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The Great American Biotic Interchange: Patterns and Processes Author(s): S. David Webb Source: Annals of the Missouri Botanical Garden, Vol. 93, No. 2 (Aug., 2006), pp. 245-257 Published by: Missouri Botanical Garden Press Stable URL: http://www.jstor.org/stable/40035724 . Accessed: 08/04/2014 23:14

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This content downloaded from 137.111.226.20 on Tue, 8 Apr 2014 23:14:05 PM All use subject to JSTOR Terms and Conditions THE GREAT AMERICAN BIOTIC S. David Webb2 INTERCHANGE: PATTERNS AND PROCESSES1

Abstract

Whenthe Panamanianland bridgewas emplacedabout 2.7 Ma, it triggeredthe GreatAmerican Biotic Interchange(GABI), a major mingling of land faunas between North and South America. Four families of northern immigrants (Procyonidae,, Tayassuidae,and )diversified at moderaterates, while four others, , Mustelidae, Cervidae, and especially Muridae, evolved explosively. As a consequence, half of living South American genera are descendantsof northernimmigrants. The other major consequence of the interchangewas the conquest of tropical North Americaby immigrantsfrom Amazonia, an episode that justifies the term NeotropicalRealm. Key words: biostratigraphy,evolutionary rates, isthmianland bridge, ,Neotropical Realm.

Resumen

Cuandoel corredorterrestre panameno se ubico hace cerca de 2.7 Ma, desencadenoel GranIntercambio Biotico Americano (GABI),una mezcla importantede las faunas de mamiferosterrestres entre Americadel Norte y del Sur. Cuatrofamilias de inmigrantesdel norte (Procyonidae,Felidae, Tayassuidae,and Camelidae)se diversificarona un ritmomoderado, mientras que otras cuatro, Canidae, Mustelidae, Cervidae y especialmente Muridae, evolucionaron en forma explosiva. Por consiguiente, la mitad de generos suramericanosactuales son descendientes de inmigrantesdel norte. La otra principal consecuenciadel intercambiofue la conquistade Norteamericatropical por inmigrantesamazonicos, un episodioque justifica el terminode Reino Neotropical.

The rootsof the LatinAmerican biota can be traced living faunas, along with their predecessors, down throughthe epochs of earth history to several recordboth the rapidlychanging distributions and the formativechapters. During most of the MesozoicEra, dynamic evolutionarydiversifications that illuminate the South Americanbiota was an integral part of the the origins of the Latin Americanbiota. Gondwananbiota. Throughmost of the CenozoicEra, My own introductionto the nature of the GABI the terrestrialand freshwaterbiotas of SouthAmerica began in the 1960s when the Florida Museum of were isolated from those of and all NaturalHistory was actively filling chronologicalgaps other continents by deep ocean troughs. The most in that state's rich late Cenozoic record of land recent chapterbegins with the GreatAmerican Biotic vertebrates. One fossil site in particular opened Interchange (GABI). This occurred approximately a critical window into the late , which is three million ago during the late Pliocene, knownin the system of NorthAmerican land mammal when the powerfulforces of plate tectonics raised the ages as the Blancan. Unlike any precedingstage, that isthmianland bridge in a final phase of upliftingthe intervalintroduced to NorthAmerica a large cohortof northernand southerncordilleras to connect them as land mammalspreviously restricted to SouthAmerica. the backboneof the Americas.Such dramaticphysical Our site, Inglis 1A (Fig. 1), yielded the richest changes inevitably triggered major new biological sample of late Pliocene vertebratesin eastern North interactions between the two previously separate America. Our team excavated and screenwashed Americancontinental biotas, and that is the focus of about 100 tons of fossiliferous sediment, which this paper. yielded about 120 of land and freshwater In the following pages, I consider the major . Early in our studies, I realized that ten evolutionaryfeatures of the GABI as registered by genera of new immigranttaxa from South America land mammals.The mammalsoffer the richest, most accounted for about 20% of the entire rich fauna nearly coherent record of faunal changes in both (Webb, 1976). There were three families of ground American continents during the late Cenozoic. The ; three families of shelled edentates, ranging

1 1 thank Peter Raven and Alan Grahamfor inviting me to participatein the 51st Annual SystematicsSymposium at the MissouriBotanical Garden. I am also gratefulto manycolleagues who have expandedmy perspectivesin both biologicaland geological sciences, in particularR. H. Tedford, M. C. McKenna,B. J. MacFadden,the late J. F. Eisenberg, and the participantsin our symposium.This paper is ContributionNo. 575 fromthe FloridaMuseum of NaturalHistory. 2 FloridaMuseum of NaturalHistory, University of Florida,Gainesville, Florida 32611, U.S.A. [email protected] Ann. Missouri Bot. Gard. 93: 245-257. Published on 23 August 2006.

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Figure 1. Paleontologicalexcavations by the FloridaMuseum of NaturalHistory at Inglis 1A (late Pliocene)at cross-state barge canal, west-centralFlorida. Photo by author. fromtiny Dasypusto gigantic "\Glyptotherium3;as well esis on an intercontinentalscale. We may ask how the as two families of ,namely Erethizontidaeand modern South American fauna differ from the pre- Hydrochoeridae.The truly surprising forms were ceding fauna living in isolation.Likewise, we may ask a vampire bat, Desmodus Wied, and a giant pre- how the present CentralAmerican fauna differ from daceous named "\TitanisBrodkorb. Additionally, the preceding fauna that had lived in the southern nearly 40% of the fauna at Inglis 1A represented portion of North America. Clearly, the land bridge NorthAmerican genera, representativesof which had catalyzed a rapid remodelingof the Latin American dispersedto South Americaduring roughlythe same fauna. Such geological changes represented the time in the late Pliocene. Therewere relativesof such underlying cause that triggered major biological living Neotropicaltaxa as llamas, peccaries, , effects. jaguars, raccoons, foxes, and spectacled (cf. We begin by indicating some preliminary land Table 1 for taxa).Thus, a majorityof the land mammal mammaldispersals that precededthe GABI.I referto faunarecovered from Inglis 1A, and living in Florida these as herald taxa. Thereafter,we will consider the nearly three million years ago, were participants,in much larger cohorts that burst across a fully acces- one direction or the other, of the GABI. I was also sible Panamanianland bridge, which I refer to as astonished to realize how similar the mingled legions taxa. We also briefly review current geo- elements of the Inglis 1A local fauna were to chronological evidence regardingthe timing of the contemporaneousinterchange faunas through the GABI. Finally, we will consider evolutionary and Americantropics and all the way into Argentinaand ecological factors that influenced the origin of the the "southerncone" of the continent.Thus, in Florida South and CentralAmerican land mammalfaunas. we had stumbled fortuitouslyinto the acme of the GABI(Webb, 1976). Herald Taxa The interamerican evolution of land mammals representsa dramaticexperiment in rapid cladogen- A very small number of interamerican land mammaldispersals have been recorded earlier than 3 f representsextinct taxa. the latest Pliocene in Northand SouthAmerica. These

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Table 1. Families of land mammalsin the GABI. the of Mesoamerica "show strict North Americanaffinities." Family Commonname According to present records, the herald taxa Northernlegion taxa (17 families) consist of only two distinct genera of ground sloths Soricidae shrews in North America and one of large raccoon in Leporidae rabbits SouthAmerica. As indicatedby Tedfordet al. (2004), Heteromyidae pocket mice "\ThinobadistesHay, a mylodontidsloth, and "fPlio- Geomyidae pocket gophers metanastesHirshfeld & Webb, a megalonychidsloth, Sciuridae squirrels arrived in the early Hemphilllian about 9 million Muridae field mice years ago (Ma). One record of "fPliometanastesfrom Felidae cats Californiayields the best age estimatefor these early skunks and otters Mustelidae Thereit occursin sediments4 Canidae foxes and wolves immigrant genera. meters below the MehrtenTuff, which is radiometri- Procyonidae raccoons Ursidae bears cally dated at 8.2 Ma (Hirschfeld& Webb, 1968). Gomphotheriidae elephantoids "\ArctonasuaBaskin is a large procyonid, well Tapiridae tapirs knownin NorthAmerica during the Clarendonianand Equidae horses (Baskin, 2003). "fCyonasuaAmeghino, Tayassuidae peccaries a closely related genus, appears in the Chiquimil Camelidae llamas fauna of northwesternArgentina in the Cervidae deer land mammalage, middle to late Miocene (Marshall, Southernlegion taxa (2 1 families) 1985; Flynn & Swisher, 1995). By Chapadmalalan Didelphidae opossums time, "\Cyonasuahad been replaced by its very large Dasypodidae descendant,"\Chapalmalania Ameghino. Chlamytheriidae giant armadillos Flynn et al. (2005) suggested that two additional tank-like edentates Glyptodontidae genera of South American ground sloths separately -sized sloths ground invaded NorthAmerica. This suggestionis based on middle-sizedground sloths late Hemphilliancollections fromnear Guanajuatoin Megatheriidae elephantineground sloths central Mexico. It be more parsimonious, Bradypodidae three-toedtree sloths may to view the two identified as however, genera, Desmodontidae vampirebats "\MegalonyxLeidy and ^GlossotheriumHarlan, as Callithricidae marmosets North American descendants of the closely related Cebidae New Worldmonkeys sloth taxa already present in the early Hemphillian. Hydrochoeridae capybaras The question may be resolved by more detailed Erethizontidae porcupines analysis of the Hemphillian sloth material from Caviidae guinea pigs Guanajuato. Agoutidae pacas For three reasons, the appearancesof these herald Dasyproctidae agoutis taxa have been interpretedas waif dispersals, not as spiny rats Echimyidae of a continuous land the -likeungulates crossings bridge. Firstly, Trichechidae sea cows hiatus of some six millionyears, during which no other Phororhachidae giant predaceousbirds crossingshave been documented,suggests a fortuitous mode of island hopping. Secondly, living sloths and raccoons are particularly adept at floating and herald taxa appear during the middle Miocene some swimming, so that they are among the most likely six or seven million years earlierthan the legion taxa. groups of land mammals to make water crossings Both Mexico and CentralAmerica have increasingly (Webb, 1985). Thirdly, the very limited number of strongrecords of late Cenozoicland mammals,yet in other concurrentarrivals in either directionprovides those areas no SouthAmerican immigrants other than strong negative evidence that no broad highwayhad the heraldtaxa have been recognizedbefore the latest opened between 9 and 3 Ma. The strength of this Pliocene (Webb, 1997; Ferrusquia-Villfranca,2003). interpretationdepends on one's optimism about the Some native North American groups (e.g., the completeness of relevant parts of the fossil record. slingshot-horned Protoceratidae)that had become Suffice it to state that the late Cenozoicrecord of land increasingly rare at temperate latitudes evidently mammalsin Northand South Americais exceedingly thrivedin the more tropicallandscapes of Mesoamer- rich and continues to improveeach . ica (Webb et al., 2003). As stated by Ferrusquia- Occasionally,one reads that the muridrodents also Villfranca(2003: 321), all known mammalfaunas in jumped the isthmiangap and entered South America

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before the latest Pliocene. One early paper by mutual enrichmentof both continental faunas, they Marshall(1979) encouragedthe idea of some mid- encounter limits to diversity, a kind of carrying Tertiary murid immigration,even though the word capacity that limits the number of broadly similar "model" in the title made it quite clear that his mammaliangroups that one continentcan support. discussionwas hypothetical.In their discussion of the timing of the GABI at about 2.7 Ma, Woodburneand Chronologyof the Interchange Swisher(1995) reiteratethe possibilitythat two murid genera had reached South America during the The reciprocal arrival of a cohort of terrestrial Montehermosanstage, generally correlatedwith the mammal immigrantsdeep within each of the two latest Miocene and earliest Pliocene (ca. 7 to 4 Ma). American continents marks the inception of the The supposedrecords that they cite (by Reig, cited in interamericanland bridge and a major faunal in- Marshall,1985), however,were not explicit and have terchange. It is important to date the GABI as not been verified by subsequent faunal and strati- precisely as possible, because it representsthe datum graphic studies. Indeed, in his review of fossil murid by which ensuing evolutionary and biogeographic recordsin the Pampeanregion of Argentina,Pardinas changes can be calibrated. (1995: 229) finds the stratigraphicprovenance of The best method to date emplacement of the Reig's two type specimens to be "dubious." Panamanianland bridge comes, perhapssurprisingly, An additionalstrong inference comes frompaleon- not from any geologic data in Panama but from tological studies of muridsin Miocene-Pliocenesites excellent stratigraphic sequences with rich fossil in NorthAmerica. There the presence of appropriate faunas in temperate latitudes of North and South plesiomorphicsister groups such as 'fProsigmodon America.Only a few examples of this paleontological Jacobs & Lindsayand "\BensonomysGazin, just prior record need be cited here to establish the quality of to the time of the interchange,strengthens the view the recordand the basic chronologicalframework. that these lineages did not jump the gap prematurely. The Anza-Borrego Desert lies in southernCalifor- Jacobsand Lindsay(1984), for example,make a strong nia, just northof the Salton Sea Basin and within the case for Miocene-Pliocenediversification of muridsin San Andreas Fault zone. Sediments in that region North America followed by dispersal of multiple accumulated very rapidly during the Pliocene and branchesduring, but not before, the Blancan GABI. , first entombingmarine within the ImperialFormation, an arm of the Gulf of California, LegionsTaxa and later, non-marinevertebrates and their trackways within the Vallecito Creek Formation. The latter Table 1 recordsthe families of land mammalsthat formation provides a wealth of land mammals, moved in each direction across the land bridge. In including early appearancesof some South American additionto includingland and freshwatermammals, I immigrants,notably "\Erethizonstirtoni (White) Fra- have included the f Phororhachidae,a family of large, zier, in a vertical sequence of some 4000 meters. predaceousbirds that followed some of their favorite Furthermore,these fossil beds include a radiometric mammalianprey northwardacross the land bridge. date of 2.3 Ma and are directly intercalated with The record is based on "\Titanisfrom Inglis 1A and a long, detailed paleomagneticprofile (Opdykeet al., other Blancan sites in Florida. These data indicate 1977). Figure 2 exemplifiesthe outstandingexposures a balancedreciprocal faunal interchange,as noted by of long fossiliferous sections in the Anza-Borrego Webb (1976), Webb and Marshall (1982), and Desert. Marshallet al. (1982b). The body of paleontological An equivalent fossiliferous section in North evidence also indicates that the mingled fauna on America, in Arizona, known as the 111 Ranch each Americancontinent supported a greaterdiversity Sequence, produces the Tusker Fauna, which is than before the GABI. This increase in apparent associated both with an ash dated at 2.33 Ma and diversitylasted about a half a million years before it an excellent magnetic profile (Galushaet al., 1984). decreasedto its priorlevel (Webb, 1976; Marshallet Similarly,in southwesternNew Mexico, local faunas al., 1982b). Wilson (1992: 120) explains this bio- from the lowermost strata in the Mesilla Basin geographicpattern as follows: "When biologists see (MesillaA in the CampRice Formation)and Pearson a numbergo up followinga disturbanceand then fall Mesa clearly tie South American immigrantsinto back to the originallevel, whetherbody temperature, magnetostratigraphicallycontrolled sections (Morgan densityof bacteriain a flask, or biologicaldiversity on & Lucas, 2003). a continent, they suspect an equilibrium." The In each of these southwesternexamples, the new interchangenumbers neatly fit a large-scale example immigrants occur within an interval of normally of the species equilibriumhypothesis. After the initial orientedmagnetic samples, constrainedabove by the

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Figure 2. Vallecito CreekFormation Pliocene-Pleistocene exposures in Anza BorregoState Park,California. Dr. JohnA. White indicatingcollecting areas of Los Angeles CountyMuseum. Photo by author. radiometricdate and the Gauss/Matuyamamagnetic species withinits temperatesister genus, "\, reversalboundary (fixed at 2.58 Ma)and below by the yet it possesses triangular(plesiomorphic) caniniform Kaena Subchron(at 3.04 Ma). On this basis, mam- teeth (Webb & Perrigo,1985). malian stratigraphersoften cite the time of first Intensive geochronological and biostratigraphic appearance for Neotropical immigrants into North studies of sedimentary sequences near Guanajuato America as 2.6 or 2.7 Ma (Woodburne& Swisher, in central Mexico record several immigrantgenera 1995; Bell et al, 2004). from South America earlier in the Blancan than the The foregoingfaunas fromthe southwesternUnited well-datedsouthwestern faunas cited above (Miller& States that most concisely date the first appearances Carranza-Castaneda,2001; Flynn et al., 2005; fall within the late Blancan land mammalstage. This Montellano-Ballesteros& Jimenez-Hidalgo, 2006). same biostratigraphicrubric includes several Florida 'fPlaina, a small sister genus of "\HolmesinaSimpson, faunas,most notablythe Inglis IA site, which records is recordedat about 4.6 or 4.7 Ma, in the very early the greatest wealth of Neotropical immigrantsfrom Blancan. ~\Glyptotheriumand "\Neochoerusappear in any one locality. The unfortunateabsence of radio- the interval between 3.9 and 3.1 Ma (Flynn et al., metric controlon Floridafaunas weakens our ability 2005). This may suggest, as proposedby Flynn et al. to specify how concurrently the entire cohort of (2005), that central Mexico represented a different Blancan immigrantsfrom South America arrived in mammalianprovince than southwesternUnited States. temperateNorth America. It is reasonableto suggest It is possible that some Florida Blancan faunas, thatthey had all come withinabout a two-million-year notably Haile 15A and Santa Fe River 1, producing period,for that is the approximatespan of the Blancan these and other immigrantland mammalsfrom South interval(Bell et al., 2004). America,may also pertainto the early Blancan.These Some evidence of Blancan immigrantscomes from faunas are not well enough constrained by geo- lowerlatitudes in Mesoamerica.One unique genus is chronology,and it is notoriouslydifficult to distin- "\MeizonyxWebb & Perrigo from El Salvador.This guish early from late Blancan biostratigraphically megalonychidground sloth is largerthan any Blancan (Bell et al., 2004). The new discoveries of earlier

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Figure 3. Barrancade Los Lobos, Buenos Aires Province,Argentina, Pliocene-Pleistocene exposures. Photo by author.

Blancan immigrantsin Guanajuatoindicate that the abstract.Based on presumedcorrelations to sediments legion taxa may have reached temperate North underlyingan ash date of 9.01 Ma in the Madrede America on a more haphazardschedule than pre- Dios Formation in eastern Peru, these authors viously suggested. recognize "numerousAmazonian paleofaunas"that Criticalevidence fromsouthern, temperate parts of include "at least two species each of proboscideans, South America produces results broadly similar to peccaries, tapirs and camelids." The discrepancy those from the southwestern United States. Long between their evidence from unspecified Amazonian sequences of fairly continuousfossiliferous sediments faunas versus the wealth of previously documented, provide an essential frameworkfor integratingbio- late Mioceneland mammalfaunas in SouthAmerica is stratigraphicevidence with both radiometricdates and profound-The classical sequences at Chiquimiland paleomagneticreversal chronology(Marshall et al., CorralQuemado in CatamarcaProvince, northwestern 1982a; Flynn & Swisher, 1995). Argentina,offer a wealth of excellent fossil mammals A central part of Barrancade Los Lobos near Mar typifying the Huayquerian land mammal . del Plata in Argentina (Fig. 3), along with other Additionally,rich faunas from Micana in the eastern typical Uquian sites in the provinceof Buenos Aires, altiplano of Bolivia also span relevant, late Miocene records a number of first appearances of North intervals (see recent references in Flynn & Swisher, American taxa, including equids, mustelids, tayas- 1995). Yet the only hint of any North American suids, camelids, and murid rodents (Pascual et al., element in any of these well-studied faunas is 1985; Alberdi et al., 1995). Paleomagnetic work, "\Cyonasua,discussed earlier from the Chiquimil integratedwith land-mammalbiostratigraphy, places fauna from Argentina (Marshall, 1985; Flynn & these northern immigrantsjust below the Gauss/ Swisher,1995). Even the next youngerChapadmalalan Matuyamaboundary, justifying a first appearance and/or Montehermosanmammal ages give no hint of datumof about 2.5 Ma (Marshallet al., 1982a), later the mysteriousimmigration proposed by Campbellet revised to about 2.7 Ma (Woodburne& Swisher, al. (2000). In apparentanticipation of such skepticism, 1995). these authors claim that "ecological restrictions A curious claim of a much earlier immigrationof undoubtedlyhindered the movementof the earliest northernland mammalsinto South Americahas been dispersersout of lowlandtropical forests" (2000: 33A). advancedby Campbellet al., (2000: 33A) in a brief This ad hoc defense of such a novel hypothesis

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underlines its improbability. It would be quite southern immigrantssurvive, namely Didelphis L., astonishingif eight or more species of large, mostly DasypusL., ErethizonCuvier, and TrichechusL. herding herbivoretaxa had remainedsequestered in southeasternPeru for six or more million years. Why Did Northern Taxa Succeedin South America? Recently, the assertion of Campbell et al. (2000) received minor encouragementfrom Ferrusquia-Vil- This strikingasymmetry in the results of the GABI lafranca(2003) on the groundsthat three of the four requires explanation. In particular, the immense family groupsin question ("fGomphotheriidae,Tayas- success of northern immigrantsin South America suidae, and Camelidae) are known in the middle representsone of the greatestnatural experiments in Miocene of Mesoamerica.This might suggest that rapid evolution on a large scale. The most cogent these three family groups could have been available general hypothesis may be that the northerngroups for their supposed early dispersal into one corner of that spread into South America had a long, wide- the AmazonBasin. Such a charitable view does not ranging history not only in North America, but also relieve those who would hypothesizea much earlier before that in Eurasia.This cosmopolitanbackground dispersal by a novel, geographicroute from the need strongly contrasts with the long Cenozoic isolation to providemore substantialevidence. experiencedby the pre-GABISouth Americanfauna. A particularlyintriguing part of this inequityis the Later Featuresof the Interchange presence among the northern legions of efficient mammaliancarnivores. In SouthAmerica, by contrast, After the early events of the GABI, with balanced the only mammalian carnivores were primitively dispersals and augmentedfamilial diversity in both modified membersof the marsupialfamily, Borhyae- continental faunas, the evolutionary pathways of nidae. The group had declined markedlybefore the immigrant land mammals in the two American interchange.It seems evident that the few remaining continentsdiverge quite dramatically.Evidently, the taxa could not compete with progressivecarnivorans GABI conformedto the balanced mutualenrichment, that rapidly spread into their native continent. predicted by the species equilibrium hypothesis, Furthermore,the large and small herbivoresof South during the first million years, within an ecological American descent, lacking any previous experience time frame. Thereafter, however, within a more with advanced mammalian carnivores, were over- extended evolutionarytime frame, the northernand whelmed by the rapid onslaught of wolves, jaguars, southern legions embarked on radically different sabercats,and manysmaller kinds of carnivoresin the evolutionarypathways. families Felidae, Canidae,and Mustelidae. In SouthAmerica, the mostremarkable result of the To place the GABIin a broadercontext, let us turn GABI is the rapid diversification of many of the brieflyto the earlierand morediffuse intercontinental immigrantsfrom the north. In each successive stage, interchange between Asia and North America. the fossil record throughoutthe continent reflects Table 2 lists the times and generic numbers of a continual increase in the numbersof taxa derived immigrantcohorts that entered North America from fromthe first wave of immigrants.Webb and Marshall Asia. These data summarizerecent tabulations for (1982: 50) quantified this trend by a census of the Miocene land mammalsby Tedfordet al. (2004). Of modernmammalian fauna at the generic level. They particularinterest in this context are the several sets found that more than half (about53%) of the present of immigrantsthat reached the New World in the South American land mammal fauna consisted of middle to late Miocene.The greatestof these episodes taxa that had entered the continent by crossing occurred about 19 Ma (middle Miocene), when 17 the isthmianland bridgeless than three million years Eurasiangenera are recordedas new arrivalsin this ago. continent.In Woodburneand Swisher's(1995) similar This result becomes even more notable when one codificationof Cenozoic immigrationevents in North turns to the North Americanrecord and follows the America, this is InterchangeEvent ^6. Two million very different evolutionaryfate there of immigrants years later, another large wave of immigrations fromSouth America. Little or no diversificationtakes appeared in InterchangeEvent #7 (Woodburne& place. Some genera may be consideredquite success- Swisher, 1995). A particularlyimportant member of ful by some measures. For example, "fMegalonyx, that cohort was "\CopemysWood, a probable de- a bear-sizedground sloth, evolved fairly rapidly and scendant of a Eurasianmurid such as "fDemocriceto- extendedits rangevery widely, even reachingAlaska. don Fahlbusch. The future impact of this North However, none of the South American immigrants Americanimmigration event with respect to the GABI diversifiedabove the species level. In the recent fauna surely could not have been anticipated.Nonetheless, of temperate North America, only four genera of one epoch later, when a few inconspicuousdescen-

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Table 2. Miocene immigrantsto North America from able interpretations of their dental adaptations and on Asia.* the habits of their living relatives, required relatively mesic habitats with year-round provisions of nutritious No. of Selected Age (Ma) genera genera** browse, fruit, or seeds. 6 7 Lutra(Mustelidae), By the beginning of the Pliocene, the ecological "\Eocoileus(Cervidae), valences of immigrants from Asia began to shift "fMegantereon(Felidae), toward forms adapted to cold steppes. Such grazers as "fTrigonictis(Mustelidae) 'fMammuthus Brookes, f Bison H. Smith, and diverse 7 8 Felis (Felidae) microtine rodents most of North 8 9 spread widely through -fPlionarctos(Ursidae) America but were not involved in the 9 6 subsequently 12 2 GABI. Evidently, they were too late to avail themselves of an route the 15 9 "\Gomphotherium open-country through (Gomphotheriidae) isthmian region. There is good evidence that "\Mam- 16 2 muthus, during the , and f Bison, in 17 11 "fCopemys(Muridae) the latest Pleistocene, extended their ranges south- 19 17 ward along the relatively dry Pacific terrain into 20 4 Honduras and Nicaragua. These areas today support 23 6 extensive pine savannas and thorn scrub, especially * Figurescompiled from Tedford et al. (2004). along the seasonally drier Pacific slopes. Beyond that, ** See text. however, these grazers did not penetrate, presumably t Includes both fossil and living genera. because they were blockaded by the prevalent rainforest (Webb & Perrigo, 1984; Webb, 1997). dants of these murid rodents colonized South America, The purpose of this digression into Holarctic faunal they produced by far the greatest monofamilial movements is to show that the Bering Strait had an diversity of land mammal genera in that continent. important effect on the GABI. Clearly, many groups of The next middle Miocene immigration episode land mammals that joined the legion taxa from North introduces a taxon that is far removed from extremely America had previous evolutionary records in the murid rodents, the first in the namely, proboscidean World Continent. We suggest that this background New World. Out of Africa of Asia came the by way may help explain their success in South America. Burmeister. New elephantoid genus "fGomphotherium More than two million years after the GABI, murid World descendants of this basal member of the family rodents, cervid ruminants, and other northern families diversified in Central Amer- Gomphotheriidae greatly with similar backgrounds burgeoned into more than ica the South America. and, following GABI, half of the genera of modern South American a mid-Miocene the late Miocene in Following lull, mammals (Webb & Marshall, 1982). Wilson (1992: North America witnessed another series of strong 130) offered the following eloquent explanation: "The from Asia. New immigration episodes immigrant World Continent . . . has tested more evolutionary included the first New World Eocoileus genera deer, lines, built tougher competitors, and perfected more otters of the modern Webb; genus Lutra Bliinnich; defenses against predators and disease. This advan- a "\TrigonictisHibbard, large extinct mustelid more or tage has allowed its species to win by confrontation. less closely related to the living tropical genus Eira They have also won by insinuation: many were able to (Hamilton) Smith (the tayra); and "\Plionarctos Frick, penetrate sparsely occupied niches more decisively, the oldest known tremarctine (spectacled) bear, radiating and filling them quickly. With both presumably an early sister-genus of the living confrontation and insinuation, the World Continent Neotropical Tremarctos Gervais. Finally, two immi- mammals gained the edge." gration events occurred involving the large cats: Felis L. and "fMegantereonCroizet & Jobert, which is the Evolutionary Patterns of Northern Interchange Taxa probable antecedent of "fSmilodon Lund, the great sabercat of the Pliocene-Pleistocene. All eight of To develop a full understanding of how the legions these Miocene immigrants contributed key elements of land mammals from the north realized their full to the North American cohort during the GABI. evolutionary potential in South America remains Evidently, these Miocene immigrants extended a great challenge. More than a century of dedicated their ranges through the polar latitudes of the Bering paleontological spadework on both American con- Strait before climatic deterioration produced extreme- tinents has provided a reliable framework in two ly cold, dry conditions. Virtually all of the omnivores, respects. Firstly, it has identified the set of 17 families frugivores, and herbivores involved, based on reason- of land mammals (Table 1). Secondly, it has de-

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termined a fairly well-dated beginning point for Great Plains of North America to the Pampas of reciprocalimmigrations of legion taxa between about Argentinaduring the late Pliocene. 3.1 and 2.7 Ma (Webb, 1985; Flynn et al., 2005). The most controversial part of this supposed Yet, from an evolutionaryperspective, this is just savanna highway is the isthmian portion. In their the beginningof the story. The other end of the story comprehensivereview of the complex late Cenozoic has also been well wroughtby several generationsof history of Neotropical vegetation, Burnham and mammalogistsworking out the modern systematics, Graham(1999: 560) grant that "fossil plant data are ecology, and distribution of Neotropical mammal generally consistent with estimates of habitats (sa- groups.Taken together,these basic facts imply some vannas)and climate (temperate)based on mammalian of the most dynamic examples of mammalian fossil faunas, but with some differences."It may be evolution on any continent within the entire Age of necessaryto arguefor the GABIsavanna by calling for Mammals.However, most of the real phylogenetic relatively short-lived rain shadows during the late historyof these groupsstill remainsto be told. Pliocene. GABI data do not conflict with younger Presumably,the opening of a new continent after evidence indicating that broad belts of rainforest long isolation,accompanied by wholesaleintroduction probablydominated the region duringmost, if not all, of new kinds of mammals,provides a perfect theater of the Pleistocene (Colinvaux,1997). for rapid, innovativeevolution. The diverse natureof In South America, the remarkableradiations of topographic and ecologic opportunities in South northernimmigrants, briefly outlined below, moved America was already evident in the mid Tertiary, along similarecogeographic lines. Marquetand Cofre especially after the uplift of the Andes (Flynn & (1999) conducted detailed analyses of South Ameri- Swisher, 1995; Burnham & Graham, 1999). This can mammal diversity partitionedinto ten biomes. grandpanorama of opportunitiesmay have expanded Their results find northernimmigrant taxa dominant even morebroadly after the GABIas a consequenceof in the following three biomes: temperategrassland, increased climatic and sea level fluctuationsduring cold winter desert, and mountainsystems. the Pleistocene. Continuingsystematic studies of each of the South The basic fossil mammal data from the late American phylogenetic lines promise to fill in the Pliocene also permit an ecological generalization detailed patterns of their deployment across the about the availability of an open country route. At continent during the Pleistocene. Molecularstudies the time of the GABI,the isthmianregion was broadly provide a particularlyimportant set of independent accessed by herds of grazers and browsers (Webb, evidence. Based on the degree of its generic di- 1991). The legions of the north were primarily versification,each immigrantfamily may be assigned populatedby such large herbivoresas horses, llamas, a bradytelic,horotelic, or tachytelic rate of phyloge- and deer. An especially significant role may be netic evolution(Table 3). The nine bradytelicfamilies attributedto gomphotheres;presumably they modified are Soricidae, Sciuridae, Heteromyidae,Geomyidae, the landscapeby clearingtrees, especially duringdry Leporidae,Ursidae, Gomphotheriidae,Tapiridae, and seasons, much in the manner of African elephants Equidae.Five of these families still consist only of the today. same genus that entered the continent. The four Likewise,a majorityof the southernimmigrant taxa families exemplifying intermediate (horotelic) rates reflect the same set of open landscapes. The analogy are Procyonidae,Felidae, Tayassuidae, and Camelidae. is weakened somewhat because most of the key Withnine or ten generaeach, Canidae,Mustelidae, and families of large herbivores lack living relatives. Cervidaeexemplify rapid (tachytelic)taxonomic evo- Nonetheless, one can reasonablyimpute to toxodonts lutionfollowing the GABI.The fourthtachytelic family, the role of rhinocerotidsand confirm it with carbon the Muridae, exhibits truly explosive taxonomic isotopic data. Three or four distinct families, broadly evolution, producing dozens of genera and several brigaded as ground sloths, included grazers, mixed tribes uniquelydifferentiated in SouthAmerica. feeders, and browsers.The tank-like glyptodontsare The dazzlingdiversity of NeotropicalMuridae and generally perceived as herding grazers of savanna their interrelationshipscontinue to challenge sys- settings. In the southern set, there were also some tematists. These field mice experienced multiple aquatic herbivores,namely the Hydrochoeridae(ca- diversificationsin southern deserts, in tropical low- pybaras)and the Trichechidae(seacows); both groups lands, and in Andean uplands. The sense of their were grazers, the former arrayed along lowland succcess everywhereis captured nicely by Pearson waterways and the latter surely moving along the (1982: 280) in his work on small mammalsof the coast. In general, as emphasized by Webb (1978; altiplanoand desert regions of Peru, whereinhe cites 1997), the GABI data imply a broad highway of the Muridaeas "a tributeto the evolutionaryferment savanna and open woodlandthat extended from the in South America."

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Table 3. Generic diversification among northernland endemics, Hipppocamelus Leuckart and Pudu Gray, mammalsin South America. are shown to be members of the tribe Rangiferini (as defined by Webb, 2000) with an extinct sister taxon, No. of Family genera f Navahoceros Kurten, in the southwestern parts of Bradytelic temperate North America. This tribe of mountain deer Soricidae 1 had already diverged in North America from Mazama Sciuridae 3 Rafinesque, Ozotoceros Ameghino, and Blastocerus Heteromyidae 1 Gray, members of the tribe Odocoileini (as defined by Geomyidae 1 Webb, 2000) before their separate southward dis- 1 Leporidae persals. It seems likely that there were three or more Ursidae 2 separate entries of what are presently South American tGomphotheriidae 3 deer across the Panamanian land bridge. Thus, the Tapiridae 1 issue of Central American diversification and Equidae 3 staging of northern groups must be considered in phylogenetic Horotelic analyses of South American immigrant groups. Procyonidae 6 Felidae 4 A Southern Success Story within the American Tropics Tayassuidae 4 Camelidae 5 The great success of the northern immigrants in Tachytelic South America has been well documented by Canidae 10 in Andean Mustelidae 9 paleontologists working localities, Argen- Cervidae 9 tina, and other parts of temperate South America. Muridae 46-60 Those efforts, however, largely miss the contrary success story in which Central America was con- f Includes both fossil and living genera. quered by the tropical fauna of South America. A few sites in tropical parts of South and Central America An important consideration that will increasingly must be more intensely developed before the full concern students of phylogenetic differentiation of paleontological perspective can elaborate on this northern mammals in South America is the of question tropical counterdispersal. how much diversification had already been accom- I like to call this episode The Central American plished in tropical North America before the GABI. Paradox. During the Miocene, Central America had As noted above, the paleontological record documents been a southern adjunct of North America, widely and that some Murid and diversity (e.g., "fProsigmodon deeply separated from northern South America by the was before the GABI in low "fBensonomys) staged Bolivar Trough. Vertebrate fossil sites in Mexico, latitudes of North America the during Hemphillian Honduras (Gracias Formation), El Salvador, and and Blancan & This means (Jacobs Lindsay, 1984). Panama (Cucaracha Formation) corroborate the pa- that molecular clock estimates of times divergence leogeographic data by producing no evidence of any murid rodents date events that among may preceded land mammals from South America (Webb & Perrigo, the actual of those branches into South America. entry 1984; Ferrusquia-Villafranca, 2003). Yet today, Baskin (2003) recently described a surprising new Central America and southern Mexico are faunisti- of differentiation: the new and example pre-GABI genus cally and floristically brigaded within the Neotropical Baskin the species "fParapotos tedfordi representing Realm. This was obvious to A. R. Wallace in his great tribe Potosinae in the procyonid middle Miocene work on biogeography (Wallace, 1876). In that classic of . This taxon is the (Barstovian) only extinct synthesis, he extended the Neotropical Realm from its member and the first recorded fossil of the Potosinae. major center in Amazonia up to about the Tropic of Without this ancient kinkajou record, it would seem Cancer. The predominant groups of mammals in reasonable to assume that modern forms developed their Central America today had their origins in Amazonia arboreal, nocturnal habits and their marvelous pre- before the establishment of the land bridge. These hensile tails as post-GABI evolutionary products of their were stalwart members of the ancient isolated fauna, present range in multistratal rainforests of the Amazon including a diversity of New World monkeys; and lowland Central America (Eisenberg, 1989). edentates, such as armadillos, anteaters, and sloths; A recent phylogenetic analysis of New World deer and hystricognath rodents. (Webb, 2000) documents the geographic complexity of Unfortunately, the critical, transitional phases of another radiation that had been thought to be purely this Neotropical success story are nearly opaque to South American (Hershkovitz, 1982). The Andean paleontologists. In essence, one can study only the

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Figure 4. Paleontologicalexcavations by UniversidadeFederal do Acre party,led by Dr. Alceu Rancy,on Rio do Acre in late Cenozoicsediments. Photo by author.

Miocene, which is too early, or the modern fauna, the many studies that demonstratethe separationand which, in some sense, is too late. It is a problem divergence of marine faunas on both sides of the familiarto any paleontologistwho has attemptedto isthmus. In general, deepwater species undergo overcomethe refractorynature of the fossil record in geminatespeciation earlier than shallow-waterforms, tropicalsettings. The pressing need in this case is to and such patterns can be demonstratedin many redoubleour effortsin primaryfield workin Pliocene- organisms both across a broad range of taxonomic Pleistocene exposures throughouttropical America. levels and also by rapidlydiverging molecular systems, Ultimately,this challenge will be answeredand this notably by mitochndrialDNA (Collins, 1996). Rapid mysterywill yield to such ongoingendeavors as those divergencebetween and Pacific descendants of Lauritoet al. (1993) in CostaRica and Rancyin the of planktonic foraminifera,such as the globigerinid western Amazon (Webb & Rancy, 1996). Figure 4 "\Globorotaliamulticamerata, indicates that the seaway illustratesone of the valuablelate Cenozoiclocalities was breaking up between about 3.6 to 3.1 Ma. The on the Rio do Acre, Brazil accessible duringthe dry importanceof this process in reorganizingoceano- season. graphiccurrents and intensifyingthe Gulf Streamwas indicatedby Keigwin(1982) and Croninand Dowsett Conclusions (1996), who also noted its probablerole in generating northern hemisphere ice sheets beginning about The causes of the GABI can be traced readily and 3.2 Ma and again around2 Ma. powerfullyto the forces of plate tectonics in lower The final emplacement of a continuous isthmian Central America. Hundreds of cubic kilometers of land bridgeis faithfullyrecorded by the appearanceof ignimbritesand other massive volcanic productions legions of land vertebrates reciprocally dispersing had alreadygreatly augmented the volume of nuclear between North and South America. Substantial Central America during the middle Miocene. The evidence from long sections in temperatelatitudes of gradualshallowing of seawaysin the isthmianregion, both continents places the GABI events between driven by persistent subductionof oceanic crust by about 2.7 and 3.1 Ma (Webb, 1985; Flynn et al., Pacificplates, had majorconsequences well beforethe 2005). final emplacementof a continuousland bridge(Cronin Duringthe first million years or so of the GABI,the & Dowsett,1996). Jones and Hasson (1985) reviewed contribution of each continent to the faunal in-

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terchangewas roughlyequal at the family level, and Baskin, J. 2003. New Procyoninesfrom the Hemingfordian each continentalfauna was taxonomicallyenriched. and Barstovianof the Gulf Coast and Nevada, including the first fossil record of the Potosini. 125-146 in L. Subsequently, by early Pleistocene time, the in- Pp. Flynn (editor), Vertebrate Fossils and Their Context: terchange, as recorded by new immigrants, was Contributionsin Honorof RichardH. Tedford.Bull. Amer. essentially completed and family-group diversities Mus. Nat. Hist. had droppedback to previous levels, in accord with Bell, C. J. et al. (+ 8 authors). 2004. The Blancan, predictionsof species equilibriumtheory. ,and RancholabreanMammal Ages. Pp. 232- 314 in M. 0. Woodburne(editor), Late Cretaceousand The northernlegion taxa experienced astonishing CenozoicMammals of NorthAmerica: Biostratigraphy and evolutionarysuccess as measuredin the modernSouth Geochronology.Columbia Univ. Press, New York. American fauna, capturing more than half of the Burnham, R. J. & A. Graham. 1999. The history of present generic diversity. When that broad record is Neotropical vegetation: New developments and status. Ann. MissouriBot. Gard.86: 546-589. partitioned, it is seen that nine families simply K. entered the continent with little or no taxonomic Campbell, et al. (+ 5 authors). 2000. Late Miocene dynamics of the Great American Waifs are diversificationabove the level Table Interchange: species (cf. 3, out. J. Vertebrate Paleontol. (abstract supplement) 20: bradytelic families). Four other families of northern 33A. land mammals evolved taxonomically at moderate Colinvaux,P. 1997. The history of forests on the isthmus from the Ice to the Present. (horotelic)rates: these include Procyonidae,Felidae, Age Pp. 123-136 in A. G. Coates CentralAmerica: A Naturaland and Camelidae.The four families that (editor), Cultural Tayassuidae, History.Yale Univ. Press, New Haven. seized the new in South really opportunities America, Collins, T. 1996. Molecular comparisonsof transisthmian evolving at tachytelic rates, were Canidae, Musteli- species pairs: Rates and patternsof evolution. Pp. 303- dae, Cervidae,and especially Muridae.It is worthyof 334 in J. B. C. Jackson, A. F. Budd. & A. G. Coates note that their success focused on the (editors),Evolution and Environmentin TropicalAmerica. ecologically Univ. biomes that most resembled ChicagoPress, Chicago. very nearly temperate Cronin, T. M. & H. J. Dowsett. 1996. Biotic and had come. to biomes from whence they According oceanographicresponse to the Pliocene closing of the Marquet and Cofre's (1999) detailed analyses of CentralAmerican isthmus. Pp. 76-104 in J. B. C. Jackson, mammaliandiversity in ten biomes, northernimmi- A. F. Budd. & A. G. Coates (editors), Evolution and Environmentin America. Univ. granttaxa are dominantin temperategrassland, cold Tropical Chicago Press, Chicago. winterdesert, and mountain systems. Eisenberg, J. F. 1989. Mammalsof the Neotropics:The A countervailingconquest of Central America by NorthernNeotropics, vol. 1. Univ. ChicagoPress, Chicago. the Amazonianbiota, while nearly opaque to paleon- Ferrusquia-Villafranca,I. 2003. Mexico's Middle Miocene tologists,has been fully appreciatedby mostbiologists mammalianassemblages: An overview.Pp. 321-347 in L. since Alfred Russell Wallace the Flynn (editor), Vertebrate Fossils and Their Context: (1876) proposed Contributionsin Honorof RichardH. Tedford.Bull. Amer. NeotropicalRealm. There are hints in the relatively Mus. Nat. Hist. weak tropical portionsof the vertebratefossil record Flynn, J. J. & C. C. Swisher III. 1995. Cenozoic South that this phase of the GABI came after the Pliocene American land mammal ages: Correlation to global and that duringthe Pleistocene the Panamanianland geochronologies.Pp. 317-333 in W. A. Berggren(editor), was more rainforest Geochronology,Time Scales and Global Stratigraphic bridge fully occupied by (Webb, Correlation.SEPM PublicationNo. 54. Webb& Paleobotanicalevidence Special 1991; Rancy, 1996). et al. (+ 6 authors). 2005. Geochronologyof makes a strong case for this (Colinvaux, 1997; Hemphillian-Blancanaged strata, Guanajuato,Mexico, Burnham& Graham,1999). and implicationsfor timing of the GreatAmerican Biotic Amongland mammals,the prominentprotagonists Interchange.J. Geol. 113(3): 287-307. in this second into Central were old Galusha,T., N. M. Johnson,E. H. Lindsay,N. D. Opdyke& phase, America, R. H. Tedford. 1984. and southerntaxa xenar- Biostratigraphy magnetostrati- including marsupials,primates, graphy, late Pliocene rocks, 111 Ranch, Arizona. Geol. thrans (both cingulates and pilosans), and hystricog- Soc. Amer. Bull. 95: 714-722. nath rodents.It is not surprisingthat these same old Hershkovitz,P. 1982. Neotropicaldeer (Cervidae),Part 1. southerntaxa outnumberthe northernnewcomers in Pudus, Pudu Gray.Fieldiana, Zool. 11: 1-86. the two South American biomes Hirschfeld, S. E. & S. D. Webb. 1968. Plio-Pleistocene designated by sloths of NorthAmerica. Bull. FloridaState as rain forest Megalonychid Marquetand Cofre (1999) temperate Mus., Biol. Sci. 12: 213-296. and tropicalhumid forest. Jacobs, L. L. & E. H. Lindsay. 1984. Holarcticradiation of muroid rodents and the origin of the South AmericanCricetids. VertebratePaleontol. 4: 265-272. LiteratureCited J. Jones, D. S. & P. F. Hasson. 1985. Historyand development M. T. Alberdi, G. Leone & E. P. Tonni (editors). 1995. of the marineinvertebrate faunas separated by the Central Evolucion Biologica y Climaticade la Region Pampeana Americanisthmus. Pp. 325-355 in F. G. Stehli & S. 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