Periodic Cycles

The controversial issue as to whether mass extinctions have occurred at equally spaced intervals has stimulated interest in the periodicity of geologic events. The most striking examples of periodic oscillations between environmental states in the recent past are those between glacial maxima and glacial minima during the past 2.5 m.y. These transitions, which have affected sea-level, climates, and biotas, have been linked to periodic changes in the Earth's axial and orbital rotations—the so-called Milankovich cycles. These cycles are best documented by foraminiferal fossils from deep-sea deposits, which exhibit relative enrichment in ¹⁸O when polar glacial expansion preferentially sequesters ¹⁶O from the hydrosphere. For reasons not yet known, periodicities of ~41,000 years, reflecting the tilt cycle of the Earth's axis, dominated until about 0.8 m.y. ago, when periodicities of ~100,000 years, reflecting the shape of the Earth's orbit, began to prevail.

Cycles in some pre-Neogene marine successions appear to reflect minor changes in sea-level or biotic productivity that were forced by Milankovich controls mediated by factors that remain poorly understood but may not always have entailed changes in ice volume. Certain Mesozoic lake deposits also contain evidence for Milankovitch-driven cyclicity, perhaps related to shifting monsoons or other patterns of rainfall and evaporation.

Nonperiodic Cycles

The most profound nonperiodic cycles of global change have been long-terms oscillations between what have been termed the ''hothouse" and the "icehouse" states for oceans and atmospheres. The term hothouse is preferred to "greenhouse" because the conditions described may not always result from greenhouse warming; the hothouse states are, however, characterized by warm polar regions and warm deep oceans. In contrast, the icehouse state entails cold (usually glacial) polar conditions and a frigid deep-sea that results from the descent of cold polar waters.

The geologic record spanning the Eocene-Oligocene boundary documents the transition between a hothouse state and the icehouse state that has persisted to the present (Kennett et al., 1972). Much farther back in the geologic record, the interval spanning the Ordovician-Silurian boundary documents a similar transition, as well as the subsequent melting and retreat of glaciers and return of warmer conditions across broad regions (see Berry et al., Chapter 2).

The Eocene-Oligocene Transition

The recent ice age in the Northern Hemisphere constitutes only an intensification of the icehouse state that our planet entered about 34 m.y. ago, at the end of the Eocene Epoch. Fossil floras and vertebrate faunas reveal that early in Eocene time, subtropical conditions extended north of the Arctic Circle and that southeastern England and the Paris Basin (45 to 50°N) supported tropical rain forests. Fossil floras are, in fact, the most valuable indicators of terrestrial climates for the past 100 m.y. Not only does the taxonomic composition of fossil floras reflect climatic conditions, but so does leaf morphology, especially the percentage of species with smooth, as opposed to jagged or lobed, leaf margins; this percentage varies linearly in the modern world with mean annual temperature (Figure 1). Leaf morphology and cuticular structure also provide a guide to precipitation conditions. Fossil floras show that the Eocene-Oligocene climatic shift was profound at middle and high latitudes in both hemispheres. As warm-adapted floral elements disappeared from these regions, other types of vegetation, adapted to colder and drier conditions, expanded (see Christophel, Chapter 10).

Figure 1

Estimated changes in temperature in four areas over the course of Cenozoic time, based on percentages of species or fossil terrestrial plants having smooth leaf margins. Especially evident is dramatic cooling near the end of the Eocene Epoch (after Wolfe, (more...)

Climates actually did not undergo a simple shift between Early Eocene and Early Oligocene time. The tropical flora of England began to disappear at the end of Early Eocene time, as global temperatures began to cool, especially at high latitudes. By Late Eocene time, woodland savanna had already become the dominant vegetation of midcontinental North America (see Webb and Opdyke, Chapter 11). Whether the particular temporal pattern observed for North America characterized other continents remains uncertain, in part because of uncertain dating and in part because in some regions, such as Australia, a floral record is missing for much of the Eocene.

It is now widely agreed that the plate tectonic separation of Australia from Antarctica was a primary trigger of climatic changes near the end of the Eocene (and continuing separation caused further climatic changes after Eocene time). This event created the incipient circum-Antarctic current, which began to isolate the Antarctic continent from warm waters flowing from the north. The resulting cooling of surface waters led to the formation of cool deep waters. Enrichment of ¹⁸O in both planktonic and deep-sea benthic foraminifera and an influx of ice-rafted sediments indicate a significant, although temporary, expansion of the East Antarctic ice sheet at this time (see Kennett and Stott, Chapter 5). North Atlantic deep water (NADW), which is less dense than South Atlantic deep water (SADW), began to form slightly later, when rifting separated Greenland from Europe, permitting Arctic waters to descend into the North Atlantic (Schnitker, 1980). There is no question that climates cooled at middle and high latitudes, but four major questions remain:

1.

Fossil floras indicate that temperate conditions extended to high latitudes in both hemispheres during Early Eocene time. How was so much heat transported from the equator toward the poles?

2.

During this very warm interval, were the tropics warmer than, cooler than, or comparable to the tropics today?

3.

How did the oceanographic changes during the Eocene-Oligocene transition shut down the heat transport system that had existed previously?

4.

How did biotas throughout the world respond to the environmental changes?

Strong wind-driven currents cannot account for most of the meridional transport during the Eocene because, being dependent on steep thermal gradients, such currents are self-limiting. Most likely, a primary transport mechanism was the poleward flow of warm, saline subsurface water masses that formed at low latitudes. Whether the flux was sufficient to depress tropical temperatures below their modern levels remains a major question. Another is how the new system of thermohaline circulation thwarted this heat flux. Also at issue is the role of the greenhouse effect in producing the widespread warmth of the Early Eocene. If mean global temperature was well above that of the modern world, greenhouse warming is perhaps the most likely cause. If warmer high latitudes were accompanied by cooler equatorial conditions, then heat transport may have been the dominant control on the latitudinal temperature gradient.

More generally, one can ask how the secular changes in the greenhouse capacity of the atmosphere have interacted with increasing solar luminosity, continental geographies, and orogenic uplift to produce the significant climatic oscillations recorded throughout geologic time.

Sudden Shifts and Gradual Trends

Two issues of timing are especially difficult to resolve. One is whether important events were protracted. The other is whether protracted events were pulsatile. An incomplete geologic record can give the false appearance of suddenness for an event that was actually protracted. Similarly, an imperfect record can give the false appearance of simultaneity for physical events, such as onsets or terminations of glaciation in two or more regions. A worldwide chronology for the multiple glaciations near the end of Proterozoic time has yet to be established, for example. Events of severe extinction that appear to have been protracted or to have occurred in multiple steps warrant statistical scrutiny. A key issue is the completeness of the records of taxa before their final disappearance. Imperfect records can produce an illusion of gradual or multistep extinction for a group of taxa that actually died out simultaneously: the so-called Signor-Lipps effect.

For some major events, however, the geologic record is of sufficiently high quality to document a stepwise or pulsatile pattern. Eight steps of extinction, for example, have been identified for the Cenomanian-Turonian crisis (about 91 m.y. ago). The Ordovician crisis (about 440 m.y. ago) had two principal phases, each possibly lasting hundreds of thousands of years (see Berry et al., Chapter 2). The first pulse, at or near the Rawtheyan-Hirnantian stage boundary, coincided with glacial expansion. The second occurred within the Hirnantian (latest Hirnantian Ordovician) age, during the glacial maximum.

The geologic record documents numerous changes in the global ecosystem that spanned many millions of years. For these trends, the record, though imperfect, is too extensive to be masking a single dramatic event. We may nonetheless have difficulty in distinguishing between gradual and stepwise patterns for such trends. The classic example of this kind of trend is the climatic transition toward cooler and drier conditions on many continents between Eocene and Pleistocene times. During this time, prevailing biomes over broad regions shifted from tropical forest through savanna to grassland and steppe (see Christophel, Chapter 10; Webb and Opdyke, Chapter 11). While the terminal Eocene transition described earlier was a major early step in this trend (and was itself a complex event), the degree to which later changes were stepwise is not well established. It is, however, clear that net rates of change varied from place to place. One of the difficulties in resolving the details is in distinguishing between global changes and regional changes that resulted from such events as tectonic uplift in the American West or the Himalayan region.

The most recent geologic record offers special opportunities to establish temporal resolution for events on very short time scales. Studies of glacial varves suggest that the Younger Dryas cooling episode that interrupted deglaciation in the Northern Hemisphere between about 11,400 and 10,200 years ago developed during an interval of less than 300 years and may have ended during an interval of less than 20 years (Dansgaard et al., 1989).

The Nature of Thresholds

Even a gradual environmental change can result in a sudden change of state when a threshold is crossed. The growth and contraction of glaciers are inherently unstable processes because glaciers have a higher albedo than land. One result is that the birth of a relatively small glacier can plunge a high latitude region into an interval of widespread glaciation. The development of the Antarctic cryosphere during the Eocene-Oligocene transition is such an episode. Cooling during the Late Eocene eventually proceeded to a point where the cryosphere expanded (and it has never returned to its previous state). Another example is the abrupt shift of meltwater drainage and the resulting change in thermohaline circulation patterns that may have triggered and terminated the Younger Dryas.

Ecological limitations of organisms yield thresholds of biotic response to environmental change. For example, global circulation models suggest that during the Cretaceous Period, surface water temperatures and salinities across much of the Tethyan Ocean may have come to exceed the tolerance of most modern reef-building corals (30°C and 3.7% salinity). A shift past critical limits may explain the corals' relatively sudden loss of dominance to rudist bivalves in the central Tethyan reefs during Albian time, about 113 to 98 m.y. ago (see Barron, Chapter 6).

At the end of the Westphalian age of the Pennsylvanian Period, drier climates swept across North America and Europe, with profound consequences for vegetation (see DiMichele and Phillips, Chapter 8). As loss of swamp habitat reached a critical threshold, the arborescent lycopods that had been a conspicuous feature of landscapes for tens of millions of years disappeared rapidly. When climates amenable to swamp formation returned, ferns and tree ferns rose to dominance in these environments. The paleobotanical record shows repeated evidence for the adaptation of plants to particular environments, followed by extinction when habitats were disrupted.

Thresholds appear to have been crossed for antelopes, micromammals, and members of the human family close to 2.5 m.y. ago in Africa, with the rapid shrinkage of forests during the onset of the modern ice age. Forest-dependent species within all three groups disappeared over a broad area during an interval on the order of 10,000 years, and many species adapted to open, grassy habitats made their first appearances (Vrba, 1985). Within the human family, it appears that gracile australopithecines died out because they had depended on forests for food and refuge (see Stanley, Chapter 14). In the manner of modern chimpanzees, these animals presumably slept in trees and fled into them when threatened by predators. The characterization of paleofloras at fossil hominid sites using carbon isotopic ratios of paleosols reveals an acceleration at about 2.5 m.y. ago in the long-term Neogene shift from closed forests toward grassy habitats (Cerling, 1992). Apparently no fossil site supported a closed canopy forest after this time.

Although the preceding examples highlight the role of environmental thresholds in promoting extinction, at times environmental change has opened up new evolutionary possibilities. For example, increases in the partial pressure of oxygen must have crossed crucial thresholds for the evolution of life during Archean and Proterozoic time (see Knoll and Holland, Chapter 1). Increased partial pressure of oxygen to 1, 10, and essentially 100% of present-day levels would have cleared the environmental path for the evolution of aerobic bacteria and mitochondria-bearing eukaryotes, obligately photosynthetic eukaryotes, and large animals, respectively. In addition, an increase to levels much closer to those of today may have permitted the evolution of large animals. (As animals evolved complex circulatory and respiratory systems, they would have been able to expand into less oxygen-rich regions of the ocean and to enclose their tissues within thick mineralized shells.)

Migration

The intercontinental migration of Cenozoic land mammals has produced numerous natural experiments of faunal mixing. In interpreting the fossil record of these events it is often difficult to trace the causes of dispersal in detail. Correlation of the deep-sea oxygen isotopic record with pulses of mammalian migration between Eurasia and North America implicates land bridges produced by glacially controlled eustatic lowering of sea-level (see Webb and Opdyke, Chapter 11). The subsequent spread of taxa throughout new regions may have been influenced by climatic or other environmental changes. In addition, it is not always clear whether the excessive rates of extinction that have typified regions being invaded by new species have resulted from habitat change or adverse species interactions. What is clear at present is that during the Cenozoic there had been a strong correlation between mammalian turnover and changes in sea-level and climate.

The behavior of plant associations during floral migration has recently attracted much attention, partly because of its implications for floral changes during future global warming and partly because new evidence has contradicted the traditional view that modern biomes are ancient, coadapted associations. It appears that during the glacially induced climatic and eustatic fluctuations of the Pennsylvanian Period, coal swamp floras retained their ecological structure through many cycles of expansion and contraction (see DiMichele and Phillips, Chapter 8). Perhaps this can be attributed in part to the discrete character of the moist coal swamp environment, which did not easily exchange species with neighboring habitats. On the other hand, the pollen record of the past 20,000 years reveals that modern forest biomes of the temperate zone are transitory associations, not long-standing ones (see Webb, Chapter 13). Today in eastern North America, for example, Pinus (pines) and Quercus (oaks) have largely complementary geographic distributions outside the coastal plain, but this pattern has developed since the rapid contraction of glaciers about 10,000 years ago. During the most recent glacial maximum, pines and oaks were both largely restricted to a small region of the southeastern United States. Independent migration of plant species during future climatic changes could have important consequences for negative interactions between species of both plants and animals. Additional evidence of biotic mixing comes from small areas of Australia, where the present blending of floral provinces seems to have resulted from mid-Miocene warming.

Exactly what happened to tropical rain forests during Pleistocene glacial maxima remains unclear. Limited palynological and paleogeomorphological data suggest that the Amazon rain forest was considerably reduced in area during the last glacial maximum. Also, present geographic occurrences of certain taxa of plants and animals have been interpreted as relict distributions produced by fragmentation of rain forests during glacial maxima. This possibility needs further study, as does the more general question of coherence of rain forest communities during the past 2.5 m.y.

In the modern marine realm, many species that lived together in shallow water Pliocene environments of eastern North America are now confined to separate depth zones. Increased seasonality (especially colder winter temperatures) since the onset of the recent ice age has driven thermally intolerant forms into deeper waters (see Stanley and Ruddiman, Chapter 7).

Extinction

In recent years, numerous biological patterns—biases against certain kinds of taxa— have been detected for particular episodes of extinction. Commonalities among victims often point to causes. In global mass extinctions such as the terminal Ordovician, Cenomanian-Turonian, and terminal Cretaceous events, tropical taxa, including reef communities, suffered preferentially. This is consistent with the idea that climatic cooling played a major role in extinction, but it may also reflect the typically narrow niche breadth of tropical taxa and the high degree of interdependence among species.

High-resolution stratigraphic and paleoenvironmental studies are crucial for understanding mass extinctions. Such studies reveal that a major extinction in deep-sea benthic assemblages at the end of the Paleocene, the most profound of the last 90 m.y. for this habitat, resulted from rapid warming of the deep oceans in conjunction with global warming (see Kennett and Stott, Chapter 5). Extinctions that removed between 35 and 50% of deep-sea taxa occurred in less than 2000 years, equal to the time required for the deep water to circulate through its basins. For a few thousand years, ocean circulation underwent fundamental changes that affected the deep-sea biota. High-resolution study of this event has illustrated, first, how events that are geologically brief but not instantaneous can strongly alter the ecosystem and, second, how such changes can be largely decoupled from events in other segments of the biosphere.

Patterns of extinction can point to particular causes of mass extinction. For example, the severe extinction of western Atlantic bivalve mollusks during the onset of the modern ice age seems to have eliminated all strictly tropical species of southern Florida; all survivors have broad thermal tolerances, ranging well beyond the tropics today. Here, a thermal filter seems clearly to have operated (see Stanley and Ruddiman, Chapter 7). Similarly, that climatic change was the ultimate cause of the previously discussed severe extinction of African mammals at the start of the modern ice age (-2.5 m.y. ago) is supported not only by the evidence that forest habitats shrank at this time but also by the fact that forest-adapted species were the primary victims (Vrba, 1985).

Some patterns of extinction have characterized higher taxa in more than one mass extinction. A striking aspect of the terminal Cretaceous extinction of planktonic foraminifera was the disappearance of species with large, complex, highly ornamented skeletons (see Keller and Perch-Nielsen, Chapter 4). Survivors were inherently small species or species that became dwarfed during the crisis. Deep-water planktonic species also died out first and in the largest numbers. These patterns must be taken into account in any analysis of the proximate causes of extinction. Most species of planktonic foraminifera that became extinct during the Late Eocene to Early Oligocene extinction were also complex, highly ornamented species. These were also largely warm-adapted taxa, which is compatible with evidence that climatic changes were the primary cause of this global crisis.

If there is one general pattern for extinctions, it is the rate of environmental change and not necessarily its magnitude that places most populations in jeopardy. This consideration is highly relevant to global changes predicted for the next century. If current models are correct, the magnitude of change will not be unusual on a geological time scale, but the rate of change may be.

Evolutionary Turnover

Evidence of causation also comes from the nature of species that immigrate into a region or originate within it during or soon after a pulse of extinction. In other words, the disappearance of some species and the appearance of others during a brief episode of evolutionary turnover should offer compatible testimony about environmental change. Thus, not only did forest-adapted species of antelopes preferentially die out in Africa about 2.5 m.y. ago, but newly appearing species were virtually all adapted to grassy habitats. Simultaneously, the apparently semiarboreal gracile australopithecines gave way to early Homo, which had helpless infants and could not have climbed trees habitually for refuge (see Stanley, Chapter 14).

Not only during the Pliocene but throughout much of the Cenozoic Era, mammals experienced pulses of evolutionary turnover that produced stepwise net increases in the relative number of species adapted to savannas, grasslands, or steppes. The first pulse of evolutionary turnover came at the end of the Eocene, when the extinction event that also affected the marine realm removed numerous browsers, including the huge, rhino-like titanotheres. New mammalian taxa included numerous taxa adapted to eating coarse fodder (see Webb and Opdyke, Chapter 11).

By mid-Miocene time, the diversification of taxa—adapted to grassy habitats—had produced the greatest North American land mammal diversity of all time, in savannas that were the biotic equivalents of those in Africa today. Continuation of the trend produced drier grasslands and steppes with lower mammalian diversities later in the Neogene.

Although post-Eocene pulses of turnover for Cenozoic mammals have not yet been shown to correlate well with particular floral shifts, they have been correlated with isotopic evidence of glacial expansion. Efforts to associate turnover with global climatic changes are complicated by regional trends produced by major tectonic events, such as the uplift of the Sierra Nevada, the Colorado Plateau, and the Himalayan Plateau. Similarly, although the spectacular diversification of grasses and other plants adapted to dry, seasonal habitats clearly resulted from the general post-Eocene climatic trends, intervals of diversification have not as yet been associated with pulses of extinction of moist-adapted forms.

Delayed Recovery

Severe extinctions that are not largely offset by simultaneous immigration or speciation result in impoverished ecosystems that sometimes persist for millions of years. Several factors can contribute to delayed recovery. Sometimes a delay results from a dearth of taxa capable of responding to the opportunity created by severe extinction. A striking example is the absence throughout Mississippian and Pennsylvanian times of a framework-building reef community to replace the tabulate-stromatoporoid community that had been devastated in the Late Devonian mass extinction (James, 1984). Contrasting with this situation was the rapid diversification of sclerophyllous terrestrial plants (forms with reduced leaves and thickened cuticles) in Australia after the Eocene (see Christophel, Chapter 10). These taxa seem to have originated in nutrient-poor soils at the margins of Paleogene rain forests and were, in effect, poised for rapid evolutionary response when, because of aridification, soils deteriorated over a broad area of the continent. Similarly, the mammals' evolutionary recovery from severe Late Eocene extinction in the Northern Hemisphere was accelerated by the fact that a variety of mammalian taxa with high-crowned teeth adapted for grazing on coarse vegetation had already evolved during the Eocene, prior to the severe climatic change (see Webb and Opdyke, Chapter 11).

For reasons that remain to be explained, small brachiopods that occupied the chalky seafloor of western Europe attained their former diversity within about 1 m.y. after the terminal Cretaceous extinction (see Figure 2). In general, delayed recovery from severe extinction has typified the marine realm. After the severe extinction of Late Eocene and Early Oligocene times, for example, marine faunas remained relatively impoverished throughout the Oligocene. Delayed marine recovery appears to have two primary causes. One is the inherently slow rate of adaptive radiation that characterizes many taxa of marine animals. The other is the typical failure of postcrisis conditions in the marine realm to stimulate the adaptive radiation of new kinds of taxa adapted to these conditions—to provide a new resource base comparable to productive savannas on the land (see Stanley and Ruddiman, Chapter 7). Even as overall mammalian diversity declined in North America after mid-Miocene time, certain mammalian and other taxa favored directly or indirectly by aridification underwent spectacular adaptive radiations: songbirds and Old World rats and mice—two groups that included many species that fed on the seeds of the rampantly radiating herbs and grasses—as well as colubrid snakes, which prey on rats and mice and songbird chicks and eggs (see Figure 3).

Figure 2

Diversity of small brachiopods in the chalk of western Europe. About three-quarters of the species died out suddenly in the terminal Cretaceous extinction, but a larger number of new species then originated very rapidly, during the next million years (more...)

Figure 3

Proliferation of adaptive radiation upward from the base of the food web in terrestrial ecosystems that were favored by the global trend toward aridification during the past 25 m.y. (from Stanley, 1990). Many songbirds and Old World rats and mice feed (more...)

Pre-Cenozoic marine faunas offer many additional examples of delayed recovery. The few small planktonic foraminifera that survived the terminal Cretaceous extinction died out sequentially during the first 200,000 years or so of Paleocene time, while new species evolved (see Keller and Perch-Nielsen, Chapter 4). The new forms were initially small, simple, and unornamented. Planktonic foraminifera did not recover their pre-extinction level of diversity until late in the Early Paleocene. Very low δ¹³C values and low vertical δ¹³C gradients indicate that the crisis produced low productivity in surface waters of the ocean. Drastic reduction in the abundance of calcareous nannofossils offers similar testimony, although a small number of opportunistic species experienced regional blooms. The planktonic realm began to recover only after 250,000-300,000 years. Exactly when shallow water benthic invertebrates began to rebound from the terminal Cretaceous crisis is unknown, but their recovery occupied most of Paleocene time (Hansen, 1984).

Recovery of marine life from the Cenomanian-Turonian crisis, earlier in the Cretaceous, was also slow, in part because of the loss of basic elements of the ecosystem, such as numerous taxa of reef-building rudists (see Kauffman, Chapter 3). During the terminal Ordovician mass extinction, the cool-adapted Hirnantian fauna expanded geographically but did not diversify appreciably (see Berry et al., Chapter 2). Reradiation of graptolites and decimated benthic faunas was slow during the early phases of deglaciation. Few graptolite species survived to initiate radiations after the crisis, and brachiopods began to diversify only after sea-level began to rise and climates became warmer. Trilobite faunas remained impoverished until late in the Early Silurian, with most species tolerating a wide range of environmental conditions.