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Point-Of-View Point-of-View JOURNAL OF AVIAN BIOLOGY 33: 207–211, 2002 Splendid isolation: historical ecology of the South American passerine fauna Robert E. Ricklefs, Department of Biology, Uni7ersity of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63121-4499, USA. E-mail: [email protected] A few years ago, I had my first opportunity to visit the their way from North America. Following the establish- Amazonian Basin in eastern Ecuador. Several days of ment of a land bridge connecting North and South mist-netting and birding within an intact forest and in America about 3 million years ago (Mya), the rate of surrounding disturbed habitats turned out to be a dispersal between the continents accelerated. This pivotal experience, finally crystallizing in my mind a ‘‘Great American Interchange’’ greatly favored North pattern that every Neotropical ornithologist knows but American forms in the end (Webb 1976, 1991). Many whose significance has largely escaped us. I am refer- of these more recently invading lineages diversified and ring to the fact that most of the birds of the forest displaced endemic South American clades. understory belong to the large South American en- Birds, especially small ones, leave few traces. Taxo- demic radiation of songbirds, the suboscines, called the nomic relationships clearly show that South America infraorder Tyrannides (suborder Tyranni) by Sibley and has provided fertile ground for numerous northern Ahlquist (1990). This clade includes the ovenbirds, invaders, notably among the oscine passerines. Without woodcreepers, antbirds, manakins, cotingas, and a time line, however, we cannot fully appreciate the flycatchers, among others. Birds more familiar to North revolution that took place in the avifauna during the American’s, the oscine passerines (suborder Passeri), late Tertiary. Furthermore, we need to connect phylo- including the New World orioles, tanagers, and ember- genetic relationship to ecology to see how the endemic izine finches, dominate the forest canopy and habitats South American avifauna might have been displaced as outside the forest, along with a few species-rich clades a result. Much of the ecological space of South Amer- of tyrannine flycatchers (family Tyrannidae, subfamily ica is dominated by relatively recent arrivals from the Tyranninae). north, which presumably replaced endemic forms that South America was an isolated island continent occupied this space before the northern invasion began. throughout most of the Tertiary, during which time At least, it is difficult for an ecologist to imagine that passerine birds diversified throughout the world. As a the large resource base that now supports many species result of its isolation, however, South America sup- with North American roots was previously unexploited. ported the evolutionary diversification of many unusual Two questions come to mind. First, what were the now (compared to the rest of the world) lineages of plants missing South American endemics? Did they comprise and animals, retaining perhaps the highest level of members of groups that we are familiar with today, or, endemism of any of the continents. The unique history like the notoungulates and many of the marsupials, of the mammalian fauna of South America is well were they highly unusual local products of South known from the abundant fossils in deposits in the America’s splendid isolation? Second, what might have southern part of the continent. The paleontologist allowed the more recent invaders to replace the native George Gaylord Simpson (1980) celebrated the ‘‘splen- forms? Endemic lineages presumably are better adapted did isolation’’ of South America that led to so many to their homes than new arrivals, but the evidence from endemic forms. Fossils also reveal the fates of many faunal exchange and studies of island faunas often South American endemic mammals, including the show otherwise (Ricklefs and Cox 1972, Ricklefs and litopterns and notoungulates, as well as much of the Bermingham 1999). Thus, some lineages might have endemic marsupial fauna, as occasional migrants made intrinsically superior traits whose value is independent © JOURNAL OF AVIAN BIOLOGY JOURNAL OF AVIAN BIOLOGY 33:3 (2002) 207 of the local environment, at least under some condi- suboscines at 13.8×2.3=31.7 My, and the average age tions. Such traits may differ from ‘‘key innovations,’’ of oscine clades in South America at 5.3×2.3=12.2 which can promote diversification by allowing organ- My, that is, during the middle to late Miocene. Alterna- isms to exploit new niches or habitats (Heard and tively, we may estimate age from the node connecting Hauser 1995, Barraclough et al. 1998, Owens et al. the South American suboscines and their sister group, 1999). the pittas and broadbills (Infraorder Eurylaimides) of D Where ornithologists lack fossils, they now have southern Asia, which is at a depth of TH50=15.8°C. molecular phylogenies to provide inference about his- Setting this point at the severing of the land connection tory. The most complete appraisal of avian diversifica- between South America and Australia, approximately tion remains Sibley and Ahlquist’s (1990) study of 49 Mya, would place the deepest node in the Tyran- relationships based on DNA hybridization. Genetic nides at 42.8 Mya (middle Eocene) and the average of distance is expressed as a difference in the temperature oscine clades in South America at 16.4 Mya, during the of the melting points of homoduplexed and heterodu- mid-Miocene. plexed (hybridized) DNA. The larger the temperature The ecological displacement between suboscines and D difference ( TH50), the greater the genetic distance and the younger, newcomer oscines is apparent in both the more remote the relationship. Furthermore, if ge- habitat distribution and occurrence within habitats. D netic distance were to scale linearly with time, TH50 Ricklefs and Schluter (1993) noted that 31 of 41 species would provide a relative time scale. of passerine recorded by Karr (1971) in a Panama According to Sibley and Ahlquist (1990), the distance forest census site were suboscines, compared to 24 of 47 between the South American suboscines and their clos- species in scrub habitat. Most of the difference resulted est sister lineage, the Old World pittas and broadbills from fewer suboscines (31 versus 24) and markedly D (Infraorder Eurylaimides), is TH50=15.8°C. The more fringillid oscines (3 versus 17) in scrub. Several deepest split between endemic lineages in South Amer- lineages of tyrannine flycatchers are common in open ica, joining the Parvorder Tyrannida (538 species) to all habitats, and these are the only lineages of suboscines D other suboscines (560 species), occurred at TH50= that have been successful in North America. 13.8°C. The deepest node among oscine passerines Central America has many elements of the endemic D globally is TH50=12.8°C. Thus, the South American South American avifauna, but as one enters the Ama- suboscines are an old radiation, which has produced zonian Basin proper the proportion of suboscines in 1098 species of birds (Sibley and Munroe 1990), most forested habitats increases (Fig. 1). Further south, in of them occurring in South America (966 species; Ridg- Mediterranean and temperate environments of South ley and Tudor 1994) and tropical Central America. A America, the mix of major groups remains about the few tyrannine flycatchers (27 species in 6 genera) breed same as it is in the Amazon Basin, although the clades in North America. I have estimated elsewhere (Ricklefs within each group differ. For example, Cody (1970) in press) that, in contrast, the South American oscines listed 9 tyrannines, 11 other suboscines, and 14 oscines represent 14 clades with an average relative age of in study plots in central Chile, while Ralph (1985) listed D 9 TH50=5.3° ( 2.5° SD, range 2.0°–9.7°) C, compris- 9, 10, and 13 species, respectively, in study plots in ing 702 species. The most important South American Patagonia, Argentina. lineages of oscines, in terms of contemporary species Habitat and diet also differ among the major groups richness, are the wrens (Certhiidae: Troglodytinae: of South American passerine birds. Distribution with 9.0°C, 106 species) and three emberizid tribes of the respect to vertical strata in four Neotropical forests family Fringillidae: the emberizine finches (Fingillidae: show that non-tyrannine suboscines are most numerous Emberizini: 6.0°, 155), the New World orioles (Icterini: in the forest interior and avoid the forest canopy, 4.0°, 57), and the tanagers (Thraupini: 5.5°, 217) (Ridg- reinforcing the general impression expressed at the out- ley and Tudor 1989, Sibley and Ahlquist 1990). In each set (Fig. 1). Pearson (1971) reported a similar pattern of these individual oscine clades, the basal branches are from a dry forest site in Amazonian Peru (Table 1). represented among extant forms by South American Like the oscine passerines, however, the Tyranninae are species. The average genetic divergence encompassed by also prominent in the canopy and in open environ- the basal nodes represents a little more than one-third ments. Each of the major groups of birds includes small of the time spanned by the diversification of the en- insects as a major component of the diet. However, demic suboscines. Thus, almost two-thirds of the non-tyrannine suboscines uniquely exploit large insects, passerine history of the South American avifauna pro- often using sit-and-search tactics, while the oscines ceeded without the presently dominant lineages of make greater use of fruit resources, consistent with their canopy and open-habitat birds. dominance in the canopies of forests. Sibley and Ahlquist (1990) suggested that each degree The striking stratum and diet differences among the D Cof TH50 is equivalent to 2.3 million years of time three groups of birds suggest that they might separate (My) in small birds with short generation times. This morphologically as well.
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