Extinction may not be forever

Naturwissenschaften (2005) 92:1–19 DOI 10.1007/s00114-004-0586-9

REVIEW

L. D. Martin · T. J. Meehan

Extinction may not be forever

Published online: 16 November 2004
Springer-Verlag 2004

Abstract Here we review the phenomenon of ecomorph evolution and the hypothesis of iterative climatic cycles. Although a widely known phenomenon, convergent evolution has been underappreciated in both its scope and commonality. The power of natural selection to override genealogy to create similar morphologies (even among distantly related organisms) supports classical Darwinian evolution. That this occurs repeatedly in stratigraphically closely spaced intervals is one of the most striking features of Earth history. Periodic extinctions followed by reevolution of adaptive types (ecomorphs) are not isolated occurrences but are embedded within complex ecological systems that evolve, become extinct, and repeat themselves in temporal synchrony. These complexes of radiation and extinction bundle the biostratigraphic record and provide the basis for a global stratigraphy. At this scale, climatic change is the only mechanism adequate to explain the observed record of repeating faunas and floras. Understanding of the underlying causes may lead to predictive theories of global biostratigraphy, evolutionary processes, and climatic change.

L. D. Martin ()) Natural History Museum and Biodiversity Research Center, Department of Ecology and Evolutionary Biology, University of Kansas, 1345 Jayhawk Blvd, Lawrence, KS 66045–7561, USA e-mail: [email protected] Fax: +1-785-8645335 T. J. Meehan Division of Science, Chatham College, Buhl Hall, Woodland Rd, Pittsburgh, PA 15232–9987, USA T. J. Meehan Research Associate, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, USA

Introduction Here we review the hypothesis of iterative climatic cycles, which states that the evolution of faunas and floras and their extinction has a predictable pattern. South American pollen and North American mammalian assemblages exhibit convergent evolution in repeating A-BC cycles (van der Hammen 1957, 1965; Martin 1985; Meehan and Martin 2003), and these consecutive A-B-C communities form a chronofauna. The stability and then extinction of these communities have been correlated to cycling sedimentary and temperature profiles. This pattern is reflected in simultaneous radiations of convergent adaptive types (ecomorphs) on separate continents, indicating that it results from natural selection caused by global climatic change, as opposed to genetic or community biotic factors. An iterative pattern of hierarchical climatic cycles may form the underlying basis for biostratigraphy and explain most evolutionary trends and extinctions. The cycles recognized so far appear to represent equal units of time—2.4 Ma for each A, B, and C cycle, and 7.2 Ma for this chronofauna triplet. Whether the cycles represent equal units of time is integral to understanding the cause of these cycles, but is not integral to the main thrust of the argument; repeating ecomorph evolution and extinction among different lineages occurs synchronously, and only climatic change has broad enough effects to produce this pattern. It would be very important to establish that climatic change and evolutionary processes, including extinction, are due to random historical accidents, but it would also be a scientific dead end. A predictive model of climatic change and correlated evolutionary processes is obviously much more desirable, but can such a model be constructed? While the basis of stratigraphy and almost all geology is the Law of Superposition, we must use fossils to construct a regional or global stratigraphy. The units of biostratigraphy are unique combinations of last and first appearances of organisms. If such events were randomly distributed over the rock column, boundaries would result solely from historical accidents, and these boundaries

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might change with the whims of prevailing academic politics. It seems obvious that it would be better if a boundary corresponded to a recognizable global event. A climatic-evolutionary connection seems fundamental to biostratigraphy, and Krasilov (1974) advocated a climatic-based system in his causal biostratigraphy. He implicated overall ecological change as the key to understanding biostratigraphy and stated that the succession of ecosystems is controlled by climatic cycles. This implies that there are bundles of time that can be recognized on the basis of unique biological compositions and the impact of climate on the sedimentary record. There is a school of thought that claims that there is no visible evidence for climatic impact on evolution (e.g., Prothero 1999; Alroy 2000), but most workers see a clear connection, and Darwinian evolution seems to demand such a result. There are numerous studies of modern organisms correlating climate and adaptation, and natural selection resulting from climatic change has been observed in a three-decade study of Darwin’s finches (Grant and Grant 2002). From the fossil record, we have empirical evidence that climate changes over time and that biota are directly affected. For instance, Europe was fully tropical in the Middle Eocene, as evidenced by the famous deposits at Messel where we find rainforest trees and animals whose closest analogues are in Africa today (Schaal and Ziegler 1988), while fossils of 18,000 years ago indicate a tundra flora and fauna (von Koenigswald and Hahn 1981). The overall global trend during the past 55 Ma has been towards cooling, but we are presently experiencing a reversal of that trend. There is relatively little evidence of long periods of climatic stasis, and all long-term patterns are interrupted by periodic fluctuations where the general trend is reversed. The usual measures for climatic regime are temperature and its effects as expressed in terms of water. Hot worlds are wet worlds because of increased energy and water surface area for evaporation, while cold worlds are dry. Wet worlds favor canopy strategists (trees) and cold worlds pioneering plants and open vegetational structures (Martin 1994). Wet worlds favor sedimentary deposition with increased plant cover and a higher base level, whereas dry worlds are characterized by increased erosion. Climate is mediated locally, and it is possible for a local region to be dry when global averages are wetter. Ultimately weather patterns are interconnected, and climate cannot change greatly over any large region without affecting all regions. Usually environmental change is bad for established organisms. Changing rainforest to grassland may be bad for monkeys, while changing grassland to forest may be bad for wildebeest. Global change is likely to have a negative impact on organisms best adapted to the status quo. On the other hand, organisms that occupy marginal habitats may find their habitat greatly expanded as climate changes (e.g., Martin 1994). We may predict that rapid environmental change will result in nearly simultaneous extinction of many taxa and dramatic biogeographic reorganization of others and that

these changes will have a global signature. Some version of this scenario must lie at the root of biostratigraphy. Ecomorphs The similarities among organisms are a greater theoretical problem than differences. Differences can and should result from random events over time. Historical accidents come into full play when we examine how organisms differ, but how are we to explain characters that are conserved over vast intervals of geologic time? We see immense amounts of conserved similarity in genetic composition and cellular processes over the hundreds of millions of years that organisms have inhabited Earth. Without the action of natural selection, such similarities would soon have fallen prey to random processes. There are also not an infinite number of solutions to biological problems. In fact the number of solutions seems to be quite small judging from the number of times that the same solution is evolved independently. A computer simulation of “organisms” shows that with strong selection, convergent evolution of even a complex trait is common (Lenski et al. 2003). Natural selection produces suites of coordinated similarity resulting from shared activities, rather than shared phylogeny. If the shared activity is an integral part of an “ecological occupation,” it may predict other similarities related to that occupation. Cuvier’s great contribution to comparative anatomy was the principle of correlation—the idea that changes in one anatomical suite required concordant changes in others and that a lifestyle could be predicted from a subset of correlated structures. It is this ability of ecological position to predict anatomy independent of phylogeny that is the basis of the ecomorph concept (Martin and Naples 2002). Convergent organisms have been called ecomorphs (ecological morphotypes; Williams 1972), which can be correlated to Van Valen’s (1971) adaptive zone—an organism’s resource space together with relevant predation and parasitism. An important property of adaptive zones is that they exist as opportunities within the ecological framework and are defined by specific resources. The existence of an adaptive zone creates an opportunity for the development of a specialized organism to occupy it, but does not require or imply that such an organism exists (Martin and Naples 2002). Simpson (1953:161) anticipated this view: “Possible ways of life are always restricted in two ways: the environment must offer the opportunity and a group of organisms must have the possibility of seizing this opportunity.” Ecologies contain opportunities that define circumscribed morphologies, including physiology and behavior. Convergent forms evolve independently in separated but similar ecologies, demanding only that adequate predecessors for the morphological type be present. Similar ecomorphs generally do not evolve in the same region at the same time, but require either geographic or temporal separation (Martin and Naples 2002).

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Fig. 1A, B Correlated climatic cycles of North and South America. A Top graph: iteration of A, B, and C community types of pollen ecomorphs and the cyclic nature of abundances of the palm palynomorph group, Monocolpites medius, in South America (modified from van der Hammen 1961: Fig. 1). Increasing abundances of M. medius (shaded) indicate decreasing temperatures (towards bottom of graph). Note that more severe cooling characterizes the end of subcycle C. Bottom graph: correlated North American subcycles based on mammalian assemblages (Martin and Meehan 2002). Each A-B-C community represents a vadh climatic cycle, and this triplet forms a stout climatic cycle. B Climatic cycles and dirktooth iterative evolution. Stratigraphic distribution of latest Eocene– Pleistocene (Chadronian-Irvingtonian) mammalian faunas of North

America as compared to Stout’s (1978) sedimentary/climatic cycles of Nebraska correlate to the triplet climatic cycles of van der Hammen (1961). Martin’s interpretation (1985) of Stout’s cycles is shown, as well as the independent evolution of dirktooths within these cycles. The Barstovian and Hemphillian are poorly represented in Nebraska. The base of each sequence is characterized by heavy fluvial incision and deposition, and the top, by eolian and/or caliche horizons. The paucity of cat ecomorphs in the Hemingford Cycle is referred to as the “cat gap.” Note that in North America formational boundaries are not necessarily the exact correlates of biostratigraphic boundaries, so that these climatic cycles correlate with faunal assemblages (NALMAs or subages), and not with defined rock boundaries. Modified from Martin 1985: Fig. 5

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Convergent adaptive types plagued taxonomic work in Cuvier’s time and continue to do so. Ecomorph analysis is “free of taxonomy” (Damuth et al. 1992) and yields a perspective on evolutionary processes not attainable from a phylogenetic approach. Organisms live and evolve within communities, so perhaps taxonomic units are the wrong units for understanding causal mechanisms (Meehan and Martin 2003). Large-scale ecological analyses in deep time are rare even though the benefit of such work is widely advocated (e.g., van der Hammen 1965; Krasilov 1974; Fischer 1981; Damuth et al. 1992). Large-scale paleontological analyses of South American pollen (van der Hammen 1957; Leidelmeyer 1966) and North American mammals (Martin 1985; Meehan and Martin 2003) reveal repeated evolution and extinction of ecomorph types, suggesting the existence of global iterative climatic cycles. Hypothesis of iterative climatic cycles Van der Hammen (1957, 1961) discovered an iterative pattern in a succession of Late Cretaceous to late Cenozoic pollen assemblages from oil well core samples in Colombia, South America. Pollen shapes can be highly convergent and are not assignable to species level, but are classified as form genera (palynomorphs). Pollen classification is basically a functional one of adaptive types, similar to leaf shape ecomorphs (e.g., Wolfe 1985). Van der Hammen (1957) described pollen abundances of palms, other angiosperms, and ferns that had synchronous minima and maxima at apparently regular intervals, representing three assemblage types. Pollen community A was succeeded by a B community and the B succeeded by a C before the pattern repeated with the re-evolution of a convergent A community. This A-B-C triplet pattern was best expressed by palm pollen of the Monocolpites medius group (Fig. 1A). Abundance of M. medius pollen reflected temperature trends during the Cenozoic, with a relatively cool period in the early Paleocene, extensive warming into the early Eocene, and then overall cooling up to the Recent (van der Hammen 1961). On a smaller scale, minima and maxima of pollen abundances within each community type represented cyclic warming/cooling periods on the order of 2 Ma (Fig. 1B). Each subcycle begins relatively cool, warms considerably, is somewhat stable, and then cools sharply at the end. Extinction at the community level occurs near this temperature minimum. At the end of subcycles A and B, the temperature drop is similar in magnitude, and at the end of subcycle C, the cooling is greater. Subcycle A is warmest, B almost as warm, and C much cooler. Stout (1978) and Schultz and Stout (1980) recognized sedimentary cycles in the central Great Plains of North America that reflected regular changes in climate since the mid-Cenozoic. Studies of fluvial terraces, soil horizons, and loess deposits show a repeating pattern of valley cut-and-fill sequences related to fluctuating aridity. The

base of each sequence is dominated by fluvial incision and deposition, the middle cycle by mixed fluvial and eolian infilling, and the terminal cycle by eolian deposition and an increase in caliche paleosols. This triplet pattern reflects a wet climate at the base, a moderate climate in the middle, and a much drier climate at the top. The White River Cycle as reflected in deposits of Nebraska (latest Eocene to early Oligocene) is an excellent example of this pattern (Fig. 1B). The Chadron Formation is predominantly channel and floodplain deposits, with occasional lake and pond deposits. The Orella Member of the Brule Formation consists primarily of channel and floodplain deposits, with rare pond deposits and some eolian influence. The Whitney Member of the Brule Formation in Nebraska is a loess deposit. Schultz and Stout (1980) stated that major mammalian extinctions occur at the unconformable boundaries in these sequences and suggested that these unconformities indicate dry, cool periods with relatively little plant cover and more erosion. Soil changes, as well as faunal and floral changes, support this climatic interpretation (Clark et al. 1967; Retallack 1983). This triplet pattern matches van der Hammen’s AB-C cycles, including the terminal cooling and drying, which is most severe at the end of subcycle C. In relating Stout’s sedimentary cycles to mammalian faunas, Martin (1985) recognized an iterative A-B-C pattern in mammalian communities. Through dispersal and adaptive radiation, a community type would develop and become extinct—only to redevelop in the same place during the next sedimentary cycle. Comparing faunas from the same position within different sedimentary cycles, Martin showed that they resembled each other in diversity and ecomorph composition, being more similar to one another than to the subcycles immediately below and above in the stratigraphic sequence. Figure 1B compares Martin’s interpretation of North American land mammal “ages” (NALMAs) and their subdivisions with Stout’s climatic/sedimentary cycles. The extinction of a dirktooth ecomorph at the end of one cycle and its reevolution in the next cycle exemplify repeating ecomorph replacement. Martin (1985) proposed that there was an iterative evolution of mammalian communities with a

Fig. 2A–D The A-B-C pattern in dominance turnover of mammalian ecomorphs in the North American Cenozoic. A Dominant herbivore ecomorphs of the order Artiodactyla: s Oreodontidae I radiation; D= Oreodontidae II radiation; Moschidae and Dromomerycidae; o Antilocapridae; l Bovinae and Cervinae; B Fossorial ecomorphs of the order Rodentia (extensive burrowers, such as pocket gophers, mountain beavers, and prairie dogs): n Cylindrodontidae; o Aplodontidae and Allomyidae; ' Castoridae/ Palaeocastorinae and Geomyidae/Entoptychinae; o Mylagaulidae; s Sciuridae/Sciurinae and Geomyidae/Geomyinae; C All cat ecomorphs: s Oxyaenidae; early Nimravidae; n early Felidae and late Nimravidae; D= late Felidae; D Shrew ecomorphs (cryptic, leaf-litter insectivores): D Cimolesta; l Nyctitheriidae; o Soricidae/Heterosoricinae; Soricidae/Soricinae; minor shrew ecomorph radiations not represented for graph clarity. The 27 Cenozoic units are North American land mammal “ages” or subages that reflect vadh climatic cycles (Martin 1985; Martin and Meehan 2002); see Table 2 for abbreviations

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period of about 7 Ma. Martin also showed that the dominance turnover in selenodont artiodactyls reflects this iteration (Fig. 2A). He further argued that this pattern was climatically controlled, showing a correlation with the cyclic temperature curve of Wolfe and Hopkins (1967). Meehan and Martin (2003) reported other mammalian iteration examples in hippo, dog, and bone-crushing dog ecomorphs. This pattern is also reflected in the dominance turnover of fossorial rodent, all catlike, and shrew ecomorphs (Fig. 2B–D). Martin and Meehan (2002) preliminarily extended this pattern of climatic cycles based on North American mammalian faunas to the early Cenozoic and calculated a more refined interval. Recent radiometric dates associated with mammalian faunas suggest a subcycle duration of 2.41 Ma and 7.23 Ma for the triplet. A subcycle thus approximates the duration of a marine zone, and a cycle a marine stage. Benton (1995) reported an average Phanerozoic stage duration of 7.4 Ma. The similarity of biostratigraphic systems (e.g., shells, mammals, and pollen) and, in particular, their correlation on a regional, and sometimes global scale, reflects an underlying basis. In studying Pleistocene terrace sequences and recognizing correlations of cut-and-fill sequences across central North America, as well as worldwide correlated stratigraphic boundaries and climatic events, Schultz and Stout (1980) concluded that these sedimentary cycles represent global climatic change. Van der Hammen (1961) came to the same conclusion concerning the cause of pollen community patterns, as did Wolfe (1978) concerning fluctuations in leaf ecomorph assemblages. Martin and Meehan (2002) concurred that any force able to simultaneously affect communities in North and South America would have global ramifications. Iterative evolution of ecomorphs and community structures requires repetition of environmental parameters, which suggests that climatic cycles form the underlying basis for a global stratigraphy (van der Hammen 1957, 1961, 1965; Martin 1985; Martin and Meehan 2002; Meehan and Martin 2003). Because stratigraphic systems tend to be more localized and carry with them significant historical baggage, Martin and Meehan (2002) proposed a new nomenclature for these cycles. Each subcycle of about 2.4 Ma is termed a “vadh” for T. van der Hammen, who first characterized this pattern and recognized its importance. The complete A-BC cycle is termed a “stout,” after T.M. Stout, who discerned this pattern in sedimentary cycles of the Great Plains and recognized its global significance in relation to marine stages. Vadhs A, B, and C form a stout in this terminology for climatic cycles and may be measures of time analogous to days, years, and Milankovitch astronomical parameters. Do these cycles represent equal units of time? Van der Hammen (1961) considered these repetitions in community types to be of equal duration. He assumed equal units of time based on two criteria: (1) within each

cycle (= stout), lake sedimentation thickness for each subcycle (= vadh) was approximately equal; and (2) from a theoretical consideration, a given pollen community type would likely take a similar amount of time to develop. Although van der Hammen’s criteria are not compelling, radiometric dates from associated mammalian faunas in North America do suggest equal units of time (Martin 1985). Martin also found comparable changes in diversity of late Cenozoic mammalian communities that suggested regular cycling (Fig. 3). The terminal extinction events, which appear to be synchronous and rapid (Woodburne 1987; Webb 1989), were of similar magnitude, and generic diversity returned to a similar level (Fig. 3A). Although adaptive radiation within North America generates much of the diversity, dispersal is an important source of radiations (Martin 1985). For example, the earliest Dromomerycidae and Cervinae/Bovinae artiodactyls (refer to Fig. 2A) dispersed from Asia. The timing of these dispersals appears to be related to Stout’s cycles, suggesting that climatic change is a controlling factor, with dispersal into middle and low latitudes representing time-transgressive range extension from higher latitudes (Martin 1985, 1994). With global temperature generally decreasing since the Eocene, cooladapted immigrants from higher latitudes and their descendants were at an advantage, and the percentage of Holarctic immigrants and their descendants in North America continually increased through the late Cenozoic (Martin 1994). Based on the K/T boundary, van der Hammen (1965) estimated that a cycle lasted 7 Ma, making a subcycle 2.33 Ma. In 1985, Martin had access to more radiometric dates to test whether these subcycles were of equal duration. He plotted 72 dates correlated to mammalian faunas (latest Eocene through Pleistocene) against the biostratigraphic divisions. The data formed a highly linear relationship, suggesting equal units of time. Martin determined that the radiometric age midrange points for each unit were not statistically different from an ideal duration calculated from a radiometric date near the base of the Geringian (late Oligocene) divided by the number of subsequent vadhs (28 Ma divided by 12 vadhs). This gave an interval of 2.33 Ma. Another approach is to regress radiometric dates against vadh units so that the slope of the regression line represents the likely vadh duration. Over the past several decades, radiometric dating analyses have gone from whole-rock to single-crystal, which has improved precision. Although the radiometric dates of Evernden et al. (1964) were obtained by whole-rock analysis, their data set has the advantage of being processed in one lab and is still the most comprehensive, single report for dated NALMAs. Updating these radiometric age estimates (n=55) with the new potassium–argon half-life standard (Dalrymple 1979), and then regressing these ages against the 27 Cenozoic vadhs, yields a coefficient of 0.991 and vadh duration estimate of 2.44 Ma (Martin and Meehan 2002). Repeating the same exercise using recent (post1985), higher precision radiometric dates yields a coef-

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Fig. 3A, B Generic (ecomorph) counts of terrestrial mammals in the North American Cenozoic. A Generic abundance per vadh. Each genus is assigned an ecomorph type, so generic abundance is equivalent to ecomorph abundance. Equilibrium in mammalian communities appears to have been reached 10 Ma after the K/T extinction, and the average number of known genera from the Eocene–Pleistocene (Gray-Irvi) is 131. Sample quality generally increases the younger the rock unit, and the average from the midMiocene to Pleistocene (Bars-Irvi) is 151. Modern generic diversity correlates with land mass area (Flessa 1975), which has been fairly stable for North America since the Paleocene. The equilibrium

value for terrestrial genera is estimated to be approximately 165 (per 2.4 Ma). The North American mammalian fossil record is principally from middle latitudes of the West, so preservational/ sampling biases may preclude an accurate estimate. Number of recognized Cenozoic genera is currently 1,301 (excluding bats and marine mammals), which represents 3,375 distributional points across the 27 vadhs. B Percentages of surviving/extinct genera. n percentage of genera that survived into the next vadh; o percentage of extinct genera. Some units are not well represented in the geologic record (e.g., Monroecreekian and Lapointian). The average extinction rate since the early Eocene is 32%

ficient of 0.999 and vadh of 2.41 Ma (Martin and Meehan 2002; Fig. 4). It is important to note that vadh divisions inferred from mammalian faunas are biostratigraphic boundaries defined by other workers who did not suspect that these divisions might represent equal units of time.

Not even a regression coefficient of 99.9% statistically demonstrates that the 27 vadhs are of equal duration and represent the best linear fit for dividing Cenozoic biostratigraphy—there are too few radiometric dates (n=99). Also, many of these dates are clumped so that regressions

8 Fig. 4 Recent (post-1985) radiometric dates regressed against Cenozoic vadhs. Regression of dates associated with North American mammalian faunas against 27 units yields an estimated vadh duration of 2.41 Ma. Updated from Martin and Meehan 2002: Fig. 2

Table 1 Extrapolated Cenozoic epoch boundary dates versus predicted vadh values Epoch

Harland 1989 Marine dates

Berggren et al. 1995 Marine dates

Gradstein Ogg 2004 Marine dates

Janis et al. 1998 Terrestrial dates

Predicted vadh ages

Pleistocene a Pliocene Miocene Oligocene Eocene Paleocene Vadh estimate R-squared 95% CI

2 5 24 36 57 65 2.44 Ma 0.991 2.35–2.53

1.3 5.3 23.8 33.7 55.5 65.0 2.41 Ma 1.000 2.36–2.45

1.81 5.33 23.03 33.9 55.8 65.5 2.44 Ma 0.999 2.36–2.51

1.8 4.5 23.0 33.4 55.5 65.1 – – –

2.41 4.82 24.10 33.74 55.43 65.07 – – –

Ma Ma Ma Ma Ma Ma

a There is a climatic cooling event recorded worldwide at 2.4 Ma, and some workers have advocated that the base of the Pleistocene be moved to this position, which agrees with the terminal cooling and boundary location predicted by vadh climatic cycles. The ideal vadh ages are estimated from radiometric dates associated with mammal deposits in North America (Martin and Meehan 2002; Fig. 4). Vadh duration estimates from the marine record are equal within a 95% confidence interval (CI).

are heavily influenced by a few horizons, such as the K/T boundary. Although radiometric date regressions do not prove the existence of 27 units of equal duration, the high coefficients imply equal units, and radiometric ages cannot be used to argue against this portion of the hypothesis. There is, however, an independent, partial test of linearity of these data via epoch boundary ages from a different source: marine sediments (Martin and Meehan 2002). Assuming epoch boundaries from the marine time scale are correlated correctly with NALMAs, one would predict the same linearity when marine boundary ages are plotted against the vadhs. Using extrapolated epoch boundary ages from marine radiometric dates (Harland et al. 1989) yields a regression coefficient of 0.99 and vadh duration of 2.44 Ma (Martin and Meehan 2002). Running the same analysis from two other stratigraphic charts (Berggren et al. 1995; Gradstein and Ogg 2004) yields coefficients of 1.00 and 0.99 with estimated vadh durations of 2.41 and 2.44 Ma, respectively. These three estimates are equivalent within a 95% confidence interval (Table 1).

The Plio-Pleistocene boundary is the most divergent point (Table 1), but unlike the Pleistocene–Holocene boundary, it is not defined by a significant global climatic event. It is a political boundary where a committee drove a “golden spike” at a local foram appearance/extinction (Harland 1989:68). This golden spike philosophy was applied due to great controversy among workers, yet no dissension arises among marine and terrestrial workers about a sharp, global cooling event 2.4 Ma ago, incurring great biological consequences. This climatic change is evident in such events as (1) a drop in ocean temperatures; (2) 65% extinction of the tropical western Atlantic mollusc species; (3) abrupt change in carbonate productivity and preservation; (4) weather pattern changes in the Middle East as indicated by dust deposition; (5) a great increase in tundra habitat and loess deposition; and (6) 5C cooling in Colombia as indicated by pollen assemblages (Clark et al. 1980; Liu et al. 1985; Wolfe 1985; Stanley 1986; Jansen et al. 1988; Curry et al. 1990; Kennett and Barker 1990; Crowley and North 1991; DeMenocal et al. 1991; Hooghiemstra and Ran 1994). Var-

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ious workers have advocated that the Plio-Pleistocene boundary be defined by this cooling event (e.g., Liu et al. 1985), and in Europe, some workers have been using this event for decades as the Quaternary/Tertiary boundary because it is the start of the first pronounced glacial pulse (e.g., van der Hammen et al. 1971). Patterns consistent with iterative climatic cycles The fundamental pattern of evolution is one of relative stasis bounded by abrupt evolutionary change due to extrinsic factors. Communities rapidly evolve, remain stable for long periods, rapidly go extinct, and then a new community replaces the previous one. This pattern is so commonly recognized that it has been given many descriptors: typostatic and typogenetic/typolytic phases of evolutionary cycles (Schindewolf 1950), chronofaunas (Olson 1952), iterative climatic cycles (van der Hammen 1957; Martin 1985), biomere boundaries (Palmer 1965), punctuated equilibrium (Eldredge and Gould 1972), ecological-evolutionary units (Boucot 1975), turnover pulses (Vrba 1985a), ecosystem model (Krasilov 1987), faunistic cycles (Pascual and Jaureguizar 1990), coordinated stasis (Brett and Baird 1995), and stepwise climatic change/ extinction (e.g., Benson et al. 1984; Prothero 1989). Sometimes no specific term was used to describe this pattern, except for periodicity (e.g., Newell 1952), or the pattern was implied in recognition of climatic or sedimentary cycles (e.g., mesothems or megacycles; Busch and West 1987; Kemper 1987). Brett and Baird (1995) noted that in the late 1840s, d’Orbigny, the “father of biostratigraphy,” recognized that genera and species changed little within his defined packages of strata. Observation of evolutionary stasis bounded by abrupt change due to environmental perturbation was perhaps first recognized in a comprehensive manner by Olson’s (1952) idea of chronofaunas. A chronofauna was initially defined as a “geographically restricted, natural assemblage of interacting animal populations that has maintained its basic structure over a geologically significant period of time” (Olson 1952:181). Missing time due to erosion or nondeposition is always present at various scales, leading some workers to hypothesize erroneously that evolution makes large “jumps.” Whenever paleontologists study fossiliferous strata in finer detail, they discover that change may have occurred more rapidly than usual, but intermediate morphological steps are represented (e.g., Martin 1984). The fundamental pattern of stasis bounded by rapid change caused by extrinsic factors is consistent with hypotheses of climatic cycles. The importance of climatic cycles has been recognized by numerous workers, and many have suggested that stratigraphy be based on climatic change because it affects biota and sedimentary processes simultaneously. On a large scale, disruption of entire community patterns by extrinsic factors implies that biotic factors, such as competition are minor, as concluded by Benton (1983). Raup and Boyajian (1988:109) also

concluded that Phanerozoic extinction patterns were most likely caused by widespread environmental upheaval. In contrast, Stucky (1995) suggested that community interaction was a more important factor than the physical environment in determining survivorship. Stucky further noted a contemporaneous global trend of increased hypsodonty among mammals. Convergent trends of geographically isolated faunas indicate a cause that cannot be from competition or some other community interaction. Congruence of faunas across continents by simultaneous appearance of the same taxa, similar grade of evolution, or convergent community structure indicates that climatic change is a dominant force in large-scale evolution. Where Stucky’s data reflect stasis in community structure, we would argue that it is due to relative stasis in climate. Sedimentary cycles Sedimentary cycles have been recognized throughout the geologic record. In some cases, as in the Milankovitch cycle, their duration and mechanisms seem well understood. In other cases, their duration and periodicity is questionable. Ross and Ross (1985) described over 50 global sedimentary cycles from the Paleozoic that represent sea level rising and falling (transgression–regression) with an average duration of 2 Ma. The variation is estimated to range from 1.2 to 4 Ma; however, these durations are highly extrapolated, being based on few radiometric dates. As in other trans/regressive sequences, there is a slow rise in sea level followed by a fast drop (Ross and Ross 1985). If this pattern is true, then it is consistent with the asymmetric temperature profile of vadhs, as well as temperature profiles from oxygen isotope data (e.g., Stott and Kennett 1990). In marine stratigraphy, sedimentary cycles of various scales (e.g., synthems, mesothems, cyclothems, and PAC sequences) have been recognized across the globe, and as early as 1888, Suess suggested that a global stratigraphy could be based on trans/regressive units (Busch and West 1987). Recent workers are increasingly using temporal/ climatic models in stratigraphy, and perhaps the most encompassing model is the hierarchal genetic stratigraphy of Busch and West (1987). They defined a hierarchy of trans/regressive units bounded by transgressive and climatic surfaces that can be correlated using lithological and ecological data on a regional, and possibly global, scale. These trans/regressive units have periodicities on the order of 225–300 Ma (first order) down to 50–130 thousand years (sixth order). Periodicities of third and fourth order are comparable to vadhs and stouts (Martin and Meehan 2002), and these units have synchronous unconformities, indicating global factors linked to climatic change (Busch and West 1987).

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Stepwise extinction and iterative evolution Stepwise extinction reflects stepwise climatic change, and this pattern is widely recognized in the fossil record (e.g., Kohler et al. 1988; McGhee 1988; Holland 1989; Janis et al. 1998). Keller (1986) noted five pulses of extinction over approximately 15 Ma throughout the late Eocene– early Oligocene, which resulted in two-thirds replacement of foram species. Keller (1986:274) stated the following: Paleontological research has made it increasingly clear that both faunal and climatic changes are characterized by long periods of stability separated by brief episodes of rapid faunal turnover and climatic fluctuations. During middle Eocene to early Oligocene each faunal turnover is characterized by replacement of tropical marine faunas and floras by cooler subtropical and temperate elements as observed by [many authors]. Recently, Berger et al. (1981) discussed major faunal turnovers at the Cretaceous–Tertiary and Eocene– Oligocene boundaries and the late Miocene in terms of major steps in Cenozoic evolution. Keller (1983a, 1983b) studied one of these “steps” at the Eocene– Oligocene boundary and observed that faunal changes occurred in a series of yet smaller steps related to successively cooler climatic conditions. Such stepwise faunal changes were also observed by Kauffman (1984a, 1984b) in late Cretaceous invertebrate faunas and he redefined the late Cretaceous mass extinctions as “stepwise mass extinctions” occurring over a period of 1–3 Ma. Using the interpolated time-scale boundaries of Berggren et al. (1995), these Eo/Oligocene turnovers occurred at 40.1, 38.3, 35.3, 33.5, and 29.4 Ma. The hypothesis of iterative climatic cycles predicts seven relatively significant extinction events during this interval, occurring at 41.0, 38.6, 36.1, 33.7, 31.3 and 28.9 Ma. Predicted values are close to extrapolated ages of these foram extinctions, except that there was no notable extinction observed at about 31 Ma. The stepwise biotic and climatic nature across the Eo/ Oligocene is seen in other marine faunas, paleosols, leaf assemblages, mammalian faunas, oxygen isotope data, and ice sheet formations (Berggren et al. 1985; Wolfe 1985; Ehrmann and Mackensen 1992; Miller et al. 1991; Zachos et al. 1993; Diester-Haas et al. 1996; Bestland et al. 1997). Interpolated ages of late Eo/Oligocene mammalian faunal turnovers in North America (Prothero 1989) are also in close agreement with predicted vadh boundaries. A paleosol series from deposits of South Dakota is inferred to show climatic steps at 37, 34, 32, 29.5 Ma (Retallack 1983), which are close to predicted vadh estimates of 36.1, 33.7, 31.3, and 28.9. In addition, each step is terminated by highly dry and seasonal climates, in which reduced plant cover presumably led to increased erosion, as described in Stout’s (1978) climatic/ sedimentary cycles.

The two major Cenozoic radiations of forams have a pattern of extinction at a cooling interval, re-evolution of similar ecomorphs, and stepwise change over the long term (Cifelli 1969). This iterative pattern in forams is seen throughout the Paleozoic and Mesozoic (Stanley 1987). Cifelli (1969) noted that foram faunas of widely different ages were sometimes more alike than those from adjacent strata. He also stated that ammonoid evolution was highly iterative, paralleling foram evolutionary patterns and that convergence of ecomorphs is so high that ammonoids are sometimes classified on stratigraphic grounds because the same ecomorph type cannot be easily distinguished taxonomically. This synchronous ecomorph iteration in marine faunas resembles the terrestrial record. Chronofaunas and faunistic cycles Olson (1975) concluded that succeeding communities did not evolve gradually from the previous one, but were replaced in part or whole and that most major evolutionary change took place as new communities formed under rapid environmental change. Some described mammalian chronofaunas closely correspond to a stout climatic cycle. For example, Webb (1969) recognized a White River Chronofauna composed of the Chadronian, Orellan, and Whitneyan faunas and a Clarendonian Chronofauna as composed of the Valentinian, Clarendonian, Kimballian, and Hemphillian faunas (refer to Fig. 1). Chronofaunal or stout characters are also present in Pennsylvanian/Permian coal swamp communities. DiMichele and Phillips (1995) recognized stasis in ecomorph structure for millions of years, rapid turnover due to severe climatic change, and a new community forming by ecomorph replacement. Pascual (1992) stated that South American land mammal “ages” represent relatively balanced communities during times of stasis and that these communities were disrupted during periods of severe climatic change. A pattern of sedimentary bundles correlating with episodes in evolution has been recognized since the beginning of South American mammalian biostratigraphy, and assemblages of major bundles have the ecological structure of chronofaunas (Pascual 1992). These sedimentary bundles and extinction horizons correlate with the marine record. In turn, changes in sedimentation and evolution in marine and terrestrial provinces correlate with global climatic changes and regional effects. Pascual described extinction periods within these sedimentary bundles, but termed these “internal episodes” because these discontinuities did not break up the basic continuity of the chronofauna, which is consistent with vadh extinctions within a stout. Pascual and Jaureguizar (1990) recognized four hierarchical faunistic cycles with durations of 2.5– 25 Ma.

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Trilobite biomeres Biomeres were originally defined as regional biostratigraphic units bounded by extinctions in the dominant elements of one phylum (Palmer 1965). Rapid extinctions bound stable, ecological units of benthic trilobite faunas of North America, and replacement is iterative, with each new trilobite community radiating from the same immigrant ecomorph from open water (Palmer 1965; Stitt 1975). These extinction boundaries are not diachronous, nor restricted to benthic trilobites as first suggested. Other extinctions at biomere boundaries include inarticulate brachiopods, conodonts, agnostoid trilobites, and in the case of conodonts, the extinction has been discerned to be global (Hood 1989). Most workers have proposed that these extinctions were the result of an abrupt temperature drop. From one biomere boundary that retained original isotopic signatures, the extinction was associated with a rapid 4–5C cooling (Hood 1989). After analyzing suggested causes of these turnovers, Hood (1989) concluded that abrupt cooling caused extinction of these tropical communities (and that an anoxic water event associated with this cooling may have been a factor). Biomeres encompass multiple trilobite zones, and the Upper Cambrian represents three biomeres and about 7 Ma (Sundberg 1996; Harland et al. 1989). Palmer et al. (1995) reported the zones averaging 2.7 Ma and biomeres averaging 7 Ma, but Bowring and Erwin (1998) reported Cambrian zones averaging 1.5 Ma and biomeres 4 Ma and that the zones are not of equal duration. It is difficult to ascertain which of these absolute ages is more accurate, but the pattern of zones and biomeres is consistent with vadhs and stouts, and what is needed is to test for iterative evolution of trilobite ecomorphs and to create detailed temperature curves spanning at least 15 Ma. An abrupt 5C cooling causing trilobite community extinction (Hood 1989) is consistent with the end of a vadh cycle, and cooling of this magnitude has been reported in terrestrial and marine records at some extinction boundaries (e.g., Vella 1968; Kennett and Shackleton 1976; Hooghiemstra and Ran 1994). Coordinated stasis and turnover pulse hypothesis Defining subunits of Boucot’s (1975) ecological-evolutionary units, Brett and Baird (1995) argued that stasis of Appalachian Basin benthic communities in the Middle Paleozoic occurred on the order of 3–7 Ma. These communities went extinct due to major, rapid environmental change, and most boundaries were associated with global climatic events and extinctions. Replacement of communities occurred within 100,000–500,000 years and was followed by long intervals of stasis. This pattern agrees with the one predicted by iterative climatic cycles, and its time scale is on the order of vadhs and stouts. Brett and Baird (1995) renamed this pattern “coordinated stasis” and argued that it is seen in such varied communities as freshwater molluscs, trilobite biomeres,

and mammalian faunas, as argued here. Williamson (1981) documented nearly synchronous morphological change followed by relative stasis in several mollusc lineages in the Turkana basin. Vrba (1985a, 1985b) demonstrated comparable pulses of change and long-term stability in African bovids and hominids. Vrba (1985a) coined the term “turnover pulse,” and her hypothesis agrees with vadh characters. Besides the mammalian extinction in Africa occurring at 2.4 Ma, community recovery was rapid; antelope niches were filled by radiation and dispersal within 300,000 years (Vrba 1988). Vrba argued that abrupt climatic change breaks down stable plant and mammal communities causing rapid evolutionary change and stated the following (1985a:232): Speciation does not occur unless forced (initiated) by changes in the physical environment. Similarly, forcing by the physical environment is required to produce extinctions and most migration events. Thus, most lineage turnover in the history of life has occurred in pulses, nearly (geologically) synchronous across diverse phylogenies, and in synchrony with changes in the physical environment. This pattern exactly describes the terminal Pleistocene extinction of North America, which occurred over several thousand years (e.g., Guthrie 1984; FAUNMAP group 1996). Suggestions for further work A perennial problem in studying the geologic past is reliability of correlations, particularly on a global scale. Standard correlation charts have changed significantly on a decade basis, and workers still disagree on many aspects. The frequency and duration of missing time in marine strata may be unappreciated or not even tested (Aubrey 1995). Terrestrial sequences have far less continuity than marine sequences, with much less than 50% of time preserved in most deposits (Clark et al. 1967; Retallack 1984). In addition, many biostratigraphic boundaries correspond to times of erosion. Most of these problems could be mitigated by better absolute age control. Unfortunately radiometric dates may not be directly associated with biostratigraphically interesting assemblages and are not systematically distributed over the geologic record (Harland 1989; Berggren et al. 1995). In North American mammalian biostratigraphy, Evernden and others (1964) provide the only comprehensive dating sequence from a single study. This is an early study using techniques with comparatively low precision, but even modern dating may show significant variation among labs. A concerted effort needs to be made to control for intralab error and extend the scope and density of absolute dates, especially for the Cenozoic where such a framework could definitively decide if vadhs and stouts are chronostratigraphic.

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Another correlation difficulty results from time-transgressive climatic effects. This is particularly noticeable in high latitude marine faunas, which are first and most severely affected by climatic change (Stanley and Ruddiman 1995). Some marine biostratigraphic definitions have been changed as more has been learned of the timetransgressive nature of extinctions and first appearances. Innovations seem to occur at high latitudes first and progress to lower latitudes as climate cools. Mathematical modeling of foram species origination/extinction events indicates that extinctions are more deterministic than first appearances (Patterson and Fowler 1996), suggesting that extinction events define sharper biostratigraphic boundaries, as advocated by Martin (1985). Because the terrestrial mammalian record is mainly one of middle latitudes, the time-transgressive nature of first appearances is not easily observed. Hickey et al. (1983) concluded that many vertebrate taxa inhabited northern Canada 2–4 Ma earlier than they occurred in middle latitudes and that floral displacement was much greater, although this was disputed (Flynn et al. 1984). Not only are high latitudes affected first, but low latitudes act as refugia for warm-adapted taxa, sometimes with lineages persisting much longer after most relatives become extinct at higher latitudes (e.g., Webb 1989). The description of global ungulate distributions (Janis 1989) provides an example of latitudinal climatic offlap. Lowseasonally-adapted hindgut fermenters (such as horses and rhinos) accounted for over 50% of the Eocene ungulate fauna and occurred at high latitudes. During the Oligocene, their high latitude abundance dropped to about 25% as climate became cooler. By the mid-Miocene lower latitude abundances also dropped to 25% as global temperature decreased (Janis 1989). A strong argument for high latitudes being a center of evolution in the Northern Hemisphere is seen in the sudden, simultaneous appearance of “immigrant” taxa at middle latitudes of Asia, North America, and/or Europe with no immediate ancestors known (see Woodburne 1987). Recognition of the Holarctic as a center for evolution has been noted since early studies. As stated by Matthew (1939:7), “...the present distribution of mammals is due chiefly to migration from the great northern land mass, and the connection of this southward march with progressive refrigeration in the polar regions was made more than a century ago (1778) by Buffon.” This climatic offlap sequence of taxa is particularly variable with respect to immigrants. Climatic offlap has been better recognized in the marine record where high latitude faunas are better known (e.g., Jenkins 1974; Stanley 1987). The timing of mammalian dispersals into North America appears to be related to climatic events, with dispersal into lower latitudes representing time-transgressive range extension (Martin 1985, 1994). High latitude data need to be extended and refined. Also, marine data need to be more closely related with the terrestrial record. One promising note in correlating events is that climatic effects as reflected in the marine and terrestrial records appear synchronous, even at a fine

resolution. For example, the climatic history of the past 500,000 years as determined by pollen assemblages around a lake in Japan remarkably correlates with temperature records of the Caribbean and Pacific Oceans, sedimentary cycles of the Mediterranean, climatic trends of Central Europe, and sea-level changes of Japan and New Guinea (Fuji 1988). The Eocene warming event as expressed by carbon isotopes from various sources appears synchronous, as well as the rapid marine and terrestrial biotic turnovers at this time (Koch et al. 1992). If we assume a vadh duration of 2.4 Ma, the general temperature trend as described by van der Hammen (1961) shows overall warming to about 1.7 Ma into the vadh, followed by 700,000 years of rapid cooling, with greater cooling at the end of a C vadh. Ice volume changes in a C vadh, the Pleistocene, reflect this pattern. During the last 700,000 years, ice volume was two times greater than the previous 2 Ma (Barendregt and Irving 1998). Temperature profiles at the Paleo/Eocene and Eo/ Oligocene boundaries show similar magnitude, direction, and duration (cooling over 500,000 years; Stott and Kennett 1990), and a number of oxygen isotope data sets indicate a 5C drop at extinction boundaries (e.g., Vella 1968; Kennett and Shackleton 1976; Guilderson et al. 1994). These global temperature changes should result in environmental modification and concordant evolutionary change. On a small scale, Chiba (1998) described a pattern of rapid, synchronous morphologic changes with longer periods of stasis in five different snail lineages on different islands over the past 40,000 years, concluding that synchrony in convergence and lineage extinction was due to climatic change. We need to better demonstrate which events co-occur. Martin (1984) demonstrated that species lineages of a sabertooth felid (Megantereon-Smilodon) and muskrat (Pliopotamys-Ondatra) showed a similar pattern of body size change, with an exponential increase during the last 700,000 years of the Pleistocene vadh C. He further demonstrated the same pattern in a sabertooth nimravid lineage (Sansanosmilus-Barbourofelis) in the previous vadh C (Kimballian). These three lineages slowly evolved overall larger body sizes in vadhs A and B, and then towards the end of a vadh C, their body sizes increased exponentially. This evolutionary change is concordant with global cooling, including the glacial pulse starting 700,000 years ago. Mammal body size can be highly correlated with climate (e.g., Davis 1981; Zeveloff and Boyce 1988; Smith et al. 1995), and the body size increase in the armadillo-like Holmesina (Hulbert and Morgan 1993) exhibits a similar exponential rate at the end of the Pleistocene, exemplifying the breadth of this phenomenon. The power of climatic change to influence evolution may be further shown in humans. The evolution of the genus Homo about 2.4 Ma ago has been attributed to the appearance of more open habitat (e.g., Stanley 1995). This is a period of cooling and increased aridity based on a wide variety of evidence (and the timing of this climatic shift is predicted by vadh cycles). Ruff et al. (1997) de-

13

scribed the pattern of brain size evolution in Homo as a rapid increase from 600,000 to 150,000 years ago, which was preceded by stasis on the order of 1.8 Ma. This pattern is concordant with the exponential growth seen in muskrat and sabertooth body sizes. A remarkable coincidence if there is no underlying factor. Naples and Martin (1998) hypothesized that the evolutionary trend towards larger brain sizes among ungulates, carnivores, and primates throughout the Cenozoic is due to increased seasonality and habitat openness that resulted from global cooling. As in the other major mammalian evolutionary trends of the Cenozoic, such as increased body size and degree of hypsodonty, brain size increase is predicted to be highly correlated with mean global temperature trends. Geist (1983) noted that many Ice Age mammalian lineages (e.g., moose, mammoth, and Homo) in more seasonal environments (e.g., alpine and arctic) evolved ornate, giant members with larger brains and more generalized niches than close relatives of more southern, equable climates. One would predict that these lineages underwent the most rapid evolutionary change during the vadh cooling intervals from approximately 3.1 to 2.4 Ma ago and from 700,000 to 11,000 years ago. Analyzing evolutionary rates within a species lineage may provide a simple and powerful tool for testing the existence of these climatic cycles. Besides A-B-C dominance turnover patterns (Fig. 2), any robust, long-term data set with a climatic signal, either more direct, such as oxygen isotope data, or less direct, such as the extinction pattern of highly specialized ecomorphs, provides a test for these cycles. Although vadh C has a more severe terminal cooling, there is not more generic extinction at its end than in vadhs A or B (Fig. 3B). What we do see is that a few highly specialized ecomorphs characteristically become extinct in a vadh C (e.g., 12 of 15 sabertooths, 2 of 2 cheetah ecomorphs, and 4 of 4 aye-aye ecomorphs in the North American Cenozoic). Iterative climatic cycles—a useful hypothesis? As listed above, many hypotheses recognize the fundamental pattern of relative stasis bounded by rapid change within the fossil/sedimentary record. Though some have different theoretical bases, they share many features. Is there a significant difference among the concepts of biomere, faunistic cycle, ecological-evolutionary unit, and the older idea, chronofauna? The term punctuatedequilibrium (Eldredge and Gould 1972) became widely used, but Schindewolf (1950), Simpson (1953), and many before have stated that evolution occurs at different rates. As mentioned previously, the “father of stratigraphy” (d’Orbigny 1849) recognized the “punctuated” evolution and extinction bounding packages of strata. Given the commonality of these ideas, it is worthy to consider that they are all related and may be partial recognition of a single underlying mechanism. Meehan and Martin (2003) suggested that these hypotheses might be encompassed by a hypothesis of iterative climatic cycles. This hypothesis

was first proposed by van der Hammen (1957) and has the advantage of generating many predictions. Van der Hammen proposed that global climatic cycles exist at many scales and can be tested with numerous data sets. In his 1965 paper, he reported that Jurassic ammonoid stratigraphy reflected cycles of 7 Ma composed of three 2.33 Ma cycles, and these in turn could be divided into cycles on the order of 0.8 Ma. He also inferred a 70 Ma cycle. In this last paper on his climatic cycle hypothesis, van der Hammen reiterated that climatic cycles define stratigraphy, providing ideal chronostratigraphic units. The recognition of climatic cycles in the rock record is a common theme. For instance, many workers (Clark et al. 1967; Wolfe 1978; Collinson et al. 1981; Kemper 1987; Frakes et al. 1992) have proposed the existence of temperature cycles on the order of 10 Ma as reflected in marine and terrestrial data. Zubakov and Borzenkova (1990) reported a climatic cooling rhythm at 3.7 and 11 Ma. Kemper (1987) reported climatic cycles of 2.2 and 9 Ma bounded by abrupt temperature drops throughout most of the Cretaceous marine deposits of the Sverdrup Basin, in northern Canada. These hierarchal cycles may be equivalent to vadhs and stouts. Kemper (1987) suggested that the cycles may be due to orbital parameters, but noted that solar variation cannot be ruled out. Very small-scale solar changes, such as sunspot cycles, are reflected in the sedimentary/climatic record (e.g., Wymstra et al. 1984; Kerr 1996). There is a growing body of research showing solar forcing as a viable mechanism for Quaternary/Holocene cycles (e.g., Crowley and Kim 1996; Bond et al. 2001; van Geel et al. 2003), but do large-scale solar mechanics create vadhs, stouts, and other hierarchal cycles? Extinction may not be forever There are many uses of the term extinction. In its strictest sense, it refers to the termination of a lineage, but it is also used more generally for the end of an adaptive type such as sabertooth “cats.” In this usage it may not be final, and in the absence of human intervention, we might expect sabertooths to re-evolve, as they have done for the past 50 Ma years. When we compare mammal extinction between the two C vadhs of the Pleistocene and latest Miocene (Fig. 5), we see not only ecomorphs re-evolving, but also the same ecomorphs going extinct, such as in proboscideans (Amebelodon/Mammut), giraffe–camels (Aepycamleus/Titanotylopus), and scimitartooths (Nimravides/Homotherium). Extinction is not only similar in terms of adaptive types, but also in scope—about onethird of ecomorph genera become extinct in each vadh (Fig. 3B). The community structure between these two vadh C assemblages is comparable, except that the Pleistocene organisms are adapted to colder, more open environments, reflecting the general Cenozoic climatic trend.

14 Fig. 5 Convergent assemblages. Representative mammals that became extinct at the end of two vadh C climatic cycles (Kimballian and Irvingtonian) in North America. These intervals are 7 Ma apart. Modified from Martin 1985: Fig. 4

Evolutionary patterns are shared in many cases by ecomorphs, which start from ecologically similar ancestors and progress through similar adaptive stages, usually showing similar change rates. These changes are not constant, being slower in the A and B vadh cycles and then rapidly increasing in rate in the last third of the C cycle (see Martin 1984; Meehan and Martin 2003), correlating to the temperature cycles of van der Hammen (1961). The community extinction and replacement pattern also implies that the fossil record contains many examples of rare taxa that through subsequent diversification filled the empty adaptive zones of their ecological predecessors. In North America at middle latitudes, open habitat first became widespread in the late Oligocene, and rodents took advantage of this new adaptive zone. Beavers (Castoridae) are rare animals with little diversity in the late Eocene–early Oligocene, but in the late Oligocene– early Miocene, evolve many fossorial forms (Fig. 2B). They are accompanied by a radiation of geomyoid ro-

dents, and with them, form one of the first rodent burrowing communities. At the end of the earliest Miocene, these dry land beavers become extinct along with gopherlike geomyoids. A new fossorial rodent community dominated by aplodontoids and another group of gopherlike geomyoids replaced this first burrowing community. Some version of this community persisted until a similar, modern community of burrowing squirrels and pocket gophers replaced it. The diversity of burrowing rodents for each community was similar, but their origins were different. We might have expected rodents that first occupied burrowing niches would have continued in them to the present day. This was not the case. The modern North American fossorial rodent community is composed largely of rodents that came into this niche in the last 7 Ma. Convergent/parallel characters are so prevalent among ecomorphs in these iterative communities that an uninitiated observer would have difficulty in telling them apart, despite that they are not phylogenetically close. Many

Rancholabrean Irvingtonian Blancan Hemphillian

Pleistocene Pliocene Miocene

Eocene

Clarkforkian Tiffanian Torrejonian Puercan

Wasatchian

Bridgerian

Rancholabrean (Rlb) and Irvingtonian (Irvi1–3) = Blancan (Bl) = L Hemphillian (Hh3) = E Hemphillian (Hh1–2) = E and L Clarendonian (Cl1–2) = L Barstovian (Ba2–3) = E Barstovian (Ba1) = L Hemingfordian (He2) = E Hemingfordian and L L Arikareean (Ar4-He1) = E L Arikareean (Ar3) = L E Arikareean (Ar2) = E E Arikareean (Ar1) = Whitneyan (Wh) = Orellan (Or) = Chadronian (Ch1–3) = (Late) Duchesneand (Du) = (Early) Duchesneand (Du) = L Uintan (Ui2) = E Uintan (Ui1) = Gardnerbuttean, Blacksforkian, and Twinbuttean (Br1–3) = Lostcabinian (L Wasatchian; Wa4) = Lysitean (M Wasat.; Wa3) = Sandcouleean and Graybullian (E Wasatchian; Wa1-Wa2) = Clarkforkian (Cf1–3) = Tiffanian (Ti1–6) = Torrejonian (To1–3) = Puercan (Pu1–3) =

NALMA subdivisionsa Irvingtonian (Irvi) Blancan (Blan) Hemphillian (Hemp) Kimballian (Kimb) Clarendonian (Clar) Valentinian (Vale) Barstovian (Bars) Sheepcreekian (Shcr) Marslandian (Mars) Harrisonian (Harr) Monroecreekian (Mocr) Geringian (Geri) Whitneyan (Whit) Orellan (Orel) Chadronian (Chad) Lapointian (Lapt) Pearsonian (Pear) Mytonian (Myto) Wagonhoundian (Wghd) Bridgerian (Brid) Lostcabinian (Lcab) Lysitean (Lysi) Graybullian (Gray) Clarkforkian (Clfk) Tiffanian (Tiff) Torrejonian (Torr) Puercan (Puer)

Vadh climatic cyclesb C B A C B A C B A C B A C B A C B A C B A C B A C B A

Vadh type 1.8 4.5 6.0 8.9e 12.5e 14.5 16.8f 17.9 21.0 23.0 25.0 29 30.7 32.4 38.0 – 42.0 44.6 48.0 51.0 52.0 54.5 57.3 58.8 62.7 65.0 66.4

Basal datesa 1.8 4.5 6.0 8.8 11.0 12.5 15.8 17.5 19.2 23.0 27.7 29.4 31.9 33.4 37.1 – 39.5 41.3 45.9 50.4 53.5 54.2 55.5 56.0 60.9 63.8 65.1

Basal datesc

2.41 4.82 7.23 9.64 12.05 14.46 16.87 19.28 21.69 24.10 26.51 28.92 31.33 33.74 36.15 38.56 40.97 43.38 45.79 48.20 50.61 53.02 55.43 57.84 60.25 62.66 65.07

Predicted vadh ages

b

NALMAs are from Woodburne (1987: Fig. 10.1). Correlated vadhs from Martin (1985) and Martin and Meehan (2002); only minor changes in the importance of previously recognized biostratigraphic boundaries were made to define these climatic cycles inferred from mammalian faunas. c Data from Janis et al. (1998). d Late and early Duchesnean units were not recognized in Woodburne (1987), but see Lucas (1992). e Amended extrapolated boundary ages from Whistler and Burbank (1992). f Amended extrapolated age from Lindsay (1995). g Basal Marslandian = uppermost Arikareean (Martin 1985). E Early; M Middle; L Late. The base of the Puercan correlates to the base of Paleocene and the top of the Irvingtonian to the top of the Pleistocene, but recent correlations (Prothero 1995; Woodburne and Swisher 1995) place remaining epoch boundaries slightly offset to indicated mammalian ages by several hundred thousand years or less. Predicted ages are based on a vadh duration of 2.41 Ma (Fig. 4).

a

Paleocene

Whitneyan Orellan Chadronian Duchesnean

Uintan

Arikareean

Oligocene

Hemingfordian –g

Clarendonian Barstovian

NALMAsa

Epoch

Table 2 Cenozoic North American land mammal “ages” correlated to vadh climatic cycles

15

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such examples can be demonstrated. The most striking example is the repetitive evolution of dirktooths (Martin 1985; Fig. 1B), but the whole catlike community is involved, with scimitartooth and leopard ecomorphs becoming extinct and re-evolving in the same dominance turnover pattern (Fig. 2C). This pattern can also be seen in dog and hippo ecomorphs (Meehan and Martin 2003), as well as in dominant artiodactyl herbivore ecomorphs (Martin 1985) and shrew ecomorphs (Fig. 2A, D). The starting point for these radiations is usually a combination of survivors (of the previous extinction event) and immigrants, as Olson (1975) described in chronofaunal succession. The resemblance between ecomorphs is greatest among taxa at the end of evolutionary sequences rather than at their beginnings. For instance, Barbourofelis fricki, a lion-sized carnivore, is very similar to its lion-sized ecomorph Smilodon fatalis, but less so to the Smilodon ancestor Megantereon that is closest to Barbourofelis in time. We would infer from this pattern of succession that competition was an unlikely contributor to these extinction events; instead we find that ecological replacement is a fundamental pattern of the fossil record. Numerous lines of evidence indicate that environmental parameters fluctuate globally throughout Earth history. In many cases these fluctuations reflect changes in global heat and water balance. Extinctions have often been associated with declining temperatures and increasing aridity. Increased temperatures and moisture are reflected in increased species diversity and community complexity. Although this pattern has been observed globally through most of the geologic record, its details may be best observed in the well-preserved and wellstudied North American terrestrial Cenozoic. The most characteristic part of this pattern is the concordant extinction of a variety of organisms followed by the reappearance of the same ecomorphs in subsequent intervals. This phenomenon is not ambiguous, extends across community structure, and is largely independent of phylogenetic relationships. Only climate can simultaneously control evolutionary patterns in so many diverse and often phylogenetically distant organisms. This interpretation is further supported by the consistency of evolutionary responses across continents to what must be a global trend in environmental change. If ungulates show adaptations consistent with cooler, more open habitat, so will rodents. It is the common climatic signature that makes recognizing global epoch and era boundaries among such disparate groups as molluscs, pollen, and mammals possible. In most cases, extinction is not random, but tends to be of similar scope and affects similar ecomorph types in each episode. For this to be true, these ecomorphs would have to re-evolve time after time. That this is true is one of the most remarkable facts that we can ascertain from the fossil record. It may be easy to think of some reason, real or imagined, that could result in the extinction of a particular lineage, but it is more difficult to understand how following an extinction, the same ecomorph could re-evolve almost immediately—often from an unrelated lineage. That this happens many times in the geological

sequence can only be taken as evidence that a controlling environmental factor (climate) is fluctuating from one set of parameters to another and then back again in a geologically short period. It is less easy to demonstrate that this pattern is truly periodic, as has been implied for many of the intervals where it is recognized. Unfortunately, the paucity of radiometric dates bearing on this question presently prevents a resolution. It should be remembered that the various dating methods often vary amongst themselves when dating the same sample and that samples usually date volcanic events rather than biostratigraphic boundaries so that radiometric ages are younger or older than the event they are supposed to date. Even with these caveats, the subcycle/cycle system of triplets first proposed by van der Hammen (1957) and extended by Martin and Meehan (2002) into vadhs and stouts, predicts boundaries that agree with the various time scales for the North American terrestrial Cenozoic as well as these time scales agree with each other (Table 2). Their agreement with the marine epochal boundaries is even more striking (Table 1). In general vadhs and stouts are comparable to the durations of marine zones and stages. If in fact this periodicity is genuine, it severely limits the possible causal mechanisms. A truly regular mechanism is likely to be astronomical, and this may include varying solar mechanics and heat output. If the time intervals are more variable, they may reflect a cycling feedback system involving some factor such as atmospheric carbon dioxide. In any case, climatic cycles appear to form the ultimate basis of biostratigraphy and have a controlling effect on the overall pattern that evolution has taken. Acknowledgements We wish to thank A. Seilacher, M. Dawson, and two anonymous reviewers for editorial comments. T.J.M. wishes to thank his PhD committee at Kansas University: L.D. Martin, D. Miao, R.W. Wilson, R.M. Timm, P. Wells, and D.W. Frayer.

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