Detecting Nonadditive Biotic Interactions and Assessing Their Biological Relevance among Temperate Rainforest Trees.

AbstractInteractions between and within abiotic and biotic processes generate nonadditive density-dependent effects on species performance that can vary in strength or direction across environments. If ignored, nonadditivities can lead to inaccurate predictions of species responses to environmental and compositional changes. While there are increasing empirical efforts to test the constancy of pairwise biotic interactions along environmental and compositional gradients, few assess both simultaneously. Using a nationwide forest inventory that spans broad ambient temperature and moisture gradients throughout New Zealand, we address this gap by analyzing the diameter growth of six focal tree species as a function of neighbor densities and climate, as well as neighbor × climate and neighbor × neighbor statistical interactions. The most complex model featuring all interaction terms had the highest predictive accuracy. Compared with climate variables, biotic interactions typically had stronger effects on diameter growth, especially when subjected to nonadditivities from local climatic conditions and the density of intermediary species. Furthermore, statistically strong (or weak) nonadditivities could be biologically irrelevant (or significant) depending on whether a species pair typically interacted under average or more extreme conditions. Our study highlights the importance of considering both the statistical potential and the biological relevance of nonadditive biotic interactions when assessing species performance under global change.

Damage to tropical forests caused by cyclones is driven by wind speed but mediated by topographical exposure and tree characteristics.

Each year, an average of 45 tropical cyclones affect coastal areas and potentially impact forests. The proportion of the most intense cyclones has increased over the past four decades and is predicted to continue to do so. Yet, it remains uncertain how topographical exposure and tree characteristics can mediate the damage caused by increasing wind speed. Here, we compiled empirical data on the damage caused by 11 cyclones occurring over the past 40 years, from 74 forest plots representing tropical regions worldwide, encompassing field data for 22,176 trees and 815 species. We reconstructed the wind structure of those tropical cyclones to estimate the maximum sustained wind speed (MSW) and wind direction at the studied plots. Then, we used a causal inference framework combined with Bayesian generalised linear mixed models to understand and quantify the causal effects of MSW, topographical exposure to wind (EXP), tree size (DBH) and species wood density (ρ) on the proportion of damaged trees at the community level, and on the probability of snapping or uprooting at the tree level. The probability of snapping or uprooting at the tree level and, hence, the proportion of damaged trees at the community level, increased with increasing MSW, and with increasing EXP accentuating the damaging effects of cyclones, in particular at higher wind speeds. Higher ρ decreased the probability of snapping and to a lesser extent of uprooting. Larger trees tended to have lower probabilities of snapping but increased probabilities of uprooting. Importantly, the effect of ρ decreasing the probabilities of snapping was more marked for smaller than larger trees and was further accentuated at higher MSW. Our work emphasises how local topography, tree size and species wood density together mediate cyclone damage to tropical forests, facilitating better predictions of the impacts of such disturbances in an increasingly windier world.

Long-term exclusion of invasive ungulates alters tree recruitment and functional traits but not total forest carbon.

Forests are major carbon (C) sinks, but their ability to sequester C and thus mitigate climate change, varies with the environment, disturbance regime, and biotic interactions. Herbivory by invasive, nonnative ungulates can have profound ecosystem effects, yet its consequences for forest C stocks remain poorly understood. We determined the impact of invasive ungulates on C pools, both above- and belowground (to 30 cm), and on forest structure and diversity using 26 paired long-term (>20 years) ungulate exclosures and adjacent unfenced control plots located in native temperate rainforests across New Zealand, spanning 36-41° S. Total ecosystem C was similar between ungulate exclosure (299.93 ± 25.94 Mg C ha-1 ) and unfenced control (324.60 ± 38.39 Mg C ha-1 ) plots. Most (60%) variation in total ecosystem C was explained by the biomass of the largest tree (mean diameter at breast height [dbh]: 88 cm) within each plot. Ungulate exclusion increased the abundance and diversity of saplings and small trees (dbh ≥2.5, <10 cm) compared with unfenced controls, but these accounted for ~5% of total ecosystem C, demonstrating that a few, large trees dominate the total forest ecosystem C but are unaffected by invasive ungulates at a timescale of 20-50 years. However, changes in understory C pools, species composition, and functional diversity did occur following long-term ungulate exclusion. Our findings suggest that, although the removal of invasive herbivores may not affect total forest C at the decadal scale, major shifts in the diversity and composition of regenerating species will have longer term consequences for ecosystem processes and forest C.

Disentangling Niche Theory and Beta Diversity Change.

AbstractBeta diversity describes the differences in species composition among communities. Changes in beta diversity over time are thought to be due to selection based on species' niche characteristics. For example, theory predicts that selection that favors habitat specialists will increase beta diversity. In practice, ecologists struggle to predict how beta diversity changes. To remedy this problem, we propose a novel solution that formally measures selection's effects on beta diversity. Using the Price equation, we show how change in beta diversity over time can be partitioned into fundamental mechanisms including selection among species, variable selection among communities, drift, and immigration. A key finding of our approach is that a species' short-term impact on beta diversity cannot be predicted using information on its long-term environmental requirements (i.e., its niche). We illustrate how our approach can be used to partition causes of diversity change in a montane tropical forest before and after an intense hurricane. Previous work in this system highlighted the resistance of habitat specialists and the recruitment of light-demanding species but was unable to quantify the importance of these effects on beta diversity. Using our approach, we show that changes in beta diversity were consistent with ecological drift. We use these results to highlight the opportunities presented by a synthesis of beta diversity and formal models of selection.

Phylogenetic classification of the world's tropical forests.

Knowledge about the biogeographic affinities of the world's tropical forests helps to better understand regional differences in forest structure, diversity, composition, and dynamics. Such understanding will enable anticipation of region-specific responses to global environmental change. Modern phylogenies, in combination with broad coverage of species inventory data, now allow for global biogeographic analyses that take species evolutionary distance into account. Here we present a classification of the world's tropical forests based on their phylogenetic similarity. We identify five principal floristic regions and their floristic relationships: (i) Indo-Pacific, (ii) Subtropical, (iii) African, (iv) American, and (v) Dry forests. Our results do not support the traditional neo- versus paleotropical forest division but instead separate the combined American and African forests from their Indo-Pacific counterparts. We also find indications for the existence of a global dry forest region, with representatives in America, Africa, Madagascar, and India. Additionally, a northern-hemisphere Subtropical forest region was identified with representatives in Asia and America, providing support for a link between Asian and American northern-hemisphere forests.

Climatic limits of temperate rainforest tree species are explained by xylem embolism resistance among angiosperms but not among conifers.

Hydraulic failure explains much of the increased rates of drought-induced tree mortality around the world, underlining the importance of understanding how species distributions are shaped by their vulnerability to embolism. Here we determined which physiological traits explain species climatic limits among temperate rainforest trees in a region where chronic water limitation is uncommon. We quantified the variation in stem embolism vulnerability and leaf turgor loss point among 55 temperate rainforest tree species in New Zealand and tested which traits were most strongly related to species climatic limits. Leaf turgor loss point and stem P50 (tension at which hydraulic conductance is at 50% of maximum) were uncorrelated. Stem P50 and hydraulic safety margin were the most strongly related physiological traits to climatic limits among angiosperms, but not among conifers. Morphological traits such as wood density and leaf dry matter content did not explain species climatic limits. Stem embolism resistance and leaf turgor loss point appear to have evolved independently. Embolism resistance is the most useful predictor of the climatic limits of angiosperm trees. High embolism resistance in the curiously overbuilt New Zealand conifers suggests that their xylem properties may be more closely related to growing slowly under nutrient limitation and to resistance to microbial decomposition.

An estimate of the number of tropical tree species.

The high species richness of tropical forests has long been recognized, yet there remains substantial uncertainty regarding the actual number of tropical tree species. Using a pantropical tree inventory database from closed canopy forests, consisting of 657,630 trees belonging to 11,371 species, we use a fitted value of Fisher's alpha and an approximate pantropical stem total to estimate the minimum number of tropical forest tree species to fall between ∼ 40,000 and ∼ 53,000, i.e., at the high end of previous estimates. Contrary to common assumption, the Indo-Pacific region was found to be as species-rich as the Neotropics, with both regions having a minimum of ∼ 19,000-25,000 tree species. Continental Africa is relatively depauperate with a minimum of ∼ 4,500-6,000 tree species. Very few species are shared among the African, American, and the Indo-Pacific regions. We provide a methodological framework for estimating species richness in trees that may help refine species richness estimates of tree-dependent taxa.

Burrowing seabird effects on invertebrate communities in soil and litter are dominated by ecosystem engineering rather than nutrient addition.

Vertebrate consumers can be important drivers of the structure and functioning of ecosystems, including the soil and litter invertebrate communities that drive many ecosystem processes. Burrowing seabirds, as prevalent vertebrate consumers, have the potential to impact consumptive effects via adding marine nutrients to soil (i.e. resource subsidies) and non-consumptive effects via soil disturbance associated with excavating burrows (i.e. ecosystem engineering). However, the exact mechanisms by which they influence invertebrates are poorly understood. We examined how soil chemistry and plant and invertebrate communities changed across a gradient of seabird burrow density on two islands in northern New Zealand. Increasing seabird burrow density was associated with increased soil nutrient availability and changes in plant community structure and the abundance of nearly all the measured invertebrate groups. Increasing seabird densities had a negative effect on invertebrates that were strongly influenced by soil-surface litter, a positive effect on fungal-feeding invertebrates, and variable effects on invertebrate groups with diverse feeding strategies. Gastropoda and Araneae species richness and composition were also influenced by seabird activity. Generalized multilevel path analysis revealed that invertebrate responses were strongly driven by seabird engineering effects, via increased soil disturbance, reduced soil-surface litter, and changes in trophic interactions. Almost no significant effects of resource subsidies were detected. Our results show that seabirds, and in particular their non-consumptive effects, were significant drivers of invertebrate food web structure. Reductions in seabird populations, due to predation and human activity, may therefore have far-reaching consequences for the functioning of these ecosystems.

Functional and environmental determinants of bark thickness in fire-free temperate rain forest communities.

PREMISE OF THE STUDY: In fire-prone ecosystems, variation in bark thickness among species and communities has been explained by fire frequency; thick bark is necessary to protect cambium from lethal temperatures. Elsewhere this investment is deemed unnecessary, and thin bark is thought to prevail. However, in rain forest ecosystems where fire is rare, bark thickness varies widely among species and communities, and the causes of this variation remain enigmatic. We tested for functional explanations of bark thickness variation in temperate rain forest species and communities. METHODS: We measured bark thickness in 82 tree species throughout New Zealand temperate rain forests that historically have experienced little fire and applied two complementary analyses. First, we examined correlations between bark traits and leaf habit, and leaf and stem traits. Second, we calculated community-weighted mean (CWM) bark thickness for 272 plots distributed throughout New Zealand to identify the environments in which thicker-barked communities occur. KEY RESULTS: Conifers had higher size-independent bark thickness than evergreen angiosperms. Species with thicker bark or higher bark allocation coefficients were not associated with "slow economic" plant traits. Across 272 forest plots, communities with thicker bark occurred on infertile soils, and communities with thicker bark and higher bark allocation coefficients occurred in cooler, drier climates. CONCLUSIONS: In non-fire-prone temperate rain forest ecosystems, investment in bark is driven by soil resources, cool minimum temperatures, and seasonal moisture stress. The role of these factors in fire-prone ecosystems warrants testing.

Use of pollen and ancient DNA as conservation baselines for offshore islands in New Zealand.

Islands play a key role globally in the conservation of endemic species. Many island reserves have been highly modified since human colonization, and their restoration and management usually occur without knowledge of their prehuman state. However, conservation paleoecology is increasingly being recognized as a tool that can help to inform both restoration and conservation of island reserves by providing prehuman vegetation baselines. Many of New Zealand's mammal-free offshore islands are foci for biological diversity conservation and, like many islands in the Polynesian region, were deforested following initial human settlement. Therefore, their current restoration, replanting, and management are guided either by historic vegetation descriptions or the occurrence of species on forested islands. We analyzed pollen and ancient DNA in soil cores from an offshore island in northern New Zealand. The result was a 2000-year record of vegetation change that began >1200 years before human settlement and spanned 550 years of human occupation and 180 years of forest succession since human occupation ceased. Between prehuman and contemporary forests there was nearly a complete species turnover including the extirpation of a dominant conifer and a palm tree. The podocarp-dominated forests were replaced by a native but novel angiosperm-dominated forest. There is no modern analog of the prehuman forests on any northern New Zealand island, and those islands that are forested are dominated by angiosperms which are assumed to be climax forests. The pollen and DNA evidence for conifer- and palm-rich forests in the prehuman era challenge this climax forest assumption. Prehuman vegetation records can thus help to inform future restoration of degraded offshore islands by informing the likely rate and direction of successional change; helping to determine whether natural rates of succession are preferable to more costly replanting programs; and providing past species lists if restoration replanting is desired.

Soil-mediated indirect impacts of an invasive predator on plant growth.

While several studies have shown that invasive plant effects on soil biota influence subsequent plant performance, corresponding studies on how invasive animals affect plants through influencing soil biota are lacking. This is despite the fact that invasive animals often indirectly alter the below-ground subsystem. We studied 18 offshore islands in northern New Zealand, half of which have been invaded by rats that are predators of seabirds and severely reduce their densities, and half of which remain non-invaded; invasion of rats thwarts seabird transfer of resources from ocean to land. We used soil from each island in a glasshouse experiment involving soil sterilization treatments to determine whether rat invasion indirectly influences plant growth through the abiotic pathway (by impairing seabird-driven inputs to soil) or the biotic pathway (by altering the soil community). Rat invasion greatly impaired plant growth but entirely through the abiotic pathway. Plant growth was unaffected by the soil community or its response to invasion, meaning that the responses of plants and soil biota to invasion are decoupled. Our results provide experimental evidence for the powerful indirect effects that predator-instigated cascades can exert on plant and ecosystem productivity, with implications for the restoration of island ecosystems by predator removal.

Altered cyclone-fire interactions are changing ecosystems.

Global change is altering interactions between ecological disturbances. We review interactions between tropical cyclones and fires that affect woody biomes in many islands and coastal areas. Cyclone-induced damage to trees can increase fuel loads on the ground and dryness in the understory, which increases the likelihood, intensity, and area of subsequent fires. In forest biomes, cyclone-fire interactions may initiate a grass-fire cycle and establish stable open-canopy biomes. In cyclone-prone regions, frequent cyclone-enhanced fires may generate and maintain stable open-canopy biomes (e.g., savannas and woodlands). We discuss how global change is transforming fire and cyclone regimes, extensively altering cyclone-fire interactions. These altered cyclone-fire interactions are shifting biomes away from historical states and causing loss of biodiversity.

Invasive rats alter woody seedling composition on seabird-dominated islands in New Zealand.

Invasive rats (Rattus rattus, R. norvegicus, R. exulans) have large impacts on island habitats through both direct and indirect effects on plants. Rats affect vegetation by extirpating burrowing seabirds through consumption of eggs, chicks, and adults. These seabirds serve as ecosystem engineers, affecting plant communities by burying and trampling seeds and seedlings, and by altering microclimate. Rats also directly affect plant communities by consuming seeds and seedlings. We studied the direct and indirect impacts of rats on the seedlings of woody plants on 21 islands in northern New Zealand. We compared seedling densities and richness on islands which differed in status with respect to rats: nine islands where rats never invaded, seven islands where rats were present at the time of our study, and five islands where rats were either eradicated or where populations were likely to be small as a result of repeated eradications and re-invasions. In addition, we compared plots from a subset of the 21 islands with different burrow densities to examine the effects of burrowing seabirds on plants while controlling for other factors that differ between islands. We categorized plant communities by species composition and seedling density in a cluster analysis. We found that burrow densities explained more variation in seedling communities than rat status. In areas with high seabird burrow density seedling densities were low, especially for the smallest seedlings. Species richness and diversity of seedlings, but not seedling density, were most influenced by changes in microclimate induced by seabirds. Islands where rats had been eradicated or that had low rat populations had the lowest diversity and richness of seedlings (and adults), but the highest seedling density. Seedling communities on these islands were dominated by Pseudopanax lessonii and Coprosma macrocarpa. This indicates lasting effects of rats that may prevent islands from returning to pre-invasion states.

Effects of invasive rats and burrowing seabirds on seeds and seedlings on New Zealand islands.

Rats (Rattus rattus, Rattus norvegicus, Rattus exulans) are important invaders on islands. They alter vegetation indirectly by preying on burrowing seabirds. These seabirds affect vegetation through nutrient inputs from sea to land and physical disturbance through trampling and burrowing. Rats also directly affect vegetation though consumption of seeds and seedlings. Seedling communities on northern New Zealand islands differ in composition and densities among islands which have never been invaded by rats, are currently invaded by rats, or from which rats have been eradicated. We conducted experimental investigations to determine the mechanisms driving these patterns. When the physical disturbance of seabirds was removed, in soils collected from islands and inside exclosures, seedling densities increased with seabird burrow density. For example, seedling densities inside exclosures were 10 times greater than those outside. Thus the negative effects of seabirds on seedlings, by trampling and uprooting, overwhelm the potentially beneficial effects of high levels of seed germination, seedling emergence, and possibly seed production, which result from seed burial and nutrient additions. Potential seedling density was reduced on an island where rats were present, germination of seeds from soils of this island was approximately half that found on other islands, but on this island seedling density inside exclosures was 7 times the density outside. Although the total negative effects of seabirds and rats on seedling densities are similar (reduced seedling density), the differences in mechanisms and life stages affected result in very different filters on the plant community.

Indirect effects of invasive predators on litter decomposition and nutrient resorption on seabird-dominated islands.

Despite recent interest in the ecosystem impacts of invasive aboveground organisms, most work in this area has focused on effects of invasive plants, and the effects of invasive herbivores and predators remain poorly understood. We studied 18 forested, offshore islands in northern New Zealand. Nine of these host high densities of burrowing seabirds that serve as ecosystem drivers by transporting nutrients from the ocean to land. The other nine have been invaded over the past 50-150 years by rat species introduced from Europe which serve as predators of seabird eggs and chicks and severely reduce their densities. We collected fully expanded leaves and fresh leaf litter from invaded and uninvaded islands for each of 12 perennial plant species that represent a wide spectrum of life forms from ground dwelling to emergent canopy species. We found that, across these species, invasion by rats significantly reduced nitrogen (N) but not phosphorus (P) concentrations of foliage and litter, promoted N but not P resorption from leaves before litter fall, and reduced the release of N but not P from decomposing litter. Rat invasion also negatively affected litter decomposability but had no overall effects on litter quality variables other than N. Our results provide evidence that rat invasion causes more conservative cycling of N but not P through foliage and litter and limitation of ecological processes by N but not P. We found few instances in which the effects of rat invasion on response variables varied significantly across plant species, meaning that invasion had similar effects for species that varied greatly in growth form and foliar and litter quality. Further, correlation analyses across the 12 species showed that foliar and litter quality traits were poor predictors of how invasion effects on resorption and decomposition variables varied among species. Our results show that the effects of invasive predators on native prey can have substantial indirect effects on variables relevant for ecosystem functioning. These types of effects are probably widespread, especially given the role of seabirds in improving soil fertility in many coastal ecosystems worldwide and the wide global distribution of predators of seabirds.

Global effects of non-native tree species on multiple ecosystem services.

Non-native tree (NNT) species have been transported worldwide to create or enhance services that are fundamental for human well-being, such as timber provision, erosion control or ornamental value; yet NNTs can also produce undesired effects, such as fire proneness or pollen allergenicity. Despite the variety of effects that NNTs have on multiple ecosystem services, a global quantitative assessment of their costs and benefits is still lacking. Such information is critical for decision-making, management and sustainable exploitation of NNTs. We present here a global assessment of NNT effects on the three main categories of ecosystem services, including regulating (RES), provisioning (PES) and cultural services (CES), and on an ecosystem disservice (EDS), i.e. pollen allergenicity. By searching the scientific literature, country forestry reports, and social media, we compiled a global data set of 1683 case studies from over 125 NNT species, covering 44 countries, all continents but Antarctica, and seven biomes. Using different meta-analysis techniques, we found that, while NNTs increase most RES (e.g. climate regulation, soil erosion control, fertility and formation), they decrease PES (e.g. NNTs contribute less than native trees to global timber provision). Also, they have different effects on CES (e.g. increase aesthetic values but decrease scientific interest), and no effect on the EDS considered. NNT effects on each ecosystem (dis)service showed a strong context dependency, varying across NNT types, biomes and socio-economic conditions. For instance, some RES are increased more by NNTs able to fix atmospheric nitrogen, and when the ecosystem is located in low-latitude biomes; some CES are increased more by NNTs in less-wealthy countries or in countries with higher gross domestic products. The effects of NNTs on several ecosystem (dis)services exhibited some synergies (e.g. among soil fertility, soil formation and climate regulation or between aesthetic values and pollen allergenicity), but also trade-offs (e.g. between fire regulation and soil erosion control). Our analyses provide a quantitative understanding of the complex synergies, trade-offs and context dependencies involved for the effects of NNTs that is essential for attaining a sustained provision of ecosystem services.

Intraspecific trait variation can weaken interspecific trait correlations when assessing the whole-plant economic spectrum.

The worldwide plant economic spectrum hypothesis predicts that leaf, stem, and root traits are correlated across vascular plant species because carbon gain depends on leaves being adequately supplied with water and nutrients, and because construction of each organ involves a trade-off between performance and persistence. Despite its logical and intuitive appeal, this hypothesis has received mixed empirical support. If traits within species diverge in their responses to an environmental gradient, then interspecific trait correlations could be weakened when measured in natural ecosystems. To test this prediction, we measured relative growth rates (RGR) and seven functional traits that have been shown to be related to fluxes of water, nutrients, and carbon across 56 functionally diverse tree species on (1) juveniles in a controlled environment, (2) juveniles in forest understories, and (3) mature trees in forests. Leaf, stem, and fine root traits of juveniles grown in a controlled environment were closely correlated with each other, and with RGR. Remarkably, the seven leaf, stem, and fine root tissue traits spanned a single dimension of variation when measured in the controlled environment. Forest-grown juveniles expressed lower leaf mass per area, but higher wood and fine root tissue density, than greenhouse-grown juveniles. Traits and growth rates were decoupled in forest-grown juveniles and mature trees. Our results indicate that constraints exist on the covariation, not just the variation, among vegetative plant organs; however, divergent responses of traits within species to environmental gradients can mask interspecific trait correlations in natural environments. Correlations among organs and relationships between traits and RGR were strong when plants were compared in a standardized environment. Our results may reconcile the discrepancies seen among studies, by showing that if traits and growth rates of species are compared across varied environments, then the interorgan trait correlations observed in controlled conditions can weaken or disappear.

Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems.

Predators often exert multi-trophic cascading effects in terrestrial ecosystems. However, how such predation may indirectly impact interactions between above- and below-ground biota is poorly understood, despite the functional importance of these interactions. Comparison of rat-free and rat-invaded offshore islands in New Zealand revealed that predation of seabirds by introduced rats reduced forest soil fertility by disrupting sea-to-land nutrient transport by seabirds, and that fertility reduction in turn led to wide-ranging cascading effects on belowground organisms and the ecosystem processes they drive. Our data further suggest that some effects on the belowground food web were attributable to changes in aboveground plant nutrients and biomass, which were themselves related to reduced soil disturbance and fertility on invaded islands. These results demonstrate that, by disrupting across-ecosystem nutrient subsidies, predators can indirectly induce strong shifts in both above- and below-ground biota via multiple pathways, and in doing so, act as major ecosystem drivers.