Effects of moisture and density-dependent interactions on tropical tree diversity.

Tropical tree diversity increases with rainfall1,2. Direct physiological effects of moisture availability and indirect effects mediated by biotic interactions are hypothesized to contribute to this pantropical increase in diversity with rainfall2-6. Previous studies have demonstrated direct physiological effects of variation in moisture availability on tree survival and diversity5,7-10, but the indirect effects of variation in moisture availability on diversity mediated by biotic interactions have not been shown11. Here we evaluate the relationships between interannual variation in moisture availability, the strength of density-dependent interactions, and seedling diversity in central Panama. Diversity increased with soil moisture over the first year of life across 20 annual cohorts. These first-year changes in diversity persisted for at least 15 years. Differential survival of moisture-sensitive species did not contribute to the observed changes in diversity. Rather, negative density-dependent interactions among conspecifics were stronger and increased diversity in wetter years. This suggests that moisture availability enhances diversity indirectly through moisture-sensitive, density-dependent conspecific interactions. Pathogens and phytophagous insects mediate interactions among seedlings in tropical forests12-18, and many of these plant enemies are themselves moisture-sensitive19-27. Changes in moisture availability caused by climate change and habitat degradation may alter these interactions and tropical tree diversity.

Widespread herbivory cost in tropical nitrogen-fixing tree species.

Recent observations suggest that the large carbon sink in mature and recovering forests may be strongly limited by nitrogen1-3. Nitrogen-fixing trees (fixers) in symbiosis with bacteria provide the main natural source of new nitrogen to tropical forests3,4. However, abundances of fixers are tightly constrained5-7, highlighting the fundamental unanswered question of what limits new nitrogen entering tropical ecosystems. Here we examine whether herbivory by animals is responsible for limiting symbiotic nitrogen fixation in tropical forests. We evaluate whether nitrogen-fixing trees experience more herbivory than other trees, whether herbivory carries a substantial carbon cost, and whether high herbivory is a result of herbivores targeting the nitrogen-rich leaves of fixers8,9. We analysed 1,626 leaves from 350 seedlings of 43 tropical tree species in Panama and found that: (1) although herbivory reduces the growth and survival of all seedlings, nitrogen-fixing trees undergo 26% more herbivory than non-fixers; (2) fixers have 34% higher carbon opportunity costs owing to herbivory than non-fixers, exceeding the metabolic cost of fixing nitrogen; and (3) the high herbivory of fixers is not driven by high leaf nitrogen. Our findings reveal that herbivory may be sufficient to limit tropical symbiotic nitrogen fixation and could constrain its role in alleviating nitrogen limitation on the tropical carbon sink.

Adaptations to nitrogen availability drive ecological divergence of chemosynthetic symbionts.

Bacterial symbionts, with their shorter generation times and capacity for horizontal gene transfer (HGT), play a critical role in allowing marine organisms to cope with environmental change. The closure of the Isthmus of Panama created distinct environmental conditions in the Tropical Eastern Pacific (TEP) and Caribbean, offering a "natural experiment" for studying how closely related animals evolve and adapt under environmental change. However, the role of bacterial symbionts in this process is often overlooked. We sequenced the genomes of endosymbiotic bacteria in two sets of sister species of chemosymbiotic bivalves from the genera Codakia and Ctena (family Lucinidae) collected on either side of the Isthmus, to investigate how differing environmental conditions have influenced the selection of symbionts and their metabolic capabilities. The lucinid sister species hosted different Candidatus Thiodiazotropha symbionts and only those from the Caribbean had the genetic potential for nitrogen fixation, while those from the TEP did not. Interestingly, this nitrogen-fixing ability did not correspond to symbiont phylogeny, suggesting convergent evolution of nitrogen fixation potential under nutrient-poor conditions. Reconstructing the evolutionary history of the nifHDKT operon by including other lucinid symbiont genomes from around the world further revealed that the last common ancestor (LCA) of Ca. Thiodiazotropha lacked nif genes, and populations in oligotrophic habitats later re-acquired the nif operon through HGT from the Sedimenticola symbiont lineage. Our study suggests that HGT of the nif operon has facilitated niche diversification of the globally distributed Ca. Thiodiazotropha endolucinida species clade. It highlights the importance of nitrogen availability in driving the ecological diversification of chemosynthetic symbiont species and the role that bacterial symbionts may play in the adaptation of marine organisms to changing environmental conditions.

Soil carbon loss by experimental warming in a tropical forest.

Tropical soils contain one-third of the carbon stored in soils globally1, so destabilization of soil organic matter caused by the warming predicted for tropical regions this century2 could accelerate climate change by releasing additional carbon dioxide (CO2) to the atmosphere3-6. Theory predicts that warming should cause only modest carbon loss from tropical soils relative to those at higher latitudes5,7, but there have been no warming experiments in tropical forests to test this8. Here we show that in situ experimental warming of a lowland tropical forest soil on Barro Colorado Island, Panama, caused an unexpectedly large increase in soil CO2 emissions. Two years of warming of the whole soil profile by four degrees Celsius increased CO2 emissions by 55 per cent compared to soils at ambient temperature. The additional CO2 originated from heterotrophic rather than autotrophic sources, and equated to a loss of 8.2 ± 4.2 (one standard error) tonnes of carbon per hectare per year from the breakdown of soil organic matter. During this time, we detected no acclimation of respiration rates, no thermal compensation or change in the temperature sensitivity of enzyme activities, and no change in microbial carbon-use efficiency. These results demonstrate that soil carbon in tropical forests is highly sensitive to warming, creating a potentially substantial positive feedback to climate change.

Imprinting sets the stage for speciation.

Sexual imprinting-a phenomenon in which offspring learn parental traits and later use them as a model for their own mate preferences-can generate reproductive barriers between species1. When the target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate speciation1,2. However, in most models of speciation by sexual selection, divergent natural selection is also required; the latter acts to generate and maintain variation in the sexually selected trait or traits, and in the mating preferences that act upon them3. Here we demonstrate that imprinting, in addition to mediating female mate preferences, can shape biases in male-male aggression. These biases can act similarly to natural selection to maintain variation in traits and mate preferences, which facilitates reproductive isolation driven entirely by sexual selection. Using a cross-fostering study, we show that both male and female strawberry poison frogs (Oophaga pumilio) imprint on coloration, which is a mating trait that has diverged recently and rapidly in this species4. Cross-fostered females prefer to court mates of the same colour as their foster mother, and cross-fostered males are more aggressive towards rivals that share the colour of their foster mother. We also use a simple population-genetics model to demonstrate that when both male aggression biases and female mate preferences are formed through parental imprinting, sexual selection alone can (1) stabilize a sympatric polymorphism and (2) strengthen the trait-preference association that leads to behavioural reproductive isolation. Our study provides evidence of imprinting in an amphibian and suggests that this rarely considered combination of rival and sexual imprinting can reduce gene flow between individuals that bear divergent mating traits, which sets the stage for speciation by sexual selection.

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.

The human malaria-Aotus monkey model: a historical perspective in antimalarial chemotherapy research at the Gorgas Memorial Laboratory-Panama.

The human malaria-Aotus monkey model has served the malaria research community since its inception in 1966 at the Gorgas Memorial Laboratory (GML) in Panama. Spanning over five decades, this model has been instrumental in evaluating the in vivo efficacy and pharmacokinetics of a wide array of candidate antimalarial drugs, whether used singly or in combination. The animal model could be infected with drug-resistant and susceptible Plasmodium falciparum and Plasmodium vivax strains that follow a characteristic and reproducible course of infection, remarkably like human untreated and treated infections. Over the years, the model has enabled the evaluation of several synthetic and semisynthetic endoperoxides, for instance, artelinic acid, artesunate, artemether, arteether, and artemisone. These compounds have been evaluated alone and in combination with long-acting partner drugs, commonly referred to as artemisinin-based combination therapies, which are recommended as first-line treatment against uncomplicated malaria. Further, the model has also supported the evaluation of the primaquine analog tafenoquine against blood stages of P. vivax, contributing to its progression to clinical trials and eventual approval. Besides, the P. falciparum/Aotus model at GML has also played a pivotal role in exploring the biology, immunology, and pathogenesis of malaria and in the characterization of drug-resistant P. falciparum and P. vivax strains. This minireview offers a historical overview of the most significant contributions made by the Panamanian owl monkey (Aotus lemurinus lemurinus) to malaria chemotherapy research.

A Spatial Signal of Niche Differentiation in Tropical Forests.

AbstractExplaining diversity in tropical forests remains a challenge in community ecology. Theory tells us that species differences can stabilize communities by reducing competition, while species similarities can promote diversity by reducing fitness differences and thus prolonging the time to competitive exclusion. Combined, these processes may lead to clustering of species such that species are niche differentiated across clusters and share a niche within each cluster. Here, we characterize this partial niche differentiation in a tropical forest in Panama by measuring spatial clustering of woody plants and relating these clusters to local soil conditions. We find that species were spatially clustered and the clusters were associated with specific concentrations of soil nutrients, reflecting the existence of nutrient niches. Species were almost twice as likely to recruit in their own nutrient niche. A decision tree algorithm showed that local soil conditions correctly predicted the niche of the trees with up to 85% accuracy. Iron, zinc, phosphorus, manganese, and soil pH were among the best predictors of species clusters.

Biogeographic and seasonal differences in consumer pressure underlie strong predation in the tropics.

Biotic interactions play a critical role in shaping patterns of global biodiversity. While several macroecological studies provide evidence for stronger predation in tropical regions compared with higher latitudes, results are variable even within the tropics, and the drivers of this variability are not well understood. We conducted two complementary standardized experiments on communities of sessile marine invertebrate prey and their associated predators to test for spatial and seasonal differences in predation across the tropical Atlantic and Pacific coastlines of Panama. We further tested the prediction that higher predator diversity contributes to stronger impacts of predation, using both direct observations of predators and data from extensive reef surveys. Our results revealed substantially higher predation rates and stronger effects of predators on prey in the Pacific than in the Atlantic, demonstrating striking variation within tropical regions. While regional predator diversity was high in the Atlantic, functional diversity at local scales was markedly low. Peak predation strength in the Pacific occurred during the wet, non-upwelling season when ocean temperatures were warmer and predator communities were more functionally diverse. Our results highlight the importance of regional biotic and abiotic drivers that shape interaction strength and the maintenance of tropical communities, which are experiencing rapid environmental change.

Trees adjust nutrient acquisition strategies across tropical forest secondary succession.

Nutrient limitation may constrain the ability of recovering and mature tropical forests to serve as a carbon sink. However, it is unclear to what extent trees can utilize nutrient acquisition strategies - especially root phosphatase enzymes and mycorrhizal symbioses - to overcome low nutrient availability across secondary succession. Using a large-scale, full factorial nitrogen and phosphorus fertilization experiment of 76 plots along a secondary successional gradient in lowland wet tropical forests of Panama, we tested the extent to which root phosphatase enzyme activity and mycorrhizal colonization are flexible, and if investment shifts over succession, reflective of changing nutrient limitation. We also conducted a meta-analysis to test how tropical trees adjust these strategies in response to nutrient additions and across succession. We find that tropical trees are dynamic, adjusting investment in strategies - particularly root phosphatase - in response to changing nutrient conditions through succession. These changes reflect a shift from strong nitrogen to weak phosphorus limitation over succession. Our meta-analysis findings were consistent with our field study; we found more predictable responses of root phosphatase than mycorrhizal colonization to nutrient availability. Our findings suggest that nutrient acquisition strategies respond to nutrient availability and demand in tropical forests, likely critical for alleviating nutrient limitation.

Observed declines in body size have differential effects on survival and recruitment, but no effect on population growth in tropical birds.

Declines in body size can be an advantageous physiological response to warming temperatures, or a result of physiological and nutritional stress. Either way, studies often assume that these climate-induced trait changes have important implications for fitness and demography. We leveraged almost three decades of capture-mark-recapture data of 51 bird species in Panama to examine if body size has changed through time, how sensitive body size is to changes in weather, and if body size impacts population demography. We evaluated two metrics of body size, structural size (wing length), and body condition (residual body mass). Over the study, wing length changed in varying directions for 88% of species (23 decrease, 22 increase), but the effects were weak, and change was only significant for two species. Conversely, body condition declined for 88% of species (45), effects were stronger, and that change was significant for 22% of species (11). This suggests that nutritional stress is likely the cause of changes in body size, not an adaptive response to warming. Precipitation metrics impacted body condition across three of our four feeding guilds, while wing length was only impacted by weather metrics for two guilds. This suggests that body condition is more sensitive to change in weather metrics compared to wing length. Lastly, we found that the impact of changes in body size on survival and recruitment was variable across species, but these relationships were in the opposite direction, ultimately resulting in no change in population growth for all but one species. Thus, while different stages (adult survival and recruitment) of populations may be impacted by body size, populations appear to be buffered from changes. The lack of an effect on population growth rate suggests that populations may be more resilient to changes in body size, with implications for population persistence under expected climate change.

Chlorine Water Taste Threshold and Acceptability among Indigenous and Non-Indigenous Populations in Rural Panama.

Although gains in access to water services over the past two decades have been large, more than two billion people still lack access to safely managed drinking water. This study examines and compares free chlorine taste and acceptability thresholds of rural Indigenous Ngäbe and rural Latino Panamanians to study if taste aversion may be a limiting factor in chlorination of community systems in Panama using the three-alternative forced choice test methodology. This study is the first to establish a best-estimate taste threshold for a rural Indigenous group and the only study in Latin America to report best-estimate taste thresholds using those methods. Median taste thresholds were 0.87 mg/L Cl2 for Indigenous Ngäbe participants (n = 82) and 1.64 mg/L Cl2 for Latino participants (n = 64), higher than both the minimum concentration for biologically safe water (0.2 mg/L) and the recommended concentration range in Panama (0.3-0.8 mg/L). Median acceptability thresholds were established much higher than taste thresholds at 3.45 mg/L Cl2. The results show that the ability to accurately taste chlorine may not be the limiting factor for adoption of safe water initiatives in remote and Indigenous communities.

Pervasive phosphorus limitation of tree species but not communities in tropical forests.

Phosphorus availability is widely assumed to limit primary productivity in tropical forests, but support for this paradigm is equivocal. Although biogeochemical theory predicts that phosphorus limitation should be prevalent on old, strongly weathered soils, experimental manipulations have failed to detect a consistent response to phosphorus addition in species-rich lowland tropical forests. Here we show, by quantifying the growth of 541 tropical tree species across a steep natural phosphorus gradient in Panama, that phosphorus limitation is widespread at the level of individual species and strengthens markedly below a threshold of two parts per million exchangeable soil phosphate. However, this pervasive species-specific phosphorus limitation does not translate into a community-wide response, because some species grow rapidly on infertile soils despite extremely low phosphorus availability. These results redefine our understanding of nutrient limitation in diverse plant communities and have important implications for attempts to predict the response of tropical forests to environmental change.

Fossil dermal denticles reveal the preexploitation baseline of a Caribbean coral reef shark community.

Preexploitation shark baselines and the history of human impact on coral reef-associated shark communities in the Caribbean are tpoorly understood. We recovered shark dermal denticles from mid-Holocene (∼7 ky ago) and modern reef sediments in Bocas del Toro, Caribbean Panama, to reconstruct an empirical shark baseline before major human impact and to quantify how much the modern shark community in the region had shifted from this historical reference point. We found that denticle accumulation rates, a proxy for shark abundance, declined by 71% since the mid-Holocene. All denticle morphotypes, which reflect shark community composition, experienced significant losses, but those morphotypes found on fast-swimming, pelagic sharks (e.g., families Carcharhinidae and Sphyrnidae) declined the most. An analysis of historical records suggested that the steepest decline in shark abundance occurred in the late 20th century, coinciding with the advent of a targeted shark fishery in Panama. Although the disproportionate loss of denticles characterizing pelagic sharks was consistent with overfishing, the large reduction in denticles characterizing demersal species with low commercial value (i.e., the nurse shark Ginglymostoma cirratum) indicated that other stressors could have exacerbated these declines. We demonstrate that the denticle record can reveal changes in shark communities over long ecological timescales, helping to contextualize contemporary abundances and inform shark management and ecology.

Legume-microbiome interactions unlock mineral nutrients in regrowing tropical forests.

Legume trees form an abundant and functionally important component of tropical forests worldwide with N2-fixing symbioses linked to enhanced growth and recruitment in early secondary succession. However, it remains unclear how N2-fixers meet the high demands for inorganic nutrients imposed by rapid biomass accumulation on nutrient-poor tropical soils. Here, we show that N2-fixing trees in secondary Neotropical forests triggered twofold higher in situ weathering of fresh primary silicates compared to non-N2-fixing trees and induced locally enhanced nutrient cycling by the soil microbiome community. Shotgun metagenomic data from weathered minerals support the role of enhanced nitrogen and carbon cycling in increasing acidity and weathering. Metagenomic and marker gene analyses further revealed increased microbial potential beneath N2-fixers for anaerobic iron reduction, a process regulating the pool of phosphorus bound to iron-bearing soil minerals. We find that the Fe(III)-reducing gene pool in soil is dominated by acidophilic Acidobacteria, including a highly abundant genus of previously undescribed bacteria, Candidatus Acidoferrum, genus novus. The resulting dependence of the Fe-cycling gene pool to pH determines the high iron-reducing potential encoded in the metagenome of the more acidic soils of N2-fixers and their nonfixing neighbors. We infer that by promoting the activities of a specialized local microbiome through changes in soil pH and C:N ratios, N2-fixing trees can influence the wider biogeochemical functioning of tropical forest ecosystems in a manner that enhances their ability to assimilate and store atmospheric carbon.

First evidence of prickly shark, Echinorhinus cookei Pietschmann 1928, aggregation on seamounts in the eastern Pacific, Panama.

In May 2022, twelve prickly sharks, Echinorhinus cookei Pietschmann 1928, were sighted at 151-350 m depth in the Cordillera de Coiba seamounts, Pacific Panama. This discovery expands our knowledge of the distribution and habitat use of this rare deep-sea species. It underscores the potential significance of the Cordillera de Coiba seamounts, an offshore marine protected area, as a critical habitat for E. cookei, a species threatened by commercial fishing. Although unverified reports exist on its presence in the tropical eastern Pacific, this publication represents the first documented record of live specimens of E. cookei in Panama.

Effect of Education on Adherence to Recommended Prenatal Practices among Indigenous Ngäbe-Buglé Communities of Panama.

Background and Objectives: The primary objective of this study was to assess the adherence of Ngäbe-Buglé women to WHO-recommended prenatal practices. The secondary objective was to compare adherence levels between women who received prenatal education from official medical providers and those educated through traditional or community-based sources within Ngäbe-Buglé communities. Materials and Methods: An eight-question survey was verbally administered to 137 Ngäbe-Buglé women at clinics set up by the non-profit NGO Floating Doctors in eight communities. A two-sided Fisher's Exact test with a p = 0.05 was used to compare the results of mothers who received prenatal education from evidence-based sources to other groups. Results: Out of the 137 surveyed women, 65 reported taking prenatal vitamins, 21 had prenatal check-ups, 136 avoided alcohol, 31 increased caloric intake, and 102 maintained their activity levels. Significant differences were observed in prenatal vitamin adherence between those educated by official sources versus unofficial sources (p = 0.0029) and official sources compared to those with no prenatal education (p < 0.0001). The difference was also significant for education from an unofficial source versus no education (p = 0.0056). However, no significant differences were found in other prenatal practices based on education sources. Conclusions: Our findings highlight deficiencies in both prenatal education and adherence to recommended practices among Ngäbe-Buglé women. Prenatal education significantly improved adherence to taking prenatal vitamins, suggesting its effectiveness as an intervention. Future interventions should prioritize culturally competent prenatal education and address barriers to accessing prenatal healthcare in Ngäbe-Buglé communities.

Detection of Leishmania RNA Virus 1 in Leishmania (Viannia) panamensis Isolates, Panama.

We detected Leishmania RNA virus 1 (LRV1) in 11 isolates of Leishmania (Viannia) panamensis collected during 2014-2019 from patients from different geographic areas in Panama. The distribution suggested a spread of LRV1 in L. (V.) panamensis parasites. We found no association between LRV1 and an increase in clinical pathology.

Human Lobomycosis Caused by Paracoccidioides (Lacazia) loboi, Panama, 2022.

We report a patient from Panama who had lobomycosis caused by Paracoccidioides (Lacazia) loboi. We used combined clinical-epidemiologic and phylogenetic data, including a new gene sequence dataset on this fungus in Panama, for analysis. Findings contribute useful insights to limited knowledge of this fungal infection in the Mesoamerican Biologic Corridor.