Flower production decreases with warmer and more humid atmospheric conditions in a western Amazonian forest.

Climate models predict that everwet western Amazonian forests will face warmer and wetter atmospheric conditions, and increased cloud cover. It remains unclear how these changes will impact plant reproductive performance, such as flowering, which plays a central role in sustaining food webs and forest regeneration. Warmer and wetter nights may cause reduced flower production, via increased dark respiration rates or alteration in the reliability of flowering cue-based processes. Additionally, more persistent cloud cover should reduce the amounts of solar irradiance, which could limit flower production. We tested whether interannual variation in flower production has changed in response to fluctuations in irradiance, rainfall, temperature, and relative humidity over 18 yrs in an everwet forest in Ecuador. Analyses of 184 plant species showed that flower production declined as nighttime temperature and relative humidity increased, suggesting that warmer nights and greater atmospheric water saturation negatively impacted reproduction. Species varied in their flowering responses to climatic variables but this variation was not explained by life form or phylogeny. Our results shed light on how plant communities will respond to climatic changes in this everwet region, in which the impacts of these changes have been poorly studied compared with more seasonal Neotropical areas.

Seasonality of reproduction in an ever-wet lowland tropical forest in Amazonian Ecuador.

Flowering and fruiting phenology have been infrequently studied in the ever-wet hyperdiverse lowland forests of northwestern equatorial Amazonía. These Neotropical forests are typically called aseasonal with reference to climate because they are ever-wet, and it is often assumed they are also aseasonal with respect to phenology. The physiological limits to plant reproduction imposed by water and light availability are difficult to disentangle in seasonal forests because these variables are often temporally correlated, and both are rarely studied together, challenging our understanding of their relative importance as drivers of reproduction. Here we report on the first long-term study (18 years) of flowering and fruiting phenology in a diverse equatorial forest, Yasuní in eastern Ecuador, and the first to include a full suite of on-site monthly climate data. Using twice monthly censuses of 200 traps and >1000 species, we determined whether reproduction at Yasuní is seasonal at the community and species levels and analyzed the relationships between environmental variables and phenology. We also tested the hypothesis that seasonality in phenology, if present, is driven primarily by irradiance. Both the community- and species-level measures demonstrated strong reproductive seasonality at Yasuní. Flowering peaked in September-November and fruiting peaked in March-April, with a strong annual signal for both phenophases. Irradiance and rainfall were also highly seasonal, even though no month on average experienced drought (a month with <100 mm rainfall). Flowering was positively correlated with current or near-current irradiance, supporting our hypothesis that the extra energy available during the period of peak irradiance drives the seasonality of flowering at Yasuní. As Yasuní is representative of lowland ever-wet equatorial forests of northwestern Amazonía, we expect that reproductive phenology will be strongly seasonal throughout this region.

La fenología de floración y fructificación ha sido poco estudiada en los bosques bajos, lluviosos e hiperdiversos de la Amazonía noroccidental. Estos bosques neotropicales son típicamente llamados no estacionales debido a su clima siempre lluvioso y se asume que son no estacionales con respecto a la fenología. Los límites fisiológicos a la reproducción de las plantas impuestos por la disponibilidad de agua y luz en estos bosques son difíciles de desentrañar debido a que estas variables están a menudo correlacionadas temporalmente y las dos se estudian usualmente por separado, lo que desafía nuestra comprensión de su importancia relativa como desencadenantes de la reproducción. Este es el primer estudio de largo plazo (18 años) de la fenología de floración y fructificación en un bosque hiperdiverso de la Amazonía noroccidental ecuatorial, Yasuní, ubicado al este de Ecuador, y el primero en incluir un completo set de datos climáticos mensuales. Usando censos quincenales de 200 trampas y > 1000 especies, examinamos si la reproducción en Yasuní es estacional a nivel de comunidad y de especies y analizamos las relaciones de las variables ambientales con la fenología. También nos interesaba probar si la estacionalidad en la fenología, en caso de que esté presente está causada por la irradiancia. Tanto a nivel de comunidad como de especies, los datos demuestran una fuerte estacionalidad reproductiva en Yasuní. La floración alcanzó un máximo en septiembre-noviembre y la fructificación alcanzó un máximo en marzo-abril, con una fuerte y consistente señal anual en las dos fenofases. A su vez, la irradiancia y la lluvia fueron también marcadamente estacionales, aunque ningún mes en promedio experimentó sequía (i.e. <100 mm de lluvia). La floración fue positivamente correlacionada con la irradiación, apoyando nuestra hipótesis de que la energía extra disponible durante los periodos de mayor irradiación causa la estacionalidad de la floración en Yasuní. Debido a que Yasuní representa a los bosques ecuatoriales lluviosos de tierras bajas de la Amazonía noroccidental, esperamos que la fenología reproductiva sea fuertemente estacional a lo largo de esta región.

Multiscale phenological niches of seed fall in diverse Amazonian plant communities.

Phenology has long been hypothesized as an avenue for niche partitioning or interspecific facilitation, both promoting species coexistence. Tropical plant communities exhibit striking diversity in reproductive phenology, but many are also noted for large synchronous reproductive events. Here we study whether the phenology of seed fall in such communities is nonrandom, the temporal scales of phenological patterns, and ecological factors that drive reproductive phenology. We applied multivariate wavelet analysis to test for phenological synchrony versus compensatory dynamics (i.e., antisynchronous patterns where one species' decline is compensated by the rise of another) among species and across temporal scales. We used data from long-term seed rain monitoring of hyperdiverse plant communities in the western Amazon. We found significant synchronous whole-community phenology at multiple timescales, consistent with shared environmental responses or positive interactions among species. We also observed both compensatory and synchronous phenology within groups of species (confamilials) likely to share traits and seed dispersal mechanisms. Wind-dispersed species exhibited significant synchrony at ~6-month scales, suggesting these species might share phenological niches to match the seasonality of wind. Our results suggest that community phenology is shaped by shared environmental responses but that the diversity of tropical plant phenology may partly result from temporal niche partitioning. The scale-specificity and time-localized nature of community phenology patterns highlights the importance of multiple and shifting drivers of phenology.

The Epidemiology of Sudden Oak Death Disease Caused by Phytophthora ramorum in a Mixed Bay Laurel-Oak Woodland Provides Important Clues for Disease Management.

Epidemiological models are important for the understanding of disease progression in plants and for the design of control strategies. Phytophthora ramorum, the pathogen responsible for the disease known as Sudden Oak Death, causes lethal infection on several oaks but relies on California bay laurels for transmission. Here, repeated surveys of bay laurels and oaks indicated that bay laurel disease incidence was positively correlated with rainfall, bay laurel density, and an eastern aspect, and negatively correlated with bay laurel basal area. Oak infection only occurred in years when rainfall was higher than the 30-year average, and although infection rates were greater among larger trees, mortality was greater among smaller trees. Additionally, larger oaks closer to infected bay laurels exhibited greater infection rates. Disease incidence differed among sites, and only a fraction of bay laurels were disease superspreaders, while even fewer individuals were refugial trees harboring active infections during dry periods. Based on this study, reducing bay laurel density in denser stands and the number of superspreaders or refugial trees in less dense stands may reduce disease incidence. However, the selective removal of bay laurel trees 0-10 m from oaks is likely to be more effective in preventing infection of specific oaks.

Multicolor lineage tracing using in vivo time-lapse imaging reveals coordinated death of clonally related cells in the developing vertebrate brain.

The global mechanisms that regulate and potentially coordinate cell proliferation & death in developing neural regions are not well understood. In particular, it is not clear how or whether clonal relationships between neural progenitor cells and their progeny influence the growing brain. We have developed an approach using Brainbow in the developing zebrafish to visualize and follow multiple clones of related cells in vivo over time. This allows for clear visualization of many dividing clones of cells, deep in proliferating brain regions. As expected, in addition to undergoing interkinetic nuclear migration and cell division, cells also periodically undergo apoptosis. Interestingly, cell death occurs in a non-random manner: clonally related cells are more likely to die in a progressive fashion than cells from different clones. Multiple members of an individual clone die while neighboring clones appear healthy and continue to divide. Our results suggest that clonal relationships can influence cellular fitness and survival in the developing nervous system, perhaps through a competitive mechanism whereby clones of cells are competing with other clones. Clonal cell competition may help regulate neuronal proliferation in the vertebrate brain.

Novel disturbance interactions between fire and an emerging disease impact survival and growth of resprouting trees.

Human-altered ecological disturbances may challenge system resilience and disrupt biological legacies maintaining ecosystem recovery. Yet, the extent to which novel regimes challenge these legacies varies. This may be partially explained by differences in the vulnerability of life history strategies to disturbance characteristics. In the fire-prone, resprouter-dominated coast redwood forests of California, the introduced disease sudden oak death (SOD) alters fuel profiles, fire behavior, and aboveground tree mortality; however, this system is dominated by resprouting trees that are well-adapted to aboveground damage, and belowground survival of individuals may represent the principal biological legacy connecting pre- and post-fire communities. Much of the research exploring altered disturbances and forest recovery has focused on legacies determined by seed dispersal and aboveground survival of adults. In this work, we use pre- and post-fire data from a long-term monitoring network to assess the impacts of novel disturbance interactions between wildfire and SOD on the belowground survival and vegetative reproduction of resprouters. We found that increasing accumulation of coarse woody surface fuels from SOD-killed hosts decreased the likelihood of belowground survival for resprouting tanoak trees, but not for redwoods. Tanoaks' belowground survival was negatively related to substrate burn severity, which increased with the volume of surface fuels from hosts, suggesting heat damage as a possible mechanism influencing altered patterns of resprouter mortality. These impacts increased with decreasing tree size. By contrast, redwood and tanoak trees that survived both disturbances resprouted more vigorously, regardless of post-fire infection by P. ramorum, and generated similar recruitment at the stand level. Our results demonstrate that disease-fire interactions can narrow recruitment filters for resprouters, which could impact long-term population and demographic structure; yet, compounded disturbance may also reduce stand density and disease pressure, allowing competitive release of survivors. Resprouters displayed vulnerabilities to altered disturbance, but our research suggests that legacies maintained by resprouting may be more resilient to certain compounded disturbances, compared to seed-obligate species, because of high rates of individual survival under increasingly severe events. These trends have important implications for conservation of declining tree species in SOD-impacted forests, as well as predictions of human impacts in other disturbance-prone systems where resprouters are present.

Temporal coexistence mechanisms contribute to the latitudinal gradient in forest diversity.

The tropical forests of Borneo and Amazonia may each contain more tree species diversity in half a square kilometre than do all the temperate forests of Europe, North America, and Asia combined. Biologists have long been fascinated by this disparity, using it to investigate potential drivers of biodiversity. Latitudinal variation in many of these drivers is expected to create geographic differences in ecological and evolutionary processes, and evidence increasingly shows that tropical ecosystems have higher rates of diversification, clade origination, and clade dispersal. However, there is currently no evidence to link gradients in ecological processes within communities at a local scale directly to the geographic gradient in biodiversity. Here, we show geographic variation in the storage effect, an ecological mechanism that reduces the potential for competitive exclusion more strongly in the tropics than it does in temperate and boreal zones, decreasing the ratio of interspecific-to-intraspecific competition by 0.25% for each degree of latitude that an ecosystem is located closer to the Equator. Additionally, we find evidence that latitudinal variation in climate underpins these differences; longer growing seasons in the tropics reduce constraints on the seasonal timing of reproduction, permitting lower recruitment synchrony between species and thereby enhancing niche partitioning through the storage effect. Our results demonstrate that the strength of the storage effect, and therefore its impact on diversity within communities, varies latitudinally in association with climate. This finding highlights the importance of biotic interactions in shaping geographic diversity patterns, and emphasizes the need to understand the mechanisms underpinning ecological processes in greater detail than has previously been appreciated.

Unexpected redwood mortality from synergies between wildfire and an emerging infectious disease.

An under-examined component of global change is the alteration of disturbance regimes due to warming climates, continued species invasions, and accelerated land-use change. These drivers of global change are themselves novel ecosystem disturbances that may interact with historically occurring disturbances in complex ways. Here we use the natural experiment presented by wildfires in redwood forests impacted by an emerging infectious disease to demonstrate unexpected synergies of novel disturbance interactions. The dominant tree, coast redwood (fire resistant without negative disease impacts), experienced unexpected synergistic increases in mortality when fire and disease co-occurred. The increased mortality risk, more than fourfold at the peak of the effect, was not predictable from impacts of either disturbance alone. Changes in fire behavior associated with changes to forest fuels that occurred through disease progression overwhelmed redwood's usual resilience to wildfire. Our results demonstrate the potential for interacting disturbances to initiate novel successional trajectories and compromise ecosystem resilience.

Insect herbivores, chemical innovation, and the evolution of habit specialization in Amazonian trees.

Herbivores are often implicated in the generation of the extraordinarily diverse tropical flora. One hypothesis linking enemies to plant diversification posits that the evolution of novel defenses allows plants to escape their enemies and expand their ranges. When range expansion involves entering a new habitat type, this could accelerate defense evolution if habitats contain different assemblages of herbivores and/or divergent resource availabilities that affect plant defense allocation. We evaluated this hypothesis by investigating two sister habitat specialist ecotypes of Protium subserratum (Burseraceae), a common Amazonian tree that occurs in white-sand and terra firme forests. We collected insect herbivores feeding on the plants, assessed whether growth differences between habitats were genetically based using a reciprocal transplant experiment, and sampled multiple populations of both lineages for defense chemistry. Protium subserratum plants were attacked mainly by chrysomelid beetles and cicadellid hemipterans. Assemblages of insect herbivores were dissimilar between populations of ecotypes from different habitats, as well as from the same habitat 100 km distant. Populations from terra firme habitats grew significantly faster than white-sand populations; they were taller, produced more leaf area, and had more chlorophyll. White-sand populations expressed more dry mass of secondary compounds and accumulated more flavone glycosides and oxidized terpenes, whereas terra firme populations produced a coumaroylquinic acid that was absent from white-sand populations. We interpret these results as strong evidence that herbivores and resource availability select for divergent types and amounts of defense investment in white-sand and terra firme lineages of Protium subserratum, which may contribute to habitat-mediated speciation in these trees.

Demographic consequences of chromatic leaf defence in tropical tree communities: do red young leaves increase growth and survival?

BACKGROUND: Many tropical forest tree species delay greening their leaves until full expansion. This strategy is thought to provide newly flushing leaves with protection against damage by herbivores by keeping young leaves devoid of nutritive value. Because young leaves suffer the greatest predation from invertebrate herbivores, delayed greening could prevent costly tissue loss. Many species that delay greening also produce anthocyanin pigments in their new leaves, giving them a reddish tint. These anthocyanins may be fungicidal, protect leaves against UV damage or make leaves cryptic to herbivores blind to the red part of the spectrum. METHODS: A comprehensive survey was undertaken of seedlings, saplings and mature trees in two diverse tropical forests: a rain forest in western Amazonia (Yasuní National Park, Ecuador) and a deciduous forest in Central America (Barro Colorado Island, Panamá). A test was made of whether individuals and species with delayed greening or red-coloured young leaves showed lower mortality or higher relative growth rates than species that did not. KEY RESULTS: At both Yasuní and Barro Colorado Island, species with delayed greening or red young leaves comprised significant proportions of the seedling and tree communities. At both sites, significantly lower mortality was found in seedlings and trees with delayed greening and red-coloured young leaves. While there was little effect of leaf colour on the production of new leaves of seedlings, diameter relative growth rates of small trees were lower in species with delayed greening and red-coloured young leaves than in species with regular green leaves, and this effect remained when the trade-off between mortality and growth was accounted for. CONCLUSIONS: Herbivores exert strong selection pressure on seedlings for the expression of defence traits. A delayed greening or red-coloured young leaf strategy in seedlings appears to be associated with higher survival for a given growth rate, and may thus influence the species composition of later life stages.

The key host for an invasive forest pathogen also facilitates the pathogen's survival of wildfire in California forests.

The first wildfires in sudden oak death-impacted forests occurred in 2008 in the Big Sur region of California, creating the rare opportunity to study the interaction between an invasive forest pathogen and a historically recurring disturbance. To determine whether and how the sudden oak death pathogen, Phytophthora ramorum, survived the wildfires, we completed intensive vegetation-based surveys in forest plots that were known to be infested before the wildfires. We then used 24 plot-based variables as predictors of P. ramorum recovery following the wildfires. The likelihood of recovering P. ramorum from burned plots was lower than in unburned plots both 1 and 2 yr following the fires. Post-fire recovery of P. ramorum in burned plots was positively correlated with the number of pre-fire symptomatic California bay laurel (Umbellularia californica), the key sporulating host for this pathogen, and negatively correlated with post-fire bay laurel mortality levels. Patchy burn patterns that left green, P. ramorum-infected bay laurel amidst the charred landscape may have allowed these trees to serve as inoculum reservoirs that could lead to the infection of newly sprouting vegetation, further highlighting the importance of bay laurel in the sudden oak death disease cycle.

Palms, peccaries and perturbations: widespread effects of small-scale disturbance in tropical forests.

BACKGROUND: Disturbance is an important process structuring ecosystems worldwide and has long been thought to be a significant driver of diversity and dynamics. In forests, most studies of disturbance have focused on large-scale disturbance such as hurricanes or tree-falls. However, smaller sub-canopy disturbances could also have significant impacts on community structure. One such sub-canopy disturbance in tropical forests is abscising leaves of large arborescent palm (Arececeae) trees. These leaves can weigh up to 15 kg and cause physical damage and mortality to juvenile plants. Previous studies examining this question suffered from the use of static data at small spatial scales. Here we use data from a large permanent forest plot combined with dynamic data on the survival and growth of > 66,000 individuals over a seven-year period to address whether falling palm fronds do impact neighboring seedling and sapling communities, or whether there is an interaction between the palms and peccaries rooting for fallen palm fruit in the same area as falling leaves. We tested the wider generalisation of these hypotheses by comparing seedling and sapling survival under fruiting and non-fruiting trees in another family, the Myristicaceae. RESULTS: We found a spatially-restricted but significant effect of large arborescent fruiting palms on the spatial structure, population dynamics and species diversity of neighbouring sapling and seedling communities. However, these effects were not found around slightly smaller non-fruiting palm trees, suggesting it is seed predators such as peccaries rather than falling leaves that impact on the communities around palm trees. Conversely, this hypothesis was not supported in data from other edible species, such as those in the family Myristicaceae. CONCLUSIONS: Given the abundance of arborescent palm trees in Amazonian forests, it is reasonable to conclude that their presence does have a significant, if spatially-restricted, impact on juvenile plants, most likely on the survival and growth of seedlings and saplings damaged by foraging peccaries. Given the abundance of fruit produced by each palm, the widespread effects of these small-scale disturbances appear, over long time-scales, to cause directional changes in community structure at larger scales.

Interacting disturbances: wildfire severity affected by stage of forest disease invasion.

Sudden oak death (SOD) is an emerging forest disease causing extensive tree mortality in coastal California forests. Recent California wildfires provided an opportunity to test a major assumption underlying discussions of SOD and land management: SOD mortality will increase fire severity. We examined prefire fuels from host species in a forest monitoring plot network in Big Sur, California (USA), to understand the interactions between disease-caused mortality and wildfire severity during the 2008 Basin Complex wildfire. Detailed measurements of standing dead woody stems and downed woody debris 1-2 years prior to the Basin fire provided a rare picture of the increased fuels attributable to SOD mortality. Despite great differences in host fuel abundance, we found no significant difference in burn severity between infested and uninfested plots. Instead, the relationship between SOD and fire reflected the changing nature of the disease impacts over time. Increased SOD mortality contributed to overstory burn severity only in areas where the pathogen had recently invaded. Where longer-term disease establishment allowed dead material to fall and accumulate, increasing log volumes led to increased substrate burn severity. These patterns help inform forest management decisions regarding fire, both in Big Sur and in other areas of California as the pathogen continues to expand throughout coastal forests.

The relationship between wood density and mortality in a global tropical forest data set.

Wood density is thought to be an important indicator of plant life history because it is coupled to many aspects of whole-plant form and function. We used a hierarchical Bayesian approach to explain variation in mortality rates with wood density, drawing on data for 765,500 trees from 1639 species at 10 sites located across the Old and New World tropics. Mortality rates declined with increasing wood density at five of 10 sites. Similar negative trends were detected at four additional sites, while one site showed no relationship. Our model explained 40% of variation in mortality on average. Both wood density and mortality rates show a high degree of phylogenetic conservatism. Grouping species by family across sites in a second analysis, we found considerable variation in the relationship between wood density and mortality, with 10 of 27 families demonstrating a strong negative relationship. Our results highlight the importance of wood density as a functional trait in tropical forests, as it is strongly linked to variation in survival. However, the relationship varied among families, plots, and even census intervals within sites, indicating that the factors responsible for the relationship between wood density and mortality vary spatially, taxonomically and temporally.

Widespread density-dependent seedling mortality promotes species coexistence in a highly diverse Amazonian rain forest.

Negative density-dependent mortality can promote species coexistence through a spacing mechanism that prevents species from becoming too locally abundant. Negative density-dependent seedling mortality can be caused by interactions among seedlings or between seedlings and neighboring adults if the density of neighbors affects the strength of competition or facilitates the attack of natural enemies. We investigated the effects of seedling and adult neighborhoods on the survival of newly recruited seedlings for multiple cohorts of known age from 163 species in Yasuni National Park, Ecuador, an ever-wet, hyper-diverse lowland Amazonian rain forest. At local scales, we found a strong negative impact on first-year survival of conspecific seedling densities and adult abundance in multiple neighborhood sizes and a beneficial effect of a local tree neighborhood that is distantly related to the focal seedling. Once seedlings have survived their first year, they also benefit from a more phylogenetically dispersed seedling neighborhood. Across species, we did not find evidence that rare species have an advantage relative to more common species, or a community compensatory trend. These results suggest that the local biotic neighborhood is a strong influence on early seedling survival for species that range widely in their abundance and life history. These patterns in seedling survival demonstrate the role of density-dependent seedling dynamics in promoting and maintaining diversity in understory seedling assemblages. The assemblage-wide impacts of species abundance distributions may multiply with repeated cycles of recruitment and density-dependent seedling mortality and impact forest diversity or the abundance of individual species over longer time scales.