Taxonomic, phylogenetic and functional diversity of an urban Amazonian avifauna

The city of Belém is located in Pará state in north-east Brazil (approximately 1°S, 48°′W) and is the second largest in the Brazilian Amazon with a population of approximately 1.5 million people at a density of 1351.8 people/km² (IBGE - Instituto Brasileiro de Geografia e Estatística 2016). The city lies in the 243,000 km² Belém Center of Endemism (BCE) which has been subject to the highest proportion of forest loss of any Amazonian interfluvial region and retains less than 24% of its original primary forest cover (Almeida and Vieira 2010). Founded on 12 January 1616 the city replaced the natural climax vegetation of dense ombrophilous terra firma and várzea (seasonally flooded) forests. The climate is hot and humid with annual precipitation of 2834 mm.

We sampled a 5 km transect (Fig. S1) in the SW of the city that traversers representative sections of habitats in a district of the city with only 4.3% vegetative cover (Luz and Rodrigues 2014). The route passes both high and low rent housing areas along the Rua dos Mundurucus, a 5.2 ha urban park (the Praça Batista Campos), a stretch of the Rio Guamá along a recently gentrified promenade (Portal da Amazonia) backed by derelict ‘waste ground’ and finishes outside the Mangal das Garças park. The first half of the transect includes 1 km of tree-lined section (mostly Mangifera indica) in a more affluent suburb, whilst the Praça Batista Campos has a more diverse tree community also including Ceiba pentandra, Euterpe oleracea, Minquartia guianensis, Caesalpinia echinata and Platonia insignis. The poorer suburbs have very little tree cover, whilst the abandoned area by the Portal da Amazonia is mostly grassland with some encroaching scrub. The foreshore in front of the promenade is mudflats exposed at high tide and backed by short grassland, with some tall monodominant stands of Montrichardia linifera towards the Mangal das Garças.

We sampled birds along this 5 km transect from August 2014 to July 2015, surveys were undertaken from dawn (between 0535 and 0600) and lasted two hours. This transect was travelled 54 times, between one and eight times per month dependent on meteorological conditions, totalling 270 km. We recorded all species seen and heard along this route, obtaining voucher images of any unusual taxa, which, along with the raw data were deposited online at www.​ebird.​org. We paid special attention for any signs of breeding behaviour and used the eBird breeding codes (Supporting Information Table S1) to define the likelihood of breeding, scoring evidence as confirmed, probable and possible.

Bird species were classified to trophic guild based on (Wilman et al. 2014), we divided the community into the broad categories ‘plant/seed eaters’, ‘insectivores’, ‘omnivores’, ‘frugivores/nectarivores’, and ‘vertebrate/fish/scavenger’ feeders. Data on body mass was also extracted from Wilman et al. (2014) or genus level averages where no data was available (n = 2). We assigned species native or non-native status based on Novaes and Lima (1998). Migratory status was extracted from the Birdlife Datazone database http://​www.​birdlife.​org/​datazone/​index.​html and Parker et al. (1996). We assigned species to the categories ‘resident’ for species which remain in the Belém area throughout the year; ‘Boreal migrant’ for Nearctic-Neotropical migrants breeding in North America and migrating south to the Neotropics; ‘Austral migrant/partial austral migrant’ for species for which part or all of their population migrate north from breeding areas in southern South America to winter in Amazonia and ‘Intratropical migrant’ for species which undertake seasonal movements within Amazonia (categories sensu Faaborg et al. 2010 based on classifications from the Birdlife Datazone). We used the Parker et al. (1996) database to look at habitat affinities of the community, where species may have more than one occupied habitat type. We also used the Birdlife Datazone database to classify the threat status of species on the IUCN Global Red List.

We extracted phylogenetic trees from a global avian phylogeny (Jetz et al. 2012) based on the Hackett backbone (Hackett et al. 2008) using 500 phylogenies. The resulting phylogram was visualized and edited using the FigTree v 1.4.1 software (http://​tree.​bio.​ed.​ac.​uk/​software/​figtree/​). We calculated six measures of phylogenetic diversity monthly: phylogenetic diversity (PD), sesPD (the standard effect size (SES) of PD), MPD (mean pairwise distance), sesSMPD (adjusted for species richness, MNTD (mean nearest taxon distance), sesMNTD (MNTD adjusted for species richness). We performed these metrics using the ‘picante’ (Kembel et al. 2010). To check if there was difference among months we performed the ANOVA function and type III sums of squares in the ‘car’ package in R version 3.2.3 (R Core Development Team 2014).

We recorded 99 bird species during our survey (Fig. 1), of which five were non-native: Feral Pigeon (Columba livia var. domestica), Jandaya Parakeet (Aratinga jandaya), Common Waxbill (Estrilda astrild), House Sparrow (Passer domesticus) and Campo Troupial (Icterus jamacaii). Although representing only 5.1% of the total species richness, exotics accounted for 19.0% of total bird abundance and included 100% of the regional species pool of exotic species (Table 1). Species abundance and biomass was heavily skewed to a few numerically dominant species (Table 1, Fig. 1a, Supporting Information Table S2). The most frequently recorded of which was Black Vulture (Coragyps atratus) with 1732 individuals counted. There were more records of the most abundant eight species combined than all remaining 91 species; fewer than five individuals were recorded of 28 of these species.

Breeding evidence was ‘confirmed’ for 31 species, ‘probable’ for 20 species and ‘possible’ for 13, there was no evidence for breeding activity for the remaining 35 species (Supporting Information Table S3). Most of the species recorded were resident (66), of the remainder, nine were Boreal migrants from North America, 12 were austral/partial austral migrants and 12 intratropical migrants (Fig. 2b). However migrant species were over-represented in the totals in comparison with the total regional species pool (Table 1). Among the guilds, insectivores dominated the community with 53 species (53.3% of the total), although this included a long-tail of rarely-recorded species, a distribution not reflected in the remaining guilds. Omnivores (17 species) were the next commonest guild followed by vertebrate/fish/scavenger feeders (16), fruit/nectar feeders (10) and plant/seed eaters (7). However, as a function of the regional species pool, insectivores were in fact under-represented in comparison to omnivores, which were represented by proportionately more species Table 1). The guild of vertebrate, scavenger and piscivorous feeders dominated by weight, accounting for 40.4% of total avian biomass. All species were globally ‘Least Concern’ with the exception of the Near-Threatened Semipalmated Sandpiper (Calidris pusilla).

The taxonomic diversity of birds in our study region varied throughout the annual cycle, driven by the arrival and departure of different cohorts of migrating birds. Species richness was highest in January–April when Boreal migrants were present alongside intratropical migrants. Taxonomic diversity subsequently decreased with the departure of these species, a change which was not offset by the arrival of smaller numbers of Austral migrants and partial Austral migrants. This difference in taxonomic diversity over the annual cycle was mirrored and accentuated in terms of phylogenetic diversity given the higher phylogenetic diversity of many of the migrant taxa resulting in higher values of mean pairwise differences (Fig. 2, S2, S3). The temporal trend in mean pairwise distance also mirrored the pattern of PD with significant differences between the Boreal ‘summer’ and ‘winter periods. This loss of large phylogenetically divergent waterbirds distributed across a wide range of clades, was not temporary compensated for by the gain in Austral and partial migrants which were phylogenetically clustered. These changes resulted in changes in trophic structure through the annual cycle (Fig. 3) as fewer piscivores and more insectivores were present during the austral winter. We did not however find significant differences in the mean nearest taxon distance throughout the annual cycle (Fig. S2, S3) suggesting that despite migration there is still relative phylogenetic evenness.

Comparison of habitat affinities with the Parker et al. classifications show that the community is most similar to that occupying other ‘secondary’ habitats with 44.4% of species occurring in secondary forest, 37.3% in ‘second growth scrub’ and 19.1% in pastures/agricultural lands (Table 2). The strongest affiliation for a ‘primary habitat’ was ‘river edge forest’ which was occupied by 24% of species, followed by freshwater marshes (19.1%) and ‘riparian thickets’ (10.1%). Only 9.1% of species were typically found in ‘tropical lowland evergreen forest’ which is the region’s dominant natural climax habitat.