Diversification of the Neotropical Avifauna: Disentangling the Geographical Patterns of Persisting Ancient Taxa and Phylogenetic Expansions

ORNITOLOGIA NEOTROPICAL 23: 113–128, 2012 © The Neotropical Ornithological Society

Diversification of the Neotropical Avifauna: disentangling the geographical patterns of persisting ancient taxa and phylogenetic expansions

Jon Fjeldså

Address: Centre of Macroecology, Evolution and Climate, Zoological Museum, University of Copenhagen. Universitetsparken 15, DK-2100 Copenhagen, Denmark. E-mail: [email protected].

ABSTRACT.With the development of digital distribution databases and comprehensive molecular phylogenies it is now possible to analyze diversification processes in time and space. This can be done by contrasting geographical distributions of sister groups up through the phylogenetic hierarchy, patterns of ancient clade diversity and species representing different ages. The “tropical niche conservatism” appears to be linked with the imbalance of the net sum of birth-death processes and the higher persistence of clades with low net speciation rates in the most productive tropical lowlands, compared with a higher turnover elsewhere. Divergent geographical distributions in groups that underwent phylogenetic expansion during the Neogene suggest a strong ability to access new ecoregions, notably in the south and in the tropical Andes region, where the most intensive speciation now takes place in the tree-line zone. It is suggested that specialization and dense niche packing forms the basis for continuous high speciation rates in the Andean “hotspot”.

Biogeographic research has long been ham- 2006, Hawkins et al. 2006). Over the last two pered by the lack of communication between decades, the rapid development of digital dis- disciplines. While the macroecologists have set tribution data and molecular phylogenetic data out to exlain the large-scale trends in species has opened new perspectives for teasing apart diversity from present-day ecological condi- the environmental and evolutionary causes tions, ignoring that every species has a his- of biogeographic patterns (Jetz et al. 2004; tory, the historical biogeographers were most Hawkins et al., 2005; Weir 2006). concerned with the methods for tracing gen- Interpretations of large-scale patterns of eralized patterns of vicariance and identify- diversification have until recently been ham- ing underlying barriers. Although a significant pered by lack of phylogenetic data. Thus, bio- proportion of the large-scale variation in spe- geographic interpretations were often based on cies richness is well explained from climate- simple assumptions, such as centers of species based environmental models, this correlation richness representing centers of origin (disper- is mainly caused by the many data points rep- sal centers; Müller 1976). With the emergence resenting the most widespread species (Rah- of modern phylogenies, this was replaced by bek et al. 2006). On the other hand, the very area cladograms and recently by more sophis- aggregated distributions of range-restricted ticated ancestral area reconstructions that take species represent high residual values that are into account dispersal and uncertainties in the hard to explain from present-day environmen- phylogenetic reconstructions (e.g., Burns & tal parameters and therefore require historical Haricot 2009; Santos et al. 2011). Such meth- explanations (Jetz et al. 2004, Rahbek et al. ods cannot remove the uncertainty about how

113 Fjeldså much of the ancestral distributions that have areas), based on a supertree for all birds (com- been erased by extinctions and range dynamics piled through review of most of the published caused by past climatic perturbations, such as phylogenetic studies), and densely sampled the disappearance of the species-rich tropical- molecular phylogenies for some groups. Spe- like forest of the Argentinean Patagonia un- cial attention will given here to the endemic til the end of the Eocene (Wilf et al. 2003). suboscine radiations, because of the well re- Because of this uncertainty, I will illustrate solved and densely sampled phylogenies (no- here more general tendencies based on com- tably Irestedt et al. 2009; Ohlson et al. 2009, parison of spatial diversity patterns for ancient in review; Moyle et al. 2008; Tello et al. 2008; and terminal lineages. This will first of all be Derryberry et al. 2011), and because this is done for the endemic radiation of suboscine the largest endemic radiation that evolved in birds. On this background I will address more splendid isolation through most of the Tertia- general questions about the relative roles of ry, until the establishment of the Panama Isth- extinction, speciation, niche conservatism and mus allowed a limited amount of phylogenetic phylogenetic expansion. expansion to the north. In addition, dated phylogenies can be used Methods to reconstruct patterns of clade diversity at particular points in time. We cannot know the Species distribution data are part of a com- past distribution of a clade, but assuming that prehensive global distributional database de- it diversified in situ, by vicariance, we may esti- veloped at the Centre for Macroecology, Evo- mate the ancestral distribution by merging the lution and Climate (version July 2010). The ranges of all constituent species and remov- geographical range of each species has been ing only the peripheral areas (notably outside mapped at a resolution of 1º x 1º lat-long South America) that evidently represent dis- quadrates, following the approach outlined persal in a terminal subclade. Time windows by Rahbek & Graves (2001). Maps represent for reconstructions of clade diversity maps a conservative extent-of-occurrence for the were defined from earth history data: Assum- breeding range based on museum specimens, ing that modern bird groups flourished during published sight records and spatial distribu- the Eocene climatic maximum (when species- tion of habitats between documented records rich tropical-like forests existed south to Pata- (>1000 references used for South America), gonia; Wilf et al. 2003) but suffered a serious and has been validated by many experts. The set-back at the Eocene/Oligocene transition species level taxonomy is updated according (34 Mya) during the first Antarctic chill. New to Remsen et al. (2011). The software used crown group radiations started again late Oli- (Worldmap) calculates various diversity mea- gocene up until the mid-Miocene optimum (15 sures, such as species richness in grid-cells, Mya) (see Zachos et al. 2001). Past diversity range centers, mean range-size and endemism patterns were therefore assessed by mapping: (either number of species representing the 1st range-size quartile, viz., the 25% of all species 1 the diversity of small clades (of all birds; with smallest distributions, or the sum of in- defined as lineages with 1-3 allospecies) verse range-size values). The species distribu- that date back to the warm Eocene and tion data can then be linked with tree-spanning 2 the clade diversity for suboscine groups in measures such as mean root path (sometimes the late Oligocene (26 Mya), after the Oli- used as evidence of tropical niche conserva- gocene chill and just before the onset of in- tism, although biased towards species poor tensive diversification in crown groups, and

114 Diversification of the Neotropical Avifauna

3 the clade diversity of suboscines in the 1. The phylogenetic relict species (Fig. 1a) are mid-Miocene (15 Mya). most strongly represented in the most exten- These geographical patterns can be com- sive areas of lowland rainforests and flood- pared with diversity patterns for all South plains, corresponding well to the diversity of American birds, as a general measure of repre- the most widespread quartile of South Ameri- sentativeness (Tab. 1; r values refer to compari- can bird species (Tab.1). The other maps are son with the total diversity and with range size based on suboscine birds only. The highest lin- groups, from the 1st to 4th quartiles [25%] of eage diversity from the early phase of the di- least to most widely distributed). This provides versification of suboscine crown groups (late an indirect assessment of the ecological deter- Oligocene; Fig. 1b) is rather concentrated in minants of the illustrated pattern, which is well the southern Atlantic forests of Brazil, with documented for all endemic South American many small clades, and in the western Ama- birds and analyzed Rahbek et al. [2006] with zon area up to the sub-Andean zone; many of respect to environmental models that best ex- the old lineages being disjunctly distributed in plain the geographical patterns. both areas (Batalha-Filho et al. in press). These Recent diversification can be illustrated for ancestral patterns are also evident in the map groups with densely sampled phylogenies. Fjeldså of terminal species taxa (Fig. 1c), with the & Irestedt (2009) illustrated the spatial diversifi- quartile of most range-restricted species in cation of Furnariidae using root-path quartiles as the tropical Andes region (Fig. 1d). Very simi- a surrogate measure of age, but this can now be lar species richness patterns are found when supplemented with molecular age estimates of all comparing the richness patterns of Tyrannides terminal species taxa thanks to the very densely versus Furnariides r 5 0.94), Suboscines ver- sampled phylogeny by Derryberry et al. (2011). sus Oscines (r 5 0.85), and Suboscines versus During the preparation of this manuscript, most hummingbirds, Trochilidae (r 5 0.89; Rahbek other phylogenies of South American birds have & Graves 2001). The geographical patterns for been examined for general trends. range-restricted suboscines (Fig. 1d) is closely similar to that for all range-restricted birds Results (Tab. 1). Basal suboscine clades are widely distribut- Patterns of large scale variation in avian di- ed in the mesic tropics, notably in the ancient versity in South America is illustrated in Fig. cratonic areas north and south of the Amazon

Table1. Comparison of geographical diversity patterns (r values) of the illustrated diversity patterns (Figs 1, 2 and 3) with patterns for all endemic South American birds, as presented in Rahbek et al. (2006) (1st quartile is the 25% of species with the smallest geographical ranges; 4th quartile is the 25% of most widespread species). Because of the high autocorrelation in such datasets, it was not considered relevant to present p values).

Fig1a b c d Fig.2a Fig.3ª b c d e All 0.82 0.91 0.98 0.24 0.94 0.87 0.82 0.84 0.15 0.28 1st 0.12 0.30 0.29 0.82 0.33 0.11 0.09 0.14 0.12 0.01 2nd 0.21 0.27 0.23 0.71 0.30 0.15 0.11 0.16 0.08 0.05 3rd 0.62 0.47 0.45 0.43 0.51 0.74 0.28 0.43 0.49 0.20 4th 0.88 0.90 0.98 0.31 0.94 0.74 0.79 0.82 0.33 0.29

115 Fjeldså

FIG. 1. General characteristics of diversity of South American birds. A, variation in distribution of 65 phylogenetic relict avian species of Eocene age; b, diversity of 19 suboscine clades as of 26 million years in the late Oligocene; c, diversity of extant species; and d, of the 25% species with the most restricted distributions. Proportional colour scale, red colour representing the highest number of taxa (which is 180-285 species in map c). basin. However, some clades of Andean ori- has been very limited geographical mixing of gin appear from the Oligocene and early Mio- these faunas. Among the Amazonian clades, cene (Rhinocryptidae, Chamaeza, Geositta; and some species have apparently dispersed north Grallaria /Grallaricula), and several other ap- of the Colombian Andes or crossed the Andes pear towards the mid-Miocene. Some of these to the Chocó region, but only very few have are rather small clades (Ampelion group, Ampe- developed a decided tolerance for montane lioides, Teledromas-Rhinocrypta-Acropternis, Pygar- conditions. Similarly, only few terminal species rhicas/Ochetorhynchus, Pseudocolaptes-Premnornis- in Andean clades colonized the Amazonian Tarphonomus), suggesting a down-scaling of lowlands. diversification rates, other clades maintained The densely sampled and time calibrated high speciation rates throughout the upper phylogeny for Furnariidae (Derryberry et al. Tertiary. 2011) is used in Fig. 2 to illustrate the historical Interestingly, by the mid-Miocene (15 Mya), progress of speciation events. The oldest spe- most suboscine clades can be classified as either cies, representing speciation events around the based in the Andes region (or Andean-South mid-Miocene, are mainly found in the Amazon Brazilian uplands) or Amazonian/Guianan. basin and along its ancient drainage channel to Fig. 2 presents diversity of clades at 15 Mya, the north, and in the Chocó and to some ex- with separate colours for the two geographical tent in the Guianas and southern Atlantic for- origins in Fig. 2b (this graph excludes, though, est (Fig. 3a). The diversification then continued some clades of other, or uncertain, geographi- in the Guiana highland and in the upper (So- cal origin; see legend). It is evident from this limões/Pebas) Amazon basin, with a concen- illustration that the maximum diversity (white tration in the sub-Andean forelands becoming cells, or red cells in Figs 1 b and c) are in grid- increasingly prominent towards the Pliocene. cells located along the borderline between the An apparently high diversity along the lower Andean and Amazonas faunas, and that there Amazonian channel east of the Purus Arc (Fig.

116 Diversification of the Neotropical Avifauna

FIG. 2. Diversity of suboscine clades at 15 Mya. To the right, these have been split up into 35 clades rooted in the Andes region (green), and 36 clades rooted in tropical lowlands (purple) (ρ² 0.416). Note that mixing of these groups produce grey hues, and overall lineage diversity is expressed as brightness, with the most diverse areas appearing whie. (This comparison excludes the south Brazilean Calyptura and Carpornis and five larger groups whose biogeographic origin is difficult to place although it is most probably rooted in a broadly defined southern savanna region, namely the crown group of spinetails, thornbirds and elaenine, tyrannine and fluvicoline flycatchers).

3 b-d) marks the in-grid-cell overlap of species lines expanding out in the open, first in the inhabiting the northern and southern banks southern tropical woodland savannas, but con- (thus this does not reflect local endemism, as tinuing in the southern cone of the continent no range-restricted species are centered in this (Xolmiini) and in the Andes (Fluvicolini and area). Also the local peaks at Río Sao Francisco Xolmiini), and with phylogenetic expansions in eastern Brazil and along the western edge of out of South America in Tyrannini and Conto- the Brazilian shield (Fig. 3d) represents points pini (Tello et al. 2009; Ohlson et al. 2008 and of marginal overlap between regional faunas. in review). The tapaculos diversified along the Recent diversification took place throughout entire Andes (with gaps in the arid highlands), the southern savannas (Fig. 3d) and in the An- with three colonizations to S Brazil and one des (Fig. 3e). The high levels of Pleistocene old colonization to the Amazon lowlands. speciation along the humid eastern edge of the highest parts of the Andes (Fig. 3 d and e). Discussion Areas with no new species originating during the upper Pleistocene (white in Fig. 3e) cor- Imbalanced distribution of old and young taxa. The respond to areas of highest median range-size. illustrated species richness pattern for the en- The Tyrannida follow a similar pattern, demic suboscine radiation (Fig. 1c) resembles with basal radiations (Cotingidae, Pipridae, that for groups that colonized in recent geo- Tityridae, Rhynchocyclidae and various small logical times (tanagers; Fjeldså & Rahbek 2006), old clades) mainly in the mesic tropical low- and for other taxonomic groups, such as mam- lands, and elaenines, tyrannines and fluvico- mals (Tognelli & Kelt 2004) and plants (Barth-

117 FIG. 3. Diversification of South American furnariids, illustrated as spatial variation in richness of species in groups based on time to the most recent common ancestor, following molecular phylogenies of Derryberry et al. (2011) and Ohlson et al. (MS).A, 45 species lineages with origin 20-7.5 million years ago; B, 34 species age 7.5-5 my; C, 79 species age 2.5-5 my; D, 86 species age 2.5-1.5 my; E, 48 species age ,1.5 my. lott et al. 2005). Thus, this appears to represent edge of the continent. However, part of the a fairly general pattern of variation in terrestrial explanation may also be range-dynamics: A biodiversity in South America, at this scale of high loss of diversity in the south as a con- spatial resolution. The diversity pattern for the sequence of major climate perturbations, and most ancient avian species (Fig. 1a) resembles a higher persistence of lineages in the areas the pattern for the most widespread birds (Tab. that remained warm and humid. The disap- 1), corresponding to extensive mesic lowland pearance of the diverse tropical-like forests habitats and well explained from net primary of Patagonia during the abrupt global cooling productivity (Rahbek et al. 2006 fig. 3). Most of (Terminal Eocene Event, 34 Ma; Wilff et al. the ancient, small clades are relatively large birds 2004; Zachos et al. 2001) must have put an end that may have required extensive areas to persist to many warm-adapted groups. The Tyran- over such a long time, which may explain their nides phylogeny (Ohlson et al. 2009, MS ) has general absence inside the montane regions. a long basal branch, a single species surviving The mid-Tertiary lineage diversity pattern up until 32 Ma. This ancestor was probably a (Figs 1b and 2a) appears to be reflected in the rainforest frugivore (judging from the ecol- current species diversity pattern (r 5 0.91 and ogy of the basal tyrannid groups of manakins, 0.94; Tab. 1). Using the same distributional cotingas and some small clades). Frugivory is and phylogenetic data as this study, Sanín et al. also widespread (as a diet supplement) in other (in review) found that 81% of the variation in tyrannid groups. Such frugivorous birds may species species diversity at a spatial resolution have become brutally restricted by the global of 10x10º could be explained from the lineage cooling at the Terminal Eocene Event, and the diversity as far back as 40 mya. This would early radiation of the Tyrannides crown group seem to suggest a strong role of regional varia- therefore took place near the equator. As the tion in speciation rates. This may notably be old groups were thus shuffled together in the the case near the geologically dynamic western remaining tropical forest regions, the continu- Diversification of the Neotropical Avifauna ing diversification in the south was constrained (as well as the Tyrannidae flycatchers, sensu by the development of a large rain shadow Tello et al. 2009 and Ohlson et al. in review) area that developed as a consequence of the diversified strongly during the upper Miocene Andean uplift. in the mosaic habitats that developed with the The asymmetries of many phylogeneties spread of savannah vegetation and grasslands suggests that early bursts of diversification in the southern subtropical zone (Zachos et al. were followed by apparent down-shifts, lead- 2001). This shift of the frontier of diversifica- ing to the emergence of many small clades tion to the south is reflected in the low r values (Ricklefs 2005), which mainly survived in the in the right column in Tab. 1. Apparently, the southern part of the Brazilian Atlantic forest southern savanna region was a center diversi- and in the sub-Andean Amazon Basin (Fig. fication and expansion to riparian habitats and 1b). The high persistence of old lineages in edge habitats in the Amazon (Cranioleuca, Syn- this region has given rise to the idea of tropi- allaxis) as well as to the central parts of the cal niche conservatism as a historical narrative Andes. There has been a significant exchange for explaining such broad species richness gra- between Andean-Pampean region and the dients (Fig. 1 a, b; Hawkins et al. 2005; Weir South Brazilian highland fores. Interestingly, 2006). However, the distinct pattern in Fig. 2b as the involved groups are strongly associated suggests that also the Andean clades may also with rugged terrain (or well-drained soils), this be constrained by niche conservatism. The Andean-Brazilian track was broken by the de- Andes contains an interesting mix of radiating velopment of hydrologically unstable plains in groups and small/old clades that persisted in the Beni-Pantanal region (Fig. 2b). During the situ, mainly in the lower montane forest (e.g., climatically most unstable upper Pleistocene Laniisoma, Snowornis, Thamnistes, Premnoplex, the diversification continued only in some Margarornis, Hellmayrea and Pseudocolaptes, and clades and mostly at 13-18º south in Peru and Aphrasture in the south), with little or no net Bolivia, and mainly at the upper tree-line and diversification, at least not during the Pleisto- upper montane valleys (Fjeldså & Irestedt cene (Valderrama et al. MS). 2009). As illustrated in Fig. 3, the geographical In the New World flycatcher group, phy- patterns of diversification changed in time. logenetic expansions outside the topical low- The lowland rainforest clades diversified lands, and in open habitats, happened only mainly during the Miocene, with some shifts from the mid-Miocene, and only in one ma- over time, but apparently there was a down- jor clade (Tyrannidae sensu stricto; Ohlson et shift in the radiation of rain-forest groups, and al. 2009), with different subclades moving these groups were only moderately elevation into distinct areas, thus the Xolmini radiat- tolerant and successful in colonizing the rising ing mainly in southern open habitats and the tropical Andes region. The philydorine genus barren Andean puna, while the Ochthoecini Thripadectes, which radiated in the Andes since radiated in the montane cloud-forest zone 8-9 Mya (Derryberry et al. 2011), is the most (García-Moreno et al. 1998) and the Contopini noteworthy exception. World wide, it seems dispersed to North America. that speciation in tropical lowland biomes Oscine groups arriving from the north (Weir ceased during the last million years of great et al. 2009) diversified first of all in mountain climatic instability (Päckert et al. 2011 for Asia; ridges of Central America and Colombia (Fjeld- Fjeldså et al.2007 for Africa). så & Rahbek 2006; Klicka et al. 2007; Sedano In contrast, the Andean clades continued & Burns 2009; Lovette et al. 2010) and after a to diversify, and various synallaxine groups rapid initial burst of speciations in this region

119 Fjeldså several lineages of finches and tanagars un- habitats are often described as young environ- derwent phylogenetic expansion further south ments, but the orocline as such has a long his- in the Andes and in the tropical and southern tory (Garzione et al. 2008; Mamani et al. 2010). subtropical lowlands (like in amphibians; see As a consequence of the convergence of Santos et al. 2011). Other colonizing groups South America with the oceanic Nazca Plate, arrived through trans-oceanic sweepstakes dis- marine terranes were accreted to the north- persal (vireos, thrushes, mockingbirds, eupho- western margin of the continent (Ecuador to nias), radiated mainly in the lowlands, but over Venezuela) and a proto-Andean chain devel- all with significant flexibility in their life zone oped along the entire western plate boundary. associations. Although oscine and suboscine Here we need to acknowledge that even small groups have markedly different biogeographic mountains near tropical coasts will be distinct histories, the coarse-scale diversity patterns are from the surrounding lowlands in terms of remarkably similar. climate and habitat structure with stunted, microphyllic and epiphyte-laden cloud forest Linking diversity patterns and earth history. The down below 1000 m elevation (Foster 2001; most basal members of the extant suboscine Bruijnzeel et al. 2010). This may have allowed groups inhabit ancient cratonic areas (Gui- physiological specialization for these cool/wet ana and Brazil Shields) and some parts of the habitats and development of a distinct high- southern Andes and there is significant con- land avifauna from already from an early stage. nectance in the east between the Guianan and Increasing uplift of mountain chains lead Brazilian shield faunas. Apparently some of the to formation of several thrusting planes and old rainforest groups may have their origin in thickening of the continental crust, and this the southern Atlantic forest of Brazil but ex- load caused a subsidence of the lowlands to panded along the western edge of the Brazilian the east, first with formation of a narrow ax- cratonic shield into the western Amazon basin ial grove, whereby the water from the Andes (Batalho-Filho et al.in press). The tropical low- could flow north to the Caribbean (Maracaibo) land groups invaded the Andean habitats only or south to the Paraná. Thus, the early fauna marginally (Thripadectes); yet some clades of the of the tropical Andes (Fig. 2b) may have been mesic tropics colonized the Chocó region by more or less isolated from that of the Brazil- circumventing the Colombian cordilleras, or by Guiana area. crossing the low passes of southern Colombia During the mid-Tertiary the Bolivian oro- or northern Peru (Haffer 1974). cline underwent significant crustal thickening The comparison of Andean and Amazo- and bending (Mamani et al. 2010). The contact nian clades that diverged in the mid-Miocene, (“Chapare Buttress”) between the thrust front well before the final uplift of the northern An- of the Bolivian Andes and the subsurface edge des, is a novel demonstration of long histori- of the Brazilian Shield formed a structural di- cal isolation of clades in the Andean orocline vide between the Amazonas and Paraná sys- and specialization for this misty environment. tems and faunal exchange between the Andes The extraordinary biodiversity at the Andean- region and uplands of southern Brazil, which Amazonian interface (Fig. 1) emerges as an ef- explains why many clades are shared between fect of overlap (at the spatial resolution of this the Andes region and the southern Brazilian grid) of faunas with different histories. uplands (Fig. 2b). As the weight of the Boliv- To understand the historical separation ian Andes continued to rise there was a large of Andean and Amazonian clades we need to geological subsidence, leading to the formation look into the geological history. The Andean of the present Beni plains (Hanagarth 1993,

120 Diversification of the Neotropical Avifauna

Silva 1994), and today only small fragments of the patch dynamics and high productiv- are left in southeastern Bolivia of the former ity of the floodplains but generally within the high land surface, and the divide between the same region, until the wetlands were filled up Amazon and Paraná basins shifted south (Lun- by megafans of sediment and the drainage dberg et al. 1998: 42). The new, hydrologically towards the Atlantic Ocean was finally es- unstable environments in the Beni-Chaco re- tablished. Thus, the diverse Amazonian and gion became an insurmountable barrier for the Andean faunas could finally merge, leading to birds adapted to rugged and well-drained land- the incredible present species diversity in the scapes, leading to the divergence from the late transition zone (Fig. 2b). The establishment of Miocene to early Pleistocene of Andean and new rivers channels finally lead to distinct vi- South Brazilian sister taxa (see Fig. 2b). cariant patterns and raised species richness in Within the tropical Andes, the most recent grid-cells that include para-species occupying diversification took place in the young eastern opposite river banks (see Figs 3 c and d). Cordillera of Colombia-Venezuela (Fig. 3e) Diversification is tightly linked with- ge and Bolivia (Fig. 3d and e). In the southern ology and landscape evolution in the upper parts, this corresponds to where jagged con- Amazone basin up through the Miocene and figuration of the eastern Andean ridges form Pliocene, and in general there has been a slow- climatic pockets that are well protected against down in diversification after the present drain- the ecological disturbance by south polar age pattern was established. In general, the winds, notably during glacial periods (Fjeldså bird populations inhabiting the Brazilian and et al. 1999). This lead to an extraordinary peak Guinanan shields are widespread and have un- of specie s diversity 12-18ºS of the equator. dergone little diversification in recent geologi- Opportunities for diversification in the cal times. Amazon Basin may have shifted much in the course of the conversion from the wide- Speciation mechanisms. Low mean root-path dis- northwest-flowing flood basin to the current tance in the tropical lowland biota has been eastward-running Amazon basin since the late taken as evidence of the tropical niche con- Miocene (Hoorn & Wesselingh 2010) or even servation hypothesis, as opposed to assumed as late as the Pliocene (Latrubesse et al. 2010). innovative adaptations characterizing the more In the early Tertiary, this region was charac- terminal radiations in the Andes (Hawkins et terized by a sub-Andean grove draining north al. 2006; Fjeldså & Irestedt 2009; Löwenberg- to Maracaibo (Venezuela), but gradually shift- Neto et al. 2011). The high diversity in the ing east to form large tectonically controlled lowlands is mainly associated with the enor- sedimentation basins (Solomões/Pebas) over mous extent and complex geological history large parts of western Amazonia. Some dis- of the Amazon basin, but the lack of recent agreement exists over the nature and timing speciation in the Amazon lowlands suggests of these wetlands, but apparently there were that Pleistocene forest refuges (Haffer 1974), enormous freshwater swamp habitats and ma- if they existed, were not drivers of specia- rine incursions (Lundberg et al. 1998; Hoorn tion. During the upper Pleistocene there was & Wesselingh 2010) and in the late Miocene intensive speciation (among furnariids) only some tectonic deformation of foreland ridg- in the western Pampean region and in the An- es (Divisor-Contamana ranges) in northern des (Fig. 3e). The recent radiations are closely Peru are reflected in Figs 3 b and c. We must associated with the upper montane forest therefore assume that the Amazonian avifauna and tree-line zone (Fjeldså & Irestedt 2009), persisted by moving around, taking advantage mainly in clades that originated south of the

121 Fjeldså

Amazon area (a similar situation has now been the importance of factors that promote local described for the upper montane forest zone persistence during periods of environmental in the Sino-Himalayan mountains, where lin- stress, when many species survive only as local eages of northern temperate origin diversified relict populations. The most prominent local intensively during the Pleistocene; see Päckert aggregation of restricted range species in the et al. 2011). This represents a habitat band that southern half of the tropical Andean hotspot may be easily fragmented because of the nar- are in valley systems that are protected by sharp row configuration of this habitat band and bends on the eastern Andean ridges against the steep terrain with many physical barriers the impacts of south polar winds, which rep- (Graves 1988). In addition to this comes the resent a disturbing agent in the Pleistocene complex ways in which the topography creates climate (Fjeldså et al. 1999). The most inten- a mosaic of local climates,with local pockets sive recent radiation took place in resident spe- of very predictable conditions. Areas with cies of dense thickets and elfin forest patches intensive recent speciation in the Andes cor- (Scytalopus, Cranioleuca, Schizoeaca), where the responds closely with areas with many small amount of gene flow may be limited (cf. Kisel distributions (Fig. 1d), in contrast to the lack & Barraclough 2010), but interestingly also the of recent speciation in areas with high mean widespread Cinclodes and Muscisaxicola species range-size on the tropical savanna regions and of the barren alpine habitats maintain rapid much of the Amazon/Guiana region (Fig. 3e). speciation. Apparently, few groups were well adapted Because of the restricted distributions of to cope with highland condition and to radiate many Andean endemics, each species can ac- in this harsh environment, leading to phylo- cumulate local adaptations that allow them genetically clustered communities in the high- to become more abundant, whereas in more lands (Graham et al. 2009; Parra et al. 2010). widespread species the gene flow across sub- Most speciation took place within a narrow optimal environmental gradients and over climate window, with sister species gener- long distance may restrict local adaptation and ally replacing each other at similar elevations thus the local abundance. Species must either on different slopes (Cadena et al. 2011). This be sufficiently generalist to utilize a broad suggests niche conservatism in the therminal habitat mosaic, including suboptimal sites, or niches, while segregation in different eleva- they must survive in situ, by tracking specific tional zones (or in different structural habi- habitat zones where they can maintain dense tats) on the same slopes were often delayed populations and remain resilient (Williams et by several million years (García-Moreno & al. 2009; Reif et al. 2010). The abundance of Fjeldså 1997). There are few cases of marked many range-restricted species, which should elevational shifts (e.g., Cinclodes, Leptasthenura, be well known among Andean ornithologists Cranioleuca). Thus, the key to understand inten- (although not documented quantitatively for sive radiation may be related to conditions that these difficult habitats) is contrary to gen- allow remnant populations to persist in con- eral theory of range-abundance relationships stantly favorable local environments within the (Brown 1984; Gaston et al. 1997). Analyzing montane habitat mosaic. This is rarely possible the mutualistic networks of plants and hum- outside the tropics. Speciation has traditionally mingbirds at 31 study sites spanning a wide been explained physical barriers between areas, range of climate regimes, Dalsgaard et al. but many replacements appear to be second- (2011) found that the highest degree of mu- ary contact zones (in places with no obvious tualistic specialization in montane forests in physical barriers) and it is important to note Costa Rica, Colombia and coastal mountains

122 Diversification of the Neotropical Avifauna in southern Brazil. Across all 31 study sites, are really outstanding, considering the short the degree of mutualistic connectedness was time span and the limited geographical space well explained from “climate change velocity” within which they have radiated. With the in- (Loarie et al. 2009), which, based on global tense speciation in this region we may wonder climate models, describes the rate at which whether diversification can continue. species must migrate to keep track of climate Several studies have demonstrated declin- change. Comparing present-day conditions ing diversification rates over time, suggesting a with a global climate model for the last gla- saturation as the ecological niche space is filled cial maximum, the lowest levels of “climate up (e,g,, Phillimore & Price 2008; Rabosky change velocity” were found in tropical mon- 2009; Rabosky & Lovette 2008; Sedano & tane regions, and explains well the global varia- Burns 2010). McPeek (2008) considered that tion in occurrence of local endemic species slow-down may be a general trend, and Rabos- of amphibians, mammals and birds (Sandel et ki (2010) went on to suggest ecological limits al. 2011). Thus, high local endemism can be as an alternative to speciation and extinction in explained from conditions that allow species explaining diversity patterns. Against this view, to remain in the same geographical area, and Morton et al. 2010 and Wiens (2011) argues specialize to local biotic and abiotic conditions, that biological diversity continues to grow, and in spite of the instability of the global climate. indeed the great speciator groups of South It has been predicted that the current glob- America (core tyrannids, furnariides and tana- al change may drive montane spices out of gers; Barker 2011) could be good examples. In the local elevational gradient, leading to large- all groups, the most intensive diversification scale extinction of montane birds (Sekercioglu takes place within a rather limited geographical et al. 2008, La Sorte & Jetz 2010). This might area in the tropical Andes region. The analysis well apply to isolated, cone-shaped mountains, of furnariid disversification (Derryberry et al. but may be less relevant in large and com- 2011) suggests a continuously high rate of spe- plex montane regions, where conditions may ciation as the diversification has shifted from vary over very short distances in the complex the Amazon lowlands to other ecoregions with habitat mosaic (see Scherrer & Körner 2011). a very high landscape complexity. The most Global climate models based on interpolation recent phylogenetic expansion in this group, between widely scattered weather stations can- as well as of crown group tyrannids, moves not capture the complex local variation within northwards in the tropical Andes region, into the habitat mosaics of large mountain regions, the areas with maximum diversity of nine-pri- where pockets of extremely stable conditions maried oscines. Although these groups often may exist locally because of interactions be- feed together in mixed feeding parties, they tween wind systems, atmospheric stratification differ markedly in feeding methods and micro- and topography. habitats, and may therefore not interfere much in their use of food resources. Other examples Are communities saturated? The terminal ra- of continuously high diversification rates are diations of the super-diverse clades of hum- emerging (e.g., Fritz et al. 2011) for groups that mingbirds, tyrannids, furnariids and tanagers have undergone large geographical expansions all took place in areas characterized by low into new geographical areas. climate change velocity within the tropical It is more questionable what happens in Andes region. Some subclades (coquette and ecoregions that are structurally less complex brilliant hummingbirds; Cranioleuca, Asthenes/ and where the species are widespread, move in Schizoeaca, Scytalopus and mountain tanagers) response to climatic harshness and instability

123 Fjeldså and thus are under shifting selective pressures. and the Amazonian forests avifaunas represent Here, the general range-abundance relation- distinct historical events. J.Orn.153: xxx-yyy. ships (Brown 1984) could well apply, and the Bates JM, Cracraft J & Hackett SJ (1998) Area- generalist species may squeeze out the local relationships in the Neotropical lowlands: specialists. An hypothesis based on raw distributions of Further studies of diversification rates need Passerine birds. J. Biogeogr. 25: 783-793. to be comprehensive, covering large taxonomic Brown JH (1984) On the relationship between assemblages at continent-wide or global scale, abundance and distribution of species. Am Nat and should include data on community struc- 124:255-279. ture, phylogenetic clustering as well as niche Bruijnzeel LA, Scatena FN & Hamilton LS 2010. segregation. This next generation of studies Tropical Montane Cloud Forests. Science for can start now, as large distributional databases Conservation and Management. Cambridge U.P., and large phylogenies become available, and as Cambridge. we obtain more ecological data: we now need Burns KJ & Racicot RA 2009. Molecular to look at networks and community structure, phylogenetics of a clade of lowland tanagers. analyzing packing of niches according to mor- Implications for avian participation in the Great phological segregation (as done already for fur- American Interchange. Auk 126: 635-648. nariids; Derryberry et al. 2011) and resource Cadena CD, Kozak KH, Gómez JP, Parra JL, Mc- use, and relatedness within local communities, Cain CM, Bowie RCK, Carnaval AC, Moritz C, and also on large geographical scales. Rahbek C, Roberts TE, Sanders NJ, Schneider CJ, VanDerWal J, Zamudio KR & Graham CH Acknowledgements 2011. Latitude, elevational climatic zonation and speciation in New World vertebrates. Proc. First of all, I will thank the organizing com- R. Soc. B. doi:10.1098/rspb.2011.0720. mittee of the IX Neotropical Ornithological Dalsgaard B, Magård E, Fjeldså J, Gonzáles AMM, Congress for inviting me. Jan Ohlson and Rahbek C, Olesen JM, Ollerton J, Alarcón R, Martin Irestedt are thanked for many years of Araujo AC, Cotton PA, Lara C, Machado CG, phylogenetic work, and Louis Hansen for da- Sazima I, Sazima M, Timmermann A, Watts S, tabase management. The Danish National Sandel B, Sutherland WJ & Svenning J-C 2011. Research Foundation is acknowledged Specialization in plant-hummingbird networks for their support to the Center for Mac- associated with Quaternary climate-change ve- roecology, Evolution and Climate. locity. PloS One 6, e25891. Derryberry EP, Claramunt S, Derryberry G, References Chesser RT, Cracraft J, Aleixo A, Pérez-Emán J, Remsen JV & Brumfield RT 2011. Lineage Barker FK 2011. Phylogeny and diversification of diversification and morphological evolution in modern passerines. Pp 235-256 in G Dyke & G a large-scale continental radiation: the Neo- Kaiser (eds) Living Dinosaurs, The Evolutionary tropical ovenbirds and woodcreepers (Aves: History of Modern Birds. Wiley-Blackwell, Furnariidae). Evolution, doi:10.1111/j.1558- Chichester, U.K. 5646.2011.01374.x Barthlott, W., Mutke, J., Rafiqpoor MD, Kier G., Fjeldså J, Lambin E & Mertens B1999. Correlation Kreft H 2005.Global centres of vascular plant between endemism and local ecoclimatic sta- diversity. Nova Acta Leopoldina 92: 61-83. bility documented by comparing Andean bird Batalha-Filho H, Fjeldså J, Fabre P-H & Miyaki CY distributions and remotely sensed land surface (in press) Connections between the Atlantic data. Ecography 22: 63-78.

124 Diversification of the Neotropical Avifauna

Fjeldså, J., Irestedt, M. & Ericson, P. 2005. Molecular Hanagarth W 1993. Acerca de la geoecologia de data reveal some major adaptational shifts in the las sabanas del Beni en el noreste de Bolivia. early evolution of the most diverse avian family, Instituto de Ecología, La Paz. the Furnariidae. J. Orn. 146:1-13. Hawkins BA, Diniz-Filho JAF & Soeller SA 2005. Fjeldså J & Irestedt M 2009. Diversification of the Water links the historical and contemporary South American avifauna: patterns and implica- components of the Australian bird diversity tions for conservation in the Andes. Ann. Miss. gradient. J. Biogeogr. 32: 1035-1042. Bot. Garden 96: 398-409. Hawkins BA, Diniz-Filho JAF, Jaramillo CA & Fjeldså J, Irestedt M, Jønsson KA, Ohlson JI & Soeller SA 2006. Post-Eocene climate change, PGP Ericson (2007) Phylogeny of the oven- niche conservatism, and the latitudinal diversity bird genus Upucerthia: A case of independent gradient of New World birds. J. Biogeogr. 33: adaptations for terrestrial life. Zool. Scripta 36: 770-780. 133-141. Hoorn C & Wesselingh, F.P. (eds; 2010) Amazonia: Fjeldså J, Johansson U, Lokugalappatti LGS & Landscape and Species Evolution. A Look into Bowie RCK 2007. Diversification of African the Past. Wiley Blackwell. 482 pp. greenbuls in space and time: linking ecological Irestedt M, Fjeldså J, Dalén L & Ericson PGP and historical processes. J. Orn. DOI 10.1007/ 2009. Convergent evolution, habitat shifts and s10336-007-0179-4. variable diversification rates in the ovenbird- Fjeldså J & Rahbek C 2006. Diversification of tana- woodcreeper family (Furnariidae). BMC gers, a species rich bird group, from lowlands Evolutionary Biology 9: 268. to montane regions of South America. Integr. Jetz W, Rahbek C & Colwell RK 2004. The Comp. Biol. 46: 72-81. coincidence of rarity and richness and the Foster P 2001. The potential negative impacts of potential signature of history in centres of global climate change on tropical montane cloud endemism. Ecol. Letters 7:1180-1191. forest. Earth-Science Reviews 55: 579-582. Kisel Y & Barraclough TG 2010. Speciation has a Fritz SA, Jønsson KA, Fjeldså J & Rahbek C 2011. spatial scale that depends on levels of gene flow. Diversification and biogeographic patterns in four Amer. Nat. 175:316-334. island radiations of passerine birds. Evolution Klicka J, Burns K & Spellman GM 2007. Defining doi:10.1111/j.1558-5646.2011.01430.x a monophyletic Cardinalini: a molecular Garzione CN, Hoke GD, Libarkin JC, Withers S, perspective. Mole. Phyl. Evol. doi:10.1016/j. MacFadden B, Eiler J, Ghosh P & Mulch A (2008) ympev.2007.07.006 Rise of the Andes. Science 320: 1304-1307. La Sorte FA & Jetz W (2010) Projected range con- Garcia-Moreno J, Arctander P & Fjeldså J 1998. Pre- tractions of montane biodiversity under global Pliostecene differentiation among chat-tyrants. warming. Proc. Royal Soc. B doi:10.1098/ Condor 100: 629-640. rspb.2010.0612. Gaston KJ, Blackburn TM & Lawton JH Latrubesse E, Cozzual M, Rigsby C, Silva S, Absy 1997. Interspecific abundance-range size ML & Jaramillo C 2010. The Late Miocene relationships: An appraisal of mechanisms. J. paleogeography of the Amazon basin and the Anim. Ecol. 66: 579-601. evolution of the Amazon River. Earth Science Graham CH, Parra JL, Rahbek C & McGuire Reviews 99: 99-124. JA 2009. Phylogenetic structure in tropical Lovette IJ, Pérez-Emán JL, Sullivan JP, Banks RC, hummingbird communities. PNAS 106: 19673- Fiorentino I et al. 2010. A comprehensive multi- 19678. locus phylogeny for the wood-warblers and a re- Haffer J 1974. Avian speciation in tropical South vised classification of the Parulidae (Aves). Mol. America. Publ. Nuttall Orn. Club 14: 1-390. Phyl. Evol. Doi:10.1016/j.ympev.2010.07.018.

125 Fjeldså

Löwenberg-Neto P, de Carvalho CJB & Hawkins Phillimore AB & Price TD 2008. Density-dependent BA 2011. Tropical niche conservatism as a his- cladogenesis in birds. PLoS Biol. 6: e71. torical narrative hypothesis for the Neotropics: Rabosky DL, Donnellan SC, Talaba AL & Lovette a case study using the fly family Muscidae. J. IJ 2007. Exceptional among-lineage variation Biogeogr. 38: 1936-1947. in diversification rates during the radiation of Lundberg et al. 1998 Australia’s most diverse vertebrate clade. Proc. Mamani M, Wörner G & Sempere T 2010. Geo- Roy. Soc. B: Biol. 274: 2915-2923. chemical variations in igneous rocks of the Rabosky DL 2009. Ecological limits and diversifica- Central Andean Orocline (13º to 18ºS): Trac- tion rate: alternative paradigms to explain the ing crustal thickening and magma generation variation in species richness among clades and through time and space. Geol. Soc. Am. Bull. regions. Ecology Letters 12: 735-743. 122: 162-182. Rabosky DL 2009. Ecological limits and diversifica- McPeek MA 2008. The ecological dynamics of tion rate: alternative paradigms to explain the clade diversification and community assembly. variation in species richness among clades and Am. Nat. 172: E270-E284. regions. Ecology Letters 12: 735-743. Morton H, Potts MD & Plotkin JB 2010. Inferring Rabosky DL 2010. Primary controls on species the dynamics of diversification: a coalescent ap- richness in higher taxa. Systematic Biology 59: proach. PLoS Biology 8(9) e1000493. 634-645. Moyle RG, Chesser RT, Brumfield RT, Tello JG, Rahbek C & Graves GR 2001. Multiscale assess- Marchese DJ & Cracraft J 2009. Phylogeny ment of patterns of avian species richness. and phylogenetic classification of the antbirds, Proc. Natl. Acad. Sci. U.S.A. 98: 4534-4539. ovenbirds, woodcreepers and allies (Aves: Pas- Rahbek C, Gotelli NJ, Colwell RK, Entsminger GL, seriformes: infraorder Furnariides). Cladistics Rangel TFLBB & Graves GR 2006. Predicting 25: 386-405. continental-scale patterns of bird species Müller P 1976. The Dispersal Centres of Terrestrial richness with spatially explicit models. Proc. Vertebrates in the Neotropical Realm. Dr. W. Roy. Soc. London, Ser. B, Biol. Sci. 274:165-174. Junk, The Hague. Reif J, Hořák D, Sedláček O, Riegert J, Pešata L. Jrázs- Ohlson JI, Fjeldså J & Ericson PGP 2008. Tyrant lý Z, Janeček Š & Storch D 2006. Unusual abun- flycatchers coming out in the open: phylogeny dance-range size relationship in an Afromontane and ecological radiation of Tyrannidae (Aves: bird community: the effect of geographical isola- Passeriformes). Zool. Scripta 37: 315-335. tion. J. Biogeography 33: 1959-1968. Ohlson JI, Irestedt M, Ericson PGP & Fjeldså J Ribas CC, Aleixo A, Nogueira ACR, Miyaki CY & (in review) Phylogeny and classification of the Cracraft J 2011. A palaeobiogeographic model New World Suboscines (Aves, Passeriformes). for biotic diversification within Amazonia over Zootaxa? the past three million years. Proc. Royal Soc. B Päckert M, Martens J, Sun Y-H, Severinghaus LL, doi:10.1098/rspb.2011.1120. Nazarenko AA, Ting J, Töpfer T & Tietze DT Sandel B, Arge L, Dalsgaard B, davies RG, Gas- 2011. Horizontal and elevational phylogeographic ton KJ, Sutherland WJ & Svenning J-C 2011. patterns of Himalayan and Southeast Asian forest The influence of late quaternary climate- patterines (Aves: Passeriformes). J. Biogeogr. change velocity on species endemism. Science Doi:10.1111/j.1365-2699.2011.02606.x doi:10.1126/science.1210173. Parra JL, McGuire JA & Graham CH 2010. Sanín C, Jiménez J, Fjeldså J, Rahbek C & Cadena Incorporating clade identity in analyses of CD (in review) How much spatial variance in phylogenetic community structure: an example broad-scale species richness can be accounted with hummingbirds. Amer. Natur. 176: 573-587. for by diversification rates? BioLetters?

126 Diversification of the Neotropical Avifauna

Santos JC, Coloma LA, Summers K, Caldwell JP, the Andes on the evolutionary differentiation Ree R & Cannatella DC 2011. Amazonian am- of a montane forest bird (Premnoplex brunnescens, phibian diversity is primarily derived from late Furnariidae). J. Biogeogr. Miocene Andean lineages. PLoS Biology … Weir JT 2006. Divergent timing and patterns of Scherrer D & Körner C 2011. Topographically species accumulation in lowland and highland controlled thermal-habitat differentiation Neotropical birds. Evolution 60: 842-855. buffers alpine plant diversity against climate Weir JT, Bermingham E & Schluter D 2009. The warming. Journal of Biogeography 38: 406-416. Great American Biotic Interchange in birds. Sedano RE, Burns KJ 2008. Molecular phylogenetics PNAS 106: 21737-21742. and biogeography of a clade of Neotropical Wiens JJ 2004. Speciation and ecology revisited: tanagers (Aves: Thraupini). J. Biogeogr. 37: 325- phylogenetic niche conservatism and the origin 343. of species. Evolution 53: 193-197. Sekercioglu CH, Schneider SH, Fay JP & Loarie SR Wiens JJ 2011. The causes of species richness pat- (2007) Climate change, elevational range shifts terns across space, time, and clades and the role and bird extinctions. Conservation Biology 22: of “ecological limits”. The Quaterly Review of 140-150. Biology 86: 75-86. Silva 1994 Wilf P, Cúnero NR, Johnson KR, Hicks JF, Wing Tello JG, Moyle RG, Marchese DJ & Cracraft J SL & Obradovich JD 2003. High plant diversity 2009. Phylogeny and phylogenetic classification in Eocene South America: Evidence from of the tyrant flycatchers, cotingas, manakins Patagonia. Science 300: 122-125. and their allies (Aves: Tyrannides). Cladistics 25: Williams SE, Williams YM, VanDerWal J, Isaac 429-467. JL, Shoo LP & Johnson CN 2009. Ecological Tognelli MF & Kelt DA 2004. Analysis of determi- specialization and population size in a nants of mammalian species richness in South biodiversity hotspot: How rare species avoid America using spatial autoregressive models. extinction. PNAS 106: 19737-19741. Ecography 27:427-436. Zachos J, Pagani M, Sloan L, Thomas E & Billups Valderrama E, Pérez-Emán JL, Brumfield RT, Cuervo K 2001. Trends, rhythms, and aberrations in AM & Cadena CD (in review) The influence of global climate 65 Ma to present. Science 292: the complex topography and dynamic history of 686.693.

127