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Rivers acting as barriers for bird dispersal in the Amazon

Rivers acting as barriers for bird dispersal in the Amazon Revista Brasileira de Ornitologia, 22(4), 363-373 ARTICLE December 2014 1,5 2 3,4 3 Alexandre M. Fernandes , Mario Cohn-Haft , Tomas Hrbek and Izeni Pires Farias Universidade Federal Rural de Pernambuco, UFRPE, Unidade Acadêmica de Serra Talhada, Serra Talhada, PE, Brazil. Instituto Nacional de Pesquisas da Amazonia, INPA, Manaus, AM, Brazil. Universidade Federal do Amazonas, UFAM, Manaus, AM, Brazil. University of Puerto Rico, Rio Piedras, UPR-RP, Puerto Rico, USA. Corresponding author: fernandesornito@gmail.com Received on 19 November 2014. Accepted on 10 December 2014. ABSTRACT: Morphological, vocal and genetic studies have shown that the Madeira River and its right bank tributaries delimit populations of primates and birds. We sequenced the cytochrome b gene (approx. 950 bp) for individuals of three suboscine passerine bird species, Glyphorynchus spirurus (Furnariidae), Willisornis poecilinotus (Thamnophilidae) and Schiffornis turdina (Tityridae), on opposite banks of the Madeira River and two of its right-bank tributaries, the Aripuanã and Jiparaná rivers. Phylogenetic hypotheses (parsimony, maximum likelihood and Bayesian analysis) revealed clades that have over 3.1% genetic differentiation on opposite banks of the Madeira River for G. spirurus, W. poecilinotus and S. turdina, suggesting that this river restricts gene flow among populations of these three species. The Jiparaná and Aripuanã rivers apparently separate distinct populations of G. spirurus, the smallest species we examined, but not those of the other two heavier bodied species, W. poecilinotus and S. turdina. In G. spirurus four clades with high levels of genetic differentiation (3.2–5.5%) were found to be delimited by the three rivers evaluated, whereas in W. poecilinotus and S. turdina no genetic structure across the Jiparaná and Aripuanã rivers was detected. In general, birds that are known to show population structure across the Madeira tributaries (Glyphorynchus spirurus, Hemitriccus minor, Hypocnemis rondoni, Herpsilochmus stotzi, and Hylophylax naevius) have body masses smaller than those of both Willisornis poecilinotus and Schiffornis turdina, but some exceptions are discussed. Future studies controlling for several variables are necessary to determine the extent to which body mass is a useful predictor of genetic population structure in understory suboscine passerines. KEYWORDS: Areas of endemism, body mass, comparative phylogeography, conservation, dispersal rate, suboscine birds. INTRODUCTION Recent studies of primates and birds in the Madeira-Tapajós interfluvium (M-T), also known as the Rondônia area of endemism (Cracraft 1985), have Avian distribution patterns are reasonably well known and influential in studies of evolutionary processes. suggested that smaller rivers also limit the distributions Jürgen Haffer was one of the first authors to compile of some taxa, thus forming smaller areas of endemism in bird distribution data to describe biogeographic patterns what was referred to as “mini-interfluvia” (Cohn-Haft et al. 2007). Willis (1969), in a study of birds of the genus in South America (Haffer 1974). His work made a Rhegmatorhina, was one of the first to document complex great contribution to evolutionary studies and to the formulation of speciation hypotheses in Amazonia. patterns of bird distributions in this area. He discussed The “centres of species endemism” he described remain the parapatric occurrence of Rhegmatorhina berlepschi largely unchanged in analyses of distribution patterns for and R. hoffmannsi within the M-T and suggested that the Madeira and Tapajós rivers have occasionally changed many avian groups. They have been generally accepted in their courses, resulting in the separation of populations subsequent works, and in the Amazon basin these regions are often delimited by large rivers (Haffer 1974; Cracraft and subsequent speciation. Van Roosmalen and 1985; da Silva & Oren 1996). Bird species are usually collaborators (1998) described geographic substitutions separated by the Amazon River and its major tributaries of species in primates of the genera Callithrix and Callicebus on opposite banks of small rivers within this such as the Negro, Madeira, Tapajós and Tocantins rivers interfluvium and described a new species of marmoset, (Cohn-Haft 2000; Ribas et al. 2012; D’Horta et al. 2013; Fernandes et al. 2012, 2013, 2014). Similar patterns are Callithrix humilis, that occurs only on the west bank also found in other Amazonian vertebrate taxa, including of the Aripuanã River. Subsequently, several other bird primates and butterflies (Wallace 1852; van Roosmalen et species in this region have been found to contain vocally, morphologically or genetically distinct populations, al. 1998; Hall & Harvey 2002), suggesting that rivers are with restricted distributions and geographic substitution important barriers to dispersal. Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias on opposite banks of Madeira tributaries, such as the rivers along their lower courses are roughly 3.0, 0.8, 0.4 Aripuanã and Jiparaná (or Machado) rivers (Cohn-Haft and 0.3 km, respectively. Each collection point had a et al. 2007; Isler et al. 2007; Tobias et al. 2008; Fernandes corresponding point located on the opposite bank and et al. 2012, 2013, 2014; Whitney et al. 2013a, b, c, d, therefore in a different interfluvium. For purposes of e). Similar geographic patterns, with different races being sampling and analyses, we suggest the existence of three separated by small Amazonian rivers, have also been mini-interfluvia within the M-T: Madeira-Jiparaná (MJ), found for butterflies (Hall & Harvey 2002). Aripuanã-Jiparaná (AJ) and Aripuanã-Tapajós (AT) Sardelli (2005) found genetic differentiation (Fig. 1). A maximum of 5 individuals per species were (cytochrome b, 500 bp) among morphologically collected at each sampling point, with the total sample indistinguishable populations of the Snethlage’s Tody- as follows: Willisornis poecilinotus (n = 45), Schiffornis Tyrant (Hemitriccus minor) apparently bounded by turdina (n = 23), and Glyphorynchus spirurus (n = 25) the Jiparaná and Aripuanã rivers. This study raised the (see Appendix). Specimens were deposited in the bird possibility of the existence of cryptic endemism in mini- collection of the National Institute for Amazonian interfluvia, which was subsequently investigated for Research (INPA), Manaus, Brazil, where tissue samples the other three species of passerine birds (Myrmeciza (muscle, heart and liver) were stored in liquid nitrogen hemimelaena, Glyphorynchus spirurus, Hylophylax naevius for molecular analyses. (Fernandes et al. 2012, 2013, 2014). Fernandes (2013) cited in a review a number of publications corroborating the importance of the mini-interfluvia, highlighting that these diversity patterns are a key (and possibly unique) Amazonian feature and that despite the fact that this fine- scale endemism is well known and recognized among systematists working in the Amazon, it is not taken into account in conservation plans. Fernandes (2013) pointed out that many taxa in this region, including those yet to be given formal scientific names, may now be endangered or even extinct. Thus it is of utmost importance to consider species that present this kind of fine scale differentiation in future conservation proposals. The objective of our study was threefold: 1) describe phylogeographic patterns for three species of suboscine passerines across the Rondônia area of endemism; 2) compare these patterns to those of other species know to have populations delimited by the Madeira, Aripuanã and Jiparaná rivers; and 3) investigate the relationship between degree of phylogeographic FIGURE 1. Collection points and the interfluvia sampled. Madeira- structure and ecological attributes in the light of the Jiparaná (MJ), Aripuanã-Jiparaná (AJ), Aripuanã-Tapajós (AT) and riverine barrier hypothesis. Left bank of the Madeira River (LM). MATERIAL AND METHODS We chose to study these three target species primarily because they are common, easy to collect, and widely Species studied and sampling design distributed across the entire Amazon basin. Although all three are suboscine passerines, they represent three distinct We studied three species of passerine birds belonging families and, as such, the results obtained in this study to three different families: Glyphorynchus spirurus can be assumed to be instances of independent evolution, (Furnariidae), Willisornis poecilinotus (Thamnophilidae), and, thus, support the generality of our conclusions. All and Schiffornis turdina (Tityridae). We sampled birds three species can be found in the same habitat (terra firme at 12 sites between the Tapajós and Madeira rivers and forest) but they differ in a variety of ecological attributes: five sites on the left bank of the Madeira River (LM; Glyphorynchus spirurus – This is a polytypic species Figure 1), with the final number of localities sampled per widely distributed in Neotropical lowland forests, species differing among the three species (see Results). occurring in Amazonia, Central America and along the Individuals were collected along the Madeira, Aripuanã, Atlantic coast of Brazil (Ridgely & Tudor 1994). Marantz Jiparaná and Roosevelt (the latter representing the largest et al. (2003) recognized thirteen subspecies, six of which tributary of the Aripuanã) rivers; the widths of these occur in the Brazilian Amazon. Three of these occur Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias within or adjacent to the Madeira basin: G. s. castelnaudii volumes using a Thermo Hybaid PCR Express thermal (west of the Madeira River to the Andes), G. s. albigularis cycler under the following conditions: (1) an initial (south-eastern Bolivia and Peru), and G. s. inornatus, denaturing step at 94°C for 5 min; (2) 35 cycles of the which occurs throughout the Brazilian portion of the following: 1 min at 92°C, 1 min at 48°C, and 1 min at Madeira-Tapajós interfluvium (Peters 1951; Marantz et 72°C; (3) a 10-min extension step at 72°C. Following al. 2003). With a body mass ranging from 10.5 to 21g PCR, correct fragment size and the presence of a single (typically 12.6-14.8 g in central Amazonia; Bierregaard, amplification product was confirmed via electrophoresis 1988), this is the smallest woodcreeper (Marantz et al. on 1% agarose gel. After amplification, the PCR 2003), and it is the smallest of the three species we studied. products were purified using a salt protocol (Sambrook It occurs in both terra firme and seasonally flooded et al. 1989). Sequencing was performed by the chain forests (várzea and igapó) (Marantz et al. 2003) and it termination method (Sanger et al. 1977), using a Big is moderately sensitive to environmental perturbation Dye Termination Kit (Applied Biosystems) following (Ferraz et al. 2007). Recently, Fernandes et al. (2013) the manufacturer’s specifications. The products of the found that populations of G. s. inornatus are delimited by sequencing reaction were precipitated with Tris-HCl and the Aripuanã and Jiparaná rivers. alcohol, and resuspended in formamide and resolved by Willisornis poecilinotus – A species endemic to the capillary electrophoresis in an ABI 3130xl automatic Amazon basin, with seven subspecies recognized (Peters sequencer (Applied Biosystems). All sequences have been 1951; Zimmer & Isler 2003). Only one subspecies (W. deposited in GenBank (accession numbers: HM164938 p. griseiventris) is recognized from the middle and upper – HM165034). Madeira River basin; and there is no evidence of vocal or morphological differentiation across the Madeira, Alignment Aripuanã and Jiparaná rivers (Isler & Whitney 2011), although Bates (2000) found genetic differentiation Sequences of DNA were visualized and edited using (based on analyses of isozymes) across the Madeira River. the Bioedit program (Hall, 1999). Alignments were Occurs in the understory of terra firme forest, where it is performed in Clustal X within Bioedit (Hall, 1999). We a regular follower of army ant swarms (Zimmer & Isler used recommended precautions and are confident that all 2003). It is larger on average than Glyphorynchus, with sequences represent mitochondrial DNA for the following a body mass ranging from 15 to 19 g (Zimmer & Isler reasons: (1) DNA was extracted only from tissue samples, 2003). which have high ratios of mitochondria to nuclei relative Schiffornis turdina – Nyári (2007), with no samples to blood or skin samples; (2) no stop codons occurred from the middle or lower Madeira River basin described within the cytochrome b of any of the sequences; (3) close geographic proximity in the upper Madeira of two sequences contain no insertions or deletions relative genetically distinct forms, showing no obvious vocal or to one another or to other known avian cytochrome b plumage differences; the author proposed recognizing sequences; (4) sequences in both DNA fragments from them as distinct species (S. amazona and S. turdina), each individual were identical and unambiguous in their as adopted by the Brazilian Ornithological Records region of overlap; (5) in phylogenetic analyses, no samples Committee (2014). Schiffornis turdina (in the polytypic appeared in unexpectedly basal portions of the tree or sense used here) occurs in the understory of terra firme had exceptionally short or long branch lengths, both of and sandy-belt campinarana forests. Body mass averages which, if present, would indicate a fast evolving gene or 31 g (Snow 2004). This species is sensitive to forest an early diverged gene (a pseudogene, for example). fragmentation, disappearing from small forest fragments (Ferraz et al. 2007). Phylogenetic analyses Extraction, amplification and sequencing of DNA Phylogenetic analysis of DNA sequence data was performed using maximum parsimony (MP) and DNA was extracted from breast muscle (approximately maximum likelihood (ML) via PAUP* 4.0b10 (Swofford 0.2 g) using a standard phenol chloroform protocol 2002) and Bayesian inference (BI) implemented in (Sambrook et al. 1989). The mitochondrial MRBAYES 3.0b4 (Hulsenbeck & Ronquist 2001). cytochrome b was amplified via the polymerase chain Maximum parsimony analysis was performed using a reaction (PCR) using the primers: forward H16064 heuristic search with the following options: TBR branch- 5-ATCTCARCCTGATGAAAYTTYGG-3, reverse swapping with 10 trees held at each step. Support for L14993 5-AAGTGGTAAGTCTTCAGTCTTTGGTT-3, nodes was assessed using 1000 bootstrap replicates. both of which were designed exclusively for this project. Maximum likelihood was performed using the model All amplification reactions were performed in 25 μl parameters determined in the program Modeltest Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias (Posada & Crandall 1998). The support for nodes in RESULTS the likelihood tree was assessed using 500 bootstrap iterations. For BI analyses, two independent runs of We found significant phylogeographic structure among 8,000,000 generations each were performed; for each run populations within all three study species. The Madeira four Markov chains were simulated. Trees were sampled River clearly separates genetically distinct populations in every 500 generations and the first 4,000 samples were all of them. Within the Madeira-Tapajós interfluvium, discarded as burn-in. the degree of structure varied among species (see below). Because there is strong evidence that geographic In each species, tree topologies were identical for all four distributions of Amazonian birds are bounded by tree-building algorithms, thus we only show the tree large rivers that form areas of Neotropical endemism, resulting from the Bayesian inference analyses. The pair- we used individuals from populations from other wise genetic p-distance between individuals from opposite interfluvia as outgroups for the three species studied. banks of the three rivers ranged from 3.1 to 5.5% but the For the analysis of Glyphorynchus spirurus we used two variation within interfluvia was low (0.0–0.09%). Results individuals collected in the headwaters of the Negro for each species were as follows: River (Appendix) as the outgroup. For Willisornis poecilinotus, we used one individual collected in the Glyphorynchus spirurus Solimões-Negro River interfluvium and for Schiffornis turdina, we used as outgroups one individual collected We sequenced a total of 946 bp for 27 individuals of G. north of Manaus and also one sequence of Schiffornis spirurus. Parsimony, maximum likelihood, and Bayesian virescens from GenBank (accession number AF453816; inference analyses suggested a genetic structure in the Appendix). form of monophyletic groups on opposite banks of the Madeira, Aripuanã and Jiparaná rivers, each supported by Phylogenetic divergence analyses high bootstrap values (MP = 100, ML = 100, BI = 1.00). No barrier effect was found on opposite banks of the Phylogenetic divergence was estimated in the program Roosevelt River. Parsimony analysis yielded two equally BEAST v1.6.1 (Drummond & Rambaut 2007) using parsimonious trees (length = 170, CI = 0.8235, RI = the coalescent constant population size tree prior 0.9504). From 130 variable sites, 110 were parsimony (Drummond et al. 2002), the uncorrelated lognormal informative. Maximum likelihood (-ln L = 2012.00097) relaxed molecular clock model (Drummond et al. and Bayesian inference resulted in a topology very similar 2006), and the HKY (Hasegawa et al. 1985) models to that of the parsimony analysis. Levels of genetic of molecular evolution, including gamma-distributed divergence (uncorrected p-distance) between individuals rate heterogeneity among sites and invariant sites. of different clades ranged from 3.2% (populations of After preliminary runs, we adjusted priors and MCMC AJ versus MJ) to 5.5% (populations of LM versus AT) operators to assure optimum performance. To assess the and levels of divergence between individuals within the robustness of estimates and investigate the influence same interfluvium ranged from 0.0–0.03% (Figure 2). of the tree prior, we also performed analyses under the Coalescent analyses in the program BEAST indicate a exponential (Drummond et al. 2002) and the Bayesian 6.5 mya (1.9 – 32.7, 90% HDP) divergence between skyline (Drummond et al. 2005) tree priors. To convert populations on the left and right banks of the Madeira divergence time estimates into units of millions of River. years, we used the mean substitution rate of 0.01105 substitutions/site/lineage/million years as proposed by Willisornis poecilinotus Weir & Schluter (2008). For each set of priors, two independent MCMC We sequenced a total of 956 bp for 46 Willisornis poecilinotus individuals. The results of parsimony, analyses were run for 100 million generations, sub- sampling every 100 thousand generations. After a 10% maximum likelihood, and Bayesian inference analyses burn-in, convergence of parameter estimates was assessed were concordant, thus indicating a strong phylogenetic using the Gelman-Rubin statistic implemented in the signal supported by high bootstrap values (MP = 100, module coda in the statistical package R (R Development ML = 100, BI = 1.00) (Figure 3). Parsimony analysis yielded 100 equally parsimonious trees (length = 94, Core Team 2011). Independent chains were combined, and marginal posterior parameter means and their CI = 0.8723, RI = 0.9634). From 71 variable sites, 41 associated 90% highest probability density intervals (90% were parsimony informative. Maximum likelihood (-ln HPD) together with effective sample size (ESS) for each L = 1757.25307) and Bayesian inference resulted in a divergence time estimate were calculated in the statistical topology very similar to that of the parsimony analysis. The level of genetic divergence (uncorrected p-distance) package R (R Development Core Team 2011). Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias between individuals of the two clades separated by the interfluvium ranged from 0.0–0.09%. Coalescent Madeira River, RM (right bank of Madeira River) versus analyses in the program BEAST indicate a 2.6 mya (0.8 – LM (left bank of Madeira River), was 3.4% (Figure 3). 13.8, 90% HDP) divergence between populations on the Levels of divergence between individuals in the same left and right banks of the Madeira River. FIGURE 2. Species–area relationships (a) and Bayesian inference phylogeny (b) estimated for Glyphorynchus spirurus. Numbers at the tips of branches refer to localities where individuals were sampled. Bayesian inference (BI) posterior probabilities and genetic distance (uncorrected p-distance) values are indicated in the branches. Note grouping of a sample from the Aripuanã-Tapajós interfluvium (location 15) with those of the Madeira-Jiparaná interfluvium (see Discussion). FIGURE 3. Species–area relationships (a) and Bayesian inference phylogeny (b) estimated for Willisornis poecilinotus. Numbers at the tips of branches refer to localities where individuals were sampled. Bayesian inference (BI) posterior probabilities and genetic distance (uncorrected p-distance) values are indicated in the branches. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias Schiffornis turdina likelihood (-ln L = 2043.26577) and Bayesian inference resulted in a topology very similar to that of the parsimony We sequenced a total of 968 bp for 25 Schiffornis turdina analysis consensus topology. The maximum divergence individuals. Parsimony, maximum likelihood and (uncorrected p-distance) between individuals of the RM Bayesian inference analyses suggested genetic structure on and LM clades was 3.1% (Figure 4). Levels of divergence opposite banks of the Madeira River supported by high among individuals of the same interfluvium ranged from bootstrap values (MP = 100, ML = 98, BI = 1.00) (Figure 0.0–0.3%. Coalescent analyses in the program BEAST 4). Parsimony analysis yielded 48 equally parsimonious indicate a 3.1 mya (1.0 – 15.2, 90% HDP) divergence trees (length = 175, CI = 0.9371, RI = 0.9214). From 159 between populations on the left and right banks of the variable sites, 67 were parsimony informative. Maximum Madeira River. FIGURE 4. Species–area relationships (a) and Bayesian inference phylogeny (b) estimated for Schiffornis turdina. Numbers at the tips of branches refer to localities where individuals were sampled. Bayesian inference (BI) posterior probabilities and genetic distance (uncorrected p-distance) values are indicated in the branches. DISCUSSION taxa separated by the same geographic barrier (Ribas et al. 2012). Based on coalescent analyses (see Methods), Strong genetic differentiation in the face of highly we estimated mean divergences of 6.5 mya, 2.6 mya and conserved phenotype is at the heart of numerous 3.1 mya between populations on left and right banks of the Madeira River for G. spirurus, W. poecilinotus and S. descriptions of “cryptic species” in recent years (Whitney et al. 2013a, b, c, d, e) and appears to be a turdina, respectively. The separation of the lineages in all frequent phenomenon in the Amazon. In S. turdina, three species of passerines are clearly ancient, all lineages differentiation on opposite banks of the middle and are diagnosable by multiple molecular synapomorphies, lower reaches of the Madeira River is consistent with and all lineages are parapatrically distributed and likely represent phylogenetic species. However, it is also clear that detected earlier in the upper Madeira (Nyári 2007) and associated with species level taxa. In all that a more detailed analysis evaluating species status and three studied species, the observed molecular groups establishing species boundaries is necessary. are monophyletic and parapatrically distributed, their Irrespective of taxonomy, the pattern of geographic geographic distributions are delimited by rivers, and variation delimited by rivers is clear for all three taxa studied. Our results indicate genetically distinct the observed phylogenetic divergence between clades on opposite banks of the Madeira River (3.1–5.5%) is populations on opposite banks of the Madeira River. For consistent with interspecific divergences in other avian all three species analyzed in this study we found sister Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias clades on opposite banks of the Madeira River, and for separated by the Madeira River not to be reciprocally G. spirurus, as documented previously (Fernandes et al. monophyletic (Aleixo 2004, Patané et al. 2009, Sousa- 2013), the data further indicated sister clades on opposite Neves et al. 2013), as recovered herein for G. spirurus, banks of the smaller Aripuanã and Jiparaná rivers. Our W. poecilinotus, and S. turdina, hence supporting a more data therefore reinforce the importance of rivers as complex scenario of differentiation and a broad range of geographic barriers, and suggest a hierarchical effect in phylogeographic patterns for the same region. which larger rivers divide older clades whereas smaller Despite the importance of rivers for avian rivers are associated with more recent divergences. For differentiation, even the largest Amazonian rivers are G. spirurus, an individual collected on the right bank of not barriers for all species and smaller rivers are less the Aripuanã River that grouped in the clade Madeira/ likely to be barriers than larger rivers. There are several Jiparaná (MJ) provides evidence of upstream gene flow potential explanations for this phenomenon. Molecular across both of the same rivers (Jiparaná and Aripuanã) studies suggest that populations of canopy species are less that delimit differentiated populations in their lower structured than those of understory birds (Capparella reaches. Since rivers naturally tend to be narrower in 1988; Burney & Brumfield 2009). The latter authors the upper reaches, this result suggests that river width is showed that genetic divergence is significantly smaller important in determining a river’s likelihood of delimiting across the Andes and two Amazonian rivers (Amazon and distributions and further strengthens the hypothesis Madeira rivers) in canopy birds than in understory species. of a hierarchical effect of river width in structuring Burney & Brumfield (2009) further suggested that there populations (Haffer 1974, 1997). is a negative relationship between dispersal propensity Assuming roughly equal rates of substitution, and genetic structure. Species that occupy the understory then Willisornis poecilinotus and Schiffornis turdina are supposed to be less effective dispersers, which may populations may have differentiated across the Madeira be one reason why there are more species of understory River at about the same time; however, Glyphorynchus birds, and that they are more locally distributed. spirurus would appear to have differentiated much However, we found differences in genetic structure earlier. This implies that not all sympatric bird taxa among understory species, suggesting that other factors necessarily share the same evolutionary scenario. may also influence the diversification of birds. One Although the Madeira River currently delimits the might also expect the degree of sensitivity to disturbance distributions of the left- and right-bank clades of all or habitat specialization on primary terra firme forest to three species, the Madeira River might not necessarily predict the importance of rivers in driving or maintaining be the primary agent that has driven the observed allopatric differentiation. Ferraz et al. (2007) analyzed divergence. It may simply represent current limits of thirteen years of capture/recapture data for birds in the distribution for clades that have diverged due to other reserves managed by the Biological Dynamics of Forest abiotic or biotic forces, independent of the formation Fragmentation Project (BDFFP), located in the Brazilian of the Madeira River itself. Another non-exclusive state of Amazonas north of Manaus. These authors derived possibility is that rates of molecular substitutions are measures of the vulnerability of a species to isolation and 2–3 times faster in G. spirurus than in W. poecilinotus sensitivity due to fragment size. These two measures and S. turdina; however, such an elevated substitution reflect sensitivity to environmental change. Among the rate appears to be a rare phenomenon in passerine birds, 54 species examined by Ferraz et al. (2007), G. spirurus and has been suggested only for one case of an Old was the least sensitive to the size of the fragment and one World species (Nectarinia humbloti; Warren et al. 2003). of the ten species least vulnerable to isolation. By contrast, Finally, a third explanation suggested previously (Willis S. turdina was among the most vulnerable and most 1969, Fernandes et al. 2012, 2014) is that changes in the sensitive species. Willisornis poecilinotus was not included courses of rivers might confuse the phylogenetic pattern. in the analysis. One would therefore expect G. spirurus, There is evidence that the course of rivers in the Madeira the species least affected by isolation and fragmentation, basin changed throughout history, but remained stable to have lower genetic divergence across the rivers than for long periods of time (Latrubesse 2002). The period the other two species; however, our results contradict of stability could be enough to cause differentiation the expected pattern. Glyphorynchus spirurus, although until their course was modified again and became stable occurring in different types of forests and not being for another long period of time thus causing both spatial especially sensitive to disturbance, has populations that and temporal incongruences among phylogenies of co- are much more strongly structured than are those of the distributed species (Fernandes 2013). A comparative other two species. In this case, sensitivity to disturbance analysis including additional species and sampling and degree of specialization on primary terra firme forest nuclear markers is likely to shed more light on this issue, were not good predictors of the degree of population but at least three other studies have found populations genetic structure. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias The Jiparaná and Aripuanã rivers separate populations REFERENCES of G. spirurus, the smallest species we examined (average Aleixo, A. 2004. Historical diversification of a terra-firme forest body mass 13.7 g), but not the populations of two other bird superspecies: a phylogeographic perspective on the role of species, W. poecilinotus (15–19 g) and S. turdina (30–35.5 different hypotheses of Amazonian diversification. Evolution, 38: g). 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Ribeiro), pp. rivers as well: Thamnophilus aethiops (23-30g; Thom 145-178. Inpa, Manaus. & Aleixo 2015) and Malacoptila rufa (36-44g; Ferreira Cracraft, J. 1985. Historical biogeography and patterns of 2013). As discussed by Smith et al. (2014) differences in differentiation within South American birds: areas of endemism. life history attributes, effective population sizes, lineage Ornithological Monographs, 36: 49-84. D’Horta, F. M.; Cuervo, A. M.; Ribas, C. C.; Brumfield, R. T.; & ages, and dispersal rates can together account for highly Miyaki, C. Y. 2013. Phylogeny and comparative phylogeography disparate responses of avian lineages across important of Sclerurus (Aves: Furnariidae) reveal constant and cryptic physical barriers in the Neotropics such as the Andes diversification in an old radiation of rain forest understorey and some large Amazonian rivers, including the Madeira specialists. Journal of Biogeography, 40: 37-49. River. Further tests, controlling for phylogeny, habitat, Da Silva, J. M. C. & Oren, D. C. 1996. Application of parsimony analysis of endemicity in Amazonian biogeography: an example wing shape and loading, and behavioral responses to open with primates. Biological Journal of Linnean Society, 59: 427-437. spaces, will be necessary to determine the extent to which Drummond, A. J. & Rambaut, A. 2007. BEAST: Bayesian body mass is a useful predictor of genetic population evolutionary analysis by sampling trees. BMC Evolutionary structure in suboscine passerines. Biology, 7: 214. Drummond, A. J.; Ho, S. Y. W.; Phillips, M.J. & Rambaut, A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: 88. ACKNOWLEDGMENTS Drummond, A.J.; Rambaut, A.; Shapiro, B. & Pybus, O. G. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22: 1185- AMF was supported during his masters studies by a fellowship from Conselho Nacional de Desenvolvimento Drummond, A. J.; Nicholls, G. K.; Rodrigo, A. G. & Solomon, W. Cientifico e Tecnologico (CNPq). Financial support 2002. Estimating mutation parameters, population history and for both laboratory and field work was granted by IEB genealogy simultaneously from temporally spaced sequence data. (Instituto de Educação do Brasil, programa BECA). Genetics, 161: 1307-1320. Fernandes, A. M.; Wink, M.; Sardelli, C. H. & Aleixo, A. 2014. The research was conducted in the Laboratório de Multiple speciation across the Andes and throughout Amazonia: Evolução e Genética Animal (LEGAL) with portion the case of the spot-backed antbird species complex (Hylophylax of the analyses being done in the High Performance naevius/Hylophylax naevioides). Journal of Biogeography, DOI: Computational Facility of the University of Puerto Rico. 10.1111/jbi.12277 Fernandes, A. M. 2013. Fine-scale endemism of Amazonian birds in We want to thank F. A. Carvalho for essential help and a threatened landscape. Biodiversity and Conservation, 22, 2683- aiding in preparing the figures, L. N. Naka, T. C. H. Cole, C. A. Marantz and an anonymous reviewer for Fernandes, A. M.; Gonzales, J.; Wink, M. & Aleixo, A. 2013. useful and inspiring comments on earlier versions of this Multilocus phylogeography of the Wedge-billed Woodcreeper manuscript. Collecting permits were provided to AMF Glyphorynchus spirurus (Aves, Furnariidae) in lowland Amazonia: Widespread cryptic diversity and paraphyly reveal a complex and to MCH by IBAMA (Instituto Brasileiro do Meio diversification pattern. Molecular Phylogenetics and Evolution, 66: Ambiente). 270-282. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias Fernandes, A. M.; Wink, M. & Aleixo, A. 2012. Phylogeography of Sambrook, J.; Fritsch, E. F. & Maniatis, T. 1989. Molecular the chestnut-tailed antbird (Myrmeciza hemimelaena) clarifies the cloning: a laboratory manual, 2nd ed, Spring. Cold Spring Harbor role of rivers in Amazonian biogeography. Journal of Biogeography, Laboratory Press, Cold Spring Harbor, NY. 39: 1524-1535. Sanger, F.; Nicklen, S. & Coulson, A. R. 1977. DNA sequencing Ferraz, G.; Nichols, J. D.; Hines, J. E.; Stouffer, P. C.; Bierregaard with chain-terminating inhibitors. Proceedings of the National Jr, R. O. & Lovejoy, T. E. 2007. A large-scale deforestation Academy of Sciences of the United States of America, 24: 5463-5467. experiment: Effects of patch area and isolation on Amazon Birds. Sardelli, C. H. 2005. 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Population/Locality Taxon: Voucher/Genbank accession numbers 0/ AM: right bank of lower Juruá, RESEX Baixo Juruá, G. spirurus: INPA A 808/HM164938 comunidade Socó. 3°36’S; 66°4’W 1/ AM:”Campo do Lago Preto”, left bank of Madeira river, 39 W. poecilinotus: INPA A 420/HM164985,421/HM164980, km W Novo Aripuanã. 5°09’S; 60°44’W 422/HM164994, 424/HM164975. S. turdina: INPA A 395/ HM165029, 413/HM165028 2/ AM: right bank Purús river, Ussuã stream, tributary of W. poecilinotus: INPA A 101/HM164978 Mucuim river (right bank). 7°13’S; 64°10’W 3/ RO: left bank of the Madeira river, near Jacy Paraná, ca. 45 G. spirurus: INPA A 349/HM164942, 359/HM164941. W. km southwest Porto Velho. 9°10’S; 64°23’W poecilinotus: INPA A 345/HM164983, 347/HM164999, S. turdina INPA A 348/HM165032 4/ RO: left bank of the Madeira river, ca. 20 km N Abunã. G. spirurus: INPA A 173/HM164943, 191/HM164960. W. 9°31’S; 65°21’W poecilinotus: 182/HM164984 5/ AM: left bank of Aripuanã river, Arauazinho stream, 130 km G. spirurus: INPA A 461/HM164951, 466/HM164950, S Novo Aripuanã. 6°18’S; 60°24’W 510/HM164952, 553/HM164963, 562/HM164962. W. poecilinotus: INPA A 465/HM164974, 472/HM164967, 475/HM165009, 504/HM164971. S. turdina: INPA A 533/ HM165014 6/ AM: left bank of lower Roosevelt river, confluence with G. spirurus: INPA A 906/HM164945. W. poecilinotus: INPA A Aripuanã river. 7°35’S; 60°43’W 902/HM164976, 904/HM164992. S. turdina: INPA A 903/ HM165017. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias 7/ AM: right bank of lower Roosevelt river, confluence with G. spirurus: INPA A 895/HM164948. W. poecilinotus: INPA Aripuanã river. 7°38’S; 60°40’W A 894/HM164997, 896/HM165007, 900/HM165003, 898/ HM165001. S. turdina: INPA A 893/HM165015 8/ RO: right bank lower Jiparaná river, comunidade G. spirurus: INPA A 875/HM164946, 877/HM164958. W. Demarcação, ca. 20 km southeast Calama. 8°09’S; 62°47’W poecilinotus: INPA A 876/HM164989, 884/HM164990, 907/ HM165008. S. turdina: INPA A 885/HM165016 9/ RO: left bank of lower Jiparaná river, opp. Comunidade G. spirurus: INPA A 870/HM164964, 886/HM164940. W. Demarcação, ca. 20 km southeast Calama. 8°14’S; 62°46’W poecilinotus: INPA A 871/HM164982, 872/HM164996, 873/HM165000, 878/HM164988, 881/HM165010, 882/ HM164977. S. turdina: INPA A 874/HM165034, 880/ HM165021, 883/HM165018 10/ RO: right bank of Madeira river, 9.5 km southeast Porto G. spirurus: INPA A 329/HM164959. W. poecilinotus: INPA Velho. 8°52’S; 64°0’W A 307/HM164966, 308/HM164970, 326/HM164968, 327/ HM164973, 334/HM164972 11/ RO: right bank of Madeira river, near Jacy Paraná, ca. 45 W. poecilinotus: INPA A 367/HM165002, 368/HM164969. km southwest Porto Velho S. turdina: INPA A 371/HM165030, 372/HM165025, 374/ HM165026 12/ RO: right bank of Madeira river, ca. 20 km N Abunã. G. spirurus: INPA A 208/HM164949. W. poecilinotus: INPA 9°35’S; 65°21’W A 248/HM165005, 264/HM165006, 265/HM164993. S. turdina: INPA A 249/HM165031, 266/HM165012 13/ AM: right bank of Aripuanã, Extremo stream, 135 km S G. spirurus: INPA A 536/HM164944, 559/HM164947, 561/ Novo Aripuanã. 6°18’S; 60°20’W HM164955. W. poecilinotus: INPA A 478/HM164987, 479/ HM164979. S. turdina: INPA A 525/HM165027, 527/ HM165023, 538/HM165024 14/ AM: right bank of middle Aripuanã, confluence with G. spirurus: INPA A 890/HM164954. W. poecilinotus: INPA Roosevelt river. 7°37’S; 60°40’W A 887/HM164995, 888/HM164981, 891/HM165004. S. turdina: INPA A 892/HM165033, 889/HM165019 15/ AM: Floresta Estadual do Sucunduri, right bank of upper G. spirurus: INPA A 845/HM164957. W. poecilinotus: INPA A Sucunduri river. 8°34.5’S; 59°08.5’W 849/HM164998. S. turdina: INPA A 846/HM165013, 848/ HM165022, 850/HM165020 16/ AM: Parque Estadual do Sucunduri; right bank of Bararati G. spirurus: INPA A 852/HM164953, 855/HM164956. W. river. 8°21’S; 58°37’W poecilinotus: INPA A 856/HM164986, 857/HM164991 Outgroup/ AM: right bank of upper Negro river, 3 km SW São G. spirurus: INPA A 1153/HM164939 Gabriel da Cachoeira. 0°8’S; 67°5’W Outgroup/ AM: left bank upper Negro river, 10 km east São G. spirurus: INPA A 1118/HM164961 Gabriel da Cachoeira. 0°10’S; 66°59’W Outgroup/ AM: left bank middle Solimões river; RDS Amanã, W. poecilinotus: INPA A 398/HM164965 Comunidade Nova Canaã, Centro Grande stream. 2°36’S; 64°52’W Outgroup/ AM: ca. 60 km N Manaus; highway BR-174, km S. turdina: INPA A 777/HM165011 43; Campina reserve/INPA Revista Brasileira de Ornitologia, 22(4), 2014 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Rivers acting as barriers for bird dispersal in the Amazon

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Revista Brasileira de Ornitologia, 22(4), 363-373 ARTICLE December 2014 1,5 2 3,4 3 Alexandre M. Fernandes , Mario Cohn-Haft , Tomas Hrbek and Izeni Pires Farias Universidade Federal Rural de Pernambuco, UFRPE, Unidade Acadêmica de Serra Talhada, Serra Talhada, PE, Brazil. Instituto Nacional de Pesquisas da Amazonia, INPA, Manaus, AM, Brazil. Universidade Federal do Amazonas, UFAM, Manaus, AM, Brazil. University of Puerto Rico, Rio Piedras, UPR-RP, Puerto Rico, USA. Corresponding author: fernandesornito@gmail.com Received on 19 November 2014. Accepted on 10 December 2014. ABSTRACT: Morphological, vocal and genetic studies have shown that the Madeira River and its right bank tributaries delimit populations of primates and birds. We sequenced the cytochrome b gene (approx. 950 bp) for individuals of three suboscine passerine bird species, Glyphorynchus spirurus (Furnariidae), Willisornis poecilinotus (Thamnophilidae) and Schiffornis turdina (Tityridae), on opposite banks of the Madeira River and two of its right-bank tributaries, the Aripuanã and Jiparaná rivers. Phylogenetic hypotheses (parsimony, maximum likelihood and Bayesian analysis) revealed clades that have over 3.1% genetic differentiation on opposite banks of the Madeira River for G. spirurus, W. poecilinotus and S. turdina, suggesting that this river restricts gene flow among populations of these three species. The Jiparaná and Aripuanã rivers apparently separate distinct populations of G. spirurus, the smallest species we examined, but not those of the other two heavier bodied species, W. poecilinotus and S. turdina. In G. spirurus four clades with high levels of genetic differentiation (3.2–5.5%) were found to be delimited by the three rivers evaluated, whereas in W. poecilinotus and S. turdina no genetic structure across the Jiparaná and Aripuanã rivers was detected. In general, birds that are known to show population structure across the Madeira tributaries (Glyphorynchus spirurus, Hemitriccus minor, Hypocnemis rondoni, Herpsilochmus stotzi, and Hylophylax naevius) have body masses smaller than those of both Willisornis poecilinotus and Schiffornis turdina, but some exceptions are discussed. Future studies controlling for several variables are necessary to determine the extent to which body mass is a useful predictor of genetic population structure in understory suboscine passerines. KEYWORDS: Areas of endemism, body mass, comparative phylogeography, conservation, dispersal rate, suboscine birds. INTRODUCTION Recent studies of primates and birds in the Madeira-Tapajós interfluvium (M-T), also known as the Rondônia area of endemism (Cracraft 1985), have Avian distribution patterns are reasonably well known and influential in studies of evolutionary processes. suggested that smaller rivers also limit the distributions Jürgen Haffer was one of the first authors to compile of some taxa, thus forming smaller areas of endemism in bird distribution data to describe biogeographic patterns what was referred to as “mini-interfluvia” (Cohn-Haft et al. 2007). Willis (1969), in a study of birds of the genus in South America (Haffer 1974). His work made a Rhegmatorhina, was one of the first to document complex great contribution to evolutionary studies and to the formulation of speciation hypotheses in Amazonia. patterns of bird distributions in this area. He discussed The “centres of species endemism” he described remain the parapatric occurrence of Rhegmatorhina berlepschi largely unchanged in analyses of distribution patterns for and R. hoffmannsi within the M-T and suggested that the Madeira and Tapajós rivers have occasionally changed many avian groups. They have been generally accepted in their courses, resulting in the separation of populations subsequent works, and in the Amazon basin these regions are often delimited by large rivers (Haffer 1974; Cracraft and subsequent speciation. Van Roosmalen and 1985; da Silva & Oren 1996). Bird species are usually collaborators (1998) described geographic substitutions separated by the Amazon River and its major tributaries of species in primates of the genera Callithrix and Callicebus on opposite banks of small rivers within this such as the Negro, Madeira, Tapajós and Tocantins rivers interfluvium and described a new species of marmoset, (Cohn-Haft 2000; Ribas et al. 2012; D’Horta et al. 2013; Fernandes et al. 2012, 2013, 2014). Similar patterns are Callithrix humilis, that occurs only on the west bank also found in other Amazonian vertebrate taxa, including of the Aripuanã River. Subsequently, several other bird primates and butterflies (Wallace 1852; van Roosmalen et species in this region have been found to contain vocally, morphologically or genetically distinct populations, al. 1998; Hall & Harvey 2002), suggesting that rivers are with restricted distributions and geographic substitution important barriers to dispersal. Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias on opposite banks of Madeira tributaries, such as the rivers along their lower courses are roughly 3.0, 0.8, 0.4 Aripuanã and Jiparaná (or Machado) rivers (Cohn-Haft and 0.3 km, respectively. Each collection point had a et al. 2007; Isler et al. 2007; Tobias et al. 2008; Fernandes corresponding point located on the opposite bank and et al. 2012, 2013, 2014; Whitney et al. 2013a, b, c, d, therefore in a different interfluvium. For purposes of e). Similar geographic patterns, with different races being sampling and analyses, we suggest the existence of three separated by small Amazonian rivers, have also been mini-interfluvia within the M-T: Madeira-Jiparaná (MJ), found for butterflies (Hall & Harvey 2002). Aripuanã-Jiparaná (AJ) and Aripuanã-Tapajós (AT) Sardelli (2005) found genetic differentiation (Fig. 1). A maximum of 5 individuals per species were (cytochrome b, 500 bp) among morphologically collected at each sampling point, with the total sample indistinguishable populations of the Snethlage’s Tody- as follows: Willisornis poecilinotus (n = 45), Schiffornis Tyrant (Hemitriccus minor) apparently bounded by turdina (n = 23), and Glyphorynchus spirurus (n = 25) the Jiparaná and Aripuanã rivers. This study raised the (see Appendix). Specimens were deposited in the bird possibility of the existence of cryptic endemism in mini- collection of the National Institute for Amazonian interfluvia, which was subsequently investigated for Research (INPA), Manaus, Brazil, where tissue samples the other three species of passerine birds (Myrmeciza (muscle, heart and liver) were stored in liquid nitrogen hemimelaena, Glyphorynchus spirurus, Hylophylax naevius for molecular analyses. (Fernandes et al. 2012, 2013, 2014). Fernandes (2013) cited in a review a number of publications corroborating the importance of the mini-interfluvia, highlighting that these diversity patterns are a key (and possibly unique) Amazonian feature and that despite the fact that this fine- scale endemism is well known and recognized among systematists working in the Amazon, it is not taken into account in conservation plans. Fernandes (2013) pointed out that many taxa in this region, including those yet to be given formal scientific names, may now be endangered or even extinct. Thus it is of utmost importance to consider species that present this kind of fine scale differentiation in future conservation proposals. The objective of our study was threefold: 1) describe phylogeographic patterns for three species of suboscine passerines across the Rondônia area of endemism; 2) compare these patterns to those of other species know to have populations delimited by the Madeira, Aripuanã and Jiparaná rivers; and 3) investigate the relationship between degree of phylogeographic FIGURE 1. Collection points and the interfluvia sampled. Madeira- structure and ecological attributes in the light of the Jiparaná (MJ), Aripuanã-Jiparaná (AJ), Aripuanã-Tapajós (AT) and riverine barrier hypothesis. Left bank of the Madeira River (LM). MATERIAL AND METHODS We chose to study these three target species primarily because they are common, easy to collect, and widely Species studied and sampling design distributed across the entire Amazon basin. Although all three are suboscine passerines, they represent three distinct We studied three species of passerine birds belonging families and, as such, the results obtained in this study to three different families: Glyphorynchus spirurus can be assumed to be instances of independent evolution, (Furnariidae), Willisornis poecilinotus (Thamnophilidae), and, thus, support the generality of our conclusions. All and Schiffornis turdina (Tityridae). We sampled birds three species can be found in the same habitat (terra firme at 12 sites between the Tapajós and Madeira rivers and forest) but they differ in a variety of ecological attributes: five sites on the left bank of the Madeira River (LM; Glyphorynchus spirurus – This is a polytypic species Figure 1), with the final number of localities sampled per widely distributed in Neotropical lowland forests, species differing among the three species (see Results). occurring in Amazonia, Central America and along the Individuals were collected along the Madeira, Aripuanã, Atlantic coast of Brazil (Ridgely & Tudor 1994). Marantz Jiparaná and Roosevelt (the latter representing the largest et al. (2003) recognized thirteen subspecies, six of which tributary of the Aripuanã) rivers; the widths of these occur in the Brazilian Amazon. Three of these occur Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias within or adjacent to the Madeira basin: G. s. castelnaudii volumes using a Thermo Hybaid PCR Express thermal (west of the Madeira River to the Andes), G. s. albigularis cycler under the following conditions: (1) an initial (south-eastern Bolivia and Peru), and G. s. inornatus, denaturing step at 94°C for 5 min; (2) 35 cycles of the which occurs throughout the Brazilian portion of the following: 1 min at 92°C, 1 min at 48°C, and 1 min at Madeira-Tapajós interfluvium (Peters 1951; Marantz et 72°C; (3) a 10-min extension step at 72°C. Following al. 2003). With a body mass ranging from 10.5 to 21g PCR, correct fragment size and the presence of a single (typically 12.6-14.8 g in central Amazonia; Bierregaard, amplification product was confirmed via electrophoresis 1988), this is the smallest woodcreeper (Marantz et al. on 1% agarose gel. After amplification, the PCR 2003), and it is the smallest of the three species we studied. products were purified using a salt protocol (Sambrook It occurs in both terra firme and seasonally flooded et al. 1989). Sequencing was performed by the chain forests (várzea and igapó) (Marantz et al. 2003) and it termination method (Sanger et al. 1977), using a Big is moderately sensitive to environmental perturbation Dye Termination Kit (Applied Biosystems) following (Ferraz et al. 2007). Recently, Fernandes et al. (2013) the manufacturer’s specifications. The products of the found that populations of G. s. inornatus are delimited by sequencing reaction were precipitated with Tris-HCl and the Aripuanã and Jiparaná rivers. alcohol, and resuspended in formamide and resolved by Willisornis poecilinotus – A species endemic to the capillary electrophoresis in an ABI 3130xl automatic Amazon basin, with seven subspecies recognized (Peters sequencer (Applied Biosystems). All sequences have been 1951; Zimmer & Isler 2003). Only one subspecies (W. deposited in GenBank (accession numbers: HM164938 p. griseiventris) is recognized from the middle and upper – HM165034). Madeira River basin; and there is no evidence of vocal or morphological differentiation across the Madeira, Alignment Aripuanã and Jiparaná rivers (Isler & Whitney 2011), although Bates (2000) found genetic differentiation Sequences of DNA were visualized and edited using (based on analyses of isozymes) across the Madeira River. the Bioedit program (Hall, 1999). Alignments were Occurs in the understory of terra firme forest, where it is performed in Clustal X within Bioedit (Hall, 1999). We a regular follower of army ant swarms (Zimmer & Isler used recommended precautions and are confident that all 2003). It is larger on average than Glyphorynchus, with sequences represent mitochondrial DNA for the following a body mass ranging from 15 to 19 g (Zimmer & Isler reasons: (1) DNA was extracted only from tissue samples, 2003). which have high ratios of mitochondria to nuclei relative Schiffornis turdina – Nyári (2007), with no samples to blood or skin samples; (2) no stop codons occurred from the middle or lower Madeira River basin described within the cytochrome b of any of the sequences; (3) close geographic proximity in the upper Madeira of two sequences contain no insertions or deletions relative genetically distinct forms, showing no obvious vocal or to one another or to other known avian cytochrome b plumage differences; the author proposed recognizing sequences; (4) sequences in both DNA fragments from them as distinct species (S. amazona and S. turdina), each individual were identical and unambiguous in their as adopted by the Brazilian Ornithological Records region of overlap; (5) in phylogenetic analyses, no samples Committee (2014). Schiffornis turdina (in the polytypic appeared in unexpectedly basal portions of the tree or sense used here) occurs in the understory of terra firme had exceptionally short or long branch lengths, both of and sandy-belt campinarana forests. Body mass averages which, if present, would indicate a fast evolving gene or 31 g (Snow 2004). This species is sensitive to forest an early diverged gene (a pseudogene, for example). fragmentation, disappearing from small forest fragments (Ferraz et al. 2007). Phylogenetic analyses Extraction, amplification and sequencing of DNA Phylogenetic analysis of DNA sequence data was performed using maximum parsimony (MP) and DNA was extracted from breast muscle (approximately maximum likelihood (ML) via PAUP* 4.0b10 (Swofford 0.2 g) using a standard phenol chloroform protocol 2002) and Bayesian inference (BI) implemented in (Sambrook et al. 1989). The mitochondrial MRBAYES 3.0b4 (Hulsenbeck & Ronquist 2001). cytochrome b was amplified via the polymerase chain Maximum parsimony analysis was performed using a reaction (PCR) using the primers: forward H16064 heuristic search with the following options: TBR branch- 5-ATCTCARCCTGATGAAAYTTYGG-3, reverse swapping with 10 trees held at each step. Support for L14993 5-AAGTGGTAAGTCTTCAGTCTTTGGTT-3, nodes was assessed using 1000 bootstrap replicates. both of which were designed exclusively for this project. Maximum likelihood was performed using the model All amplification reactions were performed in 25 μl parameters determined in the program Modeltest Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias (Posada & Crandall 1998). The support for nodes in RESULTS the likelihood tree was assessed using 500 bootstrap iterations. For BI analyses, two independent runs of We found significant phylogeographic structure among 8,000,000 generations each were performed; for each run populations within all three study species. The Madeira four Markov chains were simulated. Trees were sampled River clearly separates genetically distinct populations in every 500 generations and the first 4,000 samples were all of them. Within the Madeira-Tapajós interfluvium, discarded as burn-in. the degree of structure varied among species (see below). Because there is strong evidence that geographic In each species, tree topologies were identical for all four distributions of Amazonian birds are bounded by tree-building algorithms, thus we only show the tree large rivers that form areas of Neotropical endemism, resulting from the Bayesian inference analyses. The pair- we used individuals from populations from other wise genetic p-distance between individuals from opposite interfluvia as outgroups for the three species studied. banks of the three rivers ranged from 3.1 to 5.5% but the For the analysis of Glyphorynchus spirurus we used two variation within interfluvia was low (0.0–0.09%). Results individuals collected in the headwaters of the Negro for each species were as follows: River (Appendix) as the outgroup. For Willisornis poecilinotus, we used one individual collected in the Glyphorynchus spirurus Solimões-Negro River interfluvium and for Schiffornis turdina, we used as outgroups one individual collected We sequenced a total of 946 bp for 27 individuals of G. north of Manaus and also one sequence of Schiffornis spirurus. Parsimony, maximum likelihood, and Bayesian virescens from GenBank (accession number AF453816; inference analyses suggested a genetic structure in the Appendix). form of monophyletic groups on opposite banks of the Madeira, Aripuanã and Jiparaná rivers, each supported by Phylogenetic divergence analyses high bootstrap values (MP = 100, ML = 100, BI = 1.00). No barrier effect was found on opposite banks of the Phylogenetic divergence was estimated in the program Roosevelt River. Parsimony analysis yielded two equally BEAST v1.6.1 (Drummond & Rambaut 2007) using parsimonious trees (length = 170, CI = 0.8235, RI = the coalescent constant population size tree prior 0.9504). From 130 variable sites, 110 were parsimony (Drummond et al. 2002), the uncorrelated lognormal informative. Maximum likelihood (-ln L = 2012.00097) relaxed molecular clock model (Drummond et al. and Bayesian inference resulted in a topology very similar 2006), and the HKY (Hasegawa et al. 1985) models to that of the parsimony analysis. Levels of genetic of molecular evolution, including gamma-distributed divergence (uncorrected p-distance) between individuals rate heterogeneity among sites and invariant sites. of different clades ranged from 3.2% (populations of After preliminary runs, we adjusted priors and MCMC AJ versus MJ) to 5.5% (populations of LM versus AT) operators to assure optimum performance. To assess the and levels of divergence between individuals within the robustness of estimates and investigate the influence same interfluvium ranged from 0.0–0.03% (Figure 2). of the tree prior, we also performed analyses under the Coalescent analyses in the program BEAST indicate a exponential (Drummond et al. 2002) and the Bayesian 6.5 mya (1.9 – 32.7, 90% HDP) divergence between skyline (Drummond et al. 2005) tree priors. To convert populations on the left and right banks of the Madeira divergence time estimates into units of millions of River. years, we used the mean substitution rate of 0.01105 substitutions/site/lineage/million years as proposed by Willisornis poecilinotus Weir & Schluter (2008). For each set of priors, two independent MCMC We sequenced a total of 956 bp for 46 Willisornis poecilinotus individuals. The results of parsimony, analyses were run for 100 million generations, sub- sampling every 100 thousand generations. After a 10% maximum likelihood, and Bayesian inference analyses burn-in, convergence of parameter estimates was assessed were concordant, thus indicating a strong phylogenetic using the Gelman-Rubin statistic implemented in the signal supported by high bootstrap values (MP = 100, module coda in the statistical package R (R Development ML = 100, BI = 1.00) (Figure 3). Parsimony analysis yielded 100 equally parsimonious trees (length = 94, Core Team 2011). Independent chains were combined, and marginal posterior parameter means and their CI = 0.8723, RI = 0.9634). From 71 variable sites, 41 associated 90% highest probability density intervals (90% were parsimony informative. Maximum likelihood (-ln HPD) together with effective sample size (ESS) for each L = 1757.25307) and Bayesian inference resulted in a divergence time estimate were calculated in the statistical topology very similar to that of the parsimony analysis. The level of genetic divergence (uncorrected p-distance) package R (R Development Core Team 2011). Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias between individuals of the two clades separated by the interfluvium ranged from 0.0–0.09%. Coalescent Madeira River, RM (right bank of Madeira River) versus analyses in the program BEAST indicate a 2.6 mya (0.8 – LM (left bank of Madeira River), was 3.4% (Figure 3). 13.8, 90% HDP) divergence between populations on the Levels of divergence between individuals in the same left and right banks of the Madeira River. FIGURE 2. Species–area relationships (a) and Bayesian inference phylogeny (b) estimated for Glyphorynchus spirurus. Numbers at the tips of branches refer to localities where individuals were sampled. Bayesian inference (BI) posterior probabilities and genetic distance (uncorrected p-distance) values are indicated in the branches. Note grouping of a sample from the Aripuanã-Tapajós interfluvium (location 15) with those of the Madeira-Jiparaná interfluvium (see Discussion). FIGURE 3. Species–area relationships (a) and Bayesian inference phylogeny (b) estimated for Willisornis poecilinotus. Numbers at the tips of branches refer to localities where individuals were sampled. Bayesian inference (BI) posterior probabilities and genetic distance (uncorrected p-distance) values are indicated in the branches. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias Schiffornis turdina likelihood (-ln L = 2043.26577) and Bayesian inference resulted in a topology very similar to that of the parsimony We sequenced a total of 968 bp for 25 Schiffornis turdina analysis consensus topology. The maximum divergence individuals. Parsimony, maximum likelihood and (uncorrected p-distance) between individuals of the RM Bayesian inference analyses suggested genetic structure on and LM clades was 3.1% (Figure 4). Levels of divergence opposite banks of the Madeira River supported by high among individuals of the same interfluvium ranged from bootstrap values (MP = 100, ML = 98, BI = 1.00) (Figure 0.0–0.3%. Coalescent analyses in the program BEAST 4). Parsimony analysis yielded 48 equally parsimonious indicate a 3.1 mya (1.0 – 15.2, 90% HDP) divergence trees (length = 175, CI = 0.9371, RI = 0.9214). From 159 between populations on the left and right banks of the variable sites, 67 were parsimony informative. Maximum Madeira River. FIGURE 4. Species–area relationships (a) and Bayesian inference phylogeny (b) estimated for Schiffornis turdina. Numbers at the tips of branches refer to localities where individuals were sampled. Bayesian inference (BI) posterior probabilities and genetic distance (uncorrected p-distance) values are indicated in the branches. DISCUSSION taxa separated by the same geographic barrier (Ribas et al. 2012). Based on coalescent analyses (see Methods), Strong genetic differentiation in the face of highly we estimated mean divergences of 6.5 mya, 2.6 mya and conserved phenotype is at the heart of numerous 3.1 mya between populations on left and right banks of the Madeira River for G. spirurus, W. poecilinotus and S. descriptions of “cryptic species” in recent years (Whitney et al. 2013a, b, c, d, e) and appears to be a turdina, respectively. The separation of the lineages in all frequent phenomenon in the Amazon. In S. turdina, three species of passerines are clearly ancient, all lineages differentiation on opposite banks of the middle and are diagnosable by multiple molecular synapomorphies, lower reaches of the Madeira River is consistent with and all lineages are parapatrically distributed and likely represent phylogenetic species. However, it is also clear that detected earlier in the upper Madeira (Nyári 2007) and associated with species level taxa. In all that a more detailed analysis evaluating species status and three studied species, the observed molecular groups establishing species boundaries is necessary. are monophyletic and parapatrically distributed, their Irrespective of taxonomy, the pattern of geographic geographic distributions are delimited by rivers, and variation delimited by rivers is clear for all three taxa studied. Our results indicate genetically distinct the observed phylogenetic divergence between clades on opposite banks of the Madeira River (3.1–5.5%) is populations on opposite banks of the Madeira River. For consistent with interspecific divergences in other avian all three species analyzed in this study we found sister Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias clades on opposite banks of the Madeira River, and for separated by the Madeira River not to be reciprocally G. spirurus, as documented previously (Fernandes et al. monophyletic (Aleixo 2004, Patané et al. 2009, Sousa- 2013), the data further indicated sister clades on opposite Neves et al. 2013), as recovered herein for G. spirurus, banks of the smaller Aripuanã and Jiparaná rivers. Our W. poecilinotus, and S. turdina, hence supporting a more data therefore reinforce the importance of rivers as complex scenario of differentiation and a broad range of geographic barriers, and suggest a hierarchical effect in phylogeographic patterns for the same region. which larger rivers divide older clades whereas smaller Despite the importance of rivers for avian rivers are associated with more recent divergences. For differentiation, even the largest Amazonian rivers are G. spirurus, an individual collected on the right bank of not barriers for all species and smaller rivers are less the Aripuanã River that grouped in the clade Madeira/ likely to be barriers than larger rivers. There are several Jiparaná (MJ) provides evidence of upstream gene flow potential explanations for this phenomenon. Molecular across both of the same rivers (Jiparaná and Aripuanã) studies suggest that populations of canopy species are less that delimit differentiated populations in their lower structured than those of understory birds (Capparella reaches. Since rivers naturally tend to be narrower in 1988; Burney & Brumfield 2009). The latter authors the upper reaches, this result suggests that river width is showed that genetic divergence is significantly smaller important in determining a river’s likelihood of delimiting across the Andes and two Amazonian rivers (Amazon and distributions and further strengthens the hypothesis Madeira rivers) in canopy birds than in understory species. of a hierarchical effect of river width in structuring Burney & Brumfield (2009) further suggested that there populations (Haffer 1974, 1997). is a negative relationship between dispersal propensity Assuming roughly equal rates of substitution, and genetic structure. Species that occupy the understory then Willisornis poecilinotus and Schiffornis turdina are supposed to be less effective dispersers, which may populations may have differentiated across the Madeira be one reason why there are more species of understory River at about the same time; however, Glyphorynchus birds, and that they are more locally distributed. spirurus would appear to have differentiated much However, we found differences in genetic structure earlier. This implies that not all sympatric bird taxa among understory species, suggesting that other factors necessarily share the same evolutionary scenario. may also influence the diversification of birds. One Although the Madeira River currently delimits the might also expect the degree of sensitivity to disturbance distributions of the left- and right-bank clades of all or habitat specialization on primary terra firme forest to three species, the Madeira River might not necessarily predict the importance of rivers in driving or maintaining be the primary agent that has driven the observed allopatric differentiation. Ferraz et al. (2007) analyzed divergence. It may simply represent current limits of thirteen years of capture/recapture data for birds in the distribution for clades that have diverged due to other reserves managed by the Biological Dynamics of Forest abiotic or biotic forces, independent of the formation Fragmentation Project (BDFFP), located in the Brazilian of the Madeira River itself. Another non-exclusive state of Amazonas north of Manaus. These authors derived possibility is that rates of molecular substitutions are measures of the vulnerability of a species to isolation and 2–3 times faster in G. spirurus than in W. poecilinotus sensitivity due to fragment size. These two measures and S. turdina; however, such an elevated substitution reflect sensitivity to environmental change. Among the rate appears to be a rare phenomenon in passerine birds, 54 species examined by Ferraz et al. (2007), G. spirurus and has been suggested only for one case of an Old was the least sensitive to the size of the fragment and one World species (Nectarinia humbloti; Warren et al. 2003). of the ten species least vulnerable to isolation. By contrast, Finally, a third explanation suggested previously (Willis S. turdina was among the most vulnerable and most 1969, Fernandes et al. 2012, 2014) is that changes in the sensitive species. Willisornis poecilinotus was not included courses of rivers might confuse the phylogenetic pattern. in the analysis. One would therefore expect G. spirurus, There is evidence that the course of rivers in the Madeira the species least affected by isolation and fragmentation, basin changed throughout history, but remained stable to have lower genetic divergence across the rivers than for long periods of time (Latrubesse 2002). The period the other two species; however, our results contradict of stability could be enough to cause differentiation the expected pattern. Glyphorynchus spirurus, although until their course was modified again and became stable occurring in different types of forests and not being for another long period of time thus causing both spatial especially sensitive to disturbance, has populations that and temporal incongruences among phylogenies of co- are much more strongly structured than are those of the distributed species (Fernandes 2013). A comparative other two species. In this case, sensitivity to disturbance analysis including additional species and sampling and degree of specialization on primary terra firme forest nuclear markers is likely to shed more light on this issue, were not good predictors of the degree of population but at least three other studies have found populations genetic structure. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias The Jiparaná and Aripuanã rivers separate populations REFERENCES of G. spirurus, the smallest species we examined (average Aleixo, A. 2004. Historical diversification of a terra-firme forest body mass 13.7 g), but not the populations of two other bird superspecies: a phylogeographic perspective on the role of species, W. poecilinotus (15–19 g) and S. turdina (30–35.5 different hypotheses of Amazonian diversification. Evolution, 38: g). 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Further tests, controlling for phylogeny, habitat, Da Silva, J. M. C. & Oren, D. C. 1996. Application of parsimony analysis of endemicity in Amazonian biogeography: an example wing shape and loading, and behavioral responses to open with primates. Biological Journal of Linnean Society, 59: 427-437. spaces, will be necessary to determine the extent to which Drummond, A. J. & Rambaut, A. 2007. BEAST: Bayesian body mass is a useful predictor of genetic population evolutionary analysis by sampling trees. BMC Evolutionary structure in suboscine passerines. Biology, 7: 214. Drummond, A. J.; Ho, S. Y. W.; Phillips, M.J. & Rambaut, A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: 88. ACKNOWLEDGMENTS Drummond, A.J.; Rambaut, A.; Shapiro, B. & Pybus, O. G. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22: 1185- AMF was supported during his masters studies by a fellowship from Conselho Nacional de Desenvolvimento Drummond, A. J.; Nicholls, G. K.; Rodrigo, A. G. & Solomon, W. Cientifico e Tecnologico (CNPq). Financial support 2002. Estimating mutation parameters, population history and for both laboratory and field work was granted by IEB genealogy simultaneously from temporally spaced sequence data. (Instituto de Educação do Brasil, programa BECA). Genetics, 161: 1307-1320. Fernandes, A. M.; Wink, M.; Sardelli, C. H. & Aleixo, A. 2014. The research was conducted in the Laboratório de Multiple speciation across the Andes and throughout Amazonia: Evolução e Genética Animal (LEGAL) with portion the case of the spot-backed antbird species complex (Hylophylax of the analyses being done in the High Performance naevius/Hylophylax naevioides). Journal of Biogeography, DOI: Computational Facility of the University of Puerto Rico. 10.1111/jbi.12277 Fernandes, A. M. 2013. Fine-scale endemism of Amazonian birds in We want to thank F. A. Carvalho for essential help and a threatened landscape. Biodiversity and Conservation, 22, 2683- aiding in preparing the figures, L. N. Naka, T. C. H. Cole, C. A. Marantz and an anonymous reviewer for Fernandes, A. M.; Gonzales, J.; Wink, M. & Aleixo, A. 2013. useful and inspiring comments on earlier versions of this Multilocus phylogeography of the Wedge-billed Woodcreeper manuscript. Collecting permits were provided to AMF Glyphorynchus spirurus (Aves, Furnariidae) in lowland Amazonia: Widespread cryptic diversity and paraphyly reveal a complex and to MCH by IBAMA (Instituto Brasileiro do Meio diversification pattern. Molecular Phylogenetics and Evolution, 66: Ambiente). 270-282. 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Population/Locality Taxon: Voucher/Genbank accession numbers 0/ AM: right bank of lower Juruá, RESEX Baixo Juruá, G. spirurus: INPA A 808/HM164938 comunidade Socó. 3°36’S; 66°4’W 1/ AM:”Campo do Lago Preto”, left bank of Madeira river, 39 W. poecilinotus: INPA A 420/HM164985,421/HM164980, km W Novo Aripuanã. 5°09’S; 60°44’W 422/HM164994, 424/HM164975. S. turdina: INPA A 395/ HM165029, 413/HM165028 2/ AM: right bank Purús river, Ussuã stream, tributary of W. poecilinotus: INPA A 101/HM164978 Mucuim river (right bank). 7°13’S; 64°10’W 3/ RO: left bank of the Madeira river, near Jacy Paraná, ca. 45 G. spirurus: INPA A 349/HM164942, 359/HM164941. W. km southwest Porto Velho. 9°10’S; 64°23’W poecilinotus: INPA A 345/HM164983, 347/HM164999, S. turdina INPA A 348/HM165032 4/ RO: left bank of the Madeira river, ca. 20 km N Abunã. G. spirurus: INPA A 173/HM164943, 191/HM164960. W. 9°31’S; 65°21’W poecilinotus: 182/HM164984 5/ AM: left bank of Aripuanã river, Arauazinho stream, 130 km G. spirurus: INPA A 461/HM164951, 466/HM164950, S Novo Aripuanã. 6°18’S; 60°24’W 510/HM164952, 553/HM164963, 562/HM164962. W. poecilinotus: INPA A 465/HM164974, 472/HM164967, 475/HM165009, 504/HM164971. S. turdina: INPA A 533/ HM165014 6/ AM: left bank of lower Roosevelt river, confluence with G. spirurus: INPA A 906/HM164945. W. poecilinotus: INPA A Aripuanã river. 7°35’S; 60°43’W 902/HM164976, 904/HM164992. S. turdina: INPA A 903/ HM165017. Revista Brasileira de Ornitologia, 22(4), 2014 Rivers acting as barriers for bird dispersal in the Amazon Alexandre M. Fernandes, Mario Cohn-Haft, Tomas Hrbek and Izeni Pires Farias 7/ AM: right bank of lower Roosevelt river, confluence with G. spirurus: INPA A 895/HM164948. W. poecilinotus: INPA Aripuanã river. 7°38’S; 60°40’W A 894/HM164997, 896/HM165007, 900/HM165003, 898/ HM165001. S. turdina: INPA A 893/HM165015 8/ RO: right bank lower Jiparaná river, comunidade G. spirurus: INPA A 875/HM164946, 877/HM164958. W. Demarcação, ca. 20 km southeast Calama. 8°09’S; 62°47’W poecilinotus: INPA A 876/HM164989, 884/HM164990, 907/ HM165008. S. turdina: INPA A 885/HM165016 9/ RO: left bank of lower Jiparaná river, opp. Comunidade G. spirurus: INPA A 870/HM164964, 886/HM164940. W. Demarcação, ca. 20 km southeast Calama. 8°14’S; 62°46’W poecilinotus: INPA A 871/HM164982, 872/HM164996, 873/HM165000, 878/HM164988, 881/HM165010, 882/ HM164977. S. turdina: INPA A 874/HM165034, 880/ HM165021, 883/HM165018 10/ RO: right bank of Madeira river, 9.5 km southeast Porto G. spirurus: INPA A 329/HM164959. W. poecilinotus: INPA Velho. 8°52’S; 64°0’W A 307/HM164966, 308/HM164970, 326/HM164968, 327/ HM164973, 334/HM164972 11/ RO: right bank of Madeira river, near Jacy Paraná, ca. 45 W. poecilinotus: INPA A 367/HM165002, 368/HM164969. km southwest Porto Velho S. turdina: INPA A 371/HM165030, 372/HM165025, 374/ HM165026 12/ RO: right bank of Madeira river, ca. 20 km N Abunã. G. spirurus: INPA A 208/HM164949. W. poecilinotus: INPA 9°35’S; 65°21’W A 248/HM165005, 264/HM165006, 265/HM164993. S. turdina: INPA A 249/HM165031, 266/HM165012 13/ AM: right bank of Aripuanã, Extremo stream, 135 km S G. spirurus: INPA A 536/HM164944, 559/HM164947, 561/ Novo Aripuanã. 6°18’S; 60°20’W HM164955. W. poecilinotus: INPA A 478/HM164987, 479/ HM164979. S. turdina: INPA A 525/HM165027, 527/ HM165023, 538/HM165024 14/ AM: right bank of middle Aripuanã, confluence with G. spirurus: INPA A 890/HM164954. W. poecilinotus: INPA Roosevelt river. 7°37’S; 60°40’W A 887/HM164995, 888/HM164981, 891/HM165004. S. turdina: INPA A 892/HM165033, 889/HM165019 15/ AM: Floresta Estadual do Sucunduri, right bank of upper G. spirurus: INPA A 845/HM164957. W. poecilinotus: INPA A Sucunduri river. 8°34.5’S; 59°08.5’W 849/HM164998. S. turdina: INPA A 846/HM165013, 848/ HM165022, 850/HM165020 16/ AM: Parque Estadual do Sucunduri; right bank of Bararati G. spirurus: INPA A 852/HM164953, 855/HM164956. W. river. 8°21’S; 58°37’W poecilinotus: INPA A 856/HM164986, 857/HM164991 Outgroup/ AM: right bank of upper Negro river, 3 km SW São G. spirurus: INPA A 1153/HM164939 Gabriel da Cachoeira. 0°8’S; 67°5’W Outgroup/ AM: left bank upper Negro river, 10 km east São G. spirurus: INPA A 1118/HM164961 Gabriel da Cachoeira. 0°10’S; 66°59’W Outgroup/ AM: left bank middle Solimões river; RDS Amanã, W. poecilinotus: INPA A 398/HM164965 Comunidade Nova Canaã, Centro Grande stream. 2°36’S; 64°52’W Outgroup/ AM: ca. 60 km N Manaus; highway BR-174, km S. turdina: INPA A 777/HM165011 43; Campina reserve/INPA Revista Brasileira de Ornitologia, 22(4), 2014

Journal

Ornithology Research – Springer Journals

Published: Dec 1, 2014

Keywords: Areas of endemism; body mass; comparative phylogeography; conservation; dispersal rate; suboscine birds

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