Connections Between the Atlantic and the Amazonian Forest Avifaunas Represent Distinct Historical Events

J Ornithol (2013) 154:41–50 DOI 10.1007/s10336-012-0866-7 ORIGINAL ARTICLE Connections between the Atlantic and the Amazonian forest avifaunas represent distinct historical events Henrique Batalha-Filho • Jon Fjeldsa˚ • Pierre-Henri Fabre • Cristina Yumi Miyaki Received: 4 October 2011 / Revised: 20 March 2012 / Accepted: 25 May 2012 / Published online: 16 June 2012 Ó Dt. Ornithologen-Gesellschaft e.V. 2012 Abstract There is much evidence to support past contact important roles in these connections were geotectonic between the Atlantic and the Amazon forests through the events during the late Tertiary associated with the uplift of South American dry vegetation diagonal, but the spatio- the Andes (old connections) and Quaternary climate temporal dynamics of this contact still need to be investi- changes that promoted the expansion of gallery forest gated to allow a better understanding of its biogeographic through the Cerrado and Caatinga in northeastern Brazil implications for birds. Here, we combined phylogenetic (young connections). Our results provide the first general data with distributional data using a supermatrix approach temporal and spatial model of how the Atlantic and in order to depict the historical connection dynamics Amazonian forests were connected in the past, which was between these biomes for New World suboscines. We derived using bird data. examined the variation in divergence time and then compared the spatial distributions of taxon pairs representing Keywords Neotropical region Á New World suboscines Á old and recent divergences. Our results pointed to two Supermatrix Á Worldmap Á Biogeography Á Miocene Á distinct spatiotemporal pathways connecting the Atlantic Quaternary and the Amazonian forests in the past: (1) old connections (middle to late Miocene) through the current southern Zusammenfassung Cerrado and Mato Grosso and the transition towards the Chaco and palm savannas of Bolivia and Paraguay; (2) Verbindungen zwischen atlantischen und amazonischen young connections (Pliocene to Pleistocene) that possibly Waldvogelfaunen spiegeln distinkte historische Ereig- occurred through the Cerrado and Caatinga in northeastern nisse wider Brazil. We suggest that the main events that played Zahlreiche Hinweise belegen ehemalige Kontakte zwi- Communicated by T. Gottschalk. schen atlantischen und amazonischen Wa¨ldern u¨ber die diagonal durch Su¨damerika verlaufende Trockenvegeta- Electronic supplementary material The online version of this tionszone hinweg, allerdings bedarf die raumzeitliche article (doi:10.1007/s10336-012-0866-7) contains supplementary Dynamik dieser Kontakte noch na¨herer Untersuchung, um material, which is available to authorized users. deren biogeografische Auswirkungen auf Vo¨gel besser H. Batalha-Filho (&) Á C. Y. Miyaki verstehen zu ko¨nnen. Hier fassten wir phylogenetische Laborato´rio de Gene´tica e Evoluçaõ Molecular de Aves, Daten mit Verbreitungsdaten in einer Supermatrix-Analyse Departamento de Gene´tica e Biologia Evolutiva, Instituto de zusammen, um so die Dynamik der historischen Verbin- Biocieˆncias, Universidade de Saõ Paulo, Rua do Mataõ 277, Cidade Universita´ria, Saõ Paulo, SP 05508-090, Brazil dungen zwischen diesen Biomen fu¨r Neuwelt-Suboscine e-mail: [email protected]; [email protected] abzubilden. Wir untersuchten die Variation im Zeitpunkt der Artentrennung und verglichen dann die raümliche J. Fjeldsa˚ Á P.-H. Fabre Verteilung von Taxonpaaren, die alte und rezente Tren- Center for Macroecology, Evolution and Climate at the Natural History Museum of Denmark, University of Copenhagen, nungsereignisse repra¨sentieren. Unsere Ergebnisse deuten Copenhagen, Denmark auf zwei distinkte raumzeitliche Verbindungswege zwischen 123 42 J Ornithol (2013) 154:41–50 atlantischen und amazonischen Wa¨ldern in der Vergan- et al. 2007 for plants), and this reinforces the idea that the genheit hin: (1) alte Verbindungen (Mittleres bis Oberes dry vegetation diagonal plays an important role in the Mioza¨n) durch den heutigen su¨dlichen Cerrado und Mato connection of theses biomes. Similarly, there is evidence Grosso sowie den U¨ bergang zum Chaco und den Palmsa- from Africa supporting episodes of faunal connection vannen Boliviens und Perus; (2) junge Verbindungen across the ‘‘arid corridor’’ in eastern Africa between the (Plioza¨n bis Pleistoza¨n), mo¨glicherweise durch die Cerra- main rainforest tracts and those near the Indian Ocean (the dos und die Caatinga im nordo¨stlichen Brasilien. Unserer African Rift; Couvreur et al. 2008; Tolley et al. 2011). Ansicht nach spielten die folgenden Hauptereignisse eine However, questions concerning the timing and nature of wichtige Rolle fu¨r diese Verbindungswege: geotektonische this connection are still to be conclusively answered. Such Ereignisse wa¨hrend des spa¨ten Tertia¨rs im Zusammenhang questions include: were the AF and AM biota connected mit der Auffaltung der Anden (alte Verbindungen) sowie just once in the past? Was the connection related solely to Klimaa¨nderungen im Quarta¨r, die die Ausbreitung von Quaternary climate changes? If not, when did this (these) Galeriewa¨ldern durch Cerrado und Caatinga im nordo¨stli- connection(s) occur? Were there different pathways con- chen Brasilien begu¨nstigten (junge Verbindungen). Auf der necting AM and AF? Grundlage von Vogeldaten stellen unsere Ergebnisse die Possible explanations for the observed patterns could be erste allgemeine Na¨herung fu¨r Zeitraüme und die Art und extinction, dispersal, or vicariance (Crisci et al. 2003). Weise dar, wie atlantische und amazonische Wa¨lder in der A basic assumption of vicariance biogeography (as well as Vergangenheit in Verbindung standen. panbiogeography) is that generalized patterns can be detected by searching for concordance in area cladograms (or tracks) across multiple lineages. Although there are numerous known cases of different historical events gen- Introduction erating similar patterns (e.g., Tuomisto 2007), there is still a widespread tendency to treat similar patterns as indica- It is well known that many sister species and lineages are tions of common biogeographic events. Besides, distinct disjunctly distributed in the Brazilian Atlantic Forest (AF) co-distributed taxa could present similar cladogenetic splits and in the Amazon Basin (AM), but this biogeographic if speciation and/or diversification are driven by vicariance, pattern has never been explored in depth for birds. The two as the distributions of the ancestor populations would have biomes are separated by a broad diagonal of more xeric been affected in a similar way when the barriers to dis- habitats comprising the Chaco, the Cerrado uplands, and persal formed. the Caatinga (Ab’Saber 1977), and together they encom- However, it is important to distinguish true congruence, pass one of the most diverse tropical forests of the world. where the taxa and areas share the same history (Cracraft There is much evidence to support past contact between the 1985, 1988) from ‘‘pseudocongruence’’ (Cunningham and AF and the AM through this dry vegetation diagonal (Auler Collins 1994; Donoghue and Moore 2003), where cyclical et al. 2004; Auler and Smart 2001; Behling et al. 2000; processes (such as orbitally driven climatic/vegetational Costa 2003; Oliveira et al. 1999; Patton et al. 1997; Patton changes; Bennett 1990; Hooghiemstra et al. 1993) result in and Costa 1999; Vilela et al. 2009; Por 1992; Wang et al. the repetition of historical events. This could be a repeated 2004; Willis 1992). Palynological and geological data from process of range expansion and retreat. We also need to these studies cover the late Pleistocene (the last 0.9 mya) consider whether entirely different biogeographic events, and indicate that there were wetter periods that allowed the superimposed over millions of years, may in some cases expansion of gallery forest into the Cerrado and Caatinga, result in patterns that we perceive as being congruent. providing connections between the AF and the AM (Auler Recently, the integration of distributional and phyloge- et al. 2004; Auler and Smart 2001; Behling et al. 2000; netic data has given robust insights into diversification Oliveira et al. 1999; Wang et al. 2004). Costa (2003) processes and biogeographical patterns of tropical forests compared the phylogeographic patterns of small mammals (Fjeldsa˚ et al. 2007; Fjeldsa˚ and Irestedt 2009; Fjeldsa˚ and in the AF and the AM and found lineages from either the Rahbek 2006; Roncal et al. 2011). This kind of approach AF or the AM in the Cerrado. Costa (2003) also observed connects ecological and historical biogeographies and that some taxa from northern AF are more closely related gives insight into community assembly and species rich- to AM taxa than to southern AF forms. Silva (1996) ness patterns by considering the biogeographical history of showed that several birds from the AM and the AF show the species and clades that make up these patterns (Wiens distributions that extend along the Cerrado gallery forests. and Donoghue 2004). However, there are several species with disjunct distribu- In the work described in this paper, we applied this tions in these forested biomes (e.g., see Ridgely and Tudor approach to New World suboscine birds, a monophyletic 1994 for birds; see Vivo 1997 for mammals; see Martini group (Barker et al. 2004) with 1,200 extant species. This 123 J Ornithol (2013) 154:41–50 43 group evolved within South America, but some subclades that the current species-level taxonomy reflects relation-

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