Habitat use of Amazonian birds varies by age and foraging guild along a disturbance gradient.

Patterns of habitat use directly influence a species' fitness, yet for many species an individual's age can influence patterns of habitat use. However, in tropical rainforests, which host the greatest terrestrial species diversity, little is known about how age classes of different species use different adjacent habitats of varying quality. We use long-term mist net data from the Amazon rainforest to assess patterns of habitat use among adult, adolescent (teenage) and young understory birds in forest fragments, primary and secondary forest at the Biological Dynamics of Forest Fragments Project in Brazil. Insectivore adults were most common in primary forest, adolescents were equally likely in primary and secondary forest, and all ages were the least common in forest fragments. In contrast to insectivores, frugivores and omnivores showed no differences among all three habitat types. Our results illustrate potential ideal despotic distributions among breeding populations of some guilds of understory birds where adult insectivores may competitively exclude adolescent individuals from primary forest. Secondary forest recovery appears to hold promise as a breeding habitat for frugivore and omnivore species but only as a pre-breeding habitat for insectivores, but as the forest ages, the demographic structure of bird populations should match that of primary forest.

Long-term changes in avian biomass and functional diversity within disturbed and undisturbed Amazonian rainforest.

Recent long-term studies in protected areas have revealed the loss of biodiversity, yet the ramifications for ecosystem health and resilience remain unknown. Here, we investigate how the loss of understory birds, in the lowest stratum of the forest, affects avian biomass and functional diversity in the Amazon rainforest. Across approximately 30 years in the Biological Dynamics of Forest Fragments Project, we used a historical baseline of avian communities to contrast the avian communities in today's primary forest with those in modern disturbed habitat. We found that in primary rainforest, the reduced abundance of insectivorous species led to reduced functional diversity, but no reduction of biomass, indicating that species with similar functional traits are less likely to coexist in modern primary forests. Because today's forests contain fewer functionally redundant species-those with similar traits-we argue that avian communities in modern primary Amazonian rainforests are less resilient, which may ultimately disrupt the ecosystem in dynamic and unforeseen ways.

Light and thermal niches of ground-foraging Amazonian insectivorous birds.

Insectivores of the tropical rainforest floor are consistently among the most vulnerable birds to forest clearing and fragmentation. Several hypotheses attempt to explain this pattern, including sensitivity to extreme microclimates found near forest borders, particularly brighter and warmer conditions. Importantly, this "microclimate hypothesis" has additional implications for intact forest under global climate change that could be evaluated through direct assessment of the light and temperature environment of terrestrial insectivores. In this study, we harness novel technology to directly quantify the light and thermal niches of 10 species of terrestrial insectivores in undisturbed Amazonian rainforest. Loggers placed on birds (N = 33) and their environment (N = 9) recorded nearly continuous microclimate data from 2017 to 2019, amassing >5 million measurements. We found that midday light intensity in tree fall gaps (~39,000 lux) was >40 times higher than at the ground level of forest interior (950 lux). Light intensity registered by sensors placed on birds averaged 17.4 (range 3.9-41.5) lux, with species using only 4.3% (0.9%-10.4%) of available light on the forest floor. Birds therefore selected very dark microhabitats-the light environment was >2200 times brighter in tree fall gaps. Bird thermal niche was a function of ambient temperature as well as body temperature, which averaged >40.5°C but varied among species. Forest floor temperature peaked daily at 27.0°C, whereas bird loggers averaged 35.1°C (34.5-35.7°C) at midday. The antpitta Myrmothera campanisona and the antthrush Formicarius colma used thermal conditions closest to their body temperatures, whereas leaftossers (Sclerurus spp.) and Myrmornis torquata occupied relatively cool microclimates. We found no general link between abundance trends and variation in species-specific light and thermal niches. However, all species occupied markedly dim and cool microclimates. Because such conditions are rare outside the interior of primary forest, these results support the microclimate hypothesis in disturbed landscapes. Moreover, strong avoidance of conditions that are becoming more common under climate change highlights the vulnerability of terrestrial insectivores even in the absence of disturbance and may be the reason for enigmatic declines in Amazonia and elsewhere.

Morphological consequences of climate change for resident birds in intact Amazonian rainforest.

Warming from climate change is expected to reduce body size of endotherms, but studies from temperate systems have produced equivocal results. Over four decades, we collected morphometric data on a nonmigratory understory bird community within Amazonian primary rainforest that is experiencing increasingly extreme climate. All 77 species showed lower mean mass since the early 1980s­nearly half with 95% confidence. A third of species concomitantly increased wing length, driving a decrease in mass:wing ratio for 69% of species. Seasonal precipitation patterns were generally better than temperature at explaining morphological variation. Short-term climatic conditions affected all metrics, but time trends in wing and mass:wing remained robust even after controlling for annual seasonal conditions. We attribute these results to pressures to increase resource economy under warming. Both seasonal and long-term morphological shifts suggest response to climate change and highlight its pervasive consequences, even in the heart of the world's largest rainforest.

Nest survival of Seaside Sparrows (Ammospiza maritima) in the wake of the Deepwater Horizon oil spill.

In 2010, the Deepwater Horizon oil spill released an estimated 4.9 million barrels of oil into the Gulf of Mexico, damaging coastal ecosystems. Seaside Sparrows (Ammospiza maritima)-a year-round resident of Gulf Coast salt marshes-were exposed to oil, as shown by published isotopic and molecular analyses, but fitness consequences have not been clarified. We monitored nests around two bays in Plaquemines Parish, Louisiana, USA from 2012-2017 to assess possible impacts on the nesting biology of Seaside Sparrows. A majority of nests failed (76% of known-fate nests, N = 252 nests, 3521 exposure-days) during our study, and predation was the main cause of nest failure (~91% of failed nests). Logistic exposure analysis revealed that daily nest survival rate: (1) was greater at nests with denser vegetation at nest height, (2) was higher in the more sheltered bay we studied, (3) decreased over the course of the breeding season in each year, and (4) was not correlated with either sediment polycyclic aromatic hydrocarbon concentrations or estimated predator abundance during the years for which we had those data. Although the Deepwater Horizon spill impacted other aspects of Seaside Sparrow ecology, we found no definitive effect of initial oiling or oiled sediment on nest survival during 2012-2017. Because predation was the overwhelming cause of nest failure in our study, additional work on these communities is needed to fully understand demographic and ecological impacts of storms, oil spills, other pollutants, and sea-level rise on Seaside Sparrows and their predators.

Stable isotope analyses identify trophic niche partitioning between sympatric terrestrial vertebrates in coastal saltmarshes with differing oiling histories.

Bioindicator species are commonly used as proxies to help identify the ecological effects of oil spills and other stressors. However, the utility of taxa as bioindicators is dependent on understanding their trophic niche and life history characteristics, as these factors mediate their ecological responses. Seaside sparrows (Ammospiza maritima) and marsh rice rats (Oryzomys palustris) are two ubiquitous terrestrial vertebrates that are thought to be bioindicators of oil spills in saltmarsh ecosystems. To improve the utility of these omnivorous taxa as bioindicators, we used carbon and nitrogen stable isotope analysis to quantify their trophic niches at saltmarshes in coastal Louisiana with differing oiling histories. We found that rats generally had lower trophic positions and incorporated more aquatic prey relative to seaside sparrows. The range of resources used (i.e.,trophic niche width) varied based on oiling history. Seaside sparrows had wider trophic niches than marsh rice rats at unoiled sites, but not at oiled sites. Trophic niche widths of conspecifics were less consistent at oiled sites, although marsh rice rats at oiled sites had wider trophic niches than rats at unoiled sites. These results suggest that past oiling histories may have imparted subtle, yet differing effects on the foraging ecology of these two co-occurring species. However, the temporal lag between initial oiling and our study makes identifying the ultimate drivers of differences between oiled and unoiled sites challenging. Even so, our findings provide a baseline quantification of the trophic niches of sympatric seaside sparrows and marsh rice rats that will aid in the use of these species as indicators of oiling and other environmental stressors in saltmarsh ecosystems.

Seasonal dynamics of flock interaction networks across a human-modified landscape in lowland Amazonian rain forest.

Although lowland tropical rain forests were once widely believed to be the archetype of stability, seasonal variation exists. In these environments, seasonality is defined by rainfall, leading to a predictable pattern of biotic and abiotic changes. Only the full annual cycle reveals niche breadth, yet most studies of tropical organisms ignore seasonality, thereby underestimating realized conditions. If human-modified habitats display more seasonal stress than intact habitats, then ignoring seasonality will have particularly important repercussions for conservation. We examined the seasonal dynamics of Amazonian mixed-species flocks, an important species interaction network, across three habitats with increasing human disturbance. We quantified seasonal space use, species richness and attendance, and four ecological network metrics for flocks in primary forest, small forest fragments, and regenerating secondary forest in central Amazonia. Our results indicate that, even in intact, lowland rain forest, mixed-species flocks exhibit seasonal differences. During the dry season, flocks included more species, generally ranged over larger areas, and displayed network structures that were less complex and less cohesive. We speculate that-because most flocking species nest during the dry season, a time of reduced arthropod abundance-flocks are simultaneously constrained by these two competing pressures. Moreover, these seasonal differences were most pronounced in forest fragments and secondary forest, habitats that are less buffered from the changing seasons. Our results suggest that seasonality influences the conservation value of human-modified habitats, raising important questions about how rain forest organisms will cope with an increasingly unstable climate.

Long-term change in the avifauna of undisturbed Amazonian rainforest: ground-foraging birds disappear and the baseline shifts.

How are rainforest birds faring in the Anthropocene? We use bird captures spanning > 35 years from 55 sites within a vast area of intact Amazonian rainforest to reveal reduced abundance of terrestrial and near-ground insectivores in the absence of deforestation, edge effects or other direct anthropogenic landscape change. Because undisturbed forest includes far fewer terrestrial and near-ground insectivores than it did historically, today's fragments and second growth are more impoverished than shown by comparisons with modern 'control' sites. Any goals for bird community recovery in Amazonian second growth should recognise that a modern bird community will inevitably differ from a baseline from > 35 years ago. Abundance patterns driven by landscape change may be the most conspicuous manifestation of human activity, but biodiversity declines in undisturbed forest represent hidden losses, possibly driven by climate change, that may be pervasive in intact Amazonian forests and other systems considered to be undisturbed.

Avian ecological succession in the Amazon: A long-term case study following experimental deforestation.

Approximately 20% of the Brazilian Amazon has now been deforested, and the Amazon is currently experiencing the highest rates of deforestation in a decade, leading to large-scale land-use changes. Roads have consistently been implicated as drivers of ongoing Amazon deforestation and may act as corridors to facilitate species invasions. Long-term data, however, are necessary to determine how ecological succession alters avian communities following deforestation and whether established roads lead to a constant influx of new species.We used data across nearly 40 years from a large-scale deforestation experiment in the central Amazon to examine the avian colonization process in a spatial and temporal framework, considering the role that roads may play in facilitating colonization.Since 1979, 139 species that are not part of the original forest avifauna have been recorded, including more secondary forest species than expected based on the regional species pool. Among the 35 species considered to have colonized and become established, a disproportionate number were secondary forest birds (63%), almost all of which first appeared during the 1980s. These new residents comprise about 13% of the current community of permanent residents.Widespread generalists associated with secondary forest colonized quickly following deforestation, with few new species added after the first decade, despite a stable road connection. Few species associated with riverine forest or specialized habitats colonized, despite road connection to their preferred source habitat. Colonizing species remained restricted to anthropogenic habitats and did not infiltrate old-growth forests nor displace forest birds.Deforestation and expansion of road networks into terra firme rainforest will continue to create degraded anthropogenic habitat. Even so, the initial pulse of colonization by nonprimary forest bird species was not the beginning of a protracted series of invasions in this study, and the process appears to be reversible by forest succession.

Polycyclic aromatic hydrocarbon exposure in seaside sparrows (Ammodramus maritimus) following the 2010 Deepwater Horizon oil spill.

The seaside sparrow (Ammodramus maritimus) is an abundant and permanent resident of coastal salt marshes impacted by the 2010 BP Deepwater Horizon oil spill. Such terrestrial species are often overlooked in the aftermath of marine spills, despite the potential for long-term oil exposure. We sampled the livers of seaside sparrows residing in oiled and unoiled sites from 2011 to 2014 and quantified expression of cytochrome p450 1A (CYP1A), a gene involved in the metabolism of polycyclic aromatic hydrocarbons (PAHs). In August 2011, CYP1A expression was markedly higher in birds from an oiled site compared to an unoiled site, but differences had disappeared by June 2012. In June 2013, CYP1A expression was elevated compared to 2012 levels on all sites, including those collected from sites that had not been directly oiled during the spill. This rise in CYP1A expression was possibly due to Hurricane Isaac, which made landfall near our sites between the 2012 and 2013 sampling periods. CYP1A expression was significantly attenuated again in June 2014. We also collected sediment samples from the same marshes for a total concentration analysis of PAHs. The PAH concentrations in sediment samples exhibited a similar pattern to the CYP1A data, supporting the link between marsh PAHs and bird CYP1A expression. These results indicate that contamination from marine oil spills can immediately extend to terrestrial ecosystems, and that storms, weather, or other factors may influence subsequent spatial and temporal oil exposure for several additional years.

Population genetics of seaside Sparrow (Ammodramus maritimus) subspecies along the gulf of Mexico.

Seaside Sparrows (Ammodramus maritimus) along the Gulf of Mexico are currently recognized as four subspecies, including taxa in Florida (A. m. juncicola and A. m. peninsulae) and southern Texas (Ammodramus m. sennetti), plus a widespread taxon between them (A. m. fisheri). We examined population genetic structure of this "Gulf Coast" clade using microsatellite and mtDNA data. Results of Bayesian analyses (Structure, GeneLand) of microsatellite data from nine locations do not entirely align with current subspecific taxonomy. Ammodramus m. sennetti from southern Texas is significantly differentiated from all other populations, but we found evidence of an admixture zone with A. m. fisheri near Corpus Christi. The two subspecies along the northern Gulf Coast of Florida are significantly differentiated from both A. m. sennetti and A. m. fisheri, but are not distinct from each other. We found a weak signal of isolation by distance within A. m. fisheri, indicating this population is not entirely panmictic throughout its range. Although continued conservation concern is warranted for all populations along the Gulf Coast, A. m. fisheri appears to be more secure than the far smaller populations in south Texas and the northern Florida Gulf Coast. In particular, the most genetically distinct populations, those in Texas south of Corpus Christi, occupy unique habitats within a very small geographic range.

Decay of interspecific avian flock networks along a disturbance gradient in Amazonia.

Our understanding of how anthropogenic habitat change shapes species interactions is in its infancy. This is in large part because analytical approaches such as network theory have only recently been applied to characterize complex community dynamics. Network models are a powerful tool for quantifying how ecological interactions are affected by habitat modification because they provide metrics that quantify community structure and function. Here, we examine how large-scale habitat alteration has affected ecological interactions among mixed-species flocking birds in Amazonian rainforest. These flocks provide a model system for investigating how habitat heterogeneity influences non-trophic interactions and the subsequent social structure of forest-dependent mixed-species bird flocks. We analyse 21 flock interaction networks throughout a mosaic of primary forest, fragments of varying sizes and secondary forest (SF) at the Biological Dynamics of Forest Fragments Project in central Amazonian Brazil. Habitat type had a strong effect on network structure at the levels of both species and flock. Frequency of associations among species, as summarized by weighted degree, declined with increasing levels of forest fragmentation and SF. At the flock level, clustering coefficients and overall attendance positively correlated with mean vegetation height, indicating a strong effect of habitat structure on flock cohesion and stability. Prior research has shown that trophic interactions are often resilient to large-scale changes in habitat structure because species are ecologically redundant. By contrast, our results suggest that behavioural interactions and the structure of non-trophic networks are highly sensitive to environmental change. Thus, a more nuanced, system-by-system approach may be needed when thinking about the resiliency of ecological networks.

Step selection techniques uncover the environmental predictors of space use patterns in flocks of Amazonian birds.

Understanding the behavioral decisions behind animal movement and space use patterns is a key challenge for behavioral ecology. Tools to quantify these patterns from movement and animal-habitat interactions are vital for transforming ecology into a predictive science. This is particularly important in environments undergoing rapid anthropogenic changes, such as the Amazon rainforest, where animals face novel landscapes. Insectivorous bird flocks are key elements of avian biodiversity in the Amazonian ecosystem. Therefore, disentangling and quantifying the drivers behind their movement and space use patterns is of great importance for Amazonian conservation. We use a step selection function (SSF) approach to uncover environmental drivers behind movement choices. This is used to construct a mechanistic model, from which we derive predicted utilization distributions (home ranges) of flocks. We show that movement decisions are significantly influenced by canopy height and topography, but depletion and renewal of resources do not appear to affect movement significantly. We quantify the magnitude of these effects and demonstrate that they are helpful for understanding various heterogeneous aspects of space use. We compare our results to recent analytic derivations of space use, demonstrating that the analytic approximation is only accurate when assuming that there is no persistence in the animals' movement. Our model can be translated into other environments or hypothetical scenarios, such as those given by proposed future anthropogenic actions, to make predictions of spatial patterns in bird flocks. Furthermore, our approach is quite general, so could potentially be used to understand the drivers of movement and spatial patterns for a wide variety of animal communities.

Understory bird communities in Amazonian rainforest fragments: species turnover through 25 years post-isolation in recovering landscapes.

Inferences about species loss following habitat conversion are typically drawn from short-term surveys, which cannot reconstruct long-term temporal dynamics of extinction and colonization. A long-term view can be critical, however, to determine the stability of communities within fragments. Likewise, landscape dynamics must be considered, as second growth structure and overall forest cover contribute to processes in fragments. Here we examine bird communities in 11 Amazonian rainforest fragments of 1-100 ha, beginning before the fragments were isolated in the 1980s, and continuing through 2007. Using a method that accounts for imperfect detection, we estimated extinction and colonization based on standardized mist-net surveys within discreet time intervals (1-2 preisolation samples and 4-5 post-isolation samples). Between preisolation and 2007, all fragments lost species in an area-dependent fashion, with loss of as few as <10% of preisolation species from 100-ha fragments, but up to 70% in 1-ha fragments. Analysis of individual time intervals revealed that the 2007 result was not due to gradual species loss beginning at isolation; both extinction and colonization occurred in every time interval. In the last two samples, 2000 and 2007, extinction and colonization were approximately balanced. Further, 97 of 101 species netted before isolation were detected in at least one fragment in 2007. Although a small subset of species is extremely vulnerable to fragmentation, and predictably goes extinct in fragments, developing second growth in the matrix around fragments encourages recolonization in our landscapes. Species richness in these fragments now reflects local turnover, not long-term attrition of species. We expect that similar processes could be operating in other fragmented systems that show unexpectedly low extinction.

A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds.

As compared with extensive contiguous areas, small isolated habitat patches lack many species. Some species disappear after isolation; others are rarely found in any small patch, regardless of isolation. We used a 13-year data set of bird captures from a large landscape-manipulation experiment in a Brazilian Amazon forest to model the extinction-colonization dynamics of 55 species and tested basic predictions of island biogeography and metapopulation theory. From our models, we derived two metrics of species vulnerability to changes in isolation and patch area. We found a strong effect of area and a variable effect of isolation on the predicted patch occupancy by birds.

Long-term landscape change and bird abundance in Amazonian rainforest fragments.

The rainforests of the Amazon basin are being cut by humans at a rate >20,000 km2/year leading to smaller and more isolated patches of forest, with remaining fragments often in the range of 1-100 ha. We analyzed samples of understory birds collected over 20 years from a standardized mist-netting program in 1- to 100-ha rainforest fragments in a dynamic Amazonian landscape near Manaus, Brazil. Across bird guilds, the condition of second growth immediately surrounding fragments was often as important as fragment size or local forest cover in explaining variation in abundance. Some fragments surrounded by 100 m of open pasture showed reductions in insectivorous bird abundance of over 95%, even in landscapes dominated by continuous forest and old second growth. These extreme reductions may be typical throughout Amazonia in small (< or =10 ha), isolated fragments of rainforest. Abundance for some guilds returned to preisolation levels in 10- and 100-ha fragments connected to continuous forest by 20-year-old second growth. Our results show that the consequences of Amazonian forest loss cannot be accurately described without explicit consideration of vegetation dynamics in matrix habitat. Any dichotomous classification of the landscape into 'forest" and "nonforest" misses essential information about the matrix.

Rates of species loss from Amazonian forest fragments.

In the face of worldwide habitat fragmentation, managers need to devise a time frame for action. We ask how fast do understory bird species disappear from experimentally isolated plots in the Biological Dynamics of Forest Fragments Project, central Amazon, Brazil. Our data consist of mist-net records obtained over a period of 13 years in 11 sites of 1, 10, and 100 hectares. The numbers of captures per species per unit time, analyzed under different simplifying assumptions, reveal a set of species-loss curves. From those declining numbers, we derive a scaling rule for the time it takes to lose half the species in a fragment as a function of its area. A 10-fold decrease in the rate of species loss requires a 1,000-fold increase in area. Fragments of 100 hectares lose one half of their species in <15 years, too short a time for implementing conservation measures.

Effects of Forest Fragmentation on Understory Hummingbirds in Amazonian Brazil.

We sampled understory bummingbirds in Amazonian forest fragments from before isolation through nine years after isolation. We recorded 377 captures of eight species in five 1-ba fragments and four 10-ha fragments. The three species netted before isolation, Phaethornis superciliosus, Phaethornis bourcieri, and Thalurania furcata, were nearly equally abundant at that time. After isolation abundance of P. bourcieri and T. furcata did not change, but P. superciliosus became nearly twice as common. Five additional species that were netted only after isolation represented about 10% of the post-isolation sample. The species recorded only after isolation were forest species usually found above the levels of nets; fragments were not colonized by nonforest species. Use of fragments did not differ between 1-and 10-ba fragments. The landscape surrounding the fragments included active cattle pasture, abandoned pasture, and Cecropia-dominated second growth, but this variation bad little effect on use of fragments by hummingbirds. The results suggest that these understory hummingbirds can persist in a matrix of fragments, secondary growth, and large forest patches. This response is much different than that of the insectivorous birds that dominate the understory bird community at the site, which are much more vulnerable to fragmentation. Efectos de la fragmentación del bosque sobre los colibrís de sotobosque en la Amazonia Brasileña.

Resumen: Nosotros hemos tomado muestras de colibrís de sotobosque en fragmentos forestales Amazónicos desde antes del aislamiento a través de nueve años después del aislamiento. Registramos 377 capturas de ocho especies en cinco fragmentos de 1-ha, y cuatro fragmentos de 10-ha. Las tres especies capturadas antes del aislamiento, Phaethornis superciliosus, Phaethornis bourcieri, y Thalurania furcata, presentaron casi la misma abundancia en esa época. Después del aislamiento, la abundancia de Phaethornis bourcieri y Thalurania furcata no cambió, pero Phaethornis superciliosus se hizo dos veces más común. Cinco especies más que fueron capturadas solamente después del aislamiento representaron aproximadamente el 10% de la muestra de post aislamiento. Las especies capturadas solamente después del aislamiento eran especies del bosque, las que generalmente se encuentran encima del nivel de las redes; los fragmentos no fueron colonizados por especies no-florestales. La utilización de fragmentos no se diferenció entre los fragmentos de 1- y 10-ha. El paisaje alrededor de los fragmentos incluía pasto activo de ganado vacuno, pasto abandonado, y crecimiento secundario dominado por Cecropia, pero esta variación no afectó mucho la utilización de fragmentos por colibrís. Estos resultados sugieren que estas especies de colibrís de sotobosque pueden persistir en una matriz de fragmentos, crecimiento secundario, y parches de bosque de gran tamaño. Esta reacción es muy diferente a la de los pájaros insectívoros que dominan la comunidad de pájaros del sotohosque en nuestro sitio, los cuales son mucho más vulnerables a la fragmentación.