Integrative species delimitation uncovers hidden diversity within the Pithecopus hypochondrialis species complex (Hylidae, Phyllomedusinae) and its phylogeography reveals Plio-Pleistocene connectivity among Neotropical savannas.

Despite their limited vagility and pronounced habitat heterogeneity in the tropics, many anuran species have unexpectedly extensive geographic ranges. One prominent example of this phenomenon is Pithecopus hypochondrialis, which is found in the Cerrado, Guianan savanna, and Llanos domains, as well as isolated tracts of savanna and open habitat within the Amazon Forest. The present study employs an integrative species delimitation approach to test the hypothesis that P. hypochondrialis is in fact a species complex. We also reconstruct the relationships among the lineages delimited here and other Pithecopus species. In this study, we employ Ecological Niche Modelling (ENM) and spatiotemporal phylogeographic reconstruction approaches to evaluate a multitude of scenarios of connectivity across the Neotropical savannas. We identified three divergent lineages, two of which have been described previously. The lineages were allocated to a lowland Pithecopus clade, although the relationships among these lineages are weakly supported. Both the ENM and the phylogeographic reconstruction highlight the occurrence of periods of connectivity among the Neotropical savannas over the course of the Pliocene and Pleistocene epochs. These processes extended from eastern Amazonia to the northern coast of Brazil. The findings of the present study highlight the presence of hidden diversity within P. hypochondrialis, and reinforce the need for a comprehensive taxonomic review. These findings also indicate intricate and highly dynamic patterns of connectivity across the Neotropical savannas that date back to the Pliocene.

Prevalence and genetic diversity of avian haemosporidian parasites in islands within a mega hydroelectric dam in the Brazilian Amazon.

The Brazilian Amazon supports an extremely diverse avifauna and serves as the diversification center for avian malaria parasites in South America. Construction of hydroelectric dams can drive biodiversity loss by creating islands incapable of sustaining the bird communities found in intact forest sites. Besides anthropogenic actions, the presence of parasites can also influence the dynamics and structure of bird communities. Avian malaria (Plasmodium) and related haemosporidian parasites (Haemoproteus and Leucocytozoon) are a globally distributed group of protozoan parasites recovered from all major bird groups. However, no study to date has analyzed the presence of avian haemosporidian parasites in fragmented areas such as land bridge islands formed during artificial flooding following the construction of hydroelectric dams. The aim of this study is to assess the prevalence and molecular diversity of haemosporidians in bird communities inhabiting artificial islands in the area of the Balbina Hydroelectric Dam. The reservoir area covers 443,700 ha with 3546 islands on the left bank of the Uatumã River known to contain more than 400 bird species. We surveyed haemosporidian infections in blood samples collected from 445 understory birds, belonging to 53 species, 24 families, and 8 orders. Passeriformes represented 95.5% of all analyzed samples. We found a low overall Plasmodium prevalence (2.9%), with 13 positive samples (two Plasmodium elongatum and 11 Plasmodium sp.) belonging to eight lineages. Six of these lineages were previously recorded in the Amazon, whereas two of them are new. Hypocnemis cantator, the Guianan Warbling Antbird, represented 38.5% of all infected individuals, even though it represents only 5.6% of the sampled individuals. Since comparison with Plasmodium prevalence data prior to construction of Balbina is not possible, other studies in artificially flooded areas are imperative to test if anthropogenic flooding may disrupt vector-parasite relationships leading to low Plasmodium prevalence.

Dancing drives evolution of sexual size dimorphism in manakins.

Body size mediates life history, physiology and inter- and intra-specific interactions. Within species, sexes frequently differ in size, reflecting divergent selective pressures and/or constraints. Both sexual selection and differences in environmentally mediated reproductive constraints can drive sexual size dimorphism, but empirically testing causes of dimorphism is challenging. Manakins (Pipridae), a family of Neotropical birds comprising approximately 50 species, exhibit a broad range of size dimorphism from male- to female-biased and are distributed across gradients of precipitation and elevation. Males perform courtship displays ranging from simple hops to complex aerobatic manoeuvres. We tested associations between sexual size dimorphism and (a) agility and (b) environment, analysing morphological, behavioural and environmental data for 22 manakin species in a phylogenetic framework. Sexual dimorphism in mass was most strongly related to agility, with males being lighter than females in species performing more aerial display behaviours. However, wing and tarsus length dimorphism were more strongly associated with environmental variables, suggesting that different sources of selection act on different aspects of body size. These results highlight the strength of sexual selection in shaping morphology-even atypical patterns of dimorphism-while demonstrating the importance of constraints and ecological consequences of body size evolution.

Phenotypic variation in a neotropical understory bird driven by environmental change in an urbanizing Amazonian landscape.

Environmental change through habitat fragmentation and urbanization drives biodiversity loss in the Neotropics at an alarming rate. Some individuals and species confined to habitat fragments may develop phenotypic adjustments that allow populations to persist, even in landscapes made harsh by human activities. Behavioral and morphological adjustments may enhance a population's ability to cope with anthropogenic hazards. We examined potential differences in the behavioral and morphological phenotype of populations of the neotropical Wedge-billed Woodcreeper (Glyphorynchus spirurus)-an understory forest specialist insectivorous bird-between populations from urban fragmented forests and continuous preserved forests. We evaluated exploratory behavior and morphological traits using generalized linear models and linear discriminant analysis to quantify phenotypical differences among populations. We used failure time analysis to compare latency to explore and move during exploration in a Novel Environment Test (NET). Our analyses detected differences in certain movement behaviors (latencies to move during NET), indicating that individuals from fragmented forests are slow explorers in relation to individuals from the continuous forest. We also found shorter tarsi and tails in the fragmented forest population which were attributed to an overall reduction in body size in these populations. Our results suggest that environmental change driven by fragmentation in an urban landscape is causing population differentiation, but we cannot ascribe observed variations to evolutionary processes only, as the differences observed may be explained by other processes too. However, we suggest that phenotypic differences may be aiding this small understory forest specialist to persist in an urban fragmented landscape.

Constraint and Function in the Predefinitive Plumages of Manakins (Aves: Pipridae).

Birds with delayed plumage maturation exhibit a drab predefinitive plumage, often despite gonad maturation, before developing the definitive plumage associated with increased reproductive success. Manakins are a diverse clade of neotropical lekking birds with extreme sexual dichromatism, radical sexual displays, and a unique diversity in the predefinitive plumages of males across species. Here, we provide the first full review of the natural history of manakin predefinitive plumages as the basis for qualitatively addressing the six major hypotheses about the production and function of predefinitive plumages. We find little evidence to support the possibilities that manakin predefinitive plumages are directly constrained by inflexible molt schedules, resource limitations to definitive coloration, or hormonal ties to reproductive behaviors. There is little evidence that could support a crypsis function, although direct experimentation is needed, and mimicry is refuted except for one unusual species in which predefinitive males sire young. Instead, evidence from a handful of well-studied species suggests that predefinitive plumages help young males explicitly signal their social status, and thereby gain entry to the social hierarchies which dictate future reproductive success. Our conclusions are especially influenced by the unique fact that males of at least 11 species throughout the family exhibit multiple predefinitive plumage stages with distinctively male patches. For each hypothesis, we highlight ways in which a better knowledge of female and young male birds offers critical opportunities for the use of manakins as a model clade.

Phylogenomics of manakins (Aves: Pipridae) using alternative locus filtering strategies based on informativeness.

Target capture sequencing effectively generates molecular marker arrays useful for molecular systematics. These extensive data sets are advantageous where previous studies using a few loci have failed to resolve relationships confidently. Moreover, target capture is well-suited to fragmented source DNA, allowing data collection from species that lack fresh tissues. Herein we use target capture to generate data for a phylogeny of the avian family Pipridae (manakins), a group that has been the subject of many behavioral and ecological studies. Most manakin species feature lek mating systems, where males exhibit complex behavioral displays including mechanical and vocal sounds, coordinated movements of multiple males, and high speed movements. We analyzed thousands of ultraconserved element (UCE) loci along with a smaller number of coding exons and their flanking regions from all but one species of Pipridae. We examined three different methods of phylogenetic estimation (concatenation and two multispecies coalescent methods). Phylogenetic inferences using UCE data yielded strongly supported estimates of phylogeny regardless of analytical method. Exon probes had limited capability to capture sequence data and resulted in phylogeny estimates with reduced support and modest topological differences relative to the UCE trees, although these conflicts had limited support. Two genera were paraphyletic among all analyses and data sets, with Antilophia nested within Chiroxiphia and Tyranneutes nested within Neopelma. The Chiroxiphia-Antilophia clade was an exception to the generally high support we observed; the topology of this clade differed among analyses, even those based on UCE data. To further explore relationships within this group, we employed two filtering strategies to remove low-information loci. Those analyses resulted in distinct topologies, suggesting that the relationships we identified within Chiroxiphia-Antilophia should be interpreted with caution. Despite the existence of a few continuing uncertainties, our analyses resulted in a robust phylogenetic hypothesis of the family Pipridae that provides a comparative framework for future ecomorphological and behavioral studies.

An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds.

Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector-transmitted parasites. Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity of Leucocytozoon (an avian blood parasite) at site and species levels across the New World. To explore spatial patterns in infection probability and lineage diversity for Leucocytozoon parasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high-resolution satellite remote-sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly. Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence of Leucocytozoon parasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected with Leucocytozoon increased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes. Whereas temperature partially constrains Leucocytozoon diversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, for Leucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector-transmitted parasites. Unlike other vector-transmitted diseases, our results show that Leucocytozoon diversity and prevalence will likely decrease with warming temperatures.

Host associations and turnover of haemosporidian parasites in manakins (Aves: Pipridae).

Parasites of the genera Plasmodium and Haemoproteus (Apicomplexa: Haemosporida) are a diverse group of pathogens that infect birds nearly worldwide. Despite their ubiquity, the ecological and evolutionary factors that shape the diversity and distribution of these protozoan parasites among avian communities and geographic regions are poorly understood. Based on a survey throughout the Neotropics of the haemosporidian parasites infecting manakins (Pipridae), a family of Passerine birds endemic to this region, we asked whether host relatedness, ecological similarity and geographic proximity structure parasite turnover between manakin species and local manakin assemblages. We used molecular methods to screen 1343 individuals of 30 manakin species for the presence of parasites. We found no significant correlations between manakin parasite lineage turnover and both manakin species turnover and geographic distance. Climate differences, species turnover in the larger bird community and parasite lineage turnover in non-manakin hosts did not correlate with manakin parasite lineage turnover. We also found no evidence that manakin parasite lineage turnover among host species correlates with range overlap and genetic divergence among hosts. Our analyses indicate that host switching (turnover among host species) and dispersal (turnover among locations) of haemosporidian parasites in manakins are not constrained at this scale.

Uso de florestas secundárias por aves de sub-bosque em uma paisagem fragmentada na Amazônia central / Use of secondary forests by understory birds in a fragmented landscape in central Amazonia

Na Amazônia, as taxas de desmatamento crescem desde 1991 e as previsões não são otimistas quanto à desaceleração desse processo. A devastação da floresta é acompanhada de uma expansão de florestas secundárias (FS) que se estabelecem nas áreas abandonadas. A tendência é um aumento de florestas secundárias, resultando num mosaico de floresta contínua e fragmentos separados por uma matriz de FS. Nesse cenário, autores acreditam que a Amazônia pode passar por um processo massivo de extinção de espécies. Por outro lado, a previsão de um processo massivo de extinção pode ser equivocada, pois muitas espécies florestais poderiam sobreviver nas florestas secundárias. Para avaliar o valor das florestas secundárias para espécies florestais amostramos por oito meses com redes de neblina uma capoeira (FS) em regeneração e uma floresta primária (FP) de uma paisagem fragmentada. Algumas espécies não foram capturadas na capoeira e aparentemente evitam esse tipo de hábitat. No entanto, a maioria das espécies do grupo focal não apresentou diferença na sobrevivência aparente entre os ambientes, o que nos indica que estão habitando a capoeira e a floresta primária da mesma forma. Na realidade amazônica, onde grande parte da matriz é composta por floresta secundária, a matriz tem valor para conservação e deve ser analisada como um elemento dinâmico que não apenas permite a movimentação de indivíduos, mas também serve de hábitat para muitas espécies de floresta primária. Mas ressaltamos que é fundamental a preservação de áreas de floresta primária que servirão de fonte às florestas secundárias adjacentes.

Rates of deforestation in the Brazilian Amazon have increased since 1991 and forecasts are not optimistic about the slowing of this process. Some authors believe that the Amazon may be experiencing a massive process of species extinction. However, the deforestation is accompanied by the expansion of secondary forests that are established in the abandoned areas. The trend is an increase in secondary forests cover, resulting in a mosaic of primary forest (FP) and fragments separated by an array of secondary forests (FS). In this scenario, the prediction of a massive extinction could be wrong if many species could survive in the secondary forests. To assess the importance of FS for the understory birds we sampled areas in regeneration and a continuous forest of a fragmented landscape. We conducted mist netting (24 nets/day) for six consecutive days/month, for 8 months (May-November) in 2009. Some forest species as do not seem to be adapted to the secondary forest environment and their occurrences are restricted to continuous forest environments. But most focal species showed no significant difference in apparent survival rates between the enviroments, suggesting that these species inhabit the secondary forest and the primary forest similarly. Because most of the matrix in fragmented landscapes are composed by secondary forests, such results highlights the conservation value that these habitats present in the long term. Thus, FS should be regarded as dynamic matrix that not only allows the movement of individuals but also function as habitat for many species typical of FP.

Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape.

Seed dispersal is a crucial component of plant population dynamics. Human landscape modifications, such as habitat destruction and fragmentation, can alter the abundance of fruiting plants and animal dispersers, foraging rates, vector movement, and the composition of the disperser community, all of which can singly or in concert affect seed dispersal. Here, we quantify and tease apart the effects of landscape configuration, namely, fragmentation of primary forest and the composition of the surrounding forest matrix, on individual components of seed dispersal of Heliconia acuminata, an Amazonian understory herb. First we identified the effects of landscape configuration on the abundance of fruiting plants and six bird disperser species. Although highly variable in space and time, densities of fruiting plants were similar in continuous forest and fragments. However, the two largest-bodied avian dispersers were less common or absent in small fragments. Second, we determined whether fragmentation affected foraging rates. Fruit removal rates were similar and very high across the landscape, suggesting that Heliconia fruits are a key resource for small frugivores in this landscape. Third, we used radiotelemetry and statistical models to quantify how landscape configuration influences vector movement patterns. Bird dispersers flew farther and faster, and perched longer in primary relative to secondary forests. One species also altered its movement direction in response to habitat boundaries between primary and secondary forests. Finally, we parameterized a simulation model linking data on fruit density and disperser abundance and behavior with empirical estimates of seed retention times to generate seed dispersal patterns in two hypothetical landscapes. Despite clear changes in bird movement in response to landscape configuration, our simulations demonstrate that these differences had negligible effects on dispersal distances. However, small fragments had reduced densities of Turdus albicollis, the largest-bodied disperser and the only one to both regurgitate and defecate seeds. This change in Turdus abundance acted together with lower numbers of fruiting plants in small fragments to decrease the probability of long-distance dispersal events from small patches. These findings emphasize the importance of foraging style for seed dispersal and highlight the primacy of habitat size relative to spatial configuration in preserving biotic interactions.

Effects of forest fragmentation on the seedling recruitment of a tropical herb: assessing seed vs. safe-site limitation.

Studies simultaneously evaluating the importance of safe-site and seed limitation for plant establishment are rare, particularly in human-modified landscapes. We used spatially explicit neighborhood models together with data from 10 0.5-ha mapped census plots in a fragmented landscape spanning 1000 km2 to (1) evaluate the relative importance of seed production, dispersal, and safe-site limitation for the recruitment of the understory herb Heliconia acuminata; and (2) determine how these processes differ between fragments and continuous forests. Our analyses demonstrated a large degree of variation in seed production, dispersal, and establishment among and within the 10 study plots. Seed production limitation was strong but only at small spatial scales. Average dispersal distance was less than 4 m, leading to severe dispersal limitation at most sites. Overall, safe-site limitation was the most important constraint on seedling establishment. Fragmentation led to a more heterogeneous light environment with negative consequences for seedling establishment but had little effect on seed production or dispersal. These results suggest that the effects of fragmentation on abiotic processes may be more important than the disruption of biotic interactions in driving biodiversity loss in tropical forests, at least for some functional groups. These effects may be common when the matrix surrounding fragments contains enough tree cover to enable movement of dispersers and pollinators.

Plumage carotenoids of the Pin-tailed Manakin (Ilicura militaris): evidence for the endogenous production of rhodoxanthin from a colour variant.

The Pin-tailed Manakin (Ilicura militaris) is a small, sexually dimorphic, frugivorous suboscine songbird (Pipridae; Passeriformes; Aves) endemic to the Atlantic Forest of Brazil. A variant individual of this species was recently described in which the red patches that characterise the male's Definitive plumage were replaced by orange-yellow ones. We show here that the pigments in the feathers of the colour variant are common dietary carotenoids (zeaxanthin, beta-cryptoxanthin), not carotenoids synthesised by birds, lending support to the suggestion that the individual is a colour mutant lacking the capability to transform yellow dietary pigments into the red pigments normally present in these feathers. By comparison, the yellow crown feathers of a close relative, the Golden-winged Manakin (Masius chrysopterus), contained predominantly endogenously produced epsilon-caroten-3'-ones. Surprisingly, the normal-coloured feathers of the male Pin-tailed Manakin owe their red hue to rhodoxanthin, an unusual carotenoid more commonly found in plants, rather than 4-keto-carotenoids typically found in red plumages and found lacking in previously characterised bird colour variants. The implication is that birds, like the tilapia fish, may be able to synthesise this unusual pigment endogenously from dietary precursors. A newly described carotenoid, 6-hydroxy-epsilon,epsilon-carotene-3,3'-dione, here named piprixanthin, present in the red feathers of the Pin-tailed Manakin, provides a plausible intermediate between epsilon,epsilon-carotene-3,3'-dione (canary-xanthophyll B), a bright yellow pigment found in this and other songbirds, and rhodoxanthin. It is apparent that pigeons (Columbidae, Columbiformes) also have the capability to produce rhodoxanthin, and a structurally related pigment, endogenously. The ability to synthesise rhodoxanthin might have arisen at least twice in birds.