Great American Interchange

Examples of migrant species in both Americas. Olive green silhouettes denote North American species with South American ancestors; blue silhouettes denote South American species of North American origin.

The Great American Interchange was an important paleozoogeographic event in which land and freshwater fauna migrated from North America via Central America to South America and vice versa, as the volcanic Isthmus of Panama rose up from the sea floor and bridged the formerly separated continents. The migration peaked dramatically around three million years (Ma) ago during the Piacenzian age.

It resulted in the joining of the Neotropic (roughly South America) and Nearctic (roughly North America) ecozones definitively to form the Americas. The interchange is visible from observation of both stratigraphy and nature (neontology). Its most dramatic effect is on the zoogeography of mammals but it also gave an opportunity for reptiles, amphibians, arthropods, weak-flying or flightless birds, and even freshwater fish to migrate.

The occurrence of the interchange was first discussed in 1876 by the "father of biogeography", Alfred Russel Wallace.[1][2] Wallace had spent 1848–1852 exploring and collecting specimens in the Amazon basin. Others who made significant contributions to understanding the event in the century that followed include Florentino Ameghino, W. D. Matthew, W. B. Scott, Bryan Patterson, George Gaylord Simpson and S. David Webb.[3]

Analogous interchanges occurred earlier in the Cenozoic, when the formerly isolated land masses of India[4] and Africa[5] made contact with Eurasia c. 50 and 30 Ma ago, respectively.

South America's endemic fauna

Sabertoothed sparassodont †Thylacosmilus (with †Glyptodon and toxodonts in the background)

After the late Mesozoic breakup of Gondwana, South America spent most of the Cenozoic era as an island continent whose "splendid isolation" allowed its fauna to evolve into many forms found nowhere else on Earth, most of which are now extinct.[6] Its endemic mammals initially consisted primarily of metatherians (marsupials and sparassodonts), xenarthrans, and a diverse group of native ungulates: notoungulates (the "southern ungulates"), litopterns,[n 1] astrapotheres (e.g. Trigonostylops, Astrapotherium), and pyrotheres (e.g. Pyrotherium).[n 2] A few non-therian mammals – monotremes, gondwanatheres, and possibly dryolestids and multituberculates – were also present in the Paleocene; while none of these diversified significantly and most lineages did not survive long, forms like Necrolestes and Patagonia remained as recently as the Miocene.[11]

The monito del monte, Dromiciops gliroides, South America's only australidelphian marsupial
†Astrapotherium magnum

Marsupials appear to have traveled via Gondwanan land connections from South America through Antarctica to Australia in the late Cretaceous or early Tertiary.[12][n 3] One living South American marsupial, the monito del monte, has been shown to be more closely related to Australian marsupials than to other South American marsupials; however, it is the most basal australidelphian,[n 4] meaning that this superorder arose in South America and then colonized Australia after the monito del monte split off.[12] A 61-Ma-old platypus-like monotreme fossil from Patagonia may represent an Australian immigrant. It appears that ratites (relatives of South American tinamous) migrated by this route around the same time, more likely in the direction from South America towards Australia/New Zealand.[13] Other taxa that may have dispersed by the same route (if not by flying or floating across the ocean) are parrots, chelid turtles and (extinct) meiolaniid turtles.

Marsupials present in South America included didelphimorphs (opossums) and several other small groups; larger predatory relatives of these also existed, like the borhyaenids and the sabertooth Thylacosmilus (sparassodont metatherians which are no longer considered to be true marsupials).[14]

Metatherians were the only South American mammals to specialize as carnivores; their relative inefficiency created openings for nonmammalian predators to play more prominent roles than usual (similar to the situation in Australia). Sparassodonts shared the ecological niches for large predators with fearsome flightless "terror birds" (phorusrhacids), whose closest extant relatives are the seriemas.[15][16] Through the skies over late Miocene South America (6 Ma ago) soared the largest flying bird known, the teratorn Argentavis, with a wing span of 6 m or more, which may have subsisted in part on the leftovers of Thylacosmilus kills.[17] Terrestrial ziphodont[n 5] sebecid crocodilians were also present at least through the middle Miocene[18][19][20][21] and maybe to the Miocene-Pliocene boundary.[22] Some of South America's aquatic crocodilians, such as Gryposuchus, Mourasuchus and Purussaurus, reached monstrous sizes, with lengths up to 12 m (comparable to the largest Mesozoic crocodyliforms). They shared their habitat with one of the largest turtles of all time, the 3.3 m (11 ft) Stupendemys.

The giant anteater, Myrmecophaga tridactyla, the largest living descendant of South American's early Cenozoic mammalian fauna

Xenarthrans are a curious group of mammals that developed morphological adaptations for specialized diets very early in their history.[23] In addition to those extant today (armadillos, anteaters and tree sloths), a great diversity of larger types were present, including pampatheres, the ankylosaur-like glyptodonts, various ground sloths, some of which reached the size of elephants (e.g. Megatherium), and even semiaquatic to aquatic marine sloths.[24][25]

The litoptern †Macrauchenia

The notoungulates and litopterns had many strange forms, like Macrauchenia, a camel-like litoptern with a small proboscis. They also produced a number of familiar-looking body types that represent examples of parallel or convergent evolution: one-toed Thoatherium had legs like those of a horse, Pachyrukhos resembled a rabbit, Homalodotherium was a semi-bipedal clawed browser like a chalicothere, and horned Trigodon looked like a rhino. Both groups started evolving in the Lower Paleocene, possibly from condylarth stock, diversified, dwindled before the great interchange, and went extinct at the end of the Pleistocene. The pyrotheres and astrapotheres were also strange but were less diverse and disappeared earlier, well before the interchange.

The North American fauna was a typical boreoeutherian one (supplemented with Afrotherian proboscids).

Island-hopping 'waif dispersers'

Capybara, Hydrochoerus hydrochaeris
Emperor tamarin, Saguinus imperator

The invasions of South America started about 40 Ma ago (middle Eocene), when caviomorph rodents arrived in South America.[26][27][28] Their subsequent vigorous diversification displaced some of South America's small marsupials and gave rise to – among others – capybaras, chinchillas, viscachas, and New World porcupines. (The independent development of spines by New and Old World porcupines is another example of parallel evolution.) This invasion most likely came from Africa.[29][30] The crossing from West Africa to the northeast corner of Brazil was much shorter then, due to continental drift, and may have been aided by island hopping (e.g. via St. Paul's Rocks, if they were an inhabitable island at the time) and westward oceanic currents.[31] Crossings of the ocean were accomplished when at least one fertilised female (more commonly a group of animals) accidentally floated over on driftwood or mangrove rafts. (Island-hopping caviomorphs would subsequently colonize the West Indies as far as the Bahamas,[32][33] reaching the Greater Antilles by the early Oligocene.[34]) Over time, some caviomorph rodents evolved into larger forms that competed with some of the native South American ungulates, which may have contributed to the gradual loss of diversity suffered by the latter after the early Oligocene.[6]

Later (by 36 Ma ago)[35] primates followed, again from Africa in a fashion similar to that of the rodents.[26] Primates capable of migrating had to be small. Like caviomorph rodents, South American monkeys are believed to be a clade (i.e., monophyletic). However, although they would have had little effective competition, all extant New World monkeys appear to derive from a radiation that occurred long afterwards, in the Early Miocene about 18 Ma ago.[26] Subsequent to this, monkeys apparently most closely related to titis island-hopped to Cuba, Hispaniola and Jamaica. Additionally, a find of seven 21-Ma-old apparent cebid teeth in Panama suggests that South American monkeys had dispersed across the seaway separating Central and South America by that early date. However, all extant Central American monkeys are believed to be descended from much later migrants, and there is as yet no evidence that these early Central American cebids established an extensive or long-lasting population, perhaps due to a shortage of suitable rainforest habitat at the time.[36][37]

Remarkably, the descendents of those few bedraggled waifs that crawled ashore onto South America from their rafts of African flotsam in the Eocene now constitute more than twice as many of the continent's species as the descendents of all the nonflying mammals previously resident on the continent (372 caviomorph and monkey species versus 136 marsupial and xenarthran species).[n 6]

Many of South America's bats may have arrived from Africa during roughly the same period, possibly with the aid of intervening islands, although by flying rather than floating. Noctilionoid bats ancestral to those in the neotropical families Furipteridae, Mormoopidae, Noctilionidae, Phyllostomidae, and Thyropteridae are thought to have reached South America from Africa in the Eocene,[39] possibly via Antarctica.[40] Similarly, molossid bats may have reached South America from Africa in as many as five dispersals, starting in the Eocene.[39] Emballonurid bats may have also reached South America from Africa about 30 Ma ago, based on molecular evidence.[39][41] Vespertilionid bats may have arrived in five dispersals from North America and one from Africa.[39] Natalid bats are thought to have arrived during the Pliocene from North America via the Caribbean.[39]

Red-footed tortoise, Chelonoidis carbonaria

Tortoises also arrived in South America in the Oligocene. It was long thought that they had come from North America, but a recent comparative genetic analysis concludes that the South American genus Chelonoidis (formerly part of Geochelone) is actually most closely related to African hingeback tortoises.[n 7][42] Tortoises are aided in oceanic dispersal by their ability to float with their heads up, and to survive up to six months without food or water.[42] South American tortoises then went on to colonize the West Indies[43] and Galápagos Islands. A number of clades of American geckos seem to have rafted over from Africa during both the Paleogene and Neogene.[44] Skinks of the related genera Mabuya and Trachylepis apparently dispersed across the Atlantic from Africa to South America and Fernando de Noronha, respectively, during the last 9 Ma.[45] Surprisingly, South America's burrowing amphisbaenians[46] and blind snakes[47] also appear to have rafted from Africa, as does the hoatzin, a weak-flying bird of South American rainforests.[48]

†Megalonyx wheatleyi

The earliest traditionally recognized mammalian arrival from North America was a procyonid that island-hopped from Central America before a land bridge formed, around 7.3 Ma ago.[49] This was South America's first eutherian carnivore. South American procyonids then diversified into forms now extinct (e.g. the "dog-coati" Cyonasua, which evolved into the bear-like Chapalmalania). However, all extant procyonid genera appear to have originated in North America.[50] It has been suggested that the first South American procyonids may have contributed to the extinction of sebecid crocodilians by eating their eggs, but this view has not been universally viewed as plausible.[n 8][21] The procyonids were followed to South America by rafting/island-hopping hog-nosed skunks[51] and sigmodontine rodents[52][53][54][55] The oryzomyine tribe of sigmodontine rodents went on to colonize the Lesser Antilles up to Anguilla.

One group has proposed that a number of large Neartic herbivores actually reached South America as early as 9-10 Ma ago, in the late Miocene, via the 'Baudo pathway', an early land bridge that was probably incomplete and required some swimming/island-hopping to traverse. The limited evidence for these early immigrants may reflect their presence primarily in the Amazon basin, an area where fewer fossils have been collected. These taxa are: a proboscidean (Amahuacatherium),[56][57][n 9] peccaries (Sylvochoerus and Waldochoerus),[59] tapirs and a palaeomerycid (from a family probably ancestral to cervids), Surameryx; the paleomerycids were probably unable to successfully colonize South America.[60]

Similarly, megalonychid and mylodontid ground sloths island-hopped to North America by 9 Ma ago.[52] Megalonychids had colonized the Antilles previously, by the early Miocene.[61] (Megatheriid and nothrotheriid ground sloths did not migrate north until the formation of the isthmus.) Terror birds may have also island-hopped to North America as early as 5 Ma ago.[62]

The Caribbean islands were populated primarily by species from South America. This was due to the prevailing direction of oceanic currents, rather than to a competition between North and South American forms.[32][33] (Except in the case of Jamaica, oryzomyine rodents of North American origin were able to enter the region only after invading South America.)

The Great American Biotic Interchange

The Virginia opossum, Didelphis virginiana, the only marsupial in temperate North America

The formation of the Isthmus of Panama led to the last and most conspicuous wave, the great interchange, around 3 Ma ago. This included the immigration of North American ungulates (including camelids, tapirs, deer and horses), proboscids (gomphotheres), carnivorans (including felids like cougars and saber-toothed cats, canids, mustelids, procyonids and bears) and a number of types of rodents[n 10] into South America. The larger members of the reverse migration, besides ground sloths and terror birds, were glyptodonts, pampatheres, capybaras and the notoungulate Mixotoxodon (the only South American ungulate known to have invaded Central America).

†Arctotherium bonariense, a South American short-faced bear

In general, the initial net migration was symmetrical. Later on, however, the Neotropic species proved far less successful than the Nearctic. This misfortune happened both ways. Northwardly migrating animals often were not able to compete for resources as well as the North American species already occupying the same ecological niches; those that did become established were not able to diversify much.[63] Southwardly migrating Nearctic species established themselves in larger numbers and diversified considerably more,[63] and are thought to have caused the extinction of a large proportion of the South American fauna. (There were no extinctions in North America plainly linked to South American immigrants.) Although terror birds were able to invade part of North America, their success was temporary; this lineage disappeared about two million years ago. The other large warm-blooded Neotropic predators fared no better. Native South American ungulates also did poorly, with only several of the largest forms, Macrauchenia and a few toxodontids, withstanding the northern onslaught. (Among the notoungulates, the mesotheriids and hegetotheriids did manage to hold on until the Pleistocene.)[A] On the other hand, South America's small marsupials survived in large numbers, while the primitive-looking xenarthrans proved to be surprisingly competitive and became the most successful invaders of North America. The African immigrants, the caviomorph rodents and platyrrhine monkeys, were less impacted by the interchange than most of South America's 'old-timers', although the caviomorphs suffered a significant loss of diversity,[n 11][n 12] including the elimination of the largest forms (e.g. the dinomyids). With the exception of the North American porcupine and several extinct porcupines and capybaras, however, they did not migrate past Central America.[n 13]

†Titanis walleri, the only known North American terror bird

The initial wave of southwardly migrating Nearctic carnivorans rapidly occupied the South American predatory niches, displacing phorusrhacids and sparassodonts,[n 14] as well as eliminating Chapalmalania. It has been argued that canids probably played the major role in the borhyaenids' extinction; they are ecologically and morphologically more similar to them than other carnivorans, and are also the most diverse family of modern carnivorans on the continent.[66] The paucity of early competition and plentiful prey seems to have allowed short-faced bears to rapidly evolve into the largest known bear or terrestrial mammalian carnivore species; Arctotherium angustidens is estimated to have weighed around 1600 kg. Later species of Arctotherium exhibited a trend towards smaller size and a more omnivorous diet, probably due to increasing competition from later-arriving or evolving carnivores.[67][68] In contrast, Smilodon showed a trend toward increasing body size that culminated in the appearance of S. populator, at up to nearly 500 kg the most massive felid known.

Due in large part to the success of the xenarthrans, one area of South American ecospace the Nearctic invaders were unable to dominate was the niches for megaherbivores.[69] Before 12,000 years ago, South America was home to about 25 species of herbivores weighing more than 1000 kg, consisting of Neotropic ground sloths, glyptodonts and toxodontids, as well as gomphotheres and camelids of Nearctic origin.[n 15] Native South American forms made up about 75% of these species. However, none of these megaherbivores have survived.

Armadillos, opossums and porcupines are present in North America today because of the Great American Interchange. Opossums and porcupines were among most successful northward migrants, reaching as far as Canada and Alaska, respectively. Most major groups of xenarthrans were present in North America up until the end-Pleistocene Quaternary extinction event (as a result of at least eight successful invasions of temperate North America, and at least six more invasions of Central America only). Among the megafauna, ground sloths were notably successful emigrants; Megalonyx spread as far north as the Yukon[71] and Alaska,[72] and might well have eventually reached Eurasia if the extinction event had not intervened.

Generally speaking, however, the dispersal and subsequent explosive adaptive radiation of sigmodontine rodents throughout South America (leading to over 80 currently recognized genera) was vastly more successful (both spatially and by number of species) than any northward migration of South American mammals. Other examples of North American mammal groups that diversified conspicuously in South America include canids and cervids, both of which currently have 3 or 4 genera in North America, 2 or 3 in Central America, and 6 in South America.[n 16][n 17] Although Canis currently ranges only as far south as Panama,[n 18] South America still has more extant canid genera than any other continent.[n 16]

The effect of formation of the isthmus on the marine biota of the area was the inverse of its effect on terrestrial organisms, a development that has been termed the "Great American Schism". The connection between the east Pacific Ocean and the Caribbean (the Central American Seaway) was severed, setting now-separated populations on divergent evolutionary paths.[76] Caribbean species also had to adapt to an environment of lower productivity after the inflow of nutrient-rich water of deep Pacific origin was blocked.[77]

Reasons for success or failure

A north-south climatic asymmetry in the Americas. Tropical climate zones, which are warm year-round and moist at least part of the year (blue zones Af, Am and Aw), cover much of South America and nearly all of Central America, but very little of the rest of North America.

The eventual triumph of the Nearctic migrants was ultimately based on geography, which played into the hands of the northern invaders in two crucial respects. The first was a matter of climate. Any species that reached Panama from either direction obviously had to be able to tolerate moist tropical conditions. Those migrating southward would then be able to occupy much of South America without encountering climates that were markedly different. However, northward migrants would have encountered drier and/or cooler conditions by the time they reached the vicinity of the Trans-Mexican Volcanic Belt. The challenge this climatic asymmetry (see map on right) presented was particularly acute for Neotropic species specialized for tropical rainforest environments, who had little prospect of penetrating beyond Central America. As a result, Central America currently has 41 mammal species of Neotropical origin,[n 19] compared to only 3 for temperate North America. However, species of South American origin (marsupials, xenarthrans, caviomorph rodents and monkeys) still comprise only 21% of species from nonflying, nonmarine mammal groups in Central America, while North American invaders constitute 49% of species from such groups in South America. Thus, climate alone cannot fully account for the greater success of species of Nearctic origin during the interchange.

Land areas over which ancestors of Neotropic (green) and Nearctic (red) species could wander via two-way migrations during the latter part of the Cenozoic prior to the interchange. The smaller area available for Neotropic species to evolve in tended to put them at a competitive disadvantage.

The second and more important advantage geography gave to the northerners is related to the land area available for their ancestors to evolve in. During the Cenozoic, North America was periodically connected to Eurasia via Beringia, allowing multiple migrations back and forth to unite the faunas of the two continents.[n 20] Eurasia was connected in turn to Africa, which contributed further to the species that made their way to North America.[n 21] South America, on the other hand, was connected to Antarctica and Australia, two much smaller continents, only in the earliest part of the Cenozoic, and this land connection does not seem to have carried much traffic (apparently no mammals other than marsupials and perhaps a few monotremes ever migrated by this route). This means that Northern Hemisphere species arose over a land area roughly six times greater than was available to South American species. North American species were thus products of a larger and more competitive arena,[n 22][63][78][79] where evolution would have proceeded more rapidly. They tended to be more efficient and brainier,[n 23][n 24] generally able to outrun and outwit their South American counterparts, who were products of an evolutionary backwater. These advantages can be clearly seen in the cases of ungulates and their predators, where South American forms were replaced wholesale by the invaders.

The greater eventual success of South America's African immigrants compared to its native early Cenozoic mammal fauna is another example of this phenomenon, since the former evolved over a greater land area; their ancestors migrated from Eurasia to Africa, two significantly larger continents, before finding their way to South America.[38]

Against this backdrop, the ability of South America's xenarthrans to compete effectively against the northerners represents a special case. The explanation for the xenarthrans' success lies in part in their idiosyncratic approach to defending against predation, based on possession of body armor and/or formidable claws. The xenarthrans did not need to be fleet-footed or quick-witted to survive. Such a strategy may have been forced on them by their low metabolic rate (the lowest among the therians).[87][88] Their low metabolic rate may in turn have been advantageous in allowing them to subsist on less abundant[89] and/or less nutritious food sources. Unfortunately, the defensive adaptations of the large xenarthrans would have been useless against humans armed with spears and other projectiles.

Late Pleistocene extinctions

The North American porcupine, Erethizon dorsatum, the largest surviving Neotropic migrant to temperate North America

At the end of the Pleistocene epoch, about 12,000 years ago, three dramatic developments occurred in the Americas at roughly the same time (geologically speaking). Paleoindians invaded and occupied the New World, the last glacial period came to an end, and a large fraction of the megafauna of both North and South America went extinct. This wave of extinctions swept off the face of the Earth many of the successful participants of the Great American Interchange, as well as other species that had not migrated. All the pampatheres, glyptodonts, ground sloths, equids, proboscids,[90][91][92] dire wolves, lions and Smilodon species of both continents disappeared. The last of the South and Central American notoungulates and litopterns died out, as well as North America's giant beavers, dholes, native cheetahs, scimitar cats, and many of its antilocaprid, bovid, cervid, tapirid and tayassuid ungulates. Some groups disappeared over most or all of their original range but survived in their adopted homes, e.g. South American tapirs, camelids and tremarctine bears (cougars and jaguars may have been temporarily reduced to South American refugia also). Others, such as capybaras, survived in their original range but died out in areas they had migrated to. Notably, this extinction pulse eliminated all Neotropic migrants to North America larger than about 15 kg (the size of a big porcupine), and all native South American mammals larger than about 65 kg (the size of a big capybara or giant anteater). In contrast, the largest surviving native North American mammal, the wood bison, can exceed 900 kg, and the largest surviving Nearctic migrant to South America, Baird's tapir, can reach 400 kg.

Paleo-Indians and †Glyptodon
Baird's tapir, Tapirus bairdii, the largest surviving Nearctic migrant to South America

The near-simultaneity of the megafaunal extinctions with the glacial retreat and the peopling of the Americas has led to proposals that both climate change and human hunting played a role.[69] Although the subject is contentious,[93][94][95][96][97] a number of considerations suggest that human activities were pivotal.[70][98] The extinctions did not occur selectively in the climatic zones that would have been most affected by the warming trend, and there is no plausible general climate-based megafauna-killing mechanism that could explain the continent-wide extinctions. The climate change took place worldwide, but had little effect on the megafauna in areas like Africa and southern Asia, where megafaunal species had coevolved with humans. Numerous very similar glacial retreats had occurred previously within the ice age of the last several Ma without ever producing comparable waves of extinction in the Americas or anywhere else. Similar megafaunal extinctions have occurred on other recently populated land masses (e.g. Australia,[99] Japan,[100] Madagascar,[101] New Zealand,[102] and many smaller islands around the world, such as Cyprus,[103] Crete, Tilos and New Caledonia[104]) at different times that correspond closely to the first arrival of humans at each location. These extinction pulses invariably swept rapidly over the full extent of a contiguous land mass, regardless of whether it was an island or a hemisphere-spanning set of connected continents. This was true despite the fact that all the larger land masses involved (as well as many of the smaller ones) contained multiple climatic zones that would have been affected differently by any climate changes ongoing at the time. However, on sizable islands far enough offshore from newly occupied territory to escape immediate human colonization, megafaunal species sometimes survived for many thousands of years after they or related species became extinct on the mainland; examples include giant kangaroos in Tasmania,[105][106] giant Chelonoidis tortoises of the Galápagos Islands (formerly also of South America[69]), giant Dipsochelys tortoises of the Seychelles (formerly also of Madagascar), giant meiolaniid turtles on Lord Howe Island, New Caledonia and Vanuatu (previously also of Australia),[107][n 25] ground sloths on the Antilles,[110] Steller's sea cows off the Commander Islands[111] and woolly mammoths on Wrangel Island[112] and Saint Paul Island.[113] The glacial retreat may have played a primarily indirect role in the extinctions in the Americas by simply facilitating the movement of humans southeastward from Beringia down to North America. The reason that a number of groups went extinct in North America but lived on in South America (while there are no examples of the opposite pattern) appears to be that the dense rainforest of the Amazon basin and the high peaks of the Andes provided environments that afforded a degree of protection from human predation.[114][n 26][n 27]

South American invasions of North America exclusive of Central America

Extant or extinct (†) North American taxa whose ancestors migrated out of South America:[n 28]

South American invasions that only extended to Central America

Extant or extinct (†) Central American taxa[n 31] whose ancestors migrated out of South America:[n 28]

North American invasions of South America

Extant or extinct (†) South American taxa whose ancestors migrated out of North America (considered as including Central America):[n 28]

See also

Notes

  1. ↑ During the Eocene, litopterns were also present in Antarctica.[7][8]
  2. ↑ Sequencing of collagen from fossils of one recently extinct species each of notoungulates and litopterns has indicated that these orders comprise a sister group to the perissodactyls.[9] Given that perissodactyls may have originated in India,[10] both ungulate groups may have been of Gondwanan origin, despite being laurasiatheres.
  3. ↑ Once in Australia, facing less competition, marsupials diversified to fill a much larger array of niches than in South America, where they were largely carnivorous.
  4. ↑ It is the sister group to a clade containing all other extant australidelphians (roughly 238 species).
  5. ↑ Ziphodont (lateromedially compressed, recurved and serrated) teeth tend to arise in terrestrial crocodilians because, unlike their aquatic cousins, they are unable to dispatch their prey by simply holding them underwater and drowning them; they thus need cutting teeth with which to slice open their victims.
  6. ↑ It is also notable that both simian primates (ancestral to monkeys) and hystricognath rodents (ancestral to caviomorphs) are believed to have arrived in Africa by rafting from Eurasia about 40 Ma ago.[38]
  7. ↑ North American gopher tortoises are most closely related to the Asian genus Manouria.
  8. ↑ An alternative explanation blames climatic and physiographic changes associated with the uplift of the Andes.[21]
  9. ↑ The status of Amahuacatherium is controversial, and it is sometimes considered as a misinterpreted fossil of a Pleistocene gomphothere.[58]
  10. ↑ Of the 6 families of North American rodents that did not originate in South America, only beavers and mountain beavers failed to migrate to South America. (However, introduced beavers have become serious pests in Tierra del Fuego.)
  11. ↑ Simpson, 1950, p. 382[64]
  12. ↑ Marshall, 1988, p. 386[3]
  13. ↑ Of the 11 extant families of South American caviomorph rodents, 5 are present in Central America; only 2 of these, Erethizontidae and Caviidae, ever reached North America. (The nutria/coypu has been introduced to a number of North American locales.)
  14. ↑ The dog-like borhyaenids were already in decline before the main pulse of the interchange, at a time when Thylacosmilus and phorusrhacids were still common. Suggested reasons for this decline include competition with phorusrhacids, carnivorous opossums, or early-arriving procyonids.[65] However, it is clear that the remaining sparassodonts and most of the phorusrhacids (Titanis being an exception) disappeared quickly once canids and felids reached South America.
  15. ↑ P. S. Martin (2005), pp. 30–37, 119.[70] The figure of 25 South American megaherbivore species breaks down as follows: 4 gomphotheres, 2 camelids, 9 ground sloths, 5 glyptodonts, and 5 toxodontids. This can be compared to Africa's present and recent total of 6 megaherbivores: 1 giraffe, 1 hippo, 2 rhinos and 2 elephants (considering the African forest elephant as a separate species).
  16. 1 2 The extant canid and cervid genera by continent are as follows:
    Canid genera by continent
    Cervid genera by continent
  17. ↑ Including extinct genera, South America has hosted 9 genera of cervids, 8 genera of mustelids, and 10 genera of canids. However, some of this diversity of South American forms apparently arose in North or Central America prior to the interchange.[63] There is significant disagreement in the literature concerning how much of the diversification of South America's canids occurred prior to the invasions. A number of studies concur that the grouping of endemic South American canids (excluding Urocyon and Canis, although sometimes transferring C. gezi to the South American group[73]) is a clade.[73][74][75] However, different authors conclude that members of this clade reached South America in at least two,[74] three to four,[73] or six[75] invasions from North America.
  18. ↑ Canis, e.g. Canis dirus, was present in South America until the end of the Pleistocene.
  19. 1 2 3 4 The Central American species of South American origin (opossums, xenarthrans, caviomorph rodents and platyrrhine monkeys) are as follows:
    Central American opossum species
    Central American xenarthran species
    Central American caviomorph rodent species
    Central American platyrrhine monkey species
  20. ↑ During the Miocene alone, between about 23 and 5 Ma ago, 11 episodes of invasions of North America from Eurasia have been recognized, bringing a total of 81 new genera into North America.[63]
  21. ↑ The combination of Africa, Eurasia and North America was termed the "World Continent" by George Gaylord Simpson.[64]
  22. ↑ Simpson, 1950, p. 368[64]
  23. ↑ According to data on the EQ (encephalization quotient, a measure of the brain to body size ratio adjusted for the expected effect of differences in body size) of fossil ungulates compiled by H. Jerison,[80] North American ungulates showed a trend towards greater EQs going from the Paleogene to the Neogene periods (average EQs of 0.43 and 0.64, respectively), while the EQs of South American ungulates were static over the same time interval (average EQ unchanged at 0.48).[6] This analysis was later criticized.[81] Jerison subsequently presented data suggesting that native South American ungulates also lagged in the relative size of their neocortex (a measurement not subject to the vagaries of body mass estimation).[82] It is interesting to note that the late survivor Toxodon had one of the highest EQ values (0.88) among native Neotropic ungulates.[81]
    Jerison also found that Neogene xenarthrans had low EQs, similar to those he obtained for South American ungulates.[80]
  24. ↑ The estimated EQ of Thylacosmilus atrox, 0.41 (based on a brain mass of 43.2 g, a body mass of 26.4 kg,[83] and an EQ of 43.2/[0.12*26400^(2/3)][82]), is high for a sparassodont,[84] but is lower than that of modern felids, with a mean value of 0.87.[85] Estimates of 0.38[86] and 0.59[85] have been given for the EQ of much larger Smilodon fatalis (based on body mass estimates of 330 and 175 kg, respectively).
  25. ↑ The giant tortoises of Asia and Africa[108] died out much earlier in the Quaternary than those of South America, Madagascar and Australia, while those of North America[109] died out around the same time.
  26. ↑ P. S. Martin (2005), p. 175.[70]
  27. ↑ A number of recently extinct North American (and in some cases also South American) taxa such as tapirs, equids, camelids, saiga antelope, proboscids, dholes and lions survived in the Old World, probably mostly for different reasons – tapirs being a likely exception, since their Old World representative survived only in the rainforests of Southeast Asia. (Cheetahs in the broadest sense could be added to this list, although the New and Old World forms are in different genera.) Old World herbivores may in many cases have been able to learn to be vigilant about the presence of humans during a more gradual appearance (by development or migration) of advanced human hunters in their ranges. In the cases of predators, the Old World representatives in at least some locations would thus have suffered less from extinctions of their prey species. In contrast, the musk ox represents a rare example of a megafaunal taxon that recently became extinct in Asia but survived in remote areas of arctic North America (its more southerly-distributed relatives such as Harlan's musk ox and the shrub ox were less fortunate).
  28. 1 2 3 This listing currently has fairly complete coverage of mammals, but only spotty coverage of other groups. Crossings by nonflying mammals and birds occurred during the last 10 Ma. Crossings by fish, arthropods, rafting amphibians and reptiles, and flying bats and birds were made before 10 Ma ago in many cases. Taxa listed as invasive did not necessarily cross the isthmus themselves; they may have evolved in the adopted land mass from ancestral taxa that made the crossing.
  29. ↑ While all megalonychid ground sloths are extinct, extant two-toed tree sloths are from the same family. Three-toed tree sloths, in contrast, are not closely related to any of the groups of extinct ground sloths.
  30. ↑ Mixotoxodon remains have been collected in Central America and Mexico as far north as Veracruz and Michoacán, with a possible find in Tamaulipas;[120] additionally, one fossil tooth has been identified in eastern Texas, United States.[121]
  31. ↑ For the purposes of this article, all northwardly migrating Neotropic taxa that failed to reach the territory of the continental U.S. will be treated as having only reached Central America. While Central America is usually defined physiographically as ending at the Isthmus of Tehuantepec, or less commonly, at the Trans-Mexican Volcanic Belt, most of the taxa that proceeded further but failed to reach the present Mexican border are or were confined to tropical or subtropical ecozones similar to those of Central America. Examples include the giant anteater, the grayish mouse opossum, the lowland paca and Geoffroy's spider monkey.
  32. ↑ Fossils of the giant anteater have been found as far north as northwestern Sonora, Mexico.[128]
  33. ↑ It has been proposed that monkeys invaded Central America in at least three and probably four waves, as follows: (1) an initial invasion by A. pigra and S. oerstedii ~ 3 Ma ago; (2) an invasion by A. palliata (giving rise to A. coibensis), A. geoffroyi and C. capucinus ~ 2 Ma ago; an invasion by A. zonalis and S. geoffroyi ~ 1 Ma ago; a most recent invasion by A. fusciceps. The species of the first wave have apparently been out-competed by those of the second, and now have much more restricted distributions.[129]
  34. ↑ Salamanders apparently dispersed to South America by the Early Miocene, about 23 Ma ago.[132] Nevertheless, the salamander fauna of South America, which is restricted to the tropical region, consists of only 2 clades, and has fewer species and is far less diverse than that of much smaller Central America. Salamanders are believed to have originated in northern Pangea, perhaps not long before it separated to become Laurasia,[125] and are not present anywhere else in the Southern Hemisphere (see the world salamander distribution map). In contrast, caecilians have a mostly Gondwanan distribution. Apart from a small region of overlap in southern China and northern Southeast Asia, Central America and northern South America are the only places in the world where both salamanders and caecilians are present.
  35. ↑ This is based on the definition of Sigmodontinae that excludes Neotominae and Tylomyinae.
  36. ↑ Hippidion, a relatively short-legged equid that developed in South America after invading from North America about 2.5 Ma ago, has traditionally been thought to have evolved from pliohippines.[139][140] However, recent studies of the DNA of Hippidion and other New World Pleistocene horses indicate that Hippidion is actually a member of Equus, closely related to the extant horse, E. ferus.[139][140] Another invasion of South America by Equus occurred about one Ma ago, and this lineage, traditionally viewed as the subgenus Equus (Amerhippus), appears indistinguishable from E. ferus.[140] Both these lineages became extinct at the end of the Pleistocene, but E. ferus was reintroduced from Eurasia by Europeans in the 16th century. Note: the authors of the DNA sequence study of Equus (Amerhippus) use "E. caballus" as an alternative specific name for "E. ferus".[140]
  37. ↑ Not to be confused with the American mastodon (Mammut americanum), a proboscid from a different family whose remains have been found no further south than Honduras.[141]
  38. ↑ Sometimes classified as elephantids rather than as gomphotheres.
  39. ↑ Not to be confused with the South American gray fox.
  40. ↑ Condors apparently reached South America by the late Miocene or early Pliocene (4.5 – 6.0 Ma ago), several million years before the formation of the isthmus.[156] Condor-like forms in North America date back to the Barstovian stage (middle Miocene, 11.8 – 15.5 Ma ago).[155]
  1. ^ The native South American ungulates dwindled gradually as North American ungulates invaded and diversified. The changes in number and composition of South America's ungulate genera over time are given in the table below.[157] The Quaternary extinction event that delivered the coup de grâce to the native Neotropic ungulates also dealt a heavy blow to South America's ungulate immigrants.
    Change in number of South American ungulate genera over time
    Time interval Source region of genera
    Geologic period Range (Ma ago) South America North America Both
    Huayquerian 9.0 — 6.8 13 0 13
    Montehermosan 6.8 — 4.0 12 1 13
    Chapadmalalan 4.0 — 3.0 12 1 13
    Uquian 3.0 — 1.5 5 10 15
    Ensenadan 1.5 — 0.8 3 14 17
    Lujanian 0.8 — 0.011 3 20 23
    Holocene 0.011 — 0 0 11 11

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