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

R E V I E W

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 ecomorphevolution and the hypothesis of iterative climatic cycles.Although a widely known phenomenon, convergent evo-lution has been underappreciated in both its scope andcommonality. The power of natural selection to overridegenealogy to create similar morphologies (even amongdistantly related organisms) supports classical Darwinianevolution. That this occurs repeatedly in stratigraphicallyclosely spaced intervals is one of the most striking featuresof Earth history. Periodic extinctions followed by re-evolution of adaptive types (ecomorphs) are not isolatedoccurrences but are embedded within complex ecologicalsystems that evolve, become extinct, and repeat them-selves in temporal synchrony. These complexes of radia-tion and extinction bundle the biostratigraphic record andprovide the basis for a global stratigraphy. At this scale,climatic change is the only mechanism adequate to explainthe observed record of repeating faunas and floras. Un-derstanding of the underlying causes may lead to predic-tive theories of global biostratigraphy, evolutionary pro-cesses, and climatic change.

Introduction

Here we review the hypothesis of iterative climatic cy-cles, which states that the evolution of faunas and florasand their extinction has a predictable pattern. SouthAmerican pollen and North American mammalian as-semblages exhibit convergent evolution in repeating A-B-C cycles (van der Hammen 1957, 1965; Martin 1985;Meehan and Martin 2003), and these consecutive A-B-Ccommunities form a chronofauna. The stability and thenextinction of these communities have been correlated tocycling sedimentary and temperature profiles. This pat-tern is reflected in simultaneous radiations of convergentadaptive types (ecomorphs) on separate continents, indi-cating that it results from natural selection caused byglobal climatic change, as opposed to genetic or com-munity biotic factors. An iterative pattern of hierarchicalclimatic cycles may form the underlying basis for bios-tratigraphy and explain most evolutionary trends andextinctions. The cycles recognized so far appear to re-present equal units of time—2.4 Ma for each A, B, and Ccycle, and 7.2 Ma for this chronofauna triplet. Whetherthe cycles represent equal units of time is integral tounderstanding the cause of these cycles, but is not integralto the main thrust of the argument; repeating ecomorphevolution and extinction among different lineages occurssynchronously, and only climatic change has broad en-ough effects to produce this pattern.

It would be very important to establish that climaticchange and evolutionary processes, including extinction,are due to random historical accidents, but it would alsobe a scientific dead end. A predictive model of climaticchange and correlated evolutionary processes is obviouslymuch more desirable, but can such a model be con-structed? While the basis of stratigraphy and almost allgeology is the Law of Superposition, we must use fossilsto construct a regional or global stratigraphy. The units ofbiostratigraphy are unique combinations of last and firstappearances of organisms. If such events were randomlydistributed over the rock column, boundaries would resultsolely from historical accidents, and these boundaries

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, USAe-mail: ldmartin@ku.eduFax: +1-785-8645335

T. J. MeehanDivision of Science, Chatham College,Buhl Hall, Woodland Rd, Pittsburgh, PA 15232–9987, USA

T. J. MeehanResearch Associate,Carnegie Museum of Natural History,Pittsburgh, Pennsylvania, USA

might change with the whims of prevailing academicpolitics. It seems obvious that it would be better if aboundary corresponded to a recognizable global event. Aclimatic-evolutionary connection seems fundamental tobiostratigraphy, and Krasilov (1974) advocated a climat-ic-based system in his causal biostratigraphy. He impli-cated overall ecological change as the key to under-standing biostratigraphy and stated that the succession ofecosystems is controlled by climatic cycles. This impliesthat there are bundles of time that can be recognized onthe basis of unique biological compositions and the im-pact of climate on the sedimentary record. There is aschool of thought that claims that there is no visible ev-idence for climatic impact on evolution (e.g., Prothero1999; Alroy 2000), but most workers see a clear con-nection, and Darwinian evolution seems to demand such aresult. There are numerous studies of modern organismscorrelating climate and adaptation, and natural selectionresulting from climatic change has been observed in athree-decade study of Darwin’s finches (Grant and Grant2002). From the fossil record, we have empirical evidencethat climate changes over time and that biota are directlyaffected. For instance, Europe was fully tropical in theMiddle Eocene, as evidenced by the famous deposits atMessel where we find rainforest trees and animals whoseclosest analogues are in Africa today (Schaal and Ziegler1988), while fossils of 18,000 years ago indicate a tundraflora and fauna (von Koenigswald and Hahn 1981). Theoverall global trend during the past 55 Ma has been to-wards cooling, but we are presently experiencing a re-versal of that trend. There is relatively little evidence oflong periods of climatic stasis, and all long-term patternsare interrupted by periodic fluctuations where the generaltrend is reversed.

The usual measures for climatic regime are tempera-ture and its effects as expressed in terms of water. Hotworlds are wet worlds because of increased energy andwater surface area for evaporation, while cold worlds aredry. Wet worlds favor canopy strategists (trees) and coldworlds pioneering plants and open vegetational structures(Martin 1994). Wet worlds favor sedimentary depositionwith increased plant cover and a higher base level,whereas dry worlds are characterized by increased ero-sion. Climate is mediated locally, and it is possible for alocal region to be dry when global averages are wetter.Ultimately weather patterns are interconnected, and cli-mate cannot change greatly over any large region withoutaffecting all regions. Usually environmental change is badfor established organisms. Changing rainforest to grass-land may be bad for monkeys, while changing grasslandto forest may be bad for wildebeest. Global change islikely to have a negative impact on organisms bestadapted to the status quo. On the other hand, organismsthat occupy marginal habitats may find their habitatgreatly expanded as climate changes (e.g., Martin 1994).We may predict that rapid environmental change willresult in nearly simultaneous extinction of many taxa anddramatic biogeographic reorganization of others and that

these changes will have a global signature. Some versionof this scenario must lie at the root of biostratigraphy.

Ecomorphs

The similarities among organisms are a greater theoreticalproblem than differences. Differences can and shouldresult from random events over time. Historical accidentscome into full play when we examine how organismsdiffer, but how are we to explain characters that areconserved over vast intervals of geologic time? We seeimmense amounts of conserved similarity in geneticcomposition and cellular processes over the hundreds ofmillions of years that organisms have inhabited Earth.Without the action of natural selection, such similaritieswould soon have fallen prey to random processes. Thereare also not an infinite number of solutions to biologicalproblems. In fact the number of solutions seems to bequite small judging from the number of times that thesame solution is evolved independently. A computersimulation of “organisms” shows that with strong selec-tion, convergent evolution of even a complex trait iscommon (Lenski et al. 2003). Natural selection producessuites of coordinated similarity resulting from sharedactivities, rather than shared phylogeny. If the sharedactivity is an integral part of an “ecological occupation,”it may predict other similarities related to that occupation.Cuvier’s great contribution to comparative anatomy wasthe principle of correlation—the idea that changes in oneanatomical suite required concordant changes in othersand that a lifestyle could be predicted from a subset ofcorrelated structures. It is this ability of ecological posi-tion to predict anatomy independent of phylogeny that isthe basis of the ecomorph concept (Martin and Naples2002).

Convergent organisms have been called ecomorphs(ecological morphotypes; Williams 1972), which can becorrelated to Van Valen’s (1971) adaptive zone—an or-ganism’s resource space together with relevant predationand parasitism. An important property of adaptive zonesis that they exist as opportunities within the ecologicalframework and are defined by specific resources. Theexistence of an adaptive zone creates an opportunity forthe 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) antici-pated this view: “Possible ways of life are always re-stricted in two ways: the environment must offer theopportunity and a group of organisms must have thepossibility of seizing this opportunity.” Ecologies containopportunities that define circumscribed morphologies,including physiology and behavior. Convergent formsevolve independently in separated but similar ecologies,demanding only that adequate predecessors for the mor-phological type be present. Similar ecomorphs generallydo not evolve in the same region at the same time, butrequire either geographic or temporal separation (Martinand 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 pollenecomorphs and the cyclic nature of abundances of the palm paly-nomorph group, Monocolpites medius, in South America (modifiedfrom van der Hammen 1961: Fig. 1). Increasing abundances of M.medius (shaded) indicate decreasing temperatures (towards bottomof graph). Note that more severe cooling characterizes the end ofsubcycle C. Bottom graph: correlated North American subcyclesbased on mammalian assemblages (Martin and Meehan 2002).Each A-B-C community represents a vadh climatic cycle, and thistriplet forms a stout climatic cycle. B Climatic cycles and dirktoothiterative evolution. Stratigraphic distribution of latest Eocene–Pleistocene (Chadronian-Irvingtonian) mammalian faunas of North

America as compared to Stout’s (1978) sedimentary/climatic cyclesof Nebraska correlate to the triplet climatic cycles of van derHammen (1961). Martin’s interpretation (1985) of Stout’s cycles isshown, as well as the independent evolution of dirktooths withinthese cycles. The Barstovian and Hemphillian are poorly repre-sented in Nebraska. The base of each sequence is characterized byheavy fluvial incision and deposition, and the top, by eolian and/orcaliche horizons. The paucity of cat ecomorphs in the HemingfordCycle is referred to as the “cat gap.” Note that in North Americaformational boundaries are not necessarily the exact correlates ofbiostratigraphic boundaries, so that these climatic cycles correlatewith faunal assemblages (NALMAs or subages), and not with de-fined rock boundaries. Modified from Martin 1985: Fig. 5

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Convergent adaptive types plagued taxonomic work inCuvier’s time and continue to do so. Ecomorph analysis is“free of taxonomy” (Damuth et al. 1992) and yields aperspective on evolutionary processes not attainable froma phylogenetic approach. Organisms live and evolvewithin communities, so perhaps taxonomic units are thewrong units for understanding causal mechanisms (Mee-han and Martin 2003). Large-scale ecological analyses indeep time are rare even though the benefit of such work iswidely advocated (e.g., van der Hammen 1965; Krasilov1974; Fischer 1981; Damuth et al. 1992). Large-scalepaleontological analyses of South American pollen (vander Hammen 1957; Leidelmeyer 1966) and NorthAmerican mammals (Martin 1985; Meehan and Martin2003) reveal repeated evolution and extinction of eco-morph types, suggesting the existence of global iterativeclimatic cycles.

Hypothesis of iterative climatic cycles

Van der Hammen (1957, 1961) discovered an iterativepattern in a succession of Late Cretaceous to late Ceno-zoic pollen assemblages from oil well core samples inColombia, South America. Pollen shapes can be highlyconvergent and are not assignable to species level, but areclassified as form genera (palynomorphs). Pollen classi-fication is basically a functional one of adaptive types,similar to leaf shape ecomorphs (e.g., Wolfe 1985). Vander Hammen (1957) described pollen abundances ofpalms, other angiosperms, and ferns that had synchronousminima and maxima at apparently regular intervals, rep-resenting three assemblage types. Pollen community Awas succeeded by a B community and the B succeeded bya C before the pattern repeated with the re-evolution of aconvergent A community. This A-B-C triplet pattern wasbest expressed by palm pollen of the Monocolpites mediusgroup (Fig. 1A).

Abundance of M. medius pollen reflected temperaturetrends during the Cenozoic, with a relatively cool periodin the early Paleocene, extensive warming into the earlyEocene, and then overall cooling up to the Recent (vander Hammen 1961). On a smaller scale, minima andmaxima of pollen abundances within each communitytype represented cyclic warming/cooling periods on theorder of 2 Ma (Fig. 1B). Each subcycle begins relativelycool, warms considerably, is somewhat stable, and thencools sharply at the end. Extinction at the communitylevel occurs near this temperature minimum. At the end ofsubcycles A and B, the temperature drop is similar inmagnitude, and at the end of subcycle C, the cooling isgreater. Subcycle A is warmest, B almost as warm, and Cmuch cooler.

Stout (1978) and Schultz and Stout (1980) recognizedsedimentary cycles in the central Great Plains of NorthAmerica that reflected regular changes in climate sincethe mid-Cenozoic. Studies of fluvial terraces, soil hori-zons, and loess deposits show a repeating pattern of valleycut-and-fill sequences related to fluctuating aridity. The

base of each sequence is dominated by fluvial incisionand deposition, the middle cycle by mixed fluvial andeolian infilling, and the terminal cycle by eolian deposi-tion and an increase in caliche paleosols. This tripletpattern reflects a wet climate at the base, a moderateclimate in the middle, and a much drier climate at the top.The White River Cycle as reflected in deposits of Ne-braska (latest Eocene to early Oligocene) is an excellentexample of this pattern (Fig. 1B). The Chadron Formationis predominantly channel and floodplain deposits, withoccasional lake and pond deposits. The Orella Member ofthe Brule Formation consists primarily of channel andfloodplain deposits, with rare pond deposits and someeolian influence. The Whitney Member of the BruleFormation in Nebraska is a loess deposit. Schultz andStout (1980) stated that major mammalian extinctionsoccur at the unconformable boundaries in these sequencesand suggested that these unconformities indicate dry, coolperiods with relatively little plant cover and more erosion.Soil changes, as well as faunal and floral changes, supportthis climatic interpretation (Clark et al. 1967; Retallack1983). This triplet pattern matches van der Hammen’s A-B-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 mammalianfaunas, Martin (1985) recognized an iterative A-B-Cpattern in mammalian communities. Through dispersaland adaptive radiation, a community type would developand become extinct—only to redevelop in the same placeduring the next sedimentary cycle. Comparing faunasfrom the same position within different sedimentary cy-cles, Martin showed that they resembled each other indiversity and ecomorph composition, being more similarto one another than to the subcycles immediately belowand above in the stratigraphic sequence. Figure 1B com-pares Martin’s interpretation of North American landmammal “ages” (NALMAs) and their subdivisions withStout’s climatic/sedimentary cycles. The extinction of adirktooth ecomorph at the end of one cycle and its re-evolution in the next cycle exemplify repeating ecomorphreplacement. Martin (1985) proposed that there was aniterative evolution of mammalian communities with a

Fig. 2A–D The A-B-C pattern in dominance turnover of mam-malian ecomorphs in the North American Cenozoic. A Dominantherbivore ecomorphs of the order Artiodactyla: s Oreodontidae Iradiation; D= Oreodontidae II radiation; � Moschidae and Dro-momerycidae; o Antilocapridae; l Bovinae and Cervinae; BFossorial 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 catecomorphs: s Oxyaenidae; � early Nimravidae; n early Felidaeand late Nimravidae; D= late Felidae; D Shrew ecomorphs (cryptic,leaf-litter insectivores): D Cimolesta; l Nyctitheriidae; o Sorici-dae/Heterosoricinae; � Soricidae/Soricinae; minor shrew eco-morph radiations not represented for graph clarity. The 27 Ceno-zoic units are North American land mammal “ages” or subages thatreflect vadh climatic cycles (Martin 1985; Martin and Meehan2002); see Table 2 for abbreviations

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period of about 7 Ma. Martin also showed that the dom-inance turnover in selenodont artiodactyls reflects thisiteration (Fig. 2A). He further argued that this pattern wasclimatically controlled, showing a correlation with thecyclic temperature curve of Wolfe and Hopkins (1967).Meehan and Martin (2003) reported other mammalianiteration examples in hippo, dog, and bone-crushing dogecomorphs. This pattern is also reflected in the dominanceturnover of fossorial rodent, all catlike, and shrew eco-morphs (Fig. 2B–D).

Martin and Meehan (2002) preliminarily extended thispattern of climatic cycles based on North Americanmammalian faunas to the early Cenozoic and calculated amore refined interval. Recent radiometric dates associatedwith mammalian faunas suggest a subcycle duration of2.41 Ma and 7.23 Ma for the triplet. A subcycle thusapproximates the duration of a marine zone, and a cycle amarine stage. Benton (1995) reported an averagePhanerozoic stage duration of 7.4 Ma. The similarity ofbiostratigraphic systems (e.g., shells, mammals, and pol-len) and, in particular, their correlation on a regional, andsometimes global scale, reflects an underlying basis.

In studying Pleistocene terrace sequences and recog-nizing correlations of cut-and-fill sequences across centralNorth America, as well as worldwide correlated strati-graphic boundaries and climatic events, Schultz and Stout(1980) concluded that these sedimentary cycles representglobal climatic change. Van der Hammen (1961) came tothe same conclusion concerning the cause of pollencommunity patterns, as did Wolfe (1978) concerningfluctuations in leaf ecomorph assemblages. Martin andMeehan (2002) concurred that any force able to simul-taneously affect communities in North and South Americawould have global ramifications. Iterative evolution ofecomorphs and community structures requires repetitionof environmental parameters, which suggests that climaticcycles form the underlying basis for a global stratigraphy(van der Hammen 1957, 1961, 1965; Martin 1985; Martinand Meehan 2002; Meehan and Martin 2003). Becausestratigraphic systems tend to be more localized and carrywith them significant historical baggage, Martin andMeehan (2002) proposed a new nomenclature for thesecycles. Each subcycle of about 2.4 Ma is termed a “vadh”for T. van der Hammen, who first characterized thispattern and recognized its importance. The complete A-B-C cycle is termed a “stout,” after T.M. Stout, who dis-cerned this pattern in sedimentary cycles of the GreatPlains and recognized its global significance in relation tomarine stages. Vadhs A, B, and C form a stout in thisterminology for climatic cycles and may be measures oftime analogous to days, years, and Milankovitch astro-nomical parameters.

Do these cycles represent equal units of time?

Van der Hammen (1961) considered these repetitions incommunity types to be of equal duration. He assumedequal units of time based on two criteria: (1) within each

cycle (= stout), lake sedimentation thickness for eachsubcycle (= vadh) was approximately equal; and (2) froma theoretical consideration, a given pollen communitytype would likely take a similar amount of time to de-velop. Although van der Hammen’s criteria are notcompelling, radiometric dates from associated mam-malian faunas in North America do suggest equal units oftime (Martin 1985). Martin also found comparablechanges in diversity of late Cenozoic mammalian com-munities that suggested regular cycling (Fig. 3). Theterminal extinction events, which appear to be synchro-nous and rapid (Woodburne 1987; Webb 1989), were ofsimilar magnitude, and generic diversity returned to asimilar level (Fig. 3A). Although adaptive radiationwithin North America generates much of the diversity,dispersal is an important source of radiations (Martin1985). For example, the earliest Dromomerycidae andCervinae/Bovinae artiodactyls (refer to Fig. 2A) dispersedfrom Asia. The timing of these dispersals appears to berelated to Stout’s cycles, suggesting that climatic changeis a controlling factor, with dispersal into middle and lowlatitudes representing time-transgressive range extensionfrom higher latitudes (Martin 1985, 1994). With globaltemperature generally decreasing since the Eocene, cool-adapted immigrants from higher latitudes and their de-scendants were at an advantage, and the percentage ofHolarctic immigrants and their descendants in NorthAmerica 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 subcycle2.33 Ma. In 1985, Martin had access to more radiometricdates to test whether these subcycles were of equal du-ration. He plotted 72 dates correlated to mammalianfaunas (latest Eocene through Pleistocene) against thebiostratigraphic divisions. The data formed a highly linearrelationship, suggesting equal units of time. Martin de-termined that the radiometric age midrange points foreach unit were not statistically different from an idealduration calculated from a radiometric date near the baseof the Geringian (late Oligocene) divided by the numberof subsequent vadhs (28 Ma divided by 12 vadhs). Thisgave an interval of 2.33 Ma.

Another approach is to regress radiometric datesagainst vadh units so that the slope of the regression linerepresents the likely vadh duration. Over the past severaldecades, radiometric dating analyses have gone fromwhole-rock to single-crystal, which has improved preci-sion. Although the radiometric dates of Evernden et al.(1964) were obtained by whole-rock analysis, their dataset has the advantage of being processed in one lab and isstill the most comprehensive, single report for datedNALMAs. Updating these radiometric age estimates(n=55) with the new potassium–argon half-life standard(Dalrymple 1979), and then regressing these ages againstthe 27 Cenozoic vadhs, yields a coefficient of 0.991 andvadh duration estimate of 2.44 Ma (Martin and Meehan2002). Repeating the same exercise using recent (post-1985), higher precision radiometric dates yields a coef-

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ficient of 0.999 and vadh of 2.41 Ma (Martin and Meehan2002; Fig. 4). It is important to note that vadh divisionsinferred from mammalian faunas are biostratigraphicboundaries defined by other workers who did not suspectthat these divisions might represent equal units of time.

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

Fig. 3A, B Generic (ecomorph) counts of terrestrial mammals inthe North American Cenozoic. A Generic abundance per vadh.Each genus is assigned an ecomorph type, so generic abundance isequivalent to ecomorph abundance. Equilibrium in mammaliancommunities appears to have been reached 10 Ma after the K/Textinction, and the average number of known genera from theEocene–Pleistocene (Gray-Irvi) is 131. Sample quality generallyincreases the younger the rock unit, and the average from the mid-Miocene to Pleistocene (Bars-Irvi) is 151. Modern generic diversitycorrelates with land mass area (Flessa 1975), which has been fairlystable 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 isprincipally from middle latitudes of the West, so preservational/sampling biases may preclude an accurate estimate. Number ofrecognized Cenozoic genera is currently 1,301 (excluding bats andmarine mammals), which represents 3,375 distributional pointsacross the 27 vadhs. B Percentages of surviving/extinct genera. n

percentage of genera that survived into the next vadh; o per-centage of extinct genera. Some units are not well represented inthe geologic record (e.g., Monroecreekian and Lapointian). Theaverage extinction rate since the early Eocene is 32%

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are heavily influenced by a few horizons, such as the K/Tboundary. Although radiometric date regressions do notprove the existence of 27 units of equal duration, the highcoefficients imply equal units, and radiometric agescannot be used to argue against this portion of the hy-pothesis. There is, however, an independent, partial test oflinearity of these data via epoch boundary ages from adifferent source: marine sediments (Martin and Meehan2002). Assuming epoch boundaries from the marine timescale are correlated correctly with NALMAs, one wouldpredict the same linearity when marine boundary ages areplotted against the vadhs. Using extrapolated epochboundary ages from marine radiometric dates (Harland etal. 1989) yields a regression coefficient of 0.99 and vadhduration of 2.44 Ma (Martin and Meehan 2002). Runningthe same analysis from two other stratigraphic charts(Berggren et al. 1995; Gradstein and Ogg 2004) yieldscoefficients of 1.00 and 0.99 with estimated vadh dura-tions of 2.41 and 2.44 Ma, respectively. These three es-timates are equivalent within a 95% confidence interval(Table 1).

The Plio-Pleistocene boundary is the most divergentpoint (Table 1), but unlike the Pleistocene–Holoceneboundary, it is not defined by a significant global climaticevent. It is a political boundary where a committee drovea “golden spike” at a local foram appearance/extinction(Harland 1989:68). This golden spike philosophy wasapplied due to great controversy among workers, yet nodissension arises among marine and terrestrial workersabout a sharp, global cooling event 2.4 Ma ago, incurringgreat biological consequences. This climatic change isevident in such events as (1) a drop in ocean tempera-tures; (2) 65% extinction of the tropical western Atlanticmollusc species; (3) abrupt change in carbonate produc-tivity and preservation; (4) weather pattern changes in theMiddle East as indicated by dust deposition; (5) a greatincrease in tundra habitat and loess deposition; and (6)5�C cooling in Colombia as indicated by pollen assem-blages (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; De-Menocal et al. 1991; Hooghiemstra and Ran 1994). Var-

Fig. 4 Recent (post-1985) ra-diometric dates regressedagainst Cenozoic vadhs. Re-gression of dates associatedwith North American mam-malian faunas against 27 unitsyields an estimated vadh dura-tion of 2.41 Ma. Updated fromMartin and Meehan 2002: Fig. 2

Table 1 Extrapolated Cenozoic epoch boundary dates versus predicted vadh values

Epoch Harland 1989Marine dates

Berggren et al. 1995Marine dates

Gradstein Ogg 2004Marine dates

Janis et al. 1998Terrestrial dates

Predictedvadh ages

Pleistocene a 2 1.3 1.81 1.8 2.41 MaPliocene 5 5.3 5.33 4.5 4.82 MaMiocene 24 23.8 23.03 23.0 24.10 MaOligocene 36 33.7 33.9 33.4 33.74 MaEocene 57 55.5 55.8 55.5 55.43 MaPaleocene 65 65.0 65.5 65.1 65.07 MaVadh estimate 2.44 Ma 2.41 Ma 2.44 Ma – –R-squared 0.991 1.000 0.999 – –95% CI 2.35–2.53 2.36–2.45 2.36–2.51 – –a There is a climatic cooling event recorded worldwide at 2.4 Ma, and some workers have advocated that the base of the Pleistocene bemoved to this position, which agrees with the terminal cooling and boundary location predicted by vadh climatic cycles. The ideal vadhages are estimated from radiometric dates associated with mammal deposits in North America (Martin and Meehan 2002; Fig. 4). Vadhduration estimates from the marine record are equal within a 95% confidence interval (CI).

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ious workers have advocated that the Plio-Pleistoceneboundary be defined by this cooling event (e.g., Liu et al.1985), and in Europe, some workers have been using thisevent for decades as the Quaternary/Tertiary boundarybecause 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 relativestasis bounded by abrupt evolutionary change due to ex-trinsic factors. Communities rapidly evolve, remain stablefor long periods, rapidly go extinct, and then a newcommunity replaces the previous one. This pattern is socommonly recognized that it has been given many de-scriptors: typostatic and typogenetic/typolytic phases ofevolutionary cycles (Schindewolf 1950), chronofaunas(Olson 1952), iterative climatic cycles (van der Hammen1957; Martin 1985), biomere boundaries (Palmer 1965),punctuated equilibrium (Eldredge and Gould 1972), eco-logical-evolutionary units (Boucot 1975), turnover pulses(Vrba 1985a), ecosystem model (Krasilov 1987), faunisticcycles (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 thispattern, except for periodicity (e.g., Newell 1952), or thepattern was implied in recognition of climatic or sedi-mentary cycles (e.g., mesothems or megacycles; Buschand West 1987; Kemper 1987). Brett and Baird (1995)noted that in the late 1840s, d’Orbigny, the “father ofbiostratigraphy,” recognized that genera and specieschanged little within his defined packages of strata. Ob-servation of evolutionary stasis bounded by abrupt changedue to environmental perturbation was perhaps first rec-ognized in a comprehensive manner by Olson’s (1952)idea of chronofaunas. A chronofauna was initially definedas a “geographically restricted, natural assemblage ofinteracting animal populations that has maintained itsbasic structure over a geologically significant period oftime” (Olson 1952:181).

Missing time due to erosion or nondeposition is alwayspresent at various scales, leading some workers to hy-pothesize erroneously that evolution makes large“jumps.” Whenever paleontologists study fossiliferousstrata in finer detail, they discover that change may haveoccurred more rapidly than usual, but intermediate mor-phological steps are represented (e.g., Martin 1984). Thefundamental pattern of stasis bounded by rapid changecaused by extrinsic factors is consistent with hypothesesof climatic cycles. The importance of climatic cycles hasbeen recognized by numerous workers, and many havesuggested that stratigraphy be based on climatic changebecause it affects biota and sedimentary processes si-multaneously. On a large scale, disruption of entirecommunity patterns by extrinsic factors implies that bi-otic factors, such as competition are minor, as concludedby Benton (1983). Raup and Boyajian (1988:109) also

concluded that Phanerozoic extinction patterns were mostlikely caused by widespread environmental upheaval.

In contrast, Stucky (1995) suggested that communityinteraction was a more important factor than the physicalenvironment in determining survivorship. Stucky furthernoted a contemporaneous global trend of increased hyp-sodonty among mammals. Convergent trends of geo-graphically isolated faunas indicate a cause that cannot befrom competition or some other community interaction.Congruence of faunas across continents by simultaneousappearance of the same taxa, similar grade of evolution,or convergent community structure indicates that climaticchange is a dominant force in large-scale evolution.Where Stucky’s data reflect stasis in community struc-ture, we would argue that it is due to relative stasis inclimate.

Sedimentary cycles

Sedimentary cycles have been recognized throughout thegeologic record. In some cases, as in the Milankovitchcycle, their duration and mechanisms seem well under-stood. In other cases, their duration and periodicity isquestionable. Ross and Ross (1985) described over 50global sedimentary cycles from the Paleozoic that re-present sea level rising and falling (transgression–re-gression) with an average duration of 2 Ma. The variationis estimated to range from 1.2 to 4 Ma; however, thesedurations are highly extrapolated, being based on fewradiometric 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 isconsistent with the asymmetric temperature profile ofvadhs, as well as temperature profiles from oxygen iso-tope data (e.g., Stott and Kennett 1990).

In marine stratigraphy, sedimentary cycles of variousscales (e.g., synthems, mesothems, cyclothems, and PACsequences) have been recognized across the globe, and asearly as 1888, Suess suggested that a global stratigraphycould be based on trans/regressive units (Busch and West1987). Recent workers are increasingly using temporal/climatic models in stratigraphy, and perhaps the mostencompassing model is the hierarchal genetic stratigraphyof Busch and West (1987). They defined a hierarchy oftrans/regressive units bounded by transgressive and cli-matic surfaces that can be correlated using lithologicaland ecological data on a regional, and possibly global,scale. These trans/regressive units have periodicities onthe order of 225–300 Ma (first order) down to 50–130thousand years (sixth order). Periodicities of third andfourth order are comparable to vadhs and stouts (Martinand Meehan 2002), and these units have synchronousunconformities, indicating global factors linked to cli-matic change (Busch and West 1987).

9

Stepwise extinction and iterative evolution

Stepwise extinction reflects stepwise climatic change, andthis pattern is widely recognized in the fossil record (e.g.,Kohler et al. 1988; McGhee 1988; Holland 1989; Janis etal. 1998). Keller (1986) noted five pulses of extinctionover approximately 15 Ma throughout the late Eocene–early Oligocene, which resulted in two-thirds replacementof foram species. Keller (1986:274) stated the following:

Paleontological research has made it increasingly clearthat both faunal and climatic changes are characterizedby long periods of stability separated by brief episodesof rapid faunal turnover and climatic fluctuations.During middle Eocene to early Oligocene each faunalturnover is characterized by replacement of tropicalmarine faunas and floras by cooler subtropical andtemperate elements as observed by [many authors].Recently, Berger et al. (1981) discussed major faunalturnovers at the Cretaceous–Tertiary and Eocene–Oligocene boundaries and the late Miocene in terms ofmajor steps in Cenozoic evolution. Keller (1983a,1983b) studied one of these “steps” at the Eocene–Oligocene boundary and observed that faunal changesoccurred in a series of yet smaller steps related tosuccessively cooler climatic conditions. Such stepwisefaunal changes were also observed by Kauffman(1984a, 1984b) in late Cretaceous invertebrate faunasand he redefined the late Cretaceous mass extinctionsas “stepwise mass extinctions” occurring over a periodof 1–3 Ma.

Using the interpolated time-scale boundaries ofBerggren et al. (1995), these Eo/Oligocene turnoversoccurred at 40.1, 38.3, 35.3, 33.5, and 29.4 Ma. The hy-pothesis of iterative climatic cycles predicts seven rela-tively 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 theseforam extinctions, except that there was no notable ex-tinction observed at about 31 Ma.

The stepwise biotic and climatic nature across the Eo/Oligocene is seen in other marine faunas, paleosols, leafassemblages, mammalian faunas, oxygen isotope data,and ice sheet formations (Berggren et al. 1985; Wolfe1985; Ehrmann and Mackensen 1992; Miller et al. 1991;Zachos et al. 1993; Diester-Haas et al. 1996; Bestland etal. 1997). Interpolated ages of late Eo/Oligocene mam-malian faunal turnovers in North America (Prothero1989) are also in close agreement with predicted vadhboundaries. A paleosol series from deposits of SouthDakota is inferred to show climatic steps at 37, 34, 32,29.5 Ma (Retallack 1983), which are close to predictedvadh estimates of 36.1, 33.7, 31.3, and 28.9. In addition,each step is terminated by highly dry and seasonal cli-mates, in which reduced plant cover presumably led toincreased erosion, as described in Stout’s (1978) climatic/sedimentary cycles.

The two major Cenozoic radiations of forams have apattern of extinction at a cooling interval, re-evolution ofsimilar ecomorphs, and stepwise change over the longterm (Cifelli 1969). This iterative pattern in forams is seenthroughout the Paleozoic and Mesozoic (Stanley 1987).Cifelli (1969) noted that foram faunas of widely differentages were sometimes more alike than those from adjacentstrata. He also stated that ammonoid evolution was highlyiterative, paralleling foram evolutionary patterns and thatconvergence of ecomorphs is so high that ammonoids aresometimes classified on stratigraphic grounds because thesame ecomorph type cannot be easily distinguished tax-onomically. This synchronous ecomorph iteration in ma-rine faunas resembles the terrestrial record.

Chronofaunas and faunistic cycles

Olson (1975) concluded that succeeding communities didnot evolve gradually from the previous one, but werereplaced in part or whole and that most major evolu-tionary change took place as new communities formedunder rapid environmental change. Some describedmammalian chronofaunas closely correspond to a stoutclimatic cycle. For example, Webb (1969) recognized aWhite River Chronofauna composed of the Chadronian,Orellan, and Whitneyan faunas and a ClarendonianChronofauna as composed of the Valentinian, Clarendo-nian, Kimballian, and Hemphillian faunas (refer toFig. 1). Chronofaunal or stout characters are also presentin Pennsylvanian/Permian coal swamp communities. Di-Michele and Phillips (1995) recognized stasis in eco-morph structure for millions of years, rapid turnover dueto severe climatic change, and a new community formingby ecomorph replacement.

Pascual (1992) stated that South American landmammal “ages” represent relatively balanced communi-ties during times of stasis and that these communitieswere disrupted during periods of severe climatic change.A pattern of sedimentary bundles correlating with epi-sodes in evolution has been recognized since the begin-ning of South American mammalian biostratigraphy, andassemblages of major bundles have the ecological struc-ture of chronofaunas (Pascual 1992). These sedimentarybundles and extinction horizons correlate with the marinerecord. In turn, changes in sedimentation and evolution inmarine and terrestrial provinces correlate with globalclimatic changes and regional effects. Pascual describedextinction periods within these sedimentary bundles, buttermed these “internal episodes” because these disconti-nuities did not break up the basic continuity of thechronofauna, which is consistent with vadh extinctionswithin a stout. Pascual and Jaureguizar (1990) recognizedfour hierarchical faunistic cycles with durations of 2.5–25 Ma.

10

Trilobite biomeres

Biomeres were originally defined as regional biostrati-graphic units bounded by extinctions in the dominantelements of one phylum (Palmer 1965). Rapid extinctionsbound stable, ecological units of benthic trilobite faunasof North America, and replacement is iterative, with eachnew trilobite community radiating from the same immi-grant ecomorph from open water (Palmer 1965; Stitt1975). These extinction boundaries are not diachronous,nor restricted to benthic trilobites as first suggested. Otherextinctions at biomere boundaries include inarticulatebrachiopods, conodonts, agnostoid trilobites, and in thecase of conodonts, the extinction has been discerned to beglobal (Hood 1989). Most workers have proposed thatthese extinctions were the result of an abrupt temperaturedrop. From one biomere boundary that retained originalisotopic signatures, the extinction was associated with arapid 4–5�C cooling (Hood 1989). After analyzing sug-gested causes of these turnovers, Hood (1989) concludedthat abrupt cooling caused extinction of these tropicalcommunities (and that an anoxic water event associatedwith this cooling may have been a factor).

Biomeres encompass multiple trilobite zones, and theUpper Cambrian represents three biomeres and about7 Ma (Sundberg 1996; Harland et al. 1989). Palmer et al.(1995) reported the zones averaging 2.7 Ma and biomeresaveraging 7 Ma, but Bowring and Erwin (1998) reportedCambrian zones averaging 1.5 Ma and biomeres 4 Ma andthat the zones are not of equal duration. It is difficult toascertain which of these absolute ages is more accurate,but the pattern of zones and biomeres is consistent withvadhs and stouts, and what is needed is to test for iterativeevolution of trilobite ecomorphs and to create detailedtemperature curves spanning at least 15 Ma. An abrupt5�C 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 ter-restrial 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-evolu-tionary units, Brett and Baird (1995) argued that stasis ofAppalachian Basin benthic communities in the MiddlePaleozoic occurred on the order of 3–7 Ma. These com-munities went extinct due to major, rapid environmentalchange, and most boundaries were associated with globalclimatic events and extinctions. Replacement of com-munities occurred within 100,000–500,000 years and wasfollowed by long intervals of stasis. This pattern agreeswith the one predicted by iterative climatic cycles, and itstime scale is on the order of vadhs and stouts.

Brett and Baird (1995) renamed this pattern “coordi-nated stasis” and argued that it is seen in such variedcommunities as freshwater molluscs, trilobite biomeres,

and mammalian faunas, as argued here. Williamson(1981) documented nearly synchronous morphologicalchange followed by relative stasis in several mollusclineages in the Turkana basin. Vrba (1985a, 1985b)demonstrated comparable pulses of change and long-termstability in African bovids and hominids. Vrba (1985a)coined the term “turnover pulse,” and her hypothesisagrees with vadh characters. Besides the mammalian ex-tinction in Africa occurring at 2.4 Ma, community re-covery was rapid; antelope niches were filled by radiationand dispersal within 300,000 years (Vrba 1988). Vrbaargued that abrupt climatic change breaks down stableplant and mammal communities causing rapid evolu-tionary change and stated the following (1985a:232):

Speciation does not occur unless forced (initiated) bychanges in the physical environment. Similarly, forc-ing by the physical environment is required to produceextinctions and most migration events. Thus, mostlineage turnover in the history of life has occurred inpulses, nearly (geologically) synchronous across di-verse phylogenies, and in synchrony with changes inthe physical environment.

This pattern exactly describes the terminal Pleistoceneextinction of North America, which occurred over severalthousand years (e.g., Guthrie 1984; FAUNMAP group1996).

Suggestions for further work

A perennial problem in studying the geologic past is re-liability of correlations, particularly on a global scale.Standard correlation charts have changed significantly ona decade basis, and workers still disagree on many as-pects. The frequency and duration of missing time inmarine strata may be unappreciated or not even tested(Aubrey 1995). Terrestrial sequences have far less con-tinuity than marine sequences, with much less than 50%of time preserved in most deposits (Clark et al. 1967;Retallack 1984). In addition, many biostratigraphicboundaries correspond to times of erosion.

Most of these problems could be mitigated by betterabsolute age control. Unfortunately radiometric dates maynot be directly associated with biostratigraphically inter-esting assemblages and are not systematically distributedover the geologic record (Harland 1989; Berggren et al.1995). In North American mammalian biostratigraphy,Evernden and others (1964) provide the only compre-hensive dating sequence from a single study. This is anearly study using techniques with comparatively lowprecision, but even modern dating may show significantvariation among labs. A concerted effort needs to be madeto control for intralab error and extend the scope anddensity of absolute dates, especially for the Cenozoicwhere such a framework could definitively decide ifvadhs and stouts are chronostratigraphic.

11

Another correlation difficulty results from time-trans-gressive climatic effects. This is particularly noticeable inhigh latitude marine faunas, which are first and mostseverely affected by climatic change (Stanley and Rud-diman 1995). Some marine biostratigraphic definitionshave been changed as more has been learned of the time-transgressive nature of extinctions and first appearances.Innovations seem to occur at high latitudes first andprogress to lower latitudes as climate cools. Mathematicalmodeling of foram species origination/extinction eventsindicates that extinctions are more deterministic than firstappearances (Patterson and Fowler 1996), suggesting thatextinction events define sharper biostratigraphic bound-aries, as advocated by Martin (1985).

Because the terrestrial mammalian record is mainlyone of middle latitudes, the time-transgressive nature offirst appearances is not easily observed. Hickey et al.(1983) concluded that many vertebrate taxa inhabitednorthern Canada 2–4 Ma earlier than they occurred inmiddle latitudes and that floral displacement was muchgreater, although this was disputed (Flynn et al. 1984).Not only are high latitudes affected first, but low latitudesact as refugia for warm-adapted taxa, sometimes withlineages persisting much longer after most relatives be-come extinct at higher latitudes (e.g., Webb 1989). Thedescription of global ungulate distributions (Janis 1989)provides an example of latitudinal climatic offlap. Low-seasonally-adapted hindgut fermenters (such as horsesand rhinos) accounted for over 50% of the Eocene un-gulate fauna and occurred at high latitudes. During theOligocene, their high latitude abundance dropped to about25% as climate became cooler. By the mid-Miocenelower latitude abundances also dropped to 25% as globaltemperature decreased (Janis 1989).

A strong argument for high latitudes being a center ofevolution in the Northern Hemisphere is seen in thesudden, simultaneous appearance of “immigrant” taxa atmiddle latitudes of Asia, North America, and/or Europewith no immediate ancestors known (see Woodburne1987). Recognition of the Holarctic as a center for evo-lution has been noted since early studies. As stated byMatthew (1939:7), “...the present distribution of mam-mals is due chiefly to migration from the great northernland mass, and the connection of this southward marchwith progressive refrigeration in the polar regions wasmade more than a century ago (1778) by Buffon.” Thisclimatic offlap sequence of taxa is particularly variablewith respect to immigrants. Climatic offlap has beenbetter recognized in the marine record where high latitudefaunas are better known (e.g., Jenkins 1974; Stanley1987). The timing of mammalian dispersals into NorthAmerica appears to be related to climatic events, withdispersal into lower latitudes representing time-trans-gressive range extension (Martin 1985, 1994). High lati-tude data need to be extended and refined.

Also, marine data need to be more closely related withthe terrestrial record. One promising note in correlatingevents is that climatic effects as reflected in the marineand terrestrial records appear synchronous, even at a fine

resolution. For example, the climatic history of the past500,000 years as determined by pollen assemblagesaround a lake in Japan remarkably correlates with tem-perature records of the Caribbean and Pacific Oceans,sedimentary cycles of the Mediterranean, climatic trendsof Central Europe, and sea-level changes of Japan andNew Guinea (Fuji 1988). The Eocene warming event asexpressed by carbon isotopes from various sources ap-pears synchronous, as well as the rapid marine and ter-restrial biotic turnovers at this time (Koch et al. 1992).

If we assume a vadh duration of 2.4 Ma, the generaltemperature trend as described by van der Hammen(1961) shows overall warming to about 1.7 Ma into thevadh, followed by 700,000 years of rapid cooling, withgreater cooling at the end of a C vadh. Ice volumechanges in a C vadh, the Pleistocene, reflect this pattern.During the last 700,000 years, ice volume was two timesgreater than the previous 2 Ma (Barendregt and Irving1998). Temperature profiles at the Paleo/Eocene and Eo/Oligocene boundaries show similar magnitude, direction,and duration (cooling over 500,000 years; Stott andKennett 1990), and a number of oxygen isotope data setsindicate a 5�C drop at extinction boundaries (e.g., Vella1968; Kennett and Shackleton 1976; Guilderson et al.1994). These global temperature changes should result inenvironmental modification and concordant evolutionarychange. On a small scale, Chiba (1998) described a pat-tern of rapid, synchronous morphologic changes withlonger periods of stasis in five different snail lineages ondifferent islands over the past 40,000 years, concludingthat synchrony in convergence and lineage extinction wasdue to climatic change.

We need to better demonstrate which events co-occur.Martin (1984) demonstrated that species lineages of asabertooth felid (Megantereon-Smilodon) and muskrat(Pliopotamys-Ondatra) showed a similar pattern of bodysize change, with an exponential increase during the last700,000 years of the Pleistocene vadh C. He furtherdemonstrated the same pattern in a sabertooth nimravidlineage (Sansanosmilus-Barbourofelis) in the previousvadh C (Kimballian). These three lineages slowly evolvedoverall larger body sizes in vadhs A and B, and thentowards the end of a vadh C, their body sizes increasedexponentially. This evolutionary change is concordantwith global cooling, including the glacial pulse starting700,000 years ago. Mammal body size can be highlycorrelated with climate (e.g., Davis 1981; Zeveloff andBoyce 1988; Smith et al. 1995), and the body size in-crease in the armadillo-like Holmesina (Hulbert andMorgan 1993) exhibits a similar exponential rate at theend of the Pleistocene, exemplifying the breadth of thisphenomenon.

The power of climatic change to influence evolutionmay be further shown in humans. The evolution of thegenus Homo about 2.4 Ma ago has been attributed to theappearance of more open habitat (e.g., Stanley 1995).This is a period of cooling and increased aridity based ona wide variety of evidence (and the timing of this climaticshift is predicted by vadh cycles). Ruff et al. (1997) de-

12

scribed the pattern of brain size evolution in Homo as arapid increase from 600,000 to 150,000 years ago, whichwas preceded by stasis on the order of 1.8 Ma. Thispattern is concordant with the exponential growth seen inmuskrat and sabertooth body sizes. A remarkable coin-cidence if there is no underlying factor. Naples andMartin (1998) hypothesized that the evolutionary trendtowards larger brain sizes among ungulates, carnivores,and primates throughout the Cenozoic is due to increasedseasonality and habitat openness that resulted from globalcooling. As in the other major mammalian evolutionarytrends of the Cenozoic, such as increased body size anddegree of hypsodonty, brain size increase is predicted tobe highly correlated with mean global temperature trends.Geist (1983) noted that many Ice Age mammalian lin-eages (e.g., moose, mammoth, and Homo) in more sea-sonal environments (e.g., alpine and arctic) evolved or-nate, giant members with larger brains and more gener-alized niches than close relatives of more southern,equable climates. One would predict that these lineagesunderwent the most rapid evolutionary change during thevadh cooling intervals from approximately 3.1 to 2.4 Maago and from 700,000 to 11,000 years ago. Analyzingevolutionary rates within a species lineage may provide asimple and powerful tool for testing the existence of theseclimatic cycles. Besides A-B-C dominance turnover pat-terns (Fig. 2), any robust, long-term data set with a cli-matic signal, either more direct, such as oxygen isotopedata, or less direct, such as the extinction pattern of highlyspecialized 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 invadhs A or B (Fig. 3B). What we do see is that a fewhighly specialized ecomorphs characteristically becomeextinct in a vadh C (e.g., 12 of 15 sabertooths, 2 of 2cheetah ecomorphs, and 4 of 4 aye-aye ecomorphs in theNorth American Cenozoic).

Iterative climatic cycles—a useful hypothesis?

As listed above, many hypotheses recognize the funda-mental pattern of relative stasis bounded by rapid changewithin the fossil/sedimentary record. Though some havedifferent theoretical bases, they share many features. Isthere a significant difference among the concepts ofbiomere, faunistic cycle, ecological-evolutionary unit,and the older idea, chronofauna? The term punctuated-equilibrium (Eldredge and Gould 1972) became widelyused, but Schindewolf (1950), Simpson (1953), and manybefore have stated that evolution occurs at different rates.As mentioned previously, the “father of stratigraphy”(d’Orbigny 1849) recognized the “punctuated” evolutionand extinction bounding packages of strata. Given thecommonality of these ideas, it is worthy to consider thatthey are all related and may be partial recognition of asingle underlying mechanism. Meehan and Martin (2003)suggested that these hypotheses might be encompassed bya hypothesis of iterative climatic cycles. This hypothesis

was first proposed by van der Hammen (1957) and has theadvantage of generating many predictions.

Van der Hammen proposed that global climatic cyclesexist at many scales and can be tested with numerous datasets. In his 1965 paper, he reported that Jurassic am-monoid stratigraphy reflected cycles of 7 Ma composed ofthree 2.33 Ma cycles, and these in turn could be dividedinto cycles on the order of 0.8 Ma. He also inferred a70 Ma cycle. In this last paper on his climatic cycle hy-pothesis, van der Hammen reiterated that climatic cyclesdefine stratigraphy, providing ideal chronostratigraphicunits.

The recognition of climatic cycles in the rock record isa common theme. For instance, many workers (Clark etal. 1967; Wolfe 1978; Collinson et al. 1981; Kemper1987; Frakes et al. 1992) have proposed the existence oftemperature cycles on the order of 10 Ma as reflected inmarine and terrestrial data. Zubakov and Borzenkova(1990) reported a climatic cooling rhythm at 3.7 and11 Ma. Kemper (1987) reported climatic cycles of 2.2 and9 Ma bounded by abrupt temperature drops throughoutmost of the Cretaceous marine deposits of the SverdrupBasin, in northern Canada. These hierarchal cycles maybe equivalent to vadhs and stouts.

Kemper (1987) suggested that the cycles may be due toorbital parameters, but noted that solar variation cannot beruled out. Very small-scale solar changes, such as sunspotcycles, are reflected in the sedimentary/climatic record(e.g., Wymstra et al. 1984; Kerr 1996). There is a growingbody of research showing solar forcing as a viablemechanism for Quaternary/Holocene cycles (e.g., Crow-ley 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 strictestsense, it refers to the termination of a lineage, but it is alsoused more generally for the end of an adaptive type suchas sabertooth “cats.” In this usage it may not be final, andin the absence of human intervention, we might expectsabertooths to re-evolve, as they have done for the past50 Ma years. When we compare mammal extinction be-tween the two C vadhs of the Pleistocene and latestMiocene (Fig. 5), we see not only ecomorphs re-evolving,but also the same ecomorphs going extinct, such as inproboscideans (Amebelodon/Mammut), giraffe–camels(Aepycamleus/Titanotylopus), and scimitartooths (Nim-ravides/Homotherium). Extinction is not only similar interms of adaptive types, but also in scope—about one-third of ecomorph genera become extinct in each vadh(Fig. 3B). The community structure between these twovadh C assemblages is comparable, except that thePleistocene organisms are adapted to colder, more openenvironments, reflecting the general Cenozoic climatictrend.

13

Evolutionary patterns are shared in many cases byecomorphs, which start from ecologically similar ances-tors and progress through similar adaptive stages, usuallyshowing similar change rates. These changes are notconstant, being slower in the A and B vadh cycles andthen rapidly increasing in rate in the last third of the Ccycle (see Martin 1984; Meehan and Martin 2003), cor-relating to the temperature cycles of van der Hammen(1961).

The community extinction and replacement patternalso implies that the fossil record contains many examplesof rare taxa that through subsequent diversification filledthe empty adaptive zones of their ecological predecessors.In North America at middle latitudes, open habitat firstbecame widespread in the late Oligocene, and rodentstook advantage of this new adaptive zone. Beavers(Castoridae) are rare animals with little diversity in thelate 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 bur-rowing communities. At the end of the earliest Miocene,these dry land beavers become extinct along with gopher-like geomyoids. A new fossorial rodent communitydominated by aplodontoids and another group of gopher-like geomyoids replaced this first burrowing community.Some version of this community persisted until a similar,modern community of burrowing squirrels and pocketgophers replaced it. The diversity of burrowing rodentsfor each community was similar, but their origins weredifferent. We might have expected rodents that first oc-cupied burrowing niches would have continued in them tothe present day. This was not the case. The modern NorthAmerican fossorial rodent community is composedlargely of rodents that came into this niche in the last7 Ma.

Convergent/parallel characters are so prevalent amongecomorphs in these iterative communities that an unini-tiated observer would have difficulty in telling them apart,despite that they are not phylogenetically close. Many

Fig. 5 Convergent assem-blages. Representative mam-mals that became extinct at theend of two vadh C climatic cy-cles (Kimballian and Irvingto-nian) in North America. Theseintervals are 7 Ma apart. Modi-fied from Martin 1985: Fig. 4

14

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such examples can be demonstrated. The most strikingexample is the repetitive evolution of dirktooths (Martin1985; Fig. 1B), but the whole catlike community is in-volved, with scimitartooth and leopard ecomorphs be-coming extinct and re-evolving in the same dominanceturnover pattern (Fig. 2C). This pattern can also be seen indog and hippo ecomorphs (Meehan and Martin 2003), aswell as in dominant artiodactyl herbivore ecomorphs(Martin 1985) and shrew ecomorphs (Fig. 2A, D). Thestarting point for these radiations is usually a combinationof survivors (of the previous extinction event) and im-migrants, as Olson (1975) described in chronofaunalsuccession. The resemblance between ecomorphs isgreatest among taxa at the end of evolutionary sequencesrather than at their beginnings. For instance, Barbouro-felis fricki, a lion-sized carnivore, is very similar to itslion-sized ecomorph Smilodon fatalis, but less so to theSmilodon ancestor Megantereon that is closest to Bar-bourofelis in time. We would infer from this pattern ofsuccession that competition was an unlikely contributor tothese extinction events; instead we find that ecologicalreplacement is a fundamental pattern of the fossil record.

Numerous lines of evidence indicate that environ-mental parameters fluctuate globally throughout Earthhistory. In many cases these fluctuations reflect changesin global heat and water balance. Extinctions have oftenbeen associated with declining temperatures and in-creasing aridity. Increased temperatures and moisture arereflected in increased species diversity and communitycomplexity. Although this pattern has been observedglobally through most of the geologic record, its detailsmay be best observed in the well-preserved and well-studied North American terrestrial Cenozoic. The mostcharacteristic part of this pattern is the concordant ex-tinction of a variety of organisms followed by the reap-pearance of the same ecomorphs in subsequent intervals.This phenomenon is not ambiguous, extends acrosscommunity structure, and is largely independent of phy-logenetic relationships. Only climate can simultaneouslycontrol evolutionary patterns in so many diverse and oftenphylogenetically distant organisms. This interpretation isfurther supported by the consistency of evolutionary re-sponses across continents to what must be a global trendin environmental change. If ungulates show adaptationsconsistent with cooler, more open habitat, so will rodents.It is the common climatic signature that makes recog-nizing global epoch and era boundaries among such dis-parate groups as molluscs, pollen, and mammals possible.

In most cases, extinction is not random, but tends to beof similar scope and affects similar ecomorph types ineach episode. For this to be true, these ecomorphs wouldhave to re-evolve time after time. That this is true is oneof the most remarkable facts that we can ascertain fromthe fossil record. It may be easy to think of some reason,real or imagined, that could result in the extinction of aparticular lineage, but it is more difficult to understandhow following an extinction, the same ecomorph couldre-evolve almost immediately—often from an unrelatedlineage. That this happens many times in the geological

sequence can only be taken as evidence that a controllingenvironmental factor (climate) is fluctuating from one setof parameters to another and then back again in a geo-logically short period. It is less easy to demonstrate thatthis pattern is truly periodic, as has been implied for manyof the intervals where it is recognized. Unfortunately, thepaucity of radiometric dates bearing on this questionpresently prevents a resolution. It should be rememberedthat the various dating methods often vary amongstthemselves when dating the same sample and that samplesusually date volcanic events rather than biostratigraphicboundaries so that radiometric ages are younger or olderthan the event they are supposed to date. Even with thesecaveats, the subcycle/cycle system of triplets first pro-posed by van der Hammen (1957) and extended by Martinand Meehan (2002) into vadhs and stouts, predictsboundaries that agree with the various time scales for theNorth American terrestrial Cenozoic as well as these timescales agree with each other (Table 2). Their agreementwith the marine epochal boundaries is even more striking(Table 1). In general vadhs and stouts are comparable tothe durations of marine zones and stages. If in fact thisperiodicity is genuine, it severely limits the possiblecausal mechanisms. A truly regular mechanism is likelyto be astronomical, and this may include varying solarmechanics and heat output. If the time intervals are morevariable, they may reflect a cycling feedback system in-volving some factor such as atmospheric carbon dioxide.In any case, climatic cycles appear to form the ultimatebasis of biostratigraphy and have a controlling effect onthe 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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