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Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement

Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Revista Brasileira de Ornitologia, 22(2), 107-120 ARTICLE June 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement 1,6 2 1 3 4 Alexander C. Lees , Luciano Nicolas Naka , Alexandre Aleixo , Mario Cohn-Haft , Vítor de Q. Piacentini , 5 4 Marcos Pérsio Dantas Santos and Luís Fábio Silveira Coordenação de Zoologia, Museu Paraense Emílio Goeldi, CP 399, Belém, Pará, Brazil. Laboratório de Ornitologia, Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, 1235, CEP 50670-901, Recife, Pernambuco, Brazil. Coleção de Aves, Instituto Nacional de Pesquisas da Amazônia (INPA), Avenida André Araújo 2936, Bairro Petrópolis, CEP 69060-000, Manaus, Amazonas, Brazil. Seção de Aves, Museu de Zoologia da Universidade de São Paulo (MZUSP), Avenida Nazaré 481, Ipiranga, CEP 04263-000, São Paulo, SP, Brazil. Universidade Federal do Pará, Instituto de Ciências Biológicas, Laboratório de Ecologia e Zoologia de Vertebrados, Rua Augusto Corrêa, 1, Guamá, CEP 66075-110, Belém, Pará, Brazil. Corresponding author: alexanderlees@btopenworld.com Received on 11 November 2013. Accepted on 02 March 2014. ABSTRACT: Site-based avian inventories are ubiquitous in Neotropical ornithology but are prone to error if fieldworkers are not familiar with the regional species pool, particularly in species-rich regions such as the Amazon basin. Here, we review recent species lists from the Brazilian Amazon in both the primary ornithological literature and in protected area management plans to assess the level of putative errors in terms of bird species recorded in site-based inventories that are biogeographically unlikely in the sampled region. We found errors to be frequent across all inventory types. Failure to recognize recent taxonomic modifications in a cited taxonomy was a common error in many inventories. We outline a series of steps to follow to improve the utility and accuracy of avian inventories, and stress the importance of both obtaining and archiving documentary material, which should be included in the publications as digital vouchers to facilitate detailed peer review. KEYWORDS: Amazonia, avian surveys, checklist, documentation, taxonomy, vouchers. INTRODUCTION other hand, avian inventories are likely to be cited for centuries (e.g., Snethlage 1908), which also means that Comprehensive and accurate site-based species errors can potentially propagate for decades. inventories are the backbone of macroecological studies There is little doubt that birds represent the best- known taxonomic group in the Neotropics, yet our and crucial for understanding multi-scale patterns of species richness, evolutionary processes, natural patterns knowledge of the avifauna in many regions remains of environmental heterogeneity, and species-specific poorly documented, particularly in the vast Amazon responses to environmental change (Blackburn & Gaston basin. In fact, significant knowledge gaps regarding 1998). Species lists can function as a baseline to which species identification, distribution, and taxonomy still exist in entire Amazonian regions (Aleixo 2009; Barlow et new ecological and evolutionary studies can be compared in the future (Moritz et al. 2008; Coterrill & Foissner, al. 2011). These gaps in knowledge, allied to the intrinsic 2010). However, compiling species lists can be a labor- difficulties of surveying birds in highly diverse tropical intensive and a rather unrewarding academic task, as forests, where researchers are reliant on avian vocalizations high-impact scientific journals typically do not publish to conduct accurate surveys (Remsen 1994; Cohn-Haft et al. 1997; Willis 2003) may result in false-positive species inventories. Despite the clear importance of high-quality baseline inventories in the face of global detections (i.e., species that appear in regional or site- habitat loss, fragmentation, degradation, and climate based lists that are unlikely to occur in a given region). change, avian inventories are being published in lower- Even well-trained ornithologists may make identification profile journals, which often do not demand the highest errors in these environments, which is unsurprising given the many morphologically and vocally similar species desirable scientific standards for publication. On the Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira which occur in sympatry in Amazonia. These errors METHODS have been experimentally quantified before, for aural errors in controlled studies of electronically broadcast Each Amazonian interfluve has its own unique avian avian vocalizations (e.g., Simons et al. 2007) and for assemblage, with species turnover particularly high visual errors by releasing trapped birds (of biometrically across wide rivers and in families or guilds with limited confirmed individuals) in front of field observers (e.g., dispersal capacity such as understory suboscines. These Hull et al. 2010), or even to test the subjectivity of biogeographical patterns are now increasingly well abundance estimates (Cerqueira et al. 2013). understood so that unexpected presences are reasonably Identification errors that enter the primary easy to spot. We reviewed 32 bird inventories (Appendix ornithological literature (species lists in journals) may 1) in the Brazilian Amazon published between 2000 and rapidly be spread into the secondary literature, leading to 2013 to look for instances of presumed misidentification incorrect distribution maps in widely used field guides. based on expert opinion of the distribution of allopatric This leads to further proliferation of identification errors, and parapatric Amazonian bird species (see Table 1). as ornithologists and birders alike may pay little attention These lists were published in international journals (n = 7), to the identification of ‘confusion’ species (similar-looking Brazilian journals (n = 21), and book chapters (n = 4). In and potentially sympatric species) widely considered to addition, we also reviewed 31 reserve management plans be present in a region (Robbins & Stallcup 1981; Willis (Appendix 2) from the Brazilian Amazon to compare error 2003; Rojas-Soto & de Ita 2005; McKelvey et al. 2008). rates with those lists in the primary literature. Given the Given these potential problems, we believe that species general lack of review of the grey literature, we expected inventories should be treated as rigorously as any other to find a higher rate of errors in unpublished reports. scientific enterprise and provide as much supporting Our error-checking process applied only to documentary evidence as possible (e.g., Cohn-Haft et biogeographically extremely unlikely records. When al. 1997; Silveira & D’Horta 2002; Silveira et al. 2010; searching these inventories there were many instances of Aleixo et al. 2011; Somenzari et al. 2011; Lees et al. 2012, unusual boreal and austral migrants, many of which are 2013a) to prevent ‘false presences’ becoming established difficult to identify, that we do not necessarily infer to in the literature (McKelvey et al. 2008; Silveira et al. be in error despite being presented without supporting 2010), as well as to facilitate re-evaluations of taxonomic information or documentation. Also, some species—such status in the future. as the White-rumped Swallow Tachycineta leucorrhoa— Corrections of previous mistakes have already are often reported from Amazonian sites, yet they lack been published in the recent Amazonian literature. For any documentation, and we assume many reports to be example: Cohn-Haft et al. (1997) removed seven species in error although we do not highlight them herein. We from the list of Stotz & Bierregaard (1989) of the birds also reviewed which supporting information was supplied north of Manaus; Naka (2006) removed, or included with species’ lists—form of documentation listed, digital as hypothetical, 15 species previously reported for the vouchers included—and whether abundance and habitat Brazilian state of Roraima; Whittaker et al. (2008) type information were incorporated in the data. re-identified or removed 30 species from the initial checklist of the birds of the upper Rio Urucú, originally RESULTS published by Peres & Whittaker (1991); Lopes et al. (2009) re-identified and corrected 52 species from the Chapada dos Guimarães; Lees et al. (2013a) moved We found evidence of presumed misidentifications in 25 to ‘hypothetical species appendix’ or removed entirely inventories (78%) involving 107 records of 82 species 10 species from the lists of Sanaiotti & Cintra (2001) (Table 1). The number of assumed misidentifications and Henriques et al. (2003) from around Santarém; varied between 0 (none) and 15 (X,¯ = 3.3, SD = 4.1, and Lees et al. (2013b) removed three species from 0-3.7% of the total list). Errors could be broadly divided the checklist of Alta Floresta (Zimmer et al. 1997) and into two groups: a) misidentification of a species that is moved another nine taxa to a ‘hypothetical species’ not known to occur in the Amazonian interfluve sampled appendix. However, we consider this issue likely more (n = 74, 70.4%); and b) confusion with replacement widespread and here evaluate the pervasiveness of species (taxonomic errors) for which the wrong member problems related to bird misidentifications in both the of a species pair or super-species complex was listed ‘primary’ and ‘grey’ Brazilian ornithological literature. In (n = 31, X,¯ = 29.0%), often because of a failure to this article, we judge the ubiquity and nature of errors account for shifts in nomenclature and ‘splits.’ in 63 Amazonian bird inventories (including all of our We found that 25% of surveys informed the type own) and point out likely cases of misidentification. We of documentation obtained during the survey but then suggest a roadmap for producing less error-prone only 4% provided links to digital vouchers, although avian inventories. some of these web-based resources have only become Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira available recently. Nearly 20% of the surveys included more heterogeneous in their error rates with the number qualitative abundance estimates and almost 60% of assumed misidentifications varying between 0 and 35 included information of which habitat types species were (n =84, X,¯ = 2.71, SD = 6.64) accounting for between 0 encountered. Reserve management plans (n = 31) were and 7.9% of all records. TABLE 1. A compilation of inferred errors from Amazonian avifaunal inventories between 2000 and 2013. All inferred errors represent apparently undocumented records which are not explicitly discussed in the text, some may of course be genuine, but given their biogeographic significance should be adequately documented before being presented as ‘confirmed’. Species denoted with an asterix* indicate taxonomic rather than identification errors. Citations can be found in Appendix 1. Aguiar et al. 2010. Comments Lago Piratuba, Amapá Sterna hirundinacea Undocumented north of Bahia, would be a first for the biome. Undocumented from Amapá or anywhere in the eastern half of the Guianan Synallaxis propinqua Shield. Aleixo & Poletto 2007. BX44 Polygon, Mato Grosso/ Amazonas Hylophilus hypoxanthus Replaced by Hylophilus muscicapinus in this interfluve (Madeira-Tapajós). Aleixo et al. 2010. Tanguro, Mato Grosso Hypocnemis cantator* Taxonomy followed unclear but should be H. striata. Undocumented east of the rio Xingu where replaced by Hemitriccus minor - Lophotriccus galeatus as reported nearby by Mestre et al. 2011. Borges & Almeida 2011. Jau National Park, Amazonas Trogon ramonianus south of the rio Amazonas and west of the rio Negro Trogon violaceus* following CBRO (2009). Schiffornis amazonum north of the rio Amazonas and west of the rio Madeira Schiffornis turdina* following CBRO (2009). Dantas et al. 2011. FLONA de Pau-Rosa, Amazonas Polytmus guainumbi Unknown in central Brazilian Amazonia, more likely to be P. theresiae. Unknown in this interfluve (Madeira-Tapajós) where replaced by D. Dendrocolaptes picumnus hoffmannsi. Hylophilus hypoxanthus Replaced by Hylophilus muscicapinus in this interfluve (Madeira-Tapajós). Favaro & Flores 2009. Terra do Meio, Pará Does not occur south of the rio Amazonas, based on CBRO (2008) this Hylexetastes perrotii* should be H. uniformis. Reported here as sympatric with A. paraensis but highly unlikely as infuscatus Automolus infuscatus is undocumented east of the Madeira. Pipra aureola Not expected in the interior of the Tapajós-Xingu interfluve. Reported as sympatric with P. coraya but the two are replacement species; Pheugopedius genibarbis genibarbis unknown north of the Serra do Cachimbo between the Tapajós and Tocantins. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Aleixo & Guilherme 2010. Estação Ecológica do Rio Acre, Acre Chaetura spinicaudus Undocumented in SW Amazonia; best treated as hypothetical. Lees et al. 2008. Serra dos Caiabis, Mato Grosso Synallaxis cherriei Listed in error, record pertains to S. rutilans. Lees et al. 2012. Paragominas, Pará Phaeothlypis rivularis* Based on CBRO (2011) this should be P. mesoleuca. Archived digital voucher (a photo) appears to be a juvenile T. episcopus, Tangara sayaca which are very similar to T. sayaca. The latter would represent a significant range extension. Archived digital voucher (a photo) is ambiguous; we consider it better to Euphonia chrysopasta treat this record and others east of the rio Tocantins as hypothetical until better documentation available. Lees et al. 2013b. Santarém, Pará Phaeothlypis rivularis* Based on CBRO (2011) this should be P. mesoleuca. Mestre et al. 2010 . RESEX Chico Mendes, Acre Aulacorhynchus prasinus This should be Aulacorhynchus atrogularis following CBRO (2009). Mestre et al. 2011. Querencia, Mato Grosso Only P. latirostris expected in this region - as reported nearby by Aleixo et al. Poecilotriccus fumifrons Pacheco & Olmos 2005. BR163, Pará Does not occur between the Tapajós and Xingu north of the Teles Pires Hemitriccus minor where replaced by Lophotriccus galeatus. Pacheco et al. 2007. Carajas, Pará The taxonomic position of this species in relation to P. maranhaoensis is Phaethornis nattereri* unresolved but only the latter is expected in this region. Myrmotherula sclateri Undocumented east of the rio Xingu. Undocumented east of the rio Xingu, this species was removed from the Hyloctistes subulatus Carajás list by Aleixo et al. 2012. Does not occur in this interfluve (Xingu-Tocantins) see e.g. Cohn-Haft Lophotriccus galeatus (2000), Lees et al. (2013a). Undocumented as far south as Carajás, where similarly looking P. fasciicauda Pipra aureola has been documented, this species was removed from the Carajás list by Aleixo et al. 2012. As currently mapped this species is not expected in eastern Amazonia where Turdus hauxwelli T. fumigatus is usually reported. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Undocumented east of the rio Tapajós, this species was removed from the Hylophilus muscicapinus Carajás list by Aleixo et al. 2012. Portes et al. 2011. Belem Centre of Endemism, Pará Milvago chimango Clerical error, should be M. chimachima. Myrmeciza atrothorax Undocumented east of rio Tocantins. Thamnophilus schistaceus Undocumented east of rio Tocantins. Thamnophilus stictocephalus Undocumented east of rio Tocantins. Cranioleuca gutturata Undocumented east of rio Tocantins. Furnarius rufus Undocumented in the Belém centre of endemism. Undocumented east of rio Tocantins, recording likely pertain to a recently Hemitriccus minimus discovered and as yet undescribed Myiornis taxon. Hylophilus hypoxanthus Undocumented east of rio Tocantins. Tangara chilensis Undocumented east of rio Tocantins. Based on CBRO (2011) this should be P. mesoleuca, which was recently split Phaeothlypis rivularis* from P. rivularis. Euphonia chrysopasta Undocumented east of rio Tocantins. Oliveira et al. 2011. Cotriguaçu, Mato Grosso This species is restricted to the Atlantic Forest and is not expected in Leucopternis lacernulatus Amazonia, record likely relates to a similar species. This would represent the first record from anywhere in central or north Circus cinereus Brazil and would require extensive documentation. This should be P. amazonum or P. snethlageae in this region, although the Pyrrhura picta* taxonomy followed in this inventory is unclear. This species is undocumented from northern Mato Grosso and would Pionus maximiliani represent a significant range extension. Notharchus macrorhynchus* Only N. hyperrhynchus occurs south of the Amazon. Colaptes campestris Not expected in NW Mato Grosso. Thamnomanes ardesiacus Undocumented east of the rio Madeira. Dysithamnus mentalis Not expected in NW Mato Grosso, should preferably be documented. This should be Schistocichla (formerly Percnostola) rufifacies in this region, Schistocichla leucostigma* although the taxonomy being followed in this inventory is unclear. X. spixii does not occur west of the rio Juruena (or Teles Pires), only X. Xiphorhynchus spixii elegans is expected. A. infuscatus is undocumented east of the rio Madeira; this will likely pertain Automolus infuscatus to A. paraensis. Hemitriccus zosterops Replaced by H. griseipectus south of the rio Amazonas. Fluvicola pica* Undocumented and unexpected in southern Amazonia. Reported as occurring sympatrically with T. hauxwelli, only T. hauxwelli Turdus fumigatus expected in this interfluve (Madeira-Juruena). Olmos et al. 2011. Rondônia Galbula albirostris Unknown south of the rio Amazonas, G. cyanicollis occurs in this region. Notharchus macrorhynchos* Only N. hyperrhynchus occurs south of the Amazon. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Capito niger only occurs north of the rio Amazonas; this record should Capito niger pertain to C. auratus based on current taxonomy. Unknown south of the rio Amazonas, P. bitorquatus occurs east of the Pteroglossus azara Madeira. Within Amazonia, unknown away from the floodplain forest along the main Celeus flavescens channel of the lower Amazon River; it would represent a significant range extension requiring documentation. Dysithamnus mentalis Documentation would be preferable for such a significant range extension. This should be Schistocichla (formerly Percnostola) rufifacies east of the Schistocichla leucostigma* Madeira and S. humaythae west of the Madeira following CBRO (2011). Dendrocolaptes picumnus Unknown in this interfluve where replaced by D. hoffmannsi. Hemitriccus griseipectus Undocumented in the Madeira-Tapajós interfluve. Schiffornis amazonum north of the rio Amazonas and west of the rio Madeira Schiffornis turdina* following CBRO (2011). Hylophilus hypoxanthus Replaced by Hylophilus muscicapinus in this interfluve (Madeira-Tapajós). Distribution of this species rather poorly known, but contemporary wisdom Turdus fumigatus suggests that T. hauxwelli occurs in this interfluve. Santos et al. 2011a. Juruti, Pará Pyrrhura picta* Based on CBRO (2011) this should be P. snethlageae or P. amazonum. Neomorphus geoffroyi By range more likely to be N. squamiger. A biogeographically extraordinary record given allopatry in Capito barbets, Capito dayi suggest should be treated as hypothetical if no photo or specimen. Unexpected in sympatry with P. varzae, which becomes more heavily barred Picumnus cirratus towards the western end of its distribution inviting confusion with cirratus. A. infuscatus does not occur east of the rio Madeira; this will pertain to A. Automolus infuscatus paraensis. Pipra aureola Sympatry with P. fasciicauda unknown from most of Amazonia. Not expected to occur sympatrically with P. latirostris in this interfluve Poecilotriccus fumifrons (Madeira-Tapajós). Replaced by I. croconotus in most of Amazonia, including the Madeira- Icterus jamacaii Tapajós interfluve. An extremely significant range extension not discussed in the text, unknown Gnorimopsar chopi from central Amazonia. Santos et al. 2011b. Jí-Paraná, Rondônia Megascops watsonii* Replaced by M. usta south of the rio Amazonas. Based on current taxonomy does not occur west of the Tapajós, P. malaris Phaethornis superciliosus expected in this region. Absent from this interfluve (Madeira-Tapajós) where replaced by H. Hypocnemis subflava ochrogyna (in this case) and the recently described H. rondoni. Does not occur south of the rio Amazonas, based on CBRO (2011) this Hylexetastes perrotii* should be H. uniformis. A. infuscatus is undocumented east of the rio Madeira, this will likely pertain Automolus infuscatus to A. paraensis. Schiffornis turdina south of the rio Amazonas and east of the rio Madeira Schiffornis amazona* following CBRO (2011). Distribution of this species rather poorly known, but contemporary wisdom Turdus fumigatus suggests that T. hauxwelli occurs in this interfluve. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Santos et al. 2011c. Serra do Cachimbo, Pará Endemic to north-east Brazil, the Ortalis occurring in this region is O. Ortalis superciliaris motmot. Psophia viridis* Based on CBRO (2011) this should be P. dextralis. Pyrrhura picta* Based on CBRO (2011) this should be P. amazonum or P. snethlageae. Unknown east of the Tapajós and would represent a significant range Brotogeris cyanoptera extension, better documentation is desirable. Unknown in central Brazilian Amazonia, more likely to be P. theresiae which Polytmus guainumbi is common on the Serra do Cachimbo and in other Amazonian savannah regions (e.g. Pacheco & Olmos 2005). Pteroglossus viridis* An old record that pertains to P. inscriptus pre-split. Thamnophilus murinus Undocumented east of the rio Tapajós. Unexpected in sympatry with H. maculicauda and is unrecorded on the Hypocnemoides melanopogon Tapajós south of the mouth. Synallaxis albigularis Undocumented east of the rio Madeira. Does not occur between the Tapajós and Xingu north of the Teles Pires Hemitriccus minor where replaced by Lophotriccus galeatus. Listed in error because of a mislabelled specimen collected by Hidasi, which was likely taken in Goias given the date (but not the locality) on the Corythopis delalandi specimen label. The specimen was collected within a day of a series taken at o o the ‘Rio Araguaia, margem direita, Aragarças (15 55’S, 52 15’W)’. Fluvicola pica* An old record that pertains to F. albiventer pre-split. Hylophilus brunneiceps A clerical error only occurs in NW Amazonia. Schunck et al. 2011. two localities Amapá Undocumented north of the rio Amazonas and east of the rio Branco, where Venilliornis affinis replaced by V. cassini. Silveira & D’Horta 2002. Vila Bela da Santíssima Trindade, Mato Grosso Not expected in this interfluve, presumably a mislabelled or misidentified Neopelma sulphureiventer historical specimen. Not expected in this interfluve, old specimen likely H. pectoralis, with which Hylophilus thoracicus this species was historically lumped, see Pacheco et al. (2011). Somenzari et al. 2011. Amazonia-Cerrado ecotone, Mato Grosso/Pará Based on CBRO (2011) this should be Trogon ramonianus, T. violaceus only Trogon violaceus* occurs north of the rio Amazonas and east of the rio Negro. This species was listed in error; the record pertains to S. hypoleuca, which is Serpophaga nigricans expected in this region. P. genibarbis and P. coraya are not expected to occur sympatrically in this Pheugopedius genibarbis region, an undocumented audio record is insufficient evidence for an important range extension. Phaeothlypis rivularis* Based on CBRO (2011) this should be P. mesoleuca. Undocumented south of the rio Amazonas between the rios Tapajós and Caryothraustes canadensis Tocantins. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Vasconcelos et al. 2011. Monte Alegre, Pará Questions over specimen provenance, likely taken on the south bank as Notharchus ordii discussed in Lees et al. 2013a. Pteroglossus bitorquatus Unknown on north bank of the Amazon. Whittaker 2009. Rio Roosevelt, Amazonas Based on current taxonomy does not occur west of the Tapajós, P. malaris Phaethornis superciliosus expected in this region. DISCUSSION be very tenuous. In fact, reliable field identification of most species of swifts requires a highly trained observer to obtain very good, preferably prolonged, views. We Our analysis indicates that errors are near ubiquitous, albeit at a low frequency in Amazonian avian inventories in peer- must also recognize that our taxonomy of some groups reviewed papers, book chapters, and reserve management such as swifts may suffer far more serious identification plans. Many errors may reflect a lack of prior knowledge problems than "use of outdated taxonomy" if our working of a recent split—in which case the parent species was knowledge is not based on identification of topotypical material, a step rarely acknowledged as a requirement for listed (despite the authors referring to a contemporary taxonomic arrangement that acknowledges the split) or to accurate taxon identification. assignment of the wrong member of a species complex. In some cases, errors have been propagated by authors who The way forward—a road-map for included historical data, but failed to adjust for subsequent writing species inventories. changes in taxonomy split (e.g., Lopes et al. 2009). In many cases, inaccurate distributional maps, frequently That all inventories published in peer-reviewed journals seen in field guides and some online sites, proliferate fall within the 95% confidence interval of accuracy is an errors. For example the tyrant flycatchers Helmeted obviously satisfying statistic to report, but we believe that Pygmy-Tyrant Lophotriccus galeatus and Snethlage’s Tody- reducing error rates in species inventories still further is an easily achievable goal. Such reductions increase the Tyrant Hemitriccus minor are erroneously mapped as occurring sympatrically in southern Amazonia by some utility of such lists for macroecologists and taxonomists authors (e.g., Ridgely & Tudor 1994; Van Perlo 2009; studying variation in Neotropical birds, and to increase Sigrist 2009) when no such instances of sympatry have transparency, we suggest a series of guidelines that may been confirmed (Cohn-Haft 2000). improve the accuracy and utility of species lists. Our review highlights apparent knowledge gaps in our collective understanding of the distribution of 1. Obtain good documentation many difficult-to-separate Amazonian species pairs e.g., in the swifts Chaetura chapmani/viridipennis, the While in the field, ornithologists should make every thrushes Turdus fumigatus/hauxwelli, and the manakins effort to collect as much documentary evidence to prove the presence of a given species. Obviously it is not always Pipra aureola/fasciicauda which are inadequately mapped in the literature and require more robust surveys feasible, nor strictly necessary to provide voucher material (preferably with voucher specimens) to ascertain their for widespread common species such as Great Kiskadee actual distributional limits and zones of contact within Pitangus sulphuratus and House Wren Troglodytes the basin (e.g., O'Neill et al. 2011). In the case of the musculus in every inventory (although the effort to obtain documentation for these species should be negligible and swifts we have not listed their occurrences in Table 1 as most inventories have followed the ‘expected’ pattern is certainly welcomed). However, evidence must certainly of occurrence in Amazonia based on a few specimen be obtained and presented for any rarer species or poorly records, as published by Marin (1997). However we note known species, particularly any that are not anticipated that Chaetura chapmani/viridipennis are not separable in the region. These species would typically be afforded a separate species account in the body of the text in in the field, nor readily diagnosable by genetic analysis (Vaseghi & Chesser 2011), so the accepted pattern of which details of these important observations can be occurrence universally followed since 1997 appears to amplified. Evidence is ideally a combination of specimens Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira (including tissue samples), photographs, and sound- 3. If in doubt, leave it out recordings (e.g., Carlos et al. 2010). Detailed field notes are obviously useful (particularly in the absence of other If doubt remains over an identification of a difficult-to- evidence), but do not represent unquestionable proof and identify species pair or species complex, then a record cannot be accepted as hard evidence. The accumulation can be either excluded or included as hypothetical, of evidentiary information of these types can essentially ideally with some discussion of the potential record. eliminate pre-publication errors of identification as they Future fieldwork will likely result in confirmed records. become available for evaluation by outside experts. If Over-confidence may lead to future identification error such expert review is not obtained, then at least it will cascades and should be avoided. be possible for future review to correct errors. Obtaining highly accurate GPS coordinates (not coordinates taken 4. Include as much supporting life history data as from a map or Google Earth) at all inventory sites that space allows will be listed separately in the published paper is also extremely important. These coordinates should be taken As highlighted above, many inventories include supporting in decimal degrees, with all decimals provided by unit life history information such as a) a qualitative (or better recorded, and include the datum and an error estimate quantitative) abundance estimate or calculation, b) (Chapman & Wieczorek 2006). Great care should be (micro)habitat usage, c) seasonality, d) breeding behavior taken to identify which riverbanks were surveyed. If both (e.g., nest records, brood patches, gonadal data). These banks of rivers are surveyed, they should have separate types of data add scientific value to a paper and make it coordinates and indications in the list (B. M. Whitney more citable. in litt.). 5. Archive digital vouchers 2. Present documentation hierarchically and transparently We believe it is not simply enough to indicate that documentation is archived in the author’s private Once documentary evidence has been obtained, the collections and we urge journals not to accept manuscripts level of documentation for each species should be that state that documentary material will be archived “at listed for each species and ranked hierarchically, with some point in the future.” On many occasions we have permanent archived voucher material: 1) specimens, 2) solicited documentary evidence and it has not been video, preferably with commentary; 3) still photographs forthcoming. If documentary evidence in the form of and/or sound recordings (ranked over sight records). images and sound recordings is placed online in the If supporting documentation is not available, authors public domain, then peer-review is immediate and the should indicate the identity of the observers involved in whole process becomes more transparent (e.g., Lees et the record, and whether the record is auditory, visual, or al. 2012, 2013a, 2013b). Such digital vouchers are not both (Willis 2003). On some occasions video may be the intended to supplant traditional specimen vouchers but most unambiguous, complete form of documentation instead provide an opportunity for peer review of unusual for a rare species (B. M. Whitney in litt.). If a record is records, which is not possible if material is inaccessible. undocumented and of significant biogeographic interest, Field photographs can be archived on the Brazilian avian then authors can include morphological descriptions database Wikiaves (WA: www.wikiaves.com.br) where that lead to the species identification. If in doubt, a they are searchable by accession number (which can be record should be considered as hypothetical, pending provided in appendices), whereas both field and in-hand future confirmation, and excluded from the main list, or photographs can be archived on the Internet Bird Collection identified to the genus or species complex level. Accession (IBC: ibc.lynxeds.com/). Although both of these sites are numbers should be provided for important specimen not currently institutionally hosted and therefore their records, and if possible, images of important specimens existence cannot be guaranteed in perpetuity, they seem should be included as photo figures within manuscripts or to represent long-term projects that will remain active as supplementary online material (SOM), which should for many years. Sound recordings can be archived in be permanently archived at a stable URL. Museums several collections, including a) Wikiaves; b) the global should be encouraged to provide digital space to facilitate avian sound library Xeno-canto (XC: www.xeno-canto. this archiving (F. Olmos in litt.). It should be noted that org), where multiple ‘background’ species can be listed the highest quality evidence for different species may to reduce workload for documenting common species; c) vary—a sound recording of an Elaenia may be of more the Macaulay Library (ML: http://macaulaylibrary.org/) value than a photograph or a prepared specimen, whereas and d) the Avian Vocalizations Center (AVoCet: avocet. sound recordings of many species may not be diagnosable zoology.msu.edu/) where online peer-review is also from closely related heterospecifics. possible. Many other sound archives are available, and Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira all of them should be able to provide accession numbers latitudes knowledge of spatio-temporal patterns of and be readily searchable on the internet. For a digital bird distribution is collated principally by amateur voucher to be functional, the diagnostic field marks and ornithologists, and data is increasingly being compiled vocal traits need to be visible in photographs or audible using the internet (e.g., Sullivan et al. 2009). Similarly, in sound recordings. Presentation of undiagnosable and the submission of digital vouchers (photographs or ambiguous material should be avoided (e.g., Jackson recordings) by amateur ornithologists using sites such 2006). Digitalization of specimen skins is also a highly as Wikiaves and Xeno-canto, or through the use of desirable future prospect (e.g., Monk & Baker 2001) online checklist sites such as eBird (ebird.org/content/ that will allow for general web-based peer review and ebird/) promises to increase our knowledge of tropical museums should ideally include their holdings on an avifaunas as long as expert ornithologists maintain a close online database. scrutiny to filter out probable erroneous submissions. We recommend that compilers of lists use data from third 6. Conduct rigorous searches for historical records parties, but we suggest that authors carry out a thorough prior error-checking, particularly if the record is unusual. Incorporating old specimen records is extremely This error-checking should include: 1) verifying that the important to add historical depth and may function as image/recording is identifiable and similar species can reference point to quantify shifting baselines. Authors be eliminated; and 2) checking to see if there are any should make efforts to solicit specimen records from grounds to doubt whether the voucher was taken in the both domestic and foreign museums (Alberch 1993). locality to which it is attributed. This can be achieved by Currently, ornithological data from 42 institutions verifying that the other images and/or recordings taken can be searched using the digital database Ornithology by the same author around the same time are in complete Information System (ORNIS: www.ornisnet.org/) and agreement and have undoctored Exif files, i.e., confirm more collections will be available for online search in that there is no evidence of image tampering (see e.g., the near future. Collecting localities can be roughly Harrop et al. 2012). Such error-checking should not be located using Paynter & Traylor (1991), which are freely restricted to web-based resources to which members of available online from the Biodiversity Heritage Library the general public upload vouchers; errors may remain (BHL: www.biodiversitylibrary.org/), which is itself an undetected or uncorrected for years in institutional-based essential resource in searching for historic records along archives, particularly those that do not carefully follow with the Searchable Ornithological Research Archive current taxonomies. Many new digital cameras come (SORA: sora.unm.edu/). However, care should be taken with inbuilt GPS that further reduce the possibility of in the interpretation of historical data. Although it has fraudulent photographic evidence; one such camera was frequently been argued that physical specimens provide recently used in documenting the first Brazilian record of the most reliable evidence for assessing species presence Corncrake Crex crex (Burgos & Olmos 2013). (e.g., McKelvey et al. 2008), there are numerous studies indicating that specimen data are only as reliable as the 8. Ensure a consistent taxonomy is followed associated collection details (Knox 2003; Boessenkool et al. 2010). We encourage compilers of inventories to As our literature trawl revealed, incorrect taxonomy is check any biogeographically unusual historical record a major source and propagator of errors in biodiversity by visiting the collection to physically check specimens inventories (see also Bortolus 2008). Some inventories and their labels. If this is not possible, then curatorial do not state which taxonomy is being followed, which staff could provide images of the specimens in question can make interpretation of the results difficult. We (see examples in Silveira & D’Horta 2002; Lees et al. recommend that authors use the most recent version 2013a). In the event that the identification is deemed of the checklist prepared by the Comitê Brasileiro de secure then it may be worth double-checking collectors’ Registros Ornitológicos (CBRO 2014: www.cbro.org. itineraries and conferring against the data to make sure br/CBRO/listabr.htm) if focusing only on Brazil, or that no mistake was made—see the example of Southern the South American Classification Committee’s checklist Antpipit Corythopis delalandi discussed in Table 1. (Remsen 2013; SACC: www.museum.lsu.edu/~Remsen/ SACCBaseline.html) for the wider South American 7. Take care in citing digital vouchers of third region, although it should be noted that these currently parties diverge significantly, with SACC retaining a more conservative taxonomy. Many errors in the Amazonian inventories reflected a lack of knowledge of the most In addition to providing digital archives of the authors' recent definitions on species limits, or a failure to cross- own records, some inventories also include data and/ reference current taxonomy against older species lists. or digital vouchers of other observers' sightings, Fortunately, and as our evaluations for this paper have including those of amateur ornithologists. At temperate Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. 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Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira APPENDIX 1: Amazonian avifaunal inventories (published between 2000 and 2013) subject to the meta-analysis. Aguiar, K. M. O.; Naiff, R. H.; & Xavier, B. 2010. Aves da Reserva Biológica do Lago Piratuba, Amapá, Brasil. Ornitholgia, 4: 1–14. Aleixo, A. & Poletto, F. 2007. Birds of an open vegetation enclave in southern Brazilian Amazonia. The Wilson Journal of Ornithology, 119: 610-630. Aleixo, A.; Poletto, F.; Portes, E.; Silva, M.; & Lima, F. 2008. Avaliação do estado do conhecimento da avifauna na região da BR- 163 no estado do Pará, v. 2, p. 73-81. In: Ferreira, L. V. (org.). Zoneamento ecológico-econômico da área de influência da rodovia BR-163 (baixo Amazonas, Transamazônica e Xingu) com ênfase na biodiversidade. Belém. Aleixo, A. & Guilherme, E. 2010. Avifauna of the Estação Ecológica do Rio Acre, state of Acre, on the Brazil/Peru border: composition, ecological distribution, and noteworthy records. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais 5: 279–309. Aleixo, A.; Poletto, F.; Portes, E. & Lima, M. F. C. 2010. Aves, p 53-56. In: Oliveira, A. C. M.; Santos, J. B. & Santos-Costa, M. C. (orgs.): Os animais da Tanguro, Mato Grosso: diversidade na zona de transição entre a Floresta Amazônica e o Cerrado: MPEG/ UFPA/IPAM, Belém. Aleixo, A.; Poletto, F.; Lima, M. F. C.; Castro, M.; Portes, E.; & Miranda, L. S. 2011. Notes on the vertebrates of northern Pará, Brazil: a forgotten part of the Guianan Region, II. Avifauna. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais, 6: 11–65. Aleixo, A.; Carneiro L.; & Dantas, S.M. 2012. Aves, p 102–141. In: Martins, F. D.; Castilho, A. F.; Campos, J.; Hatano, F. M.; Rolim, S. G. (orgs.). Fauna da Floresta Nacional de Carajás: estudos sobre vertebrados terrestres, 1 ed. São Paulo: Nitro Imagens. Almeida, A.; Couto, H.; & Almeida, A. 2003. Diversidade beta de aves em hábitats secundários da Pré-Amazônia maranhense e interação com modelos nulos. Ararajuba, 11: 157–171. Borges, S. H. & de Almeida, R. A. M. 2011. Birds of the Jaú National Park and adjacent areas, Brazilian Amazon: new species records with reanalysis of a previous checklist. Revista Brasileira de Ornitologia, 19: 108–133. Cohn-Haft, M.; Pacheco, A. M. F.; Bechtoldt, C. L.; Torres, M. F. N. M.; Fernandes, A. M.; Sardelli, C. H.; & Macêdo, I. T. 2007. Capítulo 10. Inventário ornitológico, p. 145–178. In: Rapp Py-Daniel, L.; Deus, C.P.; Henriques, A.L.; Pimpão, D.M.; Ribeiro, O.M. (orgs.). Biodiversidade do Médio Madeira: Bases científicas para propostas de conservação. INPA: Manaus. Dantas, S. M.; Faccio, M. S.; & Lima, M. d. F. 2011. Avifaunal inventory of the Floresta Nacional de Pau-Rosa, Maués, state of Amazonas, Brazil. Revista Brasileira de Ornitologia, 19: 154–166. Fávaro, F. L. & Flores, J. M. 2009. Aves da Estação Ecológica Terra do Meio, Pará, Brasil: resultados preliminares. Ornithologia, 3: 115–131. Guilherme, E. 2007. Levantamento preliminar da avifauna do complexo de Florestas Públicas Estaduais do Mogno e dos Rios Liberdade e Gregório, município de Tarauacá, estado do Acre, como subsídio para elaboração de seus planos de manejo. Atualidades Ornitológicas, 136: 1–8. Guilherme, E. & Borges, S. H. 2011. Ornithological records from a campina/campinarana enclave on the upper Juruá river, Acre, Brazil. Wilson Journal of Ornithology, 123: 24–32. Guilherme, E. & Dantas, S. M. 2011. Avifauna of the Upper Purus River, State of Acre, Brazil. Revista Brasileira de Ornitologia, 19, 185–199. Lees, A. C.; Davis, B. J. W.; Oliveira, V. E.; & Peres, C. A. 2008. Avifauna of a structurally heterogeneous forest landscape in the Serra dos Caiabis, Mato Grosso, Brazil: a preliminary assessment. Cotinga, 29: 149–159. Lees, A. C.; Moura, N. G.; Silva, A. S.; Aleixo, A. L. P.; Barlow, J.; Berenguer, E.; Ferreira, J.; & Gardner, T. A. 2012. Paragominas: a quantitative baseline inventory of an Eastern Amazonian avifauna. Revista Brasileira de Ornitologia, 20: 93–118. Lees, A. C.; Moura, N. G.; Andretti, C. B.; Davis, B. J. W.; Lopes, E. V.; Henriques, L. M. P.; Aleixo, A.; Barlow, J.; Ferreira, J.; & Gardner, T. A. 2013a. One hundred and thirty-five years of avifaunal surveys around Santarém, central Brazilian Amazonia. Revista Brasileira de Ornitologia, 21: 16–57. Lees, A. C.; Zimmer, K. J.; Marantz, C. M.; Whittaker, A.; Davis, B. J. W.; &Whitney, B. M. 2013b. Alta Floresta revisited: an updated review of the avifauna of the most intensively surveyed site in south-central Amazonia. Bulletin of the British Ornithologists’ Club, 133: 178–239. Mestre, L. A. M.; Thom, G.; Cochrane, M. A.; & Barlow, J. 2010. The birds of Reserva Extrativista Chico Mendes, South Acre, Brazil. Boletim do Museu Paraense Emílio Goeldi: Ciências Naturais, 5: 311–333. Mestre, L. A. M.; Rechetelo, J.; Cochrane, M. A.; & Barlow, J. 2011. Avifaunal inventory of a Southern Amazonian transitional forest site: the São Luiz farm, Mato Grosso, Brazil. Boletim do Museu Paraense Emilio Goeldi: Ciências Naturais 6: 147–161. Oliveira, D. M. M.; Novack, L.; Florêncio, F. D.; Assumpção, I. T.; Silveira, R. M. L.; Almeida, E. C.; & Weiss, B. 2011. Aves da Fazenda São Nicolau, Cotriguaçu - Mato Grosso. Diversidade, Endemismo e Conservação. p. 171-202. In: Rodrigues, D.J.; Izzo, T.J.; Battirola, L.D. Descobrindo a Amazônia Meridional: biodiversidade da Fazenda São Nicolau. Cuiabá-MT: Editora Pau e Prosa Comunicação Ltda. Olmos, F.; Silveira, L. F.; & Benedicto, G. A. 2011. A Contribution to the ornithology of Rondônia, southwest of the Brazilian Amazon. Revista Brasileira de Ornitologia, 19: 200–229. Pacheco, J. F. & Olmos, F. 2005. Birds of a latitudinal transect in the Tapajós-Xingu interfluvium, eastern Brazilian Amazônia. Revista Brasileira de Ornitologia, 13: 29–46. Pacheco, J. F.; Kirwan, G. M.; Aleixo, A.; Whitney, B. M.; Whittaker, A.; Minns, J.; Zimmer, K. J.; Fonseca, P. S. M.; Lima, M. F. C.; & Oren, D. C. 2007. An avifaunal inventory of the CVRD Serra dos Carajás project, Pará, Brazil. Cotinga, 27: 15–30. Portes, C. E. B.; Carneiro, L. S.; Schunck, F.; Silva, M. S. S.; Zimmer, K. J.; Whittaker, A.; Poletto, F.; Silveira, L. F.; & Aleixo. A. 2011. Annotated checklist of birds recorded between 1998 and 2009 at nine areas in the Belém area of endemism, with notes on some range extensions and the conservation status of endangered species. Revista Brasileira de Ornitologia, 19: 167–184. Santos, M. P. D.; Aleixo, A. L. P.; Horta, F. M.; & Portes, E. 2011a. Avifauna of the Juruti region, Pará, Brazil. Revista Brasileira de Ornitologia, 19: 134–153. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Santos, M. P. D.; da Silva, G. K.; & dos Reis, A. L. 2011b. Birds of the Igarapé Lourdes Indigenous Territory, Jí-Paraná, Rondônia, Brazil. Revista Brasileira de Ornitologia, 19: 230–243. Santos, M. P. D.; Silveira, L. F., & da Silva, J.M.C. 2011c. Birds of Serra do Cachimbo, Pará State, Brazil. Revista Brasileira de Ornitologia, 19: 244–259. Schunck, F.; De Luca, A. C.; Piacentini, V. Q.; Rego, M. A.; Rennó B.; & Corrêa, A. H. 2011. Avifauna of two localities in the south of Amapá, Brazil, with comments on the distribution and taxonomy of some species. Revista Brasileira de Ornitologia, 19: 93–107. Silveira, L. F. & Horta, F. M. 2002. A avifauna da região de Vila Bela da Santíssima Trindade, Mato Grosso. Papéis Avulsos de Zoologia (São Paulo), 42: 265–286. Somenzari, M.; Silveira, L. F.; Piacentini, V. Q.; Rego, M. A.; Schunck, F.; & Cavarzere, V. 2011. Birds of an Amazonia-Cerrado ecotone in Southern Pará, Brazil, and the efficiency of associating multiple methods in avifaunal inventories. Revista Brasileira de Ornitologia, 19: 260–275. Vasconcelos, M. F.; Pacheco, J. F.; & Parrini, R. 2007. Levantamento preliminar e conservação da avifauna na zona urbana de Marabá, Pará, Brasil. Cotinga, 28: 45–51. Vasconcelos, M. F.; Dantas, S. M.; & Silva, J. M. C. 2011. Avifaunal inventory of the Amazonian savannas and adjacent habitats of the Monte Alegre region (Pará, Brazil), with comments on biogeography and conservation. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais, 6: 119–145. Whittaker, A. 2009. Pousada Rio Roosevelt: a provisional avifaunal inventory in south-western Amazonian Brazil, with information on life history, new distributional data and comments on taxonomy. Cotinga, 31: 20–43. APPENDIX 2: Reserve management plans with bird lists subject to analysis. ESEC Rio Acre, FLONA de Carajás, FLONA de Crepori, FLONA do Amanã, FLONA do Jamanxim, FLONA do Purus, FLONA do Trairão, FLONA Macauã, FLONA Mapiá-Inauini, FLONA Tapajós, FLONA Tapirape-aquiri, PARNA Campos Amazônicos, PARNA da Serra da Cutia, PARNA da Serra do Divisor, PARNA de Anavilhanas, PARNA de Juruena, PARNA do Araguaia, PARNA do Cabo Orange, PARNA do Monte Roraima, PARNA Montanhas do Tumucumaque, PARNA Pacaás Novos, REBIO de Uatumã, REBIO do Gurupi, REBIO do Jaru, REBIO do Rio Trombetas, REBIO do Tapirapé, REBIO Guaporé, REBIO Nascentes da Serra do Cachimbo, RESEX Arapixi, RESEX Baixo Juruá, RESEX, Capanã Grande, RESEX do Cazumbá-Iracema, RESEX Rio Iriri, RESEX Riozinho do Anfrísio & RESEX Tapajós-Arapiuns. Revista Brasileira de Ornitologia, 22(2), 2014 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement

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Revista Brasileira de Ornitologia, 22(2), 107-120 ARTICLE June 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement 1,6 2 1 3 4 Alexander C. Lees , Luciano Nicolas Naka , Alexandre Aleixo , Mario Cohn-Haft , Vítor de Q. Piacentini , 5 4 Marcos Pérsio Dantas Santos and Luís Fábio Silveira Coordenação de Zoologia, Museu Paraense Emílio Goeldi, CP 399, Belém, Pará, Brazil. Laboratório de Ornitologia, Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, 1235, CEP 50670-901, Recife, Pernambuco, Brazil. Coleção de Aves, Instituto Nacional de Pesquisas da Amazônia (INPA), Avenida André Araújo 2936, Bairro Petrópolis, CEP 69060-000, Manaus, Amazonas, Brazil. Seção de Aves, Museu de Zoologia da Universidade de São Paulo (MZUSP), Avenida Nazaré 481, Ipiranga, CEP 04263-000, São Paulo, SP, Brazil. Universidade Federal do Pará, Instituto de Ciências Biológicas, Laboratório de Ecologia e Zoologia de Vertebrados, Rua Augusto Corrêa, 1, Guamá, CEP 66075-110, Belém, Pará, Brazil. Corresponding author: alexanderlees@btopenworld.com Received on 11 November 2013. Accepted on 02 March 2014. ABSTRACT: Site-based avian inventories are ubiquitous in Neotropical ornithology but are prone to error if fieldworkers are not familiar with the regional species pool, particularly in species-rich regions such as the Amazon basin. Here, we review recent species lists from the Brazilian Amazon in both the primary ornithological literature and in protected area management plans to assess the level of putative errors in terms of bird species recorded in site-based inventories that are biogeographically unlikely in the sampled region. We found errors to be frequent across all inventory types. Failure to recognize recent taxonomic modifications in a cited taxonomy was a common error in many inventories. We outline a series of steps to follow to improve the utility and accuracy of avian inventories, and stress the importance of both obtaining and archiving documentary material, which should be included in the publications as digital vouchers to facilitate detailed peer review. KEYWORDS: Amazonia, avian surveys, checklist, documentation, taxonomy, vouchers. INTRODUCTION other hand, avian inventories are likely to be cited for centuries (e.g., Snethlage 1908), which also means that Comprehensive and accurate site-based species errors can potentially propagate for decades. inventories are the backbone of macroecological studies There is little doubt that birds represent the best- known taxonomic group in the Neotropics, yet our and crucial for understanding multi-scale patterns of species richness, evolutionary processes, natural patterns knowledge of the avifauna in many regions remains of environmental heterogeneity, and species-specific poorly documented, particularly in the vast Amazon responses to environmental change (Blackburn & Gaston basin. In fact, significant knowledge gaps regarding 1998). Species lists can function as a baseline to which species identification, distribution, and taxonomy still exist in entire Amazonian regions (Aleixo 2009; Barlow et new ecological and evolutionary studies can be compared in the future (Moritz et al. 2008; Coterrill & Foissner, al. 2011). These gaps in knowledge, allied to the intrinsic 2010). However, compiling species lists can be a labor- difficulties of surveying birds in highly diverse tropical intensive and a rather unrewarding academic task, as forests, where researchers are reliant on avian vocalizations high-impact scientific journals typically do not publish to conduct accurate surveys (Remsen 1994; Cohn-Haft et al. 1997; Willis 2003) may result in false-positive species inventories. Despite the clear importance of high-quality baseline inventories in the face of global detections (i.e., species that appear in regional or site- habitat loss, fragmentation, degradation, and climate based lists that are unlikely to occur in a given region). change, avian inventories are being published in lower- Even well-trained ornithologists may make identification profile journals, which often do not demand the highest errors in these environments, which is unsurprising given the many morphologically and vocally similar species desirable scientific standards for publication. On the Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira which occur in sympatry in Amazonia. These errors METHODS have been experimentally quantified before, for aural errors in controlled studies of electronically broadcast Each Amazonian interfluve has its own unique avian avian vocalizations (e.g., Simons et al. 2007) and for assemblage, with species turnover particularly high visual errors by releasing trapped birds (of biometrically across wide rivers and in families or guilds with limited confirmed individuals) in front of field observers (e.g., dispersal capacity such as understory suboscines. These Hull et al. 2010), or even to test the subjectivity of biogeographical patterns are now increasingly well abundance estimates (Cerqueira et al. 2013). understood so that unexpected presences are reasonably Identification errors that enter the primary easy to spot. We reviewed 32 bird inventories (Appendix ornithological literature (species lists in journals) may 1) in the Brazilian Amazon published between 2000 and rapidly be spread into the secondary literature, leading to 2013 to look for instances of presumed misidentification incorrect distribution maps in widely used field guides. based on expert opinion of the distribution of allopatric This leads to further proliferation of identification errors, and parapatric Amazonian bird species (see Table 1). as ornithologists and birders alike may pay little attention These lists were published in international journals (n = 7), to the identification of ‘confusion’ species (similar-looking Brazilian journals (n = 21), and book chapters (n = 4). In and potentially sympatric species) widely considered to addition, we also reviewed 31 reserve management plans be present in a region (Robbins & Stallcup 1981; Willis (Appendix 2) from the Brazilian Amazon to compare error 2003; Rojas-Soto & de Ita 2005; McKelvey et al. 2008). rates with those lists in the primary literature. Given the Given these potential problems, we believe that species general lack of review of the grey literature, we expected inventories should be treated as rigorously as any other to find a higher rate of errors in unpublished reports. scientific enterprise and provide as much supporting Our error-checking process applied only to documentary evidence as possible (e.g., Cohn-Haft et biogeographically extremely unlikely records. When al. 1997; Silveira & D’Horta 2002; Silveira et al. 2010; searching these inventories there were many instances of Aleixo et al. 2011; Somenzari et al. 2011; Lees et al. 2012, unusual boreal and austral migrants, many of which are 2013a) to prevent ‘false presences’ becoming established difficult to identify, that we do not necessarily infer to in the literature (McKelvey et al. 2008; Silveira et al. be in error despite being presented without supporting 2010), as well as to facilitate re-evaluations of taxonomic information or documentation. Also, some species—such status in the future. as the White-rumped Swallow Tachycineta leucorrhoa— Corrections of previous mistakes have already are often reported from Amazonian sites, yet they lack been published in the recent Amazonian literature. For any documentation, and we assume many reports to be example: Cohn-Haft et al. (1997) removed seven species in error although we do not highlight them herein. We from the list of Stotz & Bierregaard (1989) of the birds also reviewed which supporting information was supplied north of Manaus; Naka (2006) removed, or included with species’ lists—form of documentation listed, digital as hypothetical, 15 species previously reported for the vouchers included—and whether abundance and habitat Brazilian state of Roraima; Whittaker et al. (2008) type information were incorporated in the data. re-identified or removed 30 species from the initial checklist of the birds of the upper Rio Urucú, originally RESULTS published by Peres & Whittaker (1991); Lopes et al. (2009) re-identified and corrected 52 species from the Chapada dos Guimarães; Lees et al. (2013a) moved We found evidence of presumed misidentifications in 25 to ‘hypothetical species appendix’ or removed entirely inventories (78%) involving 107 records of 82 species 10 species from the lists of Sanaiotti & Cintra (2001) (Table 1). The number of assumed misidentifications and Henriques et al. (2003) from around Santarém; varied between 0 (none) and 15 (X,¯ = 3.3, SD = 4.1, and Lees et al. (2013b) removed three species from 0-3.7% of the total list). Errors could be broadly divided the checklist of Alta Floresta (Zimmer et al. 1997) and into two groups: a) misidentification of a species that is moved another nine taxa to a ‘hypothetical species’ not known to occur in the Amazonian interfluve sampled appendix. However, we consider this issue likely more (n = 74, 70.4%); and b) confusion with replacement widespread and here evaluate the pervasiveness of species (taxonomic errors) for which the wrong member problems related to bird misidentifications in both the of a species pair or super-species complex was listed ‘primary’ and ‘grey’ Brazilian ornithological literature. In (n = 31, X,¯ = 29.0%), often because of a failure to this article, we judge the ubiquity and nature of errors account for shifts in nomenclature and ‘splits.’ in 63 Amazonian bird inventories (including all of our We found that 25% of surveys informed the type own) and point out likely cases of misidentification. We of documentation obtained during the survey but then suggest a roadmap for producing less error-prone only 4% provided links to digital vouchers, although avian inventories. some of these web-based resources have only become Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira available recently. Nearly 20% of the surveys included more heterogeneous in their error rates with the number qualitative abundance estimates and almost 60% of assumed misidentifications varying between 0 and 35 included information of which habitat types species were (n =84, X,¯ = 2.71, SD = 6.64) accounting for between 0 encountered. Reserve management plans (n = 31) were and 7.9% of all records. TABLE 1. A compilation of inferred errors from Amazonian avifaunal inventories between 2000 and 2013. All inferred errors represent apparently undocumented records which are not explicitly discussed in the text, some may of course be genuine, but given their biogeographic significance should be adequately documented before being presented as ‘confirmed’. Species denoted with an asterix* indicate taxonomic rather than identification errors. Citations can be found in Appendix 1. Aguiar et al. 2010. Comments Lago Piratuba, Amapá Sterna hirundinacea Undocumented north of Bahia, would be a first for the biome. Undocumented from Amapá or anywhere in the eastern half of the Guianan Synallaxis propinqua Shield. Aleixo & Poletto 2007. BX44 Polygon, Mato Grosso/ Amazonas Hylophilus hypoxanthus Replaced by Hylophilus muscicapinus in this interfluve (Madeira-Tapajós). Aleixo et al. 2010. Tanguro, Mato Grosso Hypocnemis cantator* Taxonomy followed unclear but should be H. striata. Undocumented east of the rio Xingu where replaced by Hemitriccus minor - Lophotriccus galeatus as reported nearby by Mestre et al. 2011. Borges & Almeida 2011. Jau National Park, Amazonas Trogon ramonianus south of the rio Amazonas and west of the rio Negro Trogon violaceus* following CBRO (2009). Schiffornis amazonum north of the rio Amazonas and west of the rio Madeira Schiffornis turdina* following CBRO (2009). Dantas et al. 2011. FLONA de Pau-Rosa, Amazonas Polytmus guainumbi Unknown in central Brazilian Amazonia, more likely to be P. theresiae. Unknown in this interfluve (Madeira-Tapajós) where replaced by D. Dendrocolaptes picumnus hoffmannsi. Hylophilus hypoxanthus Replaced by Hylophilus muscicapinus in this interfluve (Madeira-Tapajós). Favaro & Flores 2009. Terra do Meio, Pará Does not occur south of the rio Amazonas, based on CBRO (2008) this Hylexetastes perrotii* should be H. uniformis. Reported here as sympatric with A. paraensis but highly unlikely as infuscatus Automolus infuscatus is undocumented east of the Madeira. Pipra aureola Not expected in the interior of the Tapajós-Xingu interfluve. Reported as sympatric with P. coraya but the two are replacement species; Pheugopedius genibarbis genibarbis unknown north of the Serra do Cachimbo between the Tapajós and Tocantins. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Aleixo & Guilherme 2010. Estação Ecológica do Rio Acre, Acre Chaetura spinicaudus Undocumented in SW Amazonia; best treated as hypothetical. Lees et al. 2008. Serra dos Caiabis, Mato Grosso Synallaxis cherriei Listed in error, record pertains to S. rutilans. Lees et al. 2012. Paragominas, Pará Phaeothlypis rivularis* Based on CBRO (2011) this should be P. mesoleuca. Archived digital voucher (a photo) appears to be a juvenile T. episcopus, Tangara sayaca which are very similar to T. sayaca. The latter would represent a significant range extension. Archived digital voucher (a photo) is ambiguous; we consider it better to Euphonia chrysopasta treat this record and others east of the rio Tocantins as hypothetical until better documentation available. Lees et al. 2013b. Santarém, Pará Phaeothlypis rivularis* Based on CBRO (2011) this should be P. mesoleuca. Mestre et al. 2010 . RESEX Chico Mendes, Acre Aulacorhynchus prasinus This should be Aulacorhynchus atrogularis following CBRO (2009). Mestre et al. 2011. Querencia, Mato Grosso Only P. latirostris expected in this region - as reported nearby by Aleixo et al. Poecilotriccus fumifrons Pacheco & Olmos 2005. BR163, Pará Does not occur between the Tapajós and Xingu north of the Teles Pires Hemitriccus minor where replaced by Lophotriccus galeatus. Pacheco et al. 2007. Carajas, Pará The taxonomic position of this species in relation to P. maranhaoensis is Phaethornis nattereri* unresolved but only the latter is expected in this region. Myrmotherula sclateri Undocumented east of the rio Xingu. Undocumented east of the rio Xingu, this species was removed from the Hyloctistes subulatus Carajás list by Aleixo et al. 2012. Does not occur in this interfluve (Xingu-Tocantins) see e.g. Cohn-Haft Lophotriccus galeatus (2000), Lees et al. (2013a). Undocumented as far south as Carajás, where similarly looking P. fasciicauda Pipra aureola has been documented, this species was removed from the Carajás list by Aleixo et al. 2012. As currently mapped this species is not expected in eastern Amazonia where Turdus hauxwelli T. fumigatus is usually reported. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Undocumented east of the rio Tapajós, this species was removed from the Hylophilus muscicapinus Carajás list by Aleixo et al. 2012. Portes et al. 2011. Belem Centre of Endemism, Pará Milvago chimango Clerical error, should be M. chimachima. Myrmeciza atrothorax Undocumented east of rio Tocantins. Thamnophilus schistaceus Undocumented east of rio Tocantins. Thamnophilus stictocephalus Undocumented east of rio Tocantins. Cranioleuca gutturata Undocumented east of rio Tocantins. Furnarius rufus Undocumented in the Belém centre of endemism. Undocumented east of rio Tocantins, recording likely pertain to a recently Hemitriccus minimus discovered and as yet undescribed Myiornis taxon. Hylophilus hypoxanthus Undocumented east of rio Tocantins. Tangara chilensis Undocumented east of rio Tocantins. Based on CBRO (2011) this should be P. mesoleuca, which was recently split Phaeothlypis rivularis* from P. rivularis. Euphonia chrysopasta Undocumented east of rio Tocantins. Oliveira et al. 2011. Cotriguaçu, Mato Grosso This species is restricted to the Atlantic Forest and is not expected in Leucopternis lacernulatus Amazonia, record likely relates to a similar species. This would represent the first record from anywhere in central or north Circus cinereus Brazil and would require extensive documentation. This should be P. amazonum or P. snethlageae in this region, although the Pyrrhura picta* taxonomy followed in this inventory is unclear. This species is undocumented from northern Mato Grosso and would Pionus maximiliani represent a significant range extension. Notharchus macrorhynchus* Only N. hyperrhynchus occurs south of the Amazon. Colaptes campestris Not expected in NW Mato Grosso. Thamnomanes ardesiacus Undocumented east of the rio Madeira. Dysithamnus mentalis Not expected in NW Mato Grosso, should preferably be documented. This should be Schistocichla (formerly Percnostola) rufifacies in this region, Schistocichla leucostigma* although the taxonomy being followed in this inventory is unclear. X. spixii does not occur west of the rio Juruena (or Teles Pires), only X. Xiphorhynchus spixii elegans is expected. A. infuscatus is undocumented east of the rio Madeira; this will likely pertain Automolus infuscatus to A. paraensis. Hemitriccus zosterops Replaced by H. griseipectus south of the rio Amazonas. Fluvicola pica* Undocumented and unexpected in southern Amazonia. Reported as occurring sympatrically with T. hauxwelli, only T. hauxwelli Turdus fumigatus expected in this interfluve (Madeira-Juruena). Olmos et al. 2011. Rondônia Galbula albirostris Unknown south of the rio Amazonas, G. cyanicollis occurs in this region. Notharchus macrorhynchos* Only N. hyperrhynchus occurs south of the Amazon. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Capito niger only occurs north of the rio Amazonas; this record should Capito niger pertain to C. auratus based on current taxonomy. Unknown south of the rio Amazonas, P. bitorquatus occurs east of the Pteroglossus azara Madeira. Within Amazonia, unknown away from the floodplain forest along the main Celeus flavescens channel of the lower Amazon River; it would represent a significant range extension requiring documentation. Dysithamnus mentalis Documentation would be preferable for such a significant range extension. This should be Schistocichla (formerly Percnostola) rufifacies east of the Schistocichla leucostigma* Madeira and S. humaythae west of the Madeira following CBRO (2011). Dendrocolaptes picumnus Unknown in this interfluve where replaced by D. hoffmannsi. Hemitriccus griseipectus Undocumented in the Madeira-Tapajós interfluve. Schiffornis amazonum north of the rio Amazonas and west of the rio Madeira Schiffornis turdina* following CBRO (2011). Hylophilus hypoxanthus Replaced by Hylophilus muscicapinus in this interfluve (Madeira-Tapajós). Distribution of this species rather poorly known, but contemporary wisdom Turdus fumigatus suggests that T. hauxwelli occurs in this interfluve. Santos et al. 2011a. Juruti, Pará Pyrrhura picta* Based on CBRO (2011) this should be P. snethlageae or P. amazonum. Neomorphus geoffroyi By range more likely to be N. squamiger. A biogeographically extraordinary record given allopatry in Capito barbets, Capito dayi suggest should be treated as hypothetical if no photo or specimen. Unexpected in sympatry with P. varzae, which becomes more heavily barred Picumnus cirratus towards the western end of its distribution inviting confusion with cirratus. A. infuscatus does not occur east of the rio Madeira; this will pertain to A. Automolus infuscatus paraensis. Pipra aureola Sympatry with P. fasciicauda unknown from most of Amazonia. Not expected to occur sympatrically with P. latirostris in this interfluve Poecilotriccus fumifrons (Madeira-Tapajós). Replaced by I. croconotus in most of Amazonia, including the Madeira- Icterus jamacaii Tapajós interfluve. An extremely significant range extension not discussed in the text, unknown Gnorimopsar chopi from central Amazonia. Santos et al. 2011b. Jí-Paraná, Rondônia Megascops watsonii* Replaced by M. usta south of the rio Amazonas. Based on current taxonomy does not occur west of the Tapajós, P. malaris Phaethornis superciliosus expected in this region. Absent from this interfluve (Madeira-Tapajós) where replaced by H. Hypocnemis subflava ochrogyna (in this case) and the recently described H. rondoni. Does not occur south of the rio Amazonas, based on CBRO (2011) this Hylexetastes perrotii* should be H. uniformis. A. infuscatus is undocumented east of the rio Madeira, this will likely pertain Automolus infuscatus to A. paraensis. Schiffornis turdina south of the rio Amazonas and east of the rio Madeira Schiffornis amazona* following CBRO (2011). Distribution of this species rather poorly known, but contemporary wisdom Turdus fumigatus suggests that T. hauxwelli occurs in this interfluve. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Santos et al. 2011c. Serra do Cachimbo, Pará Endemic to north-east Brazil, the Ortalis occurring in this region is O. Ortalis superciliaris motmot. Psophia viridis* Based on CBRO (2011) this should be P. dextralis. Pyrrhura picta* Based on CBRO (2011) this should be P. amazonum or P. snethlageae. Unknown east of the Tapajós and would represent a significant range Brotogeris cyanoptera extension, better documentation is desirable. Unknown in central Brazilian Amazonia, more likely to be P. theresiae which Polytmus guainumbi is common on the Serra do Cachimbo and in other Amazonian savannah regions (e.g. Pacheco & Olmos 2005). Pteroglossus viridis* An old record that pertains to P. inscriptus pre-split. Thamnophilus murinus Undocumented east of the rio Tapajós. Unexpected in sympatry with H. maculicauda and is unrecorded on the Hypocnemoides melanopogon Tapajós south of the mouth. Synallaxis albigularis Undocumented east of the rio Madeira. Does not occur between the Tapajós and Xingu north of the Teles Pires Hemitriccus minor where replaced by Lophotriccus galeatus. Listed in error because of a mislabelled specimen collected by Hidasi, which was likely taken in Goias given the date (but not the locality) on the Corythopis delalandi specimen label. The specimen was collected within a day of a series taken at o o the ‘Rio Araguaia, margem direita, Aragarças (15 55’S, 52 15’W)’. Fluvicola pica* An old record that pertains to F. albiventer pre-split. Hylophilus brunneiceps A clerical error only occurs in NW Amazonia. Schunck et al. 2011. two localities Amapá Undocumented north of the rio Amazonas and east of the rio Branco, where Venilliornis affinis replaced by V. cassini. Silveira & D’Horta 2002. Vila Bela da Santíssima Trindade, Mato Grosso Not expected in this interfluve, presumably a mislabelled or misidentified Neopelma sulphureiventer historical specimen. Not expected in this interfluve, old specimen likely H. pectoralis, with which Hylophilus thoracicus this species was historically lumped, see Pacheco et al. (2011). Somenzari et al. 2011. Amazonia-Cerrado ecotone, Mato Grosso/Pará Based on CBRO (2011) this should be Trogon ramonianus, T. violaceus only Trogon violaceus* occurs north of the rio Amazonas and east of the rio Negro. This species was listed in error; the record pertains to S. hypoleuca, which is Serpophaga nigricans expected in this region. P. genibarbis and P. coraya are not expected to occur sympatrically in this Pheugopedius genibarbis region, an undocumented audio record is insufficient evidence for an important range extension. Phaeothlypis rivularis* Based on CBRO (2011) this should be P. mesoleuca. Undocumented south of the rio Amazonas between the rios Tapajós and Caryothraustes canadensis Tocantins. Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Vasconcelos et al. 2011. Monte Alegre, Pará Questions over specimen provenance, likely taken on the south bank as Notharchus ordii discussed in Lees et al. 2013a. Pteroglossus bitorquatus Unknown on north bank of the Amazon. Whittaker 2009. Rio Roosevelt, Amazonas Based on current taxonomy does not occur west of the Tapajós, P. malaris Phaethornis superciliosus expected in this region. DISCUSSION be very tenuous. In fact, reliable field identification of most species of swifts requires a highly trained observer to obtain very good, preferably prolonged, views. We Our analysis indicates that errors are near ubiquitous, albeit at a low frequency in Amazonian avian inventories in peer- must also recognize that our taxonomy of some groups reviewed papers, book chapters, and reserve management such as swifts may suffer far more serious identification plans. Many errors may reflect a lack of prior knowledge problems than "use of outdated taxonomy" if our working of a recent split—in which case the parent species was knowledge is not based on identification of topotypical material, a step rarely acknowledged as a requirement for listed (despite the authors referring to a contemporary taxonomic arrangement that acknowledges the split) or to accurate taxon identification. assignment of the wrong member of a species complex. In some cases, errors have been propagated by authors who The way forward—a road-map for included historical data, but failed to adjust for subsequent writing species inventories. changes in taxonomy split (e.g., Lopes et al. 2009). In many cases, inaccurate distributional maps, frequently That all inventories published in peer-reviewed journals seen in field guides and some online sites, proliferate fall within the 95% confidence interval of accuracy is an errors. For example the tyrant flycatchers Helmeted obviously satisfying statistic to report, but we believe that Pygmy-Tyrant Lophotriccus galeatus and Snethlage’s Tody- reducing error rates in species inventories still further is an easily achievable goal. Such reductions increase the Tyrant Hemitriccus minor are erroneously mapped as occurring sympatrically in southern Amazonia by some utility of such lists for macroecologists and taxonomists authors (e.g., Ridgely & Tudor 1994; Van Perlo 2009; studying variation in Neotropical birds, and to increase Sigrist 2009) when no such instances of sympatry have transparency, we suggest a series of guidelines that may been confirmed (Cohn-Haft 2000). improve the accuracy and utility of species lists. Our review highlights apparent knowledge gaps in our collective understanding of the distribution of 1. Obtain good documentation many difficult-to-separate Amazonian species pairs e.g., in the swifts Chaetura chapmani/viridipennis, the While in the field, ornithologists should make every thrushes Turdus fumigatus/hauxwelli, and the manakins effort to collect as much documentary evidence to prove the presence of a given species. Obviously it is not always Pipra aureola/fasciicauda which are inadequately mapped in the literature and require more robust surveys feasible, nor strictly necessary to provide voucher material (preferably with voucher specimens) to ascertain their for widespread common species such as Great Kiskadee actual distributional limits and zones of contact within Pitangus sulphuratus and House Wren Troglodytes the basin (e.g., O'Neill et al. 2011). In the case of the musculus in every inventory (although the effort to obtain documentation for these species should be negligible and swifts we have not listed their occurrences in Table 1 as most inventories have followed the ‘expected’ pattern is certainly welcomed). However, evidence must certainly of occurrence in Amazonia based on a few specimen be obtained and presented for any rarer species or poorly records, as published by Marin (1997). However we note known species, particularly any that are not anticipated that Chaetura chapmani/viridipennis are not separable in the region. These species would typically be afforded a separate species account in the body of the text in in the field, nor readily diagnosable by genetic analysis (Vaseghi & Chesser 2011), so the accepted pattern of which details of these important observations can be occurrence universally followed since 1997 appears to amplified. Evidence is ideally a combination of specimens Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira (including tissue samples), photographs, and sound- 3. If in doubt, leave it out recordings (e.g., Carlos et al. 2010). Detailed field notes are obviously useful (particularly in the absence of other If doubt remains over an identification of a difficult-to- evidence), but do not represent unquestionable proof and identify species pair or species complex, then a record cannot be accepted as hard evidence. The accumulation can be either excluded or included as hypothetical, of evidentiary information of these types can essentially ideally with some discussion of the potential record. eliminate pre-publication errors of identification as they Future fieldwork will likely result in confirmed records. become available for evaluation by outside experts. If Over-confidence may lead to future identification error such expert review is not obtained, then at least it will cascades and should be avoided. be possible for future review to correct errors. Obtaining highly accurate GPS coordinates (not coordinates taken 4. Include as much supporting life history data as from a map or Google Earth) at all inventory sites that space allows will be listed separately in the published paper is also extremely important. These coordinates should be taken As highlighted above, many inventories include supporting in decimal degrees, with all decimals provided by unit life history information such as a) a qualitative (or better recorded, and include the datum and an error estimate quantitative) abundance estimate or calculation, b) (Chapman & Wieczorek 2006). Great care should be (micro)habitat usage, c) seasonality, d) breeding behavior taken to identify which riverbanks were surveyed. If both (e.g., nest records, brood patches, gonadal data). These banks of rivers are surveyed, they should have separate types of data add scientific value to a paper and make it coordinates and indications in the list (B. M. Whitney more citable. in litt.). 5. Archive digital vouchers 2. Present documentation hierarchically and transparently We believe it is not simply enough to indicate that documentation is archived in the author’s private Once documentary evidence has been obtained, the collections and we urge journals not to accept manuscripts level of documentation for each species should be that state that documentary material will be archived “at listed for each species and ranked hierarchically, with some point in the future.” On many occasions we have permanent archived voucher material: 1) specimens, 2) solicited documentary evidence and it has not been video, preferably with commentary; 3) still photographs forthcoming. If documentary evidence in the form of and/or sound recordings (ranked over sight records). images and sound recordings is placed online in the If supporting documentation is not available, authors public domain, then peer-review is immediate and the should indicate the identity of the observers involved in whole process becomes more transparent (e.g., Lees et the record, and whether the record is auditory, visual, or al. 2012, 2013a, 2013b). Such digital vouchers are not both (Willis 2003). On some occasions video may be the intended to supplant traditional specimen vouchers but most unambiguous, complete form of documentation instead provide an opportunity for peer review of unusual for a rare species (B. M. Whitney in litt.). If a record is records, which is not possible if material is inaccessible. undocumented and of significant biogeographic interest, Field photographs can be archived on the Brazilian avian then authors can include morphological descriptions database Wikiaves (WA: www.wikiaves.com.br) where that lead to the species identification. If in doubt, a they are searchable by accession number (which can be record should be considered as hypothetical, pending provided in appendices), whereas both field and in-hand future confirmation, and excluded from the main list, or photographs can be archived on the Internet Bird Collection identified to the genus or species complex level. Accession (IBC: ibc.lynxeds.com/). Although both of these sites are numbers should be provided for important specimen not currently institutionally hosted and therefore their records, and if possible, images of important specimens existence cannot be guaranteed in perpetuity, they seem should be included as photo figures within manuscripts or to represent long-term projects that will remain active as supplementary online material (SOM), which should for many years. Sound recordings can be archived in be permanently archived at a stable URL. Museums several collections, including a) Wikiaves; b) the global should be encouraged to provide digital space to facilitate avian sound library Xeno-canto (XC: www.xeno-canto. this archiving (F. Olmos in litt.). It should be noted that org), where multiple ‘background’ species can be listed the highest quality evidence for different species may to reduce workload for documenting common species; c) vary—a sound recording of an Elaenia may be of more the Macaulay Library (ML: http://macaulaylibrary.org/) value than a photograph or a prepared specimen, whereas and d) the Avian Vocalizations Center (AVoCet: avocet. sound recordings of many species may not be diagnosable zoology.msu.edu/) where online peer-review is also from closely related heterospecifics. possible. Many other sound archives are available, and Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira all of them should be able to provide accession numbers latitudes knowledge of spatio-temporal patterns of and be readily searchable on the internet. For a digital bird distribution is collated principally by amateur voucher to be functional, the diagnostic field marks and ornithologists, and data is increasingly being compiled vocal traits need to be visible in photographs or audible using the internet (e.g., Sullivan et al. 2009). Similarly, in sound recordings. Presentation of undiagnosable and the submission of digital vouchers (photographs or ambiguous material should be avoided (e.g., Jackson recordings) by amateur ornithologists using sites such 2006). Digitalization of specimen skins is also a highly as Wikiaves and Xeno-canto, or through the use of desirable future prospect (e.g., Monk & Baker 2001) online checklist sites such as eBird (ebird.org/content/ that will allow for general web-based peer review and ebird/) promises to increase our knowledge of tropical museums should ideally include their holdings on an avifaunas as long as expert ornithologists maintain a close online database. scrutiny to filter out probable erroneous submissions. We recommend that compilers of lists use data from third 6. Conduct rigorous searches for historical records parties, but we suggest that authors carry out a thorough prior error-checking, particularly if the record is unusual. Incorporating old specimen records is extremely This error-checking should include: 1) verifying that the important to add historical depth and may function as image/recording is identifiable and similar species can reference point to quantify shifting baselines. Authors be eliminated; and 2) checking to see if there are any should make efforts to solicit specimen records from grounds to doubt whether the voucher was taken in the both domestic and foreign museums (Alberch 1993). locality to which it is attributed. This can be achieved by Currently, ornithological data from 42 institutions verifying that the other images and/or recordings taken can be searched using the digital database Ornithology by the same author around the same time are in complete Information System (ORNIS: www.ornisnet.org/) and agreement and have undoctored Exif files, i.e., confirm more collections will be available for online search in that there is no evidence of image tampering (see e.g., the near future. Collecting localities can be roughly Harrop et al. 2012). Such error-checking should not be located using Paynter & Traylor (1991), which are freely restricted to web-based resources to which members of available online from the Biodiversity Heritage Library the general public upload vouchers; errors may remain (BHL: www.biodiversitylibrary.org/), which is itself an undetected or uncorrected for years in institutional-based essential resource in searching for historic records along archives, particularly those that do not carefully follow with the Searchable Ornithological Research Archive current taxonomies. Many new digital cameras come (SORA: sora.unm.edu/). However, care should be taken with inbuilt GPS that further reduce the possibility of in the interpretation of historical data. Although it has fraudulent photographic evidence; one such camera was frequently been argued that physical specimens provide recently used in documenting the first Brazilian record of the most reliable evidence for assessing species presence Corncrake Crex crex (Burgos & Olmos 2013). (e.g., McKelvey et al. 2008), there are numerous studies indicating that specimen data are only as reliable as the 8. Ensure a consistent taxonomy is followed associated collection details (Knox 2003; Boessenkool et al. 2010). We encourage compilers of inventories to As our literature trawl revealed, incorrect taxonomy is check any biogeographically unusual historical record a major source and propagator of errors in biodiversity by visiting the collection to physically check specimens inventories (see also Bortolus 2008). Some inventories and their labels. If this is not possible, then curatorial do not state which taxonomy is being followed, which staff could provide images of the specimens in question can make interpretation of the results difficult. We (see examples in Silveira & D’Horta 2002; Lees et al. recommend that authors use the most recent version 2013a). In the event that the identification is deemed of the checklist prepared by the Comitê Brasileiro de secure then it may be worth double-checking collectors’ Registros Ornitológicos (CBRO 2014: www.cbro.org. itineraries and conferring against the data to make sure br/CBRO/listabr.htm) if focusing only on Brazil, or that no mistake was made—see the example of Southern the South American Classification Committee’s checklist Antpipit Corythopis delalandi discussed in Table 1. (Remsen 2013; SACC: www.museum.lsu.edu/~Remsen/ SACCBaseline.html) for the wider South American 7. Take care in citing digital vouchers of third region, although it should be noted that these currently parties diverge significantly, with SACC retaining a more conservative taxonomy. Many errors in the Amazonian inventories reflected a lack of knowledge of the most In addition to providing digital archives of the authors' recent definitions on species limits, or a failure to cross- own records, some inventories also include data and/ reference current taxonomy against older species lists. or digital vouchers of other observers' sightings, Fortunately, and as our evaluations for this paper have including those of amateur ornithologists. At temperate Revista Brasileira de Ornitologia, 22(2), 2014 Conducting rigorous avian inventories: Amazonian case studies and a roadmap for improvement Alexander C. Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. 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São Paulo: Nitro Imagens. Almeida, A.; Couto, H.; & Almeida, A. 2003. Diversidade beta de aves em hábitats secundários da Pré-Amazônia maranhense e interação com modelos nulos. Ararajuba, 11: 157–171. Borges, S. H. & de Almeida, R. A. M. 2011. Birds of the Jaú National Park and adjacent areas, Brazilian Amazon: new species records with reanalysis of a previous checklist. Revista Brasileira de Ornitologia, 19: 108–133. Cohn-Haft, M.; Pacheco, A. M. F.; Bechtoldt, C. L.; Torres, M. F. N. M.; Fernandes, A. M.; Sardelli, C. H.; & Macêdo, I. T. 2007. Capítulo 10. Inventário ornitológico, p. 145–178. In: Rapp Py-Daniel, L.; Deus, C.P.; Henriques, A.L.; Pimpão, D.M.; Ribeiro, O.M. (orgs.). Biodiversidade do Médio Madeira: Bases científicas para propostas de conservação. INPA: Manaus. Dantas, S. M.; Faccio, M. S.; & Lima, M. d. F. 2011. Avifaunal inventory of the Floresta Nacional de Pau-Rosa, Maués, state of Amazonas, Brazil. Revista Brasileira de Ornitologia, 19: 154–166. Fávaro, F. 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P.; Barlow, J.; Berenguer, E.; Ferreira, J.; & Gardner, T. A. 2012. Paragominas: a quantitative baseline inventory of an Eastern Amazonian avifauna. Revista Brasileira de Ornitologia, 20: 93–118. Lees, A. C.; Moura, N. G.; Andretti, C. B.; Davis, B. J. W.; Lopes, E. V.; Henriques, L. M. P.; Aleixo, A.; Barlow, J.; Ferreira, J.; & Gardner, T. A. 2013a. One hundred and thirty-five years of avifaunal surveys around Santarém, central Brazilian Amazonia. Revista Brasileira de Ornitologia, 21: 16–57. Lees, A. C.; Zimmer, K. J.; Marantz, C. M.; Whittaker, A.; Davis, B. J. W.; &Whitney, B. M. 2013b. Alta Floresta revisited: an updated review of the avifauna of the most intensively surveyed site in south-central Amazonia. Bulletin of the British Ornithologists’ Club, 133: 178–239. Mestre, L. A. M.; Thom, G.; Cochrane, M. A.; & Barlow, J. 2010. The birds of Reserva Extrativista Chico Mendes, South Acre, Brazil. Boletim do Museu Paraense Emílio Goeldi: Ciências Naturais, 5: 311–333. Mestre, L. 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Lees, Luciano Nicolas Naka, Alexandre Aleixo, Mario Cohn-Haft, Vítor de Q. Piacentini, Marcos Pérsio Dantas Santos and Luís Fábio Silveira Santos, M. P. D.; da Silva, G. K.; & dos Reis, A. L. 2011b. Birds of the Igarapé Lourdes Indigenous Territory, Jí-Paraná, Rondônia, Brazil. Revista Brasileira de Ornitologia, 19: 230–243. Santos, M. P. D.; Silveira, L. F., & da Silva, J.M.C. 2011c. Birds of Serra do Cachimbo, Pará State, Brazil. Revista Brasileira de Ornitologia, 19: 244–259. Schunck, F.; De Luca, A. C.; Piacentini, V. Q.; Rego, M. A.; Rennó B.; & Corrêa, A. H. 2011. Avifauna of two localities in the south of Amapá, Brazil, with comments on the distribution and taxonomy of some species. Revista Brasileira de Ornitologia, 19: 93–107. Silveira, L. F. & Horta, F. M. 2002. A avifauna da região de Vila Bela da Santíssima Trindade, Mato Grosso. Papéis Avulsos de Zoologia (São Paulo), 42: 265–286. Somenzari, M.; Silveira, L. F.; Piacentini, V. Q.; Rego, M. A.; Schunck, F.; & Cavarzere, V. 2011. Birds of an Amazonia-Cerrado ecotone in Southern Pará, Brazil, and the efficiency of associating multiple methods in avifaunal inventories. Revista Brasileira de Ornitologia, 19: 260–275. Vasconcelos, M. F.; Pacheco, J. F.; & Parrini, R. 2007. Levantamento preliminar e conservação da avifauna na zona urbana de Marabá, Pará, Brasil. Cotinga, 28: 45–51. Vasconcelos, M. F.; Dantas, S. M.; & Silva, J. M. C. 2011. Avifaunal inventory of the Amazonian savannas and adjacent habitats of the Monte Alegre region (Pará, Brazil), with comments on biogeography and conservation. Boletim do Museu Paraense Emílio Goeldi Ciências Naturais, 6: 119–145. Whittaker, A. 2009. Pousada Rio Roosevelt: a provisional avifaunal inventory in south-western Amazonian Brazil, with information on life history, new distributional data and comments on taxonomy. Cotinga, 31: 20–43. APPENDIX 2: Reserve management plans with bird lists subject to analysis. ESEC Rio Acre, FLONA de Carajás, FLONA de Crepori, FLONA do Amanã, FLONA do Jamanxim, FLONA do Purus, FLONA do Trairão, FLONA Macauã, FLONA Mapiá-Inauini, FLONA Tapajós, FLONA Tapirape-aquiri, PARNA Campos Amazônicos, PARNA da Serra da Cutia, PARNA da Serra do Divisor, PARNA de Anavilhanas, PARNA de Juruena, PARNA do Araguaia, PARNA do Cabo Orange, PARNA do Monte Roraima, PARNA Montanhas do Tumucumaque, PARNA Pacaás Novos, REBIO de Uatumã, REBIO do Gurupi, REBIO do Jaru, REBIO do Rio Trombetas, REBIO do Tapirapé, REBIO Guaporé, REBIO Nascentes da Serra do Cachimbo, RESEX Arapixi, RESEX Baixo Juruá, RESEX, Capanã Grande, RESEX do Cazumbá-Iracema, RESEX Rio Iriri, RESEX Riozinho do Anfrísio & RESEX Tapajós-Arapiuns. Revista Brasileira de Ornitologia, 22(2), 2014

Journal

Ornithology ResearchSpringer Journals

Published: Jun 1, 2014

Keywords: Amazonia; avian surveys; checklist; documentation; taxonomy; vouchers

References