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- Springer Journals
- Copyright
- Copyright © Sociedade Brasileira de Ornitologia 2017
- eISSN
- 2178-7875
- DOI
- 10.1007/bf03544380
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- See Article on Publisher Site
Abstract
Revista Brasileira de Ornitologia 25(1): 71–74. SHORT-COMMUNICA ARTICLE TION March 2017 A new population of the White Bellbird Procnias albus (Hermann, 1783) from lowland southern Brazilian Amazonia, with comments on genetic variation in bellbirds 1,3 1 2 1 Sidnei de Melo Dantas , Leonardo de Sousa Miranda , André Luis Ravetta & Alexandre Aleixo Museu Paraense Emilio Goeldi, Coordenação de Zoologia. Avenida Perimetral, 1901, Terra Firme, Belém, PA, Brazil. Museu Paraense Emilio Goeldi, Coordenação de Ciências da Terra e Ecologia. Avenida Perimetral, 1901, Terra Firme, Belém, PA, Brazil. Corresponding author: smdantas@yahoo.com Received on 09 September 2016. Accepted on 23 April 2017. ABSTRACT: We report on a recently discovered population of the White Bellbird (Procnias albus) in southern Amazonia. Contrary to expectations based on geography and morphological analyses, a recently collected specimen from this new population is genetically closer to the northern subspecies, at the same time that it confirms the overall lack of genetic structure previously reported for the species. Our data reinforces the notion that the subspecies of P. albus may not be diagnosable by morphological and molecular characters. The discovery of a new Procnias albus population not far from the largest human settlement in Brazilian Amazonia underscores the need for more research to better understand avian distribution in this under-studied region. KEY-WORDS: Cotingidae, distribution, phylogeography, subspecies, taxonomy. The White Bellbir d, Procnias albus (Cotingidae) has the Muratuba River (02°06'44.5''S; 50°22'15.8''W), c. a disjunct distribution in Amazonia; the nominate 260 km (161 miles) to the west of Belém, in the state subspecies occurs north of the Amazon River in Venezuela, of Pará, Brazil. The region is covered by upland terra the Guianas, and northernmost Brazil, whilst P. a. firme forest with canopy heights averaging 30 m, as well wallacei occurs south of the Amazon River on the Serra as igapó (black water forest), and campinas (white-sand dos Carajás in southeastern Pará state, Brazil (Snow & forest). Four leks were found between 19 and 22 June Sharpe 2016). Procnias a. wallacei is listed as “Vulnerable” 2015 in the municipality of Bagre (Fig. 1). Three leks according to the Brazilian list of threatened species (MMA were found in a terra firme forest area of approximately 25 2014). The species was first reported south of the Amazon km . These three leks combined contained at least nine River by Wallace (1889) near the city of Belém, more adult males, a young male and some females. A fourth lek than 450 km north of Carajás, but no voucher specimen was located in várzea forest. One adult male from the first for this record has been found and until now there have lek was collected on 22 June 2015 (MPEG 80706; Table been no other records from the region. Thus, Wallace's 1). Digital sound fi les were deposited in Xeno-canto (1889) record has either been disregarded for lack of (www.xeno-canto.org: XC261271, XC263193) and documentation (Moura et al. 2014) or, alternatively, photographs were deposited in WikiAves (www.wikiaves. considered an instance of vagrancy or even a currently com.br: WA1773951, WA1773933, WA1771028). extinct population (Snow 1982). According to Berv & To compare morphometrics of this collected Prum (2014), the two subspecies currently recognized individual with those of known populations, S.M.D. in P. albus are not distinct genetically, but more study is measured six additional adult male specimens of P. albus needed to clarify the taxonomy of this patchily distributed deposited in the ornithological collection of Museu species. Here, we report on a newly discovered southern Paraense Emílio Goeldi (MPEG), as follows: P. a. albus Amazonian population of P. albus, and comment on the (MPEG 32489 from Paru de Leste River, Aramapucú, genetic structure of the species. state of Pará) and P. a. wallacei (MPEG 37213, 37214, The new recor d was obtained during a biodiversity 35042, 30543, all from Serra dos Carajás, Parauapebas, inventory of the northernmost part of the Xingu- state of Pará). Measurements taken were bill length Tocantins interfluve at the municipality of Bagre, near (exposed culmen), bill width at nostrils, bill height at A new population of the White Bellbird Procnias albus in Amazonia Dantas et al. nostrils, left tarsus length, left wing length, and tail length. with Principal Component Analysis (PCA) performed Measurements were taken with a Vonder electronic caliper in XLSTAT (Addinsoft 2007). A Pearson's correlation to the next 0.01 mm and a ruler. The morphometric matrix was used in the analysis, and the two factors that data was analyzed by plotting each measured specimen best explained the results were plotted against each other. Figure 1. Currently known distribution of Procnias albus (gray), with the new location where the species has been documented shown in black. Question mark signs a location (Belém) where there is an historical report. Source: www.birdlife.org. Plumage and soft color parts of MPEG 80706 were from Genbank (Berv & Prum 2014) and used in the the same as in the nominate and P. a. wallacei subspecies analysis. The down loaded sequences of P. albus were from (Oren & Novaes 1985), which shared a pure white samples AMNH 12002, KUNHM 1244 (both from plumage and tiny white plumes on the black wattle. The subspecies P. a. albus) and MPEG 37214 (P. a. wallacei). maxilla was black with a greyish edge and the mandible We conducted a phylogenetic analysis using was grayish with a black tip, and the feet were gray. Bayesian Inference (BI) with BEAST (Drummond & Females and one young male observed at the second lek Rambaut 2007) and Maximum Likelihood (ML) using were streaked yellow and olive below as in other P. albus RAxML-7.0.3 (Stamatakis 2006). The best fitting model populations (Kirwan & Green 2011). selected by jModelTest 2.1.3 (Darriba et al. 2012) was To explore possible genetic differences the DNA HKY (ti/tv = 5.1282). We also constructed a median- of MPEG 80706, the specimen collected during our joining network (Bandelt et al. 1999) using NETWORK avifaunal survey at Bagre, was extracted using a phenol- 4.5.1.0 (www.fluxus-engineering.com). chloroform protocol (Sambrook & Russel 2001) and The first two axes of the PCA explained 81.23% of the PCR-amplified for the mitochondrial gene NADH morphometric variability among the examined specimens Dehydrogenase Subunit 2 (ND2); the PCR product was (eigenvalues F1 = 3.187 and F2 = 1.69) and were plotted purified using a solution of 20% polyet hylene glycol 8000 against each other (Fig. 2). Axis 1 failed to discriminate (PEG) and Sanger sequencing was performed on an ABI between specimens of P. a. albus and P. a. wallacei, whereas PRISM 3130 (Applied Biosystems ). Sequences of ND2 axis 2 completely separated specimens of P. a. albus (with for all Procnias species and outgroups were downloaded negative values) and P. a. wallacei (with positive values). Revista Brasileira de Ornitologia 25(1): 2017 A new population of the White Bellbird Procnias albus in Amazonia Dantas et al. The Bagre specimen (MP EG 80706) grouped on axis This paper reports the second confirmed population 2 with the only P. a. albus specimen included in the of P. albus south of the Amazon River, the other being analysis (Fig. 2), which is explained by the fact that these the Carajás population known since the 1980's (Roth specimens shared similar tarsus and bill length values, the et al. 1984). The presence of a young male and several characters with the highest autocorrelation with axis 2 (i.e. singing males in at least four leks points to a breeding 0.905 and 0.900, respectively). population rather than wandering individuals. However, according to some local people interviewed, the bellbirds sing only during the onset of the dry season (i.e. between May–July) and then either disappear or remain silent and inconspicuous. Thus, whether birds remain in the region outside the dry season remains to be established. Also, the Bagre record lies about 260 km west of Belém, therefore suggesting that the old Wallace (1848) record from near Belém is likely valid. The PCA analysis indicated t hat bill and tarsus length are able to distinguish male specimens of P. albus subspecies (Fig. 3), corroborating Oren & Novaes (1985). The PCR analysis grouped t he Bagre specimen (MPEG 80706) closer to the northern subspecies, c. 500 km far and separated by the Amazonas River, than to P. a. wallacei from Carajás, which are found c. 440 km to the south and not separated by any apparent geographic barrier. Therefore, our morphometric analyses suggest that Figure 2. Result of Principal Component Analysis (PCA). The first the newly discovered population south of the Amazon two axes of PCA are plotted against each other. belongs to the nominate form. However, these results The ND2 sequence for MP EG 80706 is deposited should be interpreted with caution because we analyzed in GenBank (Accession No. KY563658.1). Both ML and only one specimen of the nominate subspecies and BI phylogenies, and the haplotype network recovered therefore purported morphometric diagnoses between the same pattern of overall lack of genetic differentiation both P. albus subspecies may not hold when a larger series between subspecies of P. albus (Fig. 3). All specimens of specimens are analyzed. The genetic data presented examined share the same haplotype (Fig. 3B) and herein suggest that the latter hypothesis is more likely although the clade uniting all P. albus specimens is strongly to be correct. Despite the Carajás individual (MPEG supported (Fig. 3A) the lack of haplotype variation within 37214) have separated from the others in the ND2 tree, the species does not allow an assessment of relationships only one haplotype was recovered for P. albus. A possible among these different populations/subspecies of P. albus explanation for this result is that the sequence for MPEG and likely suggests that these subspecies are not real 37214, extracted from skin (Berv & Prum 2014), was evolutionary entities. much shorter than the others. AB Figure 3. (A) Gene tree generated by BEAST based on 1,001 bp of ND2 sequences of all Procnias species, including both P. albus subspecies (AMNH 12002 and KUNHM 1244 - P. a. albus/MPEG 37214 - P. a. wallacei) and outgroups. Numbers above and below branches are Bayesian posterior probabilities and RaxML bootstrap support values, respectively. (B) Median joining network of all haplotypes. The size of the circles is proportional to haplotype frequency and the colors correspond to the species colors on the tree in (A). Numbers under or below bars mean number of mutations between haplotypes. Revista Brasileira de Ornitologia 25(1): 2017 A new population of the White Bellbird Procnias albus in Amazonia Dantas et al. The lack of genetic differentiation between the Bagre REFERENCES specimen and other P. albus populations both south and Addinsoft. 2007. XLStat, L’analyse de données et statistique avec MS north of the Amazon agree with Berv & Prum's (2014) Excel . New York: Addinsoft. suggestion that these subspecies “… are unlikely to be Bandelt H.-J., Forster P. & Röhl A. 1999. Median-joining networks distinct evolutionary lineages that should be recognized for inferring intraspecific phylogenies. Molecular Biology and as species”. The nominate subspecies is a short distance Evolution 16: 37–48. Berv J.S. & Prum R.O. 2014. A comprehensive multilocus phylogeny migrant, and vagrants have been recorded in Brazil and of the Neotropical cotingas (Cotingidae, Aves) with a comparative Trinidad (Novaes 1980, Snow & Sharpe 2016). 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S.M.D. is supported geolog y, and natural history of the Amazon Valley. London & New by a PCI post-doctoral fellowship from CNPq (grant York: Ward, Lock. #313351/2015-5). José Nilton da Silva Santa Brigida taxidermized the specimen collected at Bagre (MPEG Associate Editor: Jason Weckstein. 80706). Revista Brasileira de Ornitologia 25(1): 2017
Journal
Ornithology Research – Springer Journals
Published: Mar 1, 2017
Keywords: Cotingidae; distribution; phylogeography; subspecies; taxonomy