Long-term monitoring reveals widespread and severe declines of understory birds in a protected Neotropical forest.

Long-term studies on the population dynamics of tropical resident birds are few, and it remains poorly understood how their populations have fared in recent decades. Here, we analyzed a 44-y population study of a Neotropical understory bird assemblage from a protected forest reserve in central Panama to determine if and how populations have changed from 1977 to 2020. Using the number of birds captured in mist nets as an index of local abundance, we estimated trends over time for a diverse suite of 57 resident species that comprised a broad range of ecological and behavioral traits. Estimated abundances of 40 (∼70%) species declined over the sampling period, whereas only 2 increased. Furthermore, declines were severe: 35 of the 40 declining species exhibited large proportional losses in estimated abundance, amounting to ≥50% of their initial estimated abundances. Declines were largely independent of ecology (i.e., body mass, foraging guild, or initial abundance) or phylogenetic affiliation. These widespread, severe declines are particularly alarming, given that they occurred in a relatively large (∼22,000-ha) forested area in the absence of local fragmentation or recent land-use change. Our findings provide robust evidence of tropical bird declines in intact forests and bolster a large body of literature from temperate regions suggesting that bird populations may be declining at a global scale. Identifying the ecological mechanisms underlying these declines should be an urgent conservation priority.

Pre-Columbian transregional captive rearing of Amazonian parrots in the Atacama Desert.

The feathers of tropical birds were one of the most significant symbols of economic, social, and sacred status in the pre-Columbian Americas. In the Andes, finely produced clothing and textiles containing multicolored feathers of tropical parrots materialized power, prestige, and distinction and were particularly prized by political and religious elites. Here we report 27 complete or partial remains of macaws and amazon parrots from five archaeological sites in the Atacama Desert of northern Chile to improve our understanding of their taxonomic identity, chronology, cultural context, and mechanisms of acquisition. We conducted a multiproxy archaeometric study that included zooarchaeological analysis, isotopic dietary reconstruction, accelerated mass spectrometry radiocarbon dating, and paleogenomic analysis. The results reveal that during the Late Intermediate Period (1100 to 1450 CE), Atacama oasis communities acquired scarlet macaws (Ara macao) and at least five additional translocated parrot species through vast exchange networks that extended more than 500 km toward the eastern Amazonian tropics. Carbon and nitrogen stable isotopes indicate that Atacama aviculturalists sustained these birds on diets rich in marine bird guano-fertilized maize-based foods. The captive rearing of these colorful, exotic, and charismatic birds served to unambiguously signal relational wealth in a context of emergent intercommunity competition.

Latitudinal but not elevational variation in blood glucose level is linked to life history across passerine birds.

Macrophysiological research is vital to our understanding of mechanisms underpinning global life history variation and adaptation to diverse environments. Here, we examined latitudinal and elevational variation in a key substrate of energy metabolism and an emerging physiological component of pace-of-life syndromes, blood glucose concentration. Our data, collected from 61 European temperate and 99 Afrotropical passerine species, revealed that baseline blood glucose increases with both latitude and elevation, whereas blood glucose stress response shows divergent directions, being stronger at low latitudes and high elevations. Low baseline glucose in tropical birds, compared to their temperate counterparts, was mainly explained by their low fecundity, consistent with the slow pace-of-life syndrome in the tropics. In contrast, elevational variation in this trait was decoupled from fecundity, implying a unique montane pace-of-life syndrome combining slow-paced life histories with fast-paced physiology. The observed patterns suggest that pace-of-life syndromes do not evolve along the single fast-slow axis.

A hierarchical N-mixture model to estimate behavioral variation and a case study of Neotropical birds.

Understanding how and why animals use the environments where they occur is both foundational to behavioral ecology and essential to identify critical habitats for species conservation. However, some behaviors are more difficult to observe than others, which can bias analyses of raw observational data. To our knowledge, no method currently exists to model how animals use different environments while accounting for imperfect behavior-specific detection probability. We developed an extension of a binomial N-mixture model (hereafter the behavior N-mixture model) to estimate the probability of a given behavior occurring in a particular environment while accounting for imperfect detection. We then conducted a simulation to validate the model's ability to estimate the effects of environmental covariates on the probabilities of individuals performing different behaviors. We compared our model to a naïve model that does not account for imperfect detection, as well as a traditional N-mixture model. Finally, we applied the model to a bird observation data set in northwest Costa Rica to quantify how three species behave in forests and farms. Simulations and sensitivity analyses demonstrated that the behavior N-mixture model produced unbiased estimates of behaviors and their relationships with predictor variables (e.g., forest cover, habitat type). Importantly, the behavior N-mixture model accurately characterized uncertainty, unlike the naïve model, which often suggested erroneous effects of covariates on behaviors. When applied to field data, the behavior N-mixture model suggested that Hoffmann's woodpecker (Melanerpes hoffmanii) and Inca dove (Columbina inca) behaved differently in forested versus agricultural habitats, while turquoise-browed motmot (Eumomota superciliosa) did not. Thus, the behavior N-mixture model can help identify habitats that are essential to a species' life cycle (e.g., where individuals nest, forage) that nonbehavioral models would miss. Our model can greatly improve the appropriate use of behavioral survey data and conclusions drawn from them. In doing so, it provides a valuable path forward for assessing the conservation value of alternative habitat types.

Seasonality at the equator: isotope signatures and hormonal correlates of molt phenology in a non-migratory Amazonian songbird.

BACKGROUND: Birds, across their annual cycle, progress through sequences of life-history stages such as reproduction and molt. The mechanisms that control annual avian itineraries involve endocrine responses triggered by seasonal environmental factors, including changes in resource availability and/or photoperiod. However, at equatorial latitudes birds are exposed to different degrees of seasonality, and the mechanisms underlying phenology of birds near the equator remain less explored. We studied the silver-beaked tanager, an endemic Amazonian songbird, from an equatorial lowland population. Remarkably, in this species, song behavior has been shown to be seasonally aligned to minimal changes in day length near the equator. Here, we aimed to further explore the phenology of silver-beaked tanagers by assessing shifts of food sources utilization as potential ultimate factors. We measured triple isotopic tracers of carbon (δ13C), nitrogen (δ15N) and sulphur (δ34S) in blood and feathers of birds throughout a whole year. In addition, we assessed the degree of seasonality in the molting activity, in relation to circulating levels of corticosterone, as well as to testosterone as a proxy of the reproductive condition of males. RESULTS: There was important seasonal variation of δ34S values in relation to rainfall patterns and changes in estuarine water composition. Despite the seasonal rainfall, we found no substantial variation in the foraging ecology of birds over seasons. This was accompanied by uniform levels of corticosterone throughout the year, probably associated with the absence of drastic seasonal resource shortages. Even so, silver-beaked tanagers showed a marked seasonal molting schedule, which was related to variation in the circulating levels of both corticosterone and testosterone. CONCLUSIONS: These findings suggest that foraging niche is not life history stage-dependent in silver-beaked tanagers, and highlight rainfall as an important environmental cue for bird phenology. Our stable isotope results encourage further studies addressing the influence of estuarine water dynamics on bird timing. In addition, the results suggest a primary role of steroid hormones in regulating seasonal life history stages under the absence of a marked photoperiod. Contrary to what might be expected for a tropical songbird, our physiological data in silver-beaked tanagers do not support reproduction-molt overlapping.

Expression of 5α- and 5ß-reductase in spinal cord and muscle of birds with different courtship repertoires.

BACKGROUND: Through the actions of one or more isoforms of the enzyme 5α-reductase in many male reproductive tissues, circulating testosterone (T) undergoes metabolic conversion into 5α-dihydrotestosterone (DHT), which binds to and activates androgen receptors (AR) with greater potency than T. In birds, T is also subject to local inactivation into 5ß-DHT by the enzyme 5ß-reductase. Male golden-collared manakins perform an androgen-dependent and physically elaborate courtship display, and these birds express androgen receptors in skeletal muscles and spinal cord at levels far greater than those expressed in species with more limited courtship routines, including male zebra finches. To determine if local T metabolism facilitates or impedes activation of male manakin courtship, we examined expression of two isoforms of 5α-reductase, as well as 5ß-reductase, in forelimb muscles and spinal cords of males and females of the two aforementioned species. RESULTS: We found that all enzymes were expressed in all tissues, with patterns that partially predict a functional role for 5α-reductase in these birds, especially in both muscle and spinal cord of male manakins. Moreover, we found that 5ß-reductase was markedly different between species, with far lower levels in golden-collared manakins, compared to zebra finches. Thus, modification to neuromuscular deactivation of T may also play a functional role in adaptive behavioral modulation. CONCLUSIONS: Given that such a role for 5α-reductase in androgen-sensitive mammalian skeletal muscle is in dispute, our data suggest that, in birds, local metabolism may play a key role in providing active androgenic substrates to peripheral neuromuscular systems. Similarly, we provide the first evidence that 5ß-reductase is expressed broadly through an organism and may be an important factor that regulates androgenic modulation of neuromuscular functioning.

Wild gut microbiomes reveal individuals, species, and location as drivers of variation in two critically endangered Hawaiian honeycreepers.

BACKGROUND: The gut microbiome of animals is an important component that has strong influence on the health, fitness, and behavior of its host. Most research in the microbiome field has focused on human populations and commercially important species. However, researchers are now considering the link between endangered species conservation and the microbiome. In Hawai'i, several threats (e.g., avian malaria and habitat loss) have caused widespread population declines of Hawaiian honeycreepers (subfamily: Carduelinae). These threats can have a significant effect on the avian gut microbiome and may even lead to disruption of microbial function. However, the gut microbiome of honeycreeper in the wild has yet to be explored. METHODS: We collected 13 and 42 fecal samples, respectively, from two critically endangered honeycreeper species, the 'akikiki (Oreomystis bairdi) and the 'akeke'e (Loxops caeruleirostris). The 16S rRNA gene was sequenced and processed though a MOTHUR-based bioinformatics pipeline. Bacterial ASVs were identified using the DADA2 program and bacterial community analyses, including alpha and beta diversity measures, were conducted using R packages Phyloseq and vegan. RESULTS: A total of 8,958 bacterial ASVs were identified from the fecal samples. Intraspecific differences in the gut microbiome among individual birds explained most of the variation present in the dataset, however differences between species did exist. Both species had distinct microbiomes with minimal overlap in beta diversity. 'Akikiki had a more diverse microbiome compared to 'akeke'e. Additionally, small but stastically significant differences in beta diversity also exist between sampling location and sexes in 'akikiki. CONCLUSION: 'Akikiki and 'akeke'e are currently the focus of captive breeding efforts and plans to translocate the two species to other islands are underway. This baseline knowledge will help inform management decisions for these honeycreeper species in their native habitats, on other islands, and in captivity.

Basal metabolic rate in free-ranging tropical birds lacks long-term repeatability and is influenced by ambient temperature.

Tropical birds live longer, have smaller clutches and invest more resources into self-maintenance than temperate species. These "slow" life-histories in tropical birds are accompanied by low basal metabolic rate (BMR). It has recently been suggested that the low BMR of tropical species may be related not to their slow "pace of life" or high ambient temperatures (Ta ) in tropical latitudes, but to the stability of environmental conditions in tropics. Since the repeatability of metabolic traits is higher in stable environments, such as laboratory conditions, we predicted that long-term repeatability of BMR in a tropical climate should be higher than in a temperate one. Contrary to our predictions, the repeatability of mass-independent BMR in 64 individuals of free-living tropical birds from Vietnam was low and insignificant after the species affiliation was taken into account. It indicates that BMR cannot be used as an individual long-term characteristic of tropical birds. On the other hand, tropical birds showed consistent differences in their mass-independent BMR at the interspecific level. Using BMR measurements from 1543 individuals of 134 species, we also found that different characteristics of Ta within the week preceding BMR measurements had a significant impact on the mass-independent BMR of tropical birds. The most significant effect was the difference between the absolute maximum and minimum Ta within a single week. Our results indicate that the physiology of tropical birds is more subject to changes than would be expected based on the notion of the stability of climatic conditions in the tropics.

Basal metabolic rate in free-living tropical birds: the influence of phylogenetic, behavioral, and ecological factors.

The majority of our knowledge of avian energetics is based on studies of birds from temperate and high latitudes. Using the largest existing sample of wild-caught Old World tropical species, we showed that birds from Southern Vietnam had lower basal metabolic rate (BMR) than temperate species. The strongest dissimilarity between tropical and temperate species was the low scaling exponent in the allometric relation between BMR and body mass in tropical birds (the regression slope was 0.573). The passerine migrants to temperate and high latitudes had higher BMR than tropical sedentary passerines. Body mass alone accounted for 93% of the variation in BMR (body mass ranged from 5 to 252 g). Contrary to some other studies, we did not find evidence besides the above mentioned that phylogeny, taxonomy, behavior, or ecology have a significant influence on BMR variation among tropical birds.

Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor - but not oestrogen receptor - in the forelimb musculature.

1. Superior physical competence is vital to the adaptive behavioral routines of many animals, particularly those that engage in elaborate socio-sexual displays. How such traits evolve across species remains unclear. 2. Recent work suggests that activation of sex steroid receptors in neuromuscular systems is necessary for the fine motor skills needed to execute physically elaborate displays. Thus, using passerine birds as models, we test whether interspecific variation in display complexity predicts species differences in the abundance of androgen and estrogen receptors (AR and ERα) expressed in the forelimb musculature and spinal cord. 3. We find that small-scale evolutionary patterns in physical display complexity positively predict expression of the AR in the main muscles that lift and retract the wings. No such relationship is detected in the spinal cord, and we do not find a correlation between display behavior and neuromuscular expression of ERα. Also, we find that AR expression levels in different androgen targets throughout the body - namely the wing muscles, spinal cord, and testes - are not necessarily correlated, providing evidence that evolutionary forces may drive AR expression in a tissue-specific manner. 4. These results suggest co-evolution between the physical prowess necessary for display performance and levels of AR expression in avian forelimb muscles. Moreover, this relationship appears to be specific to muscle and AR-mediated, but not ERα-mediated, signaling. 5. Given that prior work suggests that activation of muscular AR is a necessary component of physical display performance, our current data support the hypothesis that sexual selection shapes levels of AR expressed in the forelimb skeletal muscles to help drive the evolution of adaptive motor abilities.