attributed the larger size of animals toward the north to clines in the productivity and quality of plants. Ideally, then, the use of body size to predict palaeotemperature should be confined to cases where there is explicit evidence from studies on the modern form, of a direct relationship between body size and temperature. In some cases, well-established correlations of size variation with glacial/interglacial conditions may provide a basis for biostratigraphic deduction, even if the causal link (temperature, food, or other) is not known, although the general caveats against the use of body size in biostratigraphy (see above) still apply.

(2) More complex characters' Morphological changes in evolution form a spectrum with the simplest - - body size - - at one end, and the most complex at the other. Generally speaking, the more complex and unique a trait in evolution, the less likely it is to be subject to non-genetic environmental effects, reversal of trends, and parallel acquisition at different times, and hence the more valuable it is in biostratigraphy. Next after body size in the scale of complexity is the simple proportioning of the body, for example the length and stockiness of the limbs. Here, too, caution still needs to be exercised, for although not quite as variable as body size, these features are often still too

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Mammalian Fossils and Quaternary Biostratigraphy

malleable by environment and evolution to be reliable as biostratigraphic markers. In pigs, for example, Weaver and Ingram (1969) found that individuals raised at 5°C had markedly stockier limbs than their siblings raised at 35°C. The best characters are complex, usually localised morphological traits such as the form of tooth cusps or the details of a bone articulation. These are more likely to have a purely genetic basis, and less likely to show precisely repeated changes. An example is the acquisition of an antler 'crown' by European red deer between the early and late Middle Pleistocene (Lister, 1986; Fig. 1). Even so, the types of evolutionary changes seen both within and between species on a Quaternary timescale, even in 'complex' characters, are usually relatively small compared to the longer-term, major transitions of evolution, and as such may still be susceptible to reversals and parallelisms. This is discussed further below. Greater confidence can be provided if a number of independent characters are assessed together, since combinations of character states are less likely than individual ones to be precisely repeated at different horizons.

The Statistical Approach The morphological variability between individuals of a species, and the relatively small scale of the transitions seen in the Quaternary, make it essential that reasonable samples of individuals, and not single specimens, be examined for biostratigraphic purposes. Where possible, with quantifiable characters, statistical testing should be employed. An example is shown in Fig. 2. The decrease in enamel thickness of the mammoth molar through the

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FIG. 2. Reduction of enamel thickness in the mammoth lineage through the Pleistocene. Measurements taken on third lower molars; each circle represents one tooth. Samples: Archidiskodon meridional/s, Lower Pleistocene, Val d'Arno, Italy; Mammuthus trogontherii, Middle Pleistocene, Mosbach, Germany; Mammuthus primigenius, Upper Pleistocene, Lea Valley, England. Three specimens have been marked with crosses to illustrate how comparisons based on single teeth could give a misleading impression of evolutionary pattern. Data original.

Pleistocene is well known. With large sample sizes, however, it can be seen that there is a substantial range of variation at each horizon, so that while there is a clear evolutionary trend in the mean value, nonetheless the ranges of variation overlap from one horizon to the next. This is, indeed, exactly what is expected for a character changing by progressive genetic replacement within a population. It means, however, that reliable biostratigraphy must be based on reasonable sample size, and not on one or a few molars as has often been the case. A very misleading picture could be obtained if specimens marked with a cross on Fig. 2 happened to be found or chosen for comparison. Variation due to individual age or to gender must also be taken into account. For example, in the case of the red deer antlers mentioned above, only male individuals are of interest as they alone bear antlers, and further, only large, mature individuals should be compared because immature or small animals, even in the late Middle Pleistocene 'coronate' population, had simpler antlers which may mimic the earlier 'acoronate' type (Lister, 1986). Antlers are a special case, but even with bones and teeth, age variation is relatively easy to take into account in fossil mammals, as most growth ceases at maturity, and fully-grown adult specimens are readily identifiable. Adult limb bones can be recognised by fusion between the epiphyses (ends) and diaphysis (shaft). In the case of the dentition, mammalian teeth are formed at full size in the jaw, and do not grow further in length and width, although there may be changes in crown height through life. Variation due to sexual dimorphism can be more difficult to eliminate. Marked dimorphism can result in two species being recorded in a fossil collection where only one actually existed. Even if the remains are recognised as a single species, chance differences in the proportions of males and females in different samples (e.g. two samples from successive horizons) may cause an evolutionary change to be wrongly deduced, the sample with more males appearing larger than that with more females. In species where males and females stay apart for much of the year, and may live in somewhat different habitats (e.g. elephants, many deer), thanato-

336

A.M. Lister

cenoces dominated by one sex or the other may not be uncommon. Occasionally (e.g. where skulls or complete skeletons are available), it may be possible to sex individual fossils and thus take account of sexual variation. More often, with isolated remains, this is not possible, and analogies with recent representatives or relatives of the species can be applied. An example showing very clear bimodality is the extinct cave bear (Ursus spelaeus), where it can be recognised as intraspecific dimorphism because it is known that bears in general tend to be strongly sexually dimorphic (Kurt6n, 1969). An example where sexual dimorphism exists but is not so marked as to produce clear bimodality in most fossil samples is red deer, Cervus elaphus. In this species, males and females live apart much of the year, so biased thanatocenoses are possible, The degree of size dimorphism is known from living populations: ca. 2% in teeth, ca. 5°/,, in limb bone diameters (Lister, unpublished data). Thus, in any study comparing size between fossil samples of red deer, no difference should be deemed significant (i.e. above the level possible purely by sex-ratio imbalance) unless greater than these figures.

The Pattern of Evolution The most pervasive beliefs about evolution which have underlain biostratigraphic work are, firstly, that all change is gradual and unidirectional; and secondly, that it occurs synchronously in different geographical areas. This has led to the following assumptions in practice: - - samples of similar morphology are of similar age; a sample intermediate in morphology between two other samples is also intermediate in age; - - the degree of morphological difference between two samples is proportional to their difference in age; - - all of the above are applicable irrespective of the geographical distance between sampling points. Evolution, however, is a complex and varied process. In some instances, some or all of the above may hold true. In others, one or more of them is violated. My contention is not that mammalian evolutionary patterns are too complex to be used in Quaternary biostratigraphy. It is that one cannot assume a priori that the above four-point pattern (or any other particular pattern) is valid for a given lineage, and then apply it in biostratigraphy. One must first establish on independent evidence the pattern of change for each lineage; this may then be applied to the dating of 'new' samples. Some of the possible complexities of evolutionary pattern are described in the following sections. -

-

(1) Rates of change Studies of evolving lineages indicate that the rate of change is often very far from constant. The~'e may be long periods of stasis, when little or no change occurs. At other times, gradual transitions may take place over considerable timespans, with a constant, or more usually fluctuating, rate of change. Finally, in certain circumstances, relatively very rapid changes may occur

where the transition would be barely if at all resolvable in the geological record (Levinton, 1988). Some of the consequences of this for biostratigraphy are: (a) Morphological similarity between two samples does not necessarily mean they are of the same age. They may be temporally separated by a period of evolutionary stasis. One consequence of this is that a sample of intermediate age between samples A and B is not necessarily of intermediate morphology, but may either still show morphology A, or already have arrived at morphology B (Fig. 3). This is particularly likely when only a single character is being examined. If many characters are examined, covering different aspects of the animal's anatomy, it becomes less likely that nothing at all will have changed over a significant period of time. Thus, Rackham (1981) examined Bison priscus fossils from a series of British Devensian (Last Cold Stage) sites, and found no significant differences between the samples on an array of biometric and morphological criteria. He therefore suggested that the samples were penecontemporaneous. (b) The degree of morphological difference between a series of samples may not be directly proportional to the time intervals between them. The prediction of age based on morphology, assuming a constant rate of morphological change as in Fig. 3a, may not be reliable unless there is clear independent evidence that this was the pattern of change. (c) The possibility of rapid evolutionary change, effecting marked morphological differences within a few thousand years, means that a significant morphological change does not necessarily point to a large interval of time, and could occur within a single Pleistocene stage. Lister (1989) demonstrated a six-fold body weight reduction in red deer (Cervus elaphus L.) within six thousand years, with associated antler and limb bone changes. This is an extreme example, in the unusual situation of an island population. Nonetheless, the 10-20 ka of a single interglacial may represent 1,000-10,000 generations of a mammalian species, depending on its body size, enough time in theory for very significant genetically based evolutionary change (Levinton, 1988). How frequently such rapid changes occur in practice is uncertain. Moreover, there must be an upper limit to the amount of change which can occur in a given period of time, which should become clearer as more independently calibrated cases are examined.

(2) b:luctuations and reversals' The majority of evolutionary trends, when viewed on a fine enough timescale, do not proceed unerringly and constantly in the overall direction of the trend, but are subject to minor fluctuations and reversals of morphology (Fig. 4). This is entirely predictable from evolutionary theory. Directional changes in gene frequencies will be subject to fluctuation due to perturbations in environmental conditions which they are tracking, exchange of genetic information between different populations of the species, and other causes (Levinton, 1988).

337

Mammalian Fossils and Quaternary Biostratigraphy

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FIG. 3. Four possible patterns in the rate of evolution of B from A. The morphological stage of the intermediate-aged sample (I) is different in each case. (a) Constant rate gradualism: I is intermediate between A and B. (b) Rapid transition: I is very sensitive to slight differences in its age (tl), and may show unusual variability around the time of transition. (c) Stasis followed by gradualism: I has the same morphology as A. (d) Gradualism followed by stasis: I has the same morphology as B.

time

/ morphology FIG. 4. An evolutionary fluctuation or reversal. Note that B is of intermediate morphology between C and D, but not of intermediate age. Moreover, a particular morphology is repeated at two different horizons (A and C).

when spacing comes down to 104-105 years. The latter timescale, corresponding roughly to between one and three average Pleistocene climatic stages, encompasses many of the specific problems of terrestrial Pleistocene chronology which we attempt to unravel. 'Minor' reversals of evolutionary trends in mammal lineages can thus assume major significance. We must not be misled, by apparently unidirectional trends evidenced from coarsely-spaced sampling points, into assuming that this unidirectionality can be applied to finer timescales. Note that if such fluctuations occurred around the morphological point deemed to represent a taxonomic boundary, an alternation of 'taxa' would result (Fig. 5).

Taxonomy In the fossil record, such fluctuations often only become apparent when our stratigraphic control is fine enough. Hedberg (1976, p. 87) stated that it is the "irreversibility of organic evolution with respect to geological time" which makes it one of the best tools for relative dating. This is unquestionably true in a broad sense, especially in relatively coarsely stratified geological sequences. Studies of Pleistocene mammals, however (Lister, in preparation), reveal that in many cases, evolutionary patterns which appear perfectly gradualistic with coarsely-spaced sampling points (10`% 106 years apart), are seen to include minor fluctuations

Name changes within an evolving lineage have often been placed at points in time which are arbitrary with regard to the evolutionary process, particularly where the underlying change is gradualistic. In both the water vole and mammoth lineages, for example, dental changes occur through the whole of the Pleistocene, in a largely cumulative and gradualistic pattern. For historical reasons and convenience of classification, each lineage has been divided into a series of chronospecies (Fig. 6). The morphological transitions between taxa, however, are no greater than those within them. If a biostratigrapher looks only at faunal lists, an apparent 'replacement' of taxa at the specific or even

338

A.M, Lister

(a) conventional taxonomic boundary taxon A

taxon

taxon B

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time j

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FIG. 5. Diagram illustrating that where an evolutionary fluctuation occurred around a morphological point defined as a taxonomic boundary, the fossil sequence would record an alternation of taxa. (a) Evolutionary pattern, (b) fossil sequence.

generic level can give an impression of major change, when in fact only a minor evolutionary step may have been responsible for crossing the taxonomic boundary. This point has been illustrated in detail by Stuart (1988) in relation to the transition between the vole genera Mimomys and Arvicola. This change is based on one step in a progressive evolutionary trend which took a million years or more. The final transition (loss of the last vestige of root formation), has been taken by biostratigraphers, perhaps influenced by the taxonomic change with which it was invested by Hinton (1926), to imply that the transition cannot have occurred within a single interglacial stage (Bishop, 1982; Currant, 1989). There may be compelling reasons for believing that Arvicola first appeared in Europe in a later interglacial than the latest Mimomys, but the degree of morphological difference between the two taxa is not one of them.

The biostratigraphic information provided by a sample with a statistical spread of morphology should be based on the statistics of that spread as a whole. Woodburne (1987a), however, has supported the notion that a chronospecies boundary in an evolving lineage could be drawn at the earliest horizon where even a single specimen of the population shows the morphology of the next species in the succession. This procedure is not recommended here, because unusual, 'advanced' outlier specimens would in many instances give an unrealistically early boundary for a species. This first occurrence would then be given biostratigraphic weight by later workers, and could inhibit correlation with another sample, of statistically indistinguishable morphology from the first, but which happened to lack a specimen of sufficiently advanced form to be deemed to have crossed the species boundary. A final taxonomic problem concerns the effect of undetected sibling species (see above) on perceived patterns of evolution. An apparent pattern of evolution (for example, any of those portrayed in Fig. 3) could be pieced together from samples which in fact pertain to different lineages. However, if the sibling species are undergoing perfectly congruent, parallel patterns of stasis and evolution, then they are biostratigraphically interchangeable. If, conversely, they are not evolving in perfect congruence, then their morphology is diverging and they are no longer sibling species, which should be detectable as bimodal morphology.

Geographical Variation and Movement (1) Geographical variation Geographical variation plays a crucial role in the evolutionary process, and has very important implications for the use of evolutionary change in biostratigraphy. Mammuthus

Arvicola

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FIG. 6. Diagram illustrating the taxonomic subdivision of two evolving lineages in the European Pleistocene: the water vole (Mimomys-Arvicola) (Chaline and Mein, 1979, p. 133) and mammoth (Archidiskodon-Mammuthus) (Garutt, 1986). Evolutionary rates (dashed lines) are schematic. [N.B. some authors (e.g. J~inossy and van der Meulen, 1975) recognise an additional species, Mimomys ostramosensis, intermediate between M. pliocaenicus and M. savini. Van Kolfschoten (1990b) regards cantiana as a subspecies of Arvicola terrestris, Dubrovo (1977) has questioned the taxonomic separation of Archidiskodon gromovi from A. meridionalis.]

339

Mammalian Fossils and Quaternary Biostratigraphy

At the present day, many mammalian species are subdivided into a number of morphologically and genetically distinct populations across their geographical range. Depending on the degree of differentiation, these populations may be known as subspecies or races. Lesser differentiation, while not distinguished by nomenclature, is also commonplace. For example, Crombrugghe et al. (1989) demonstrated significant differences in mean body size of red deer (Cervus elaphus) between four small areas of eastern Belgium. Differentiated populations may be separated by geographical breaks, or be contiguous. Sometimes the morphological boundaries between the different types are sharp; in other cases there is a gradual cline of morphology (Levinton, 1988). Transferred on to a past time plane, this fact has the immediate consequence that morphological differences between fossil samples that are geographically displaced need not imply a difference in age, but could reflect spatial variation on one time plane. Studies on living mammalian species provide models of how much differentiation can plausibly be attributed to geographical variation over a given distance. In general, smaller or less mobile species are more likely to be differentiated over short distances than larger or more mobile ones.

(2) Population movement A further complicating factor is the possibility of movement through space of populations bearing different morphologies, or the shifting of clines of morphology. This process is analogous to the movement of whole species ranges discussed earlier, but instead of affecting presence/absence records of species as a whole, can affect rather our perception of the 'evolutionary stage' within a species at a given time. As in the case of whole species movements, an understanding of this process requires sampling across the geographical range; if only one region is studied, a misleading impression of evolutionary change is likely to be obtained. The movement of populations or dines has several important consequences for biostratigraphy. First, a certain morphology (e.g. A in Fig. 7) may mark a particular time horizon in one area, but appear in other areas at different times. Second, in a given geographical area, the fossil sequence through time may record morphological changes which are due not in situ evolution, but to the immigration of successive populations or parts of a cline (Joysey, 1972; Stuart, 1982, Fig. 11.6). Such movements mimic in situ evolution: in Fig. 7, for example, the sequence A - B - C is produced at the sampling location. An example of an apparent evolutionary 'fluctuation' believed to have been caused by migration of populations has been given by van Kolfschoten (1990b). Enamel thickness differentiation in the water vole Arvicola through the Middle and Upper Pleistocene of north and central Europe shows a generally unidirec-

sampling location qptime'

A

B

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space FIG. 7. Diagram illustrating the movement through space of three morphologically differentiated parts of a species' range (A, B and C). These could either be separate populations, or parts of a continuous dine. A fossil sequence collected at one sampling location would show a succession of forms mimicking in situ evolution. After Joysey (1972).

tional trend, but with an apparent 'reversal' between the late Saalian and Eemian (Fig. 8). Van Kolfschoten (1990b, p. 46) suggests that this was due to Eemian movement of more 'primitive' populations into north and central Europe from the south-east, where even today Arvicola populations are dentally less advanced. Determining whether a particular change was due to evolution or migration can be difficult, requiring above all extensive geographic sampling between tightly correlated sequences. Examination of the animals' whole anatomy, rather than just the characters which are showing interesting evolutionary 'trends', can sometimes help to determine whether we are dealing with a replacement of populations. Characters may be found which 'mark' particular populations, and thus help us to follow them through time and space. Suitable features include the presence of particular cusps on teeth or foramina on bones. This approach has been employed in tracing human populations and their migrations (e.g. Berry, 1974), and there is scope for extending it to other Pleistocene mammal species. The movement of populations or of a cline could produce a geologically instantaneous morphological transition in a particular area, providing a further caveat against biostratigraphic deduction based on how great an 'evolutionary' transition is plausible in a given timespan. Nonetheless, the time of replacement of one population by another could itself in principle provide a biostratigraphic marker, analogous to the immigration or emigration of a species, but as in the latter case, the pattern of migrational change would have to be well known because, for example, one population could have moved repeatedly in and out of an area, and so mark more than one horizon. Often, the arrival of a particular morphology in a particular part of a species' range may occur neither by in situ origination, nor by migration of animals, but by a process in some respects intermediate: the flow of genes from their area of origin, by successive interbreeding of animals forming a chain across the species range. The rate at which morphological traits can

340

A.M. Lister approx. kyr BP 0

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Enamel Differentiation Index

FIG. 8. Changes in enamel differentiation of Arvicola (water vole) molars through the European late Middle and Upper Pleistocene. Note the reversal in trend between the Saalian and Eemian, which is probably due to movement of individuals or populations, or possibly to an evolutionary fluctuation. Inset: first lower molar in occlusal view, showing the points of measurement on one of the seven enamel loops. The Enamel Differentiation Index is calculated as the ratio between the enamel thicknesses on the trailing (t) and leading (i) edges, computed for each of the seven loops and then averaged between them. The samples are from the Netherlands, Germany and central Europe; each is plotted by its mean, total range, and number of specimens. Data from Heinrich (1987) and van Kolfschoten (1990b).

spread by this mechanism is dependent on many factors, but its maximum rate is less than that possible by actual migration of animals. In a particular region, the appearance of a new feature by this means will have many of the characteristics of an in situ evolutionary origin.

(3) Speciation Of particular importance in the evolutionary process is the origin of one species from another. In the various models of speciation which have been proposed, geographical variation and movement invariably play a key role (Levinton, 1988). One of the most widely accepted modes of speciation, for example, is Mayr's (1963) allopatric model. A small population of the parent species becomes partially or wholly isolated at the edge of, or occasionally within, the range of the parent species. The isolated population evolves new features in its local habitat, and at the same time, or on subsequent re-contact, becomes reproductively isolated from the parent. On re-invading the range of the latter, it may either displace it, or co-exist with it. Another model of evolutionary change which emphasises geographical variation is Wright's (1932) 'shifting balance' theory. Here the parent species is divided into a set of partially isolated populations, each of which may evolve new features. Occasional gene flow between the populations allows these features to spread through the species as a whole. In both of these models of speciation, novel morphological features appear in one area first, and may then spread over a wider range. At the resolution of most pre-Quaternary fossil sequences, this process would appear instantaneous. On Quaternary timescales,

however, we may pick up the transition. Figure 9 shows how the origin of one species from another by the allopatric model produces a different time of replacement in different areas. Thus, the apparent time of replacement of one species by another in a particular area may not be the time of origin of the new form, but merely the time of its migration into that area. This will be true unless we have reason to believe we are sampling in the actual area of allopatric origin. The 'first appearance' of the new taxon may therefore not be a secure basis for interregional correlation on a fine time scale. As in the case of other migrating populations or species (see earlier),

SDeciation Drocess

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FIG. 9. Diagram illustrating how a process of allopatric speciation (the origin of a new species B in a peripheral area, followed by its spread and replacement of the parent species A) can produce a different apparent time of replacement in different sampling localities 1 and 2.

Mammalian Fossils and Quaternary Biostratigraphy the time of entry into a particular area may itself still have value as a local biostratigraphic m a r k e r event. One cannot, however, m a k e deductions based on a supposed 'rate of evolution' in the sampled area. In other words, one cannot argue from a significant morphological difference between a species in horizon A, and its replacement in horizon B, that there must be a significant time interval between A and B. If the replacement was due to immigration rather than in situ evolution, it can have been effectively instantaneous. Not all of the evolutionary transitions in the fossil record which we m a r k with a change of species or even genus n a m e are the result of a speciation process in the sense of the splitting off of a new, reproductively isolated species from the parent (cladogenesis). Rather, they m a y often represent processes within a reproductively continuous lineage (anagenesis), such as the expansion of one differentiated population or part of a cline at the expense of another, or the spread of a character by gene flow, as described above. The distinction between such 'anagenetic' evolution, and the cladogenetic origin of a new species, can be difficult to determine palaeontologically. A rigorous demonstration of cladogenesis requires the contemporary occurrence of parent and daughter species in the

341

same area without interbreeding (sympatry), even if it lasts only a short time before extinction of the parent species. Such sympatry can be detectable if in an isochronous horizon, two morphological types are found which are either clearly distinct, or at least form a bimodal distribution in the morphology of a key character or characters (Fig. lOc'). In contrast, a sample in which there is continuity of ancestral and descendant character states with no clear bimodality, could be the result either of sympatric coexistence following cladogenesis (Fig. lOb'), or could alternatively represent the transitional phase of purely anagenetic evolution from the ancestral to the descendant form (Fig. lOe'). DISCUSSION AND C O N C L U S I O N S The complex patterns of change in Quaternary m a m m a l species and faunas provide a vast amount of information of potential value to biostratigraphers. The conclusion of this review is not that these patterns are too complex and variable to be usable in biostratigraphy. The conclusions are, rather, that (i) an understanding of the biological processes underlying the fossil data is essential for their interpretation and

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FIG. 10. Morphological changes in cladogenesis and anagenesis, and the resulting patterns in the fossil record. (a)-(c) Cladogenesis, (d)-(f) anagenesis. Solid curves: morphological range of the living species; dashed curves: perceived morphological range in fossil samples. The vertical line represents the same morphological point throughout. (a) The starting point of cladogenesis: a single species; (b) two daughter species in sympatry with only a slight morphological difference; (b') a fossil sample derived from (b), looking deceptively like a single species; (c) two daughter species in sympatry with a clear morphological difference; (c') a fossil sample derived from (c), the existence of two species being evident from the bimodality and broad overall range; (d) the starting point of anagenesis: a single species; (e) and (f) successive stages in anagenetic evolution: the mean shifts, without division of the species, and this is reflected directly in the fossil samples (e') and (f'). Note how fossil samples (b') and (e') could appear identical, although resulting from different patterns in the living populations.

342

A.M. Lister

biostratigraphic usage, and (ii) the pattern of change in each taxon must first be established, on independently dated samples, before it can be used in the dating of new samples. The diversity of biological processes observed in living mammals indicates that considerable variation in pattern is to be expected between fossil taxa and between different time-frames and environmental situations. The pattern of change in a given taxon or region is not predictable a priori, but must be demonstrated in the fossil record. It has been the assumption of simplistic patterns of evolution and species turnover which has prejudiced the value of much mammalian biostratigraphy in the past. This perspective can be illustrated by an example, The occurrence of hippopotamus in a British Upper Pleistocene deposit is generally taken to indicate the lpswichian (Eemian) Interglacial Stage (correlated with Oxygen Isotope Stage 5e) (Gascoyne et al., 1981; Currant, 1989). The critique of presence/absence criteria presented in this paper does not mean that the presence of hippopotamus cannot be taken as a stratigraphic marker for a particular period of time. It means, rather, that because hippopotamus was potentially capable of expanding its range into Britain on numerous occasions, the occurrence of the species at a series of sites is not in itself sufficient evidence for their contemporaneity. It must be accompanied by clear evidence that other periods of time did not harbour hippos, and that all hippos which have been independently dated are of Ipswichian age. At present, all available evidence supports this contention, so the species can be used (preferably with other lines of evidence) as a marker for the Ipswichian, even in the absence of absolute dating of the deposit from which it came. Similarly, the evolutionary history of a particular taxon may be of great potential value in biostratigraphy, but only if the detailed pattern of change has been established in advance. This requires sampling from many different dated horizons, over a sufficient geographical range. The extrapolation of a biostratigraphic framework from very few or no dated samples, on the assumption that all change will be gradual, unidirectional and congruent over the whole geographical range, is not justifiable. In addition, it is important to select appropriate morphological characters for study, and to establish changes on the basis of statistical samples. Once the framework has been established, the dating of a 'new' sample on the basis of its morphology also requires a sample of sufficient size for statistical assessment. Analogous considerations apply to the biostratigraphic use of the palaeoenvironment, as reconstructed from a mammalian fauna. Particularly with extinct taxa, and even with living ones if the occurrences are in the earlier part of the Quaternary, the palaeoenvironmental range of a species should ideally first be established on the basis of a series of sites of known climate and vegetation (from pollen, sedimentological and other studies), before the species is used to predict

the palaeoenvironment of a 'new' site. It might be argued that many of the biological processes described in this paper are not relevant to biostratigraphy since they occur at time-scales below the level of stratigraphical resolution, and/or are minor, reversible 'quirks', so that in the geological record their effects would be 'ironed out'. This may to some extent be true for the pre-Quaternary fossil record, where stratigraphic resolution is often relatively coarse. However, many of the processes described here do have significant effects at time-scales from 10°-10 ~ years, covering the intervals at which Quaternary biostratigraphy operates, and within which most of its unresolved problems occur. Processes such as the appearance of evolutionary novelties in one part of a species' range before another; fluctuations or reversals in evolutionary rate; and the extinction of a species in different areas at different times, are therefore highly germane to the biostratigraphic usage of mammalian data in the Quaternary. Another common supposition is that a particular faunal composition, or evolutionary stage of a species, is valid for the whole of a certain Quaternary chronostratigraphic or climatic stage, based on its occurrence at a few sites pertaining to that stage. This assumption is belied by the rapidity of change possible in mammalian species and faunas. The boundaries with which we choose to delimit chronostratigraphic stages do not necessarily relate to the times at which faunas or species changed. This is particularly true of the 'cold stages', which are long, complex and poorly sampled periods of time, encompassing significant changes of climate, vegetation, and inevitably mammalian faunas. A pattern of faunal or evolutionary change whose dating is known only within broad limits can still be of use in biostratigraphy, if a correspondingly broad age determination has value. For example, it was pointed out earlier that the date of extinction of Dicerorhinus etruscus and Megaloceros verticornis was between 500 and 250 ka BP, but is not known more accurately than this. The finding of these species in a deposit has value in suggesting an upper age limit of 250 ka, if no more refined method of dating is available. Such deductions are valid provided their resolution is not expected to go beyond the information on which they are based. In the characterisation of a fauna for biostratigraphic purposes, the more species that are examined, and the more morphological variables within each species, the more reliable will be the conclusions. Moreover, an individual species or character which taken alone would have little explanatory power, can make a valid contribution as part of a larger body of evidence. For example, a small wolf is consistently found in a group of broadly correlated early Middle Pleistocene sites in Europe, such as Mosbach, Germany and Westburysub-Mendip, England (Bishop, 1982). Biologically, it is entirely plausible that small wolves occurred at other times in the Quaternary, and that larger animals might have existed at other times within the early Middle Pleistocene. In isolation, the size of a wolf would be

Mammalian Fossils and Quaternary Biostratigraphy

very poor evidence of the age of a deposit, but taken with other lines of evidence, it can contribute to the decision whether a deposit is (or is not) the same age as the Mosbach/Westbury group. Establishing the details of Quaternary faunal and evolutionary history is being increasingly aided by advances in absolute dating. Techniques include amino-acid epimerisation, electron spin resonance, thermoluminescence, palaeomagnetism, and an array of radiometric methods (Cook et al., 1982). In combination with lithostratigraphic superposition and correlation, and the careful collecting of samples, these methods are allowing an increasing number of mammalian samples to be properly dated in an absolute or relative sense, so providing us with a sufficiently accurate framework of mammalian history for biostratigraphic purposes. Repenning (1987) has emphasised the importance of establishing a biostratigraphy on the basis of firm independent dating. In his North American microtine zonation, ten migration and evolutionary events in the past 7.0-0.1 Ma are calibrated, chiefly by K/Ar dating. The importance of absolute dating and lithostratigraphy for establishing patterns of faunal change, before the latter can be utilised in biostratigraphy, does not mean that biostratigraphy is relegated to a secondary or unimportant role. Once the framework is established, mammalian data provide a rapid and effective means of dating and correlation, and are often available in situations where absolute or lithostratigraphic dating is not possible. Moreover, fossils can be used to provide a relative chronology based on superposed assemblages, which can often provide finer resolution than permitted by the errors inherent in absolute dating, even if the strata are suitable for the latter (Woodburne, 1987b, p. 4). Finally, a rigorous approach to establishing the details of Quaternary faunal history will produce information of value not only to the biostratigrapher, but also to the ecologist and evolutionary biologist. The patterns of change which come to light have a great deal to contribute to our understanding of mammalian evolution and distributional history in their own right. These strictly biological fruits of Quaternary mammal research will be the subject of a forthcoming review (Lister, in preparation). As in biostratigraphy, independently dated samples are essential for studies of this nature. Samples dated on the basis of poorlyestablished evolutionary or distributional patterns introduce circularity into the study of those patterns themselves. ACKNOWLEDGEMENTS I am grateful to A.D. Barnosky, A.P. Currant, R.C. Preece, A.J. Stuart and A.J. Sutcliffe for commenting on the manuscript, and NERC for financial support.

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