Margaret R. Metz

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.

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.

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.

Insect herbivores, chemical innovation, and the evolution of habitat 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.

Temporal and spatial variability in seedling dynamics: a cross-site comparison in four lowland tropical forests

Spatialandtemporalvariationinseedlingdynamicswasassessedusingrecordsofcommunity-wideseedling demographycollectedwithidenticalmonitoringmethodsatfourtropicallowlandforestsinPanama,Malaysia,Ecuador and French Guiana for periods of between 3 and 10 y. At each site, the fates of between 8617 and 391 777 seedlings were followed through annual censuses of the 370-1008 1-m 2 seedling plots. Within-site spatial and inter-annual variation in density, recruitment, growth and mortality was compared with among-site variability using Bayesian hierarchical modelling to determine the generality of each sites patterns and potential for meaningful comparisons amongsites.TheMalaysianforest,whichexperiencescommunity-widemasting,wasthemostvariableinbothseedling density and recruitment. However, density varied year-to-year at all sites (CVamong years at site =8-43%), driven largely by high variability in recruitment rates (CV =40-117%). At all sites, recruitment was more variable than mortality (CV =5-64%) or growth (CV =12-51%). Increases in mortality rates lagged 1 y behind large recruitment events. Within-site spatial variation and inter-annual differences were greater than differences among site averages in all rates, emphasizing the value of long-term comparative studies when generalizing how spatial and temporal variation drive patterns of recruitment in tropical forests.

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 redwoods usual resilience to wildfire. Our results demonstrate the potential for interacting disturbances to initiate novel successional trajectories and compromise ecosystem resilience.

An emergent disease causes directional changes in forest species composition in coastal California

Non-native forest pathogens can cause dramatic and long-lasting changes to the composition of forests, and these changes may have cascading impacts on community interactions and ecosystem functioning. Phytophthora ramorum, the causal agent of the emergent forest disease sudden oak death (SOD), has a wide host range, but mortality is concentrated in a few dominant tree species of coastal forests in California and Oregon. We examined interactions between P. ramorum and its hosts in redwood and mixed evergreen forest types over an 80,000 ha area in the Big Sur ecoregion of central California, an area that constitutes the southernmost range of the pathogen and includes forest stands on the advancing front of pathogen invasion. We established a network of 280 long-term forest monitoring plots to understand how host composition and forest structure facilitated pathogen invasion, and whether selective mortality from SOD has led to shifts in community composition. Infested and uninfested sites differed significantly in host composition due to both historical trends and disease impacts. A reconstruction of pre-disease forest composition showed that stands that eventually became infested with the pathogen tended to be more mature with larger stems than stands that remained pathogen-free, supporting the hypothesis of aerial dispersal by the pathogen across the landscape followed by local understory spread. The change in species composition in uninfested areas was minimal over the study period, while infested stands had large changes in composition, correlated with the loss of tanoak (Notholithocarpus densiflorus), signaling the potential for SOD to dramatically change coastal forests through selective removal of a dominant host. Forest diversity plays an important role in pathogen establishment and spread, and is in turn changed by pathogen impacts. Asymmetric competency among host species means that impacts of P. ramorum on forest diversity are shaped by the combination and dominance of hosts present in a stand.

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.

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

BackgroundDisturbance 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.ResultsWe 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.ConclusionsGiven 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.

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.