Functional trait-based restoration alters nutrient cycling and invasion rates in Hawaiian lowland wet forest.

Many degraded ecosystems have altered nutrient dynamics due to invaders' possessing a suite of traits that allow them to both outcompete native species and alter the environment. In ecosystems where invasive species have increased nutrient turnover rates, it can be difficult to reduce nutrient availability. This study examined whether a functional trait-based restoration approach involving the planting of species with conservative nutrient-use traits could slow rates of nutrient cycling and consequently reduce rates of invasion. We examined a functional trait restoration initiative in a heavily invaded lowland wet forest site in Hilo, Hawai'i. Native and introduced species were chosen to create four experimental hybrid forest communities, in comparison to the invaded forest, with a factorial design in which communities varied in rates of carbon turnover (slow or moderate [SLOW, MOD]), and in the relationship of species in trait space (redundant or complementary [RED, COMP]). After the first 5 years, we evaluated community-level outcomes related to nutrient cycling: carbon (C), nitrogen (N), and phosphorus (P) via litterfall, litter decomposition, and outplant productivity and rates of invasion. We found that (1) regardless of treatment, the experimental communities had low rates of nutrient cycling through litterfall relative to the invaded reference forest, (2) the MOD communities had greater nutrient release via litterfall than the SLOW communities, (3) introduced species had greater nutrient release than native species in the two MOD experimental communities, and (4) within treatments, there was a positive relationship between nutrient levels and outplant basal area, but outplant basal area was negatively associated with rates of invasion. The negative relationships among basal area and weed invasion, particularly for the two COMP treatments, suggest species existing in different parts of trait space may help confer some degree of invasion resistance. The diversification of trait space was facilitated by the use of introduced species, a new concept in Hawaiian forest management. Although challenges remain in endeavors to restore this heavily degraded ecosystem, this study provides evidence that functional trait-based restoration approaches using carefully crafted hybrid communities can reduce rates of nutrient cycling and invasion in order to reach management goals.

Correction: Integrating tropical research into biology education is urgently needed.

[This corrects the article DOI: 10.1371/journal.pbio.3001674.].

Integrating tropical research into biology education is urgently needed.

Understanding tropical biology is important for solving complex problems such as climate change, biodiversity loss, and zoonotic pandemics, but biology curricula view research mostly via a temperate-zone lens. Integrating tropical research into biology education is urgently needed to tackle these issues.

Distribution of biomass dynamics in relation to tree size in forests across the world.

Tree size shapes forest carbon dynamics and determines how trees interact with their environment, including a changing climate. Here, we conduct the first global analysis of among-site differences in how aboveground biomass stocks and fluxes are distributed with tree size. We analyzed repeat tree censuses from 25 large-scale (4-52 ha) forest plots spanning a broad climatic range over five continents to characterize how aboveground biomass, woody productivity, and woody mortality vary with tree diameter. We examined how the median, dispersion, and skewness of these size-related distributions vary with mean annual temperature and precipitation. In warmer forests, aboveground biomass, woody productivity, and woody mortality were more broadly distributed with respect to tree size. In warmer and wetter forests, aboveground biomass and woody productivity were more right skewed, with a long tail towards large trees. Small trees (1-10 cm diameter) contributed more to productivity and mortality than to biomass, highlighting the importance of including these trees in analyses of forest dynamics. Our findings provide an improved characterization of climate-driven forest differences in the size structure of aboveground biomass and dynamics of that biomass, as well as refined benchmarks for capturing climate influences in vegetation demographic models.

Leaf trichomes in Metrosideros polymorpha can contribute to avoiding extra water stress by impeding gall formation.

BACKGROUND AND AIMS: Plants inhabiting arid environments tend to have leaf trichomes, but their adaptive significance remains unclear. Leaf trichomes are known to play a role in plant defence against herbivores, including gall makers. Because gall formation can increase water loss partly through increased surface area, we tested the novel hypothesis that leaf trichomes could contribute to avoiding extra water stress by impeding gall formation, which would have adaptive advantages in arid environments. METHODS: We focused on Metrosideros polymorpha, an endemic tree species in the Hawaiian Islands, whose leaves often suffer from galls formed by specialist insects, Hawaiian psyllids (Pariaconus spp.). There is large variation in the amount of leaf trichomes (0-40 % of leaf mass) in M. polymorpha. Three gall types are found on the island of Hawaii: the largest is the 'cone' type, followed by 'flat' and 'pit' types. We conducted laboratory experiments to quantify the extent to which gall formation is associated with leaf water relations. We also conducted a field census of 1779 individuals from 48 populations across the entire range of habitats of M. polymorpha on the island of Hawaii to evaluate associations between gall formation (presence and abundance) and the amount of leaf trichomes. KEY RESULTS: Our laboratory experiment showed that leaf minimum conductance was significantly higher in leaves with a greater number of cone- or flat-type galls but not pit-type galls. Our field census suggested that the amount of trichomes was negatively associated with probabilities of the presence of cone- or flat-type galls but not pit-type galls, irrespective of environmental factors. CONCLUSION: Our results suggest that leaf trichomes in M. polymorpha can contribute to the avoidance of extra water stress through interactions with some gall-making species, and potentially increase the fitness of plants under arid conditions.

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.

OpenNahele: the open Hawaiian forest plot database.

BACKGROUND: This data paper provides a description of OpenNahele, the open Hawaiian forest plot database. OpenNahele includes 530 forest plots across the Hawaiian archipelago containing 43,590 individuals of 185 native and alien tree, shrub and tree fern species across six islands. We include estimates of maximum plant size (D950.1 and Dmax3) for 58 woody plant species, a key functional trait associated with dispersal distance and competition for light. OpenNahele can serve as a platform to test key ecological, evolutionary and conservation questions in a hotspot archipelago. NEW INFORMATION: OpenNahele is the first database that compiles data from a large number of forest plots across the Hawaiian archipelago to allow broad and high resolution studies of biodiversity patterns.Keywords: Hawaii, forests, islands, biodiversity, community ecology, evolutionary ecology.

Climate sensitive size-dependent survival in tropical trees.

Survival rates of large trees determine forest biomass dynamics. Survival rates of small trees have been linked to mechanisms that maintain biodiversity across tropical forests. How species survival rates change with size offers insight into the links between biodiversity and ecosystem function across tropical forests. We tested patterns of size-dependent tree survival across the tropics using data from 1,781 species and over 2 million individuals to assess whether tropical forests can be characterized by size-dependent life-history survival strategies. We found that species were classifiable into four 'survival modes' that explain life-history variation that shapes carbon cycling and the relative abundance within forests. Frequently collected functional traits, such as wood density, leaf mass per area and seed mass, were not generally predictive of the survival modes of species. Mean annual temperature and cumulative water deficit predicted the proportion of biomass of survival modes, indicating important links between evolutionary strategies, climate and carbon cycling. The application of survival modes in demographic simulations predicted biomass change across forest sites. Our results reveal globally identifiable size-dependent survival strategies that differ across diverse systems in a consistent way. The abundance of survival modes and interaction with climate ultimately determine forest structure, carbon storage in biomass and future forest trajectories.

Legume abundance along successional and rainfall gradients in Neotropical forests.

The nutrient demands of regrowing tropical forests are partly satisfied by nitrogen-fixing legume trees, but our understanding of the abundance of those species is biased towards wet tropical regions. Here we show how the abundance of Leguminosae is affected by both recovery from disturbance and large-scale rainfall gradients through a synthesis of forest inventory plots from a network of 42 Neotropical forest chronosequences. During the first three decades of natural forest regeneration, legume basal area is twice as high in dry compared with wet secondary forests. The tremendous ecological success of legumes in recently disturbed, water-limited forests is likely to be related to both their reduced leaflet size and ability to fix N2, which together enhance legume drought tolerance and water-use efficiency. Earth system models should incorporate these large-scale successional and climatic patterns of legume dominance to provide more accurate estimates of the maximum potential for natural nitrogen fixation across tropical forests.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Hülsmann and Hartig suggest that ecological mechanisms other than specialized natural enemies or intraspecific competition contribute to our estimates of conspecific negative density dependence (CNDD). To address their concern, we show that our results are not the result of a methodological artifact and present a null-model analysis that demonstrates that our original findings-(i) stronger CNDD at tropical relative to temperate latitudes and (ii) a latitudinal shift in the relationship between CNDD and species abundance-persist even after controlling for other processes that might influence spatial relationships between adults and recruits.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Chisholm and Fung claim that our method of estimating conspecific negative density dependence (CNDD) in recruitment is systematically biased, and present an alternative method that shows no latitudinal pattern in CNDD. We demonstrate that their approach produces strongly biased estimates of CNDD, explaining why they do not detect a latitudinal pattern. We also address their methodological concerns using an alternative distance-weighted approach, which supports our original findings of a latitudinal gradient in CNDD and a latitudinal shift in the relationship between CNDD and species abundance.

Plant diversity increases with the strength of negative density dependence at the global scale.

Theory predicts that higher biodiversity in the tropics is maintained by specialized interactions among plants and their natural enemies that result in conspecific negative density dependence (CNDD). By using more than 3000 species and nearly 2.4 million trees across 24 forest plots worldwide, we show that global patterns in tree species diversity reflect not only stronger CNDD at tropical versus temperate latitudes but also a latitudinal shift in the relationship between CNDD and species abundance. CNDD was stronger for rare species at tropical versus temperate latitudes, potentially causing the persistence of greater numbers of rare species in the tropics. Our study reveals fundamental differences in the nature of local-scale biotic interactions that contribute to the maintenance of species diversity across temperate and tropical communities.

Reproductive response to nitrogen and phosphorus fertilization along the Hawaiian archipelago's natural soil fertility gradient.

Nitrogen (N) and phosphorus (P) are the most important nutrients involved in plant reproduction and typically the most limiting in terrestrial ecosystems. The natural soil fertility gradient of the Hawaiian archipelago, in which younger islands are N limited and older islands are P limited, provides a model system to examine questions regarding allocation of nutrients. Using fertilized plots (+N or +P) at the extreme sites of the Hawaiian archipelago, vegetative productivity (e.g., net primary productivity, growth, and litterfall) and foliar nutrient responses have previously been studied for the dominant canopy tree, Metrosideros polymorpha. Here, we investigated whether the reproductive response of M. polymorpha mirrors the previously found vegetative productivity and foliar nutrient responses, by quantifying: (1) inflorescence and seed productivity, and (2) nutrient concentration of reproductive structures. Fertilization with N and P did not significantly affect the productivity of inflorescences or seeds, or seed viability at either site. However, nutrient concentrations increased after fertilization; %P increased in inflorescences in the +P treatment at the P-limited site. Seeds and inflorescences generally contained higher nutrient concentrations than leaves at both sites. Unlike foliar data, reproductive strategies of M. polymorpha differed depending on soil nutrient limitation with emphasis on quality (higher seed viability/greater nutrient concentrations) at the P-limited site. We suggest that in response to P additions M. polymorpha employs a nutrient conservation strategy for its inflorescences and an investment strategy for its seeds. Examining N and P simultaneously challenges a basic assumption that reproductive allocation follows a similar pattern to the often measured aboveground productivity.

Forest structure in low-diversity tropical forests: a study of Hawaiian wet and dry forests.

The potential influence of diversity on ecosystem structure and function remains a topic of significant debate, especially for tropical forests where diversity can range widely. We used Center for Tropical Forest Science (CTFS) methodology to establish forest dynamics plots in montane wet forest and lowland dry forest on Hawai'i Island. We compared the species diversity, tree density, basal area, biomass, and size class distributions between the two forest types. We then examined these variables across tropical forests within the CTFS network. Consistent with other island forests, the Hawai'i forests were characterized by low species richness and very high relative dominance. The two Hawai'i forests were floristically distinct, yet similar in species richness (15 vs. 21 species) and stem density (3078 vs. 3486/ha). While these forests were selected for their low invasive species cover relative to surrounding forests, both forests averaged 5->50% invasive species cover; ongoing removal will be necessary to reduce or prevent competitive impacts, especially from woody species. The montane wet forest had much larger trees, resulting in eightfold higher basal area and above-ground biomass. Across the CTFS network, the Hawaiian montane wet forest was similar to other tropical forests with respect to diameter distributions, density, and aboveground biomass, while the Hawai'i lowland dry forest was similar in density to tropical forests with much higher diversity. These findings suggest that forest structural variables can be similar across tropical forests independently of species richness. The inclusion of low-diversity Pacific Island forests in the CTFS network provides an ∼80-fold range in species richness (15-1182 species), six-fold variation in mean annual rainfall (835-5272 mm yr(-1)) and 1.8-fold variation in mean annual temperature (16.0-28.4°C). Thus, the Hawaiian forest plots expand the global forest plot network to enable testing of ecological theory for links among species diversity, environmental variation and ecosystem function.

Litter quality versus soil microbial community controls over decomposition: a quantitative analysis.

The possible effects of soil microbial community structure on organic matter decomposition rates have been widely acknowledged, but are poorly understood. Understanding these relationships is complicated by the fact that microbial community structure and function are likely to both affect and be affected by organic matter quality and chemistry, thus it is difficult to draw mechanistic conclusions from field studies. We conducted a reciprocal soil inoculum × litter transplant laboratory incubation experiment using samples collected from a set of sites that have similar climate and plant species composition but vary significantly in bacterial community structure and litter quality. The results showed that litter quality explained the majority of variation in decomposition rates under controlled laboratory conditions: over the course of the 162-day incubation, litter quality explained nearly two-thirds (64%) of variation in decomposition rates, and a smaller proportion (25%) was explained by variation in the inoculum type. In addition, the relative importance of inoculum type on soil respiration increased over the course of the experiment, and was significantly higher in microcosms with lower litter quality relative to those with higher quality litter. We also used molecular phylogenetics to examine the relationships between bacterial community composition and soil respiration in samples through time. Pyrosequencing revealed that bacterial community composition explained 32 % of the variation in respiration rates. However, equal portions (i.e., 16%) of the variation in bacterial community composition were explained by inoculum type and litter quality, reflecting the importance of both the meta-community and the environment in bacterial assembly. Taken together, these results indicate that the effects of changing microbial community composition on decomposition are likely to be smaller than the potential effects of climate change and/or litter quality changes in response to increasing atmospheric CO2 concentrations or atmospheric nutrient deposition.

Trade-offs in seedling growth and survival within and across tropical forest microhabitats.

For niche differences to maintain coexistence of sympatric species, each species must grow and/or survive better than each of the others in at least one set of conditions (i.e., performance trade-offs). However, the extent of niche differentiation in tropical forests remains highly debated. We present the first test of performance trade-offs for wild seedlings in a tropical forest. We measured seedling relative growth rate (RGR) and survival of four common native woody species across 18 light, substrate, and topography microhabitats over 2.5 years within Hawaiian montane wet forest, an ideal location due to its low species diversity and strong species habitat associations. All six species pairs exhibited significant performance trade-offs across microhabitats and for RGR versus survival within microhabitats. We also found some evidence of performance equivalence, with species pairs having similar performance in 26% of comparisons across microhabitats. Across species, survival under low light was generally positively associated with RGR under high light. When averaged over all species, topography (slope, aspect, and elevation) explained most of the variation in RGR attributable to microhabitat variables (51-53%) followed by substrate type (35-37%) and light (11-12%). However, the relative effects of microhabitat differed among species and RGR metric (i.e., RGR for height, biomass, or leaf area). These findings indicate that performance trade-offs among species during regeneration are common in low-diversity tropical forest, although other mechanisms may better explain the coexistence of species with small performance differences.

Native trees show conservative water use relative to invasive trees: results from a removal experiment in a Hawaiian wet forest.

While the supply of freshwater is expected to decline in many regions in the coming decades, invasive plant species, often 'high water spenders', are greatly expanding their ranges worldwide. In this study, we quantified the ecohydrological differences between native and invasive trees and also the effects of woody invasive removal on plot-level water use in a heavily invaded mono-dominant lowland wet tropical forest on the Island of Hawaii. We measured transpiration rates of co-occurring native and invasive tree species with and without woody invasive removal treatments. Twenty native Metrosideros polymorpha and 10 trees each of three invasive species, Cecropia obtusifolia, Macaranga mappa and Melastoma septemnervium, were instrumented with heat-dissipation sap-flux probes in four 100 m(2) plots (two invaded, two removal) for 10 months. In the invaded plots, where both natives and invasives were present, Metrosideros had the lowest sap-flow rates per unit sapwood, but the highest sap-flow rates per whole tree, owing to its larger mean diameter than the invasive trees. Stand-level water use within the removal plots was half that of the invaded plots, even though the removal of invasives caused a small but significant increase in compensatory water use by the remaining native trees. By investigating the effects of invasive species on ecohydrology and comparing native vs. invasive physiological traits, we not only gain understanding about the functioning of invasive species, but we also highlight potential water-conservation strategies for heavily invaded mono-dominant tropical forests worldwide. Native-dominated forests free of invasive species can be conservative in overall water use, providing a strong rationale for the control of invasive species and preservation of native-dominated stands.

Groundwater availability mediates the ecosystem effects of an invasion of Prosopis pallida.

Groundwater levels in arid environments are dropping worldwide due to human extraction, and precipitation events are predicted to become rarer and more intense in many arid areas with global climate change. These changes will likely alter both primary productivity and plant­soil nutrient cycles. To better understand the nature of such alterations, we examined effects of groundwater availability on plant­soil nitrogen (N) cycling in areas invaded by the N-fixing phreatophyte, Prosopis pallida, on the dry leeward coast of Hawai'i Island. Our aims were to quantify effects of groundwater availability to P. pallida on rates of litterfall N inputs and accretion in soils and to quantify effects of groundwater availability on N mineralization and leaching rates of inorganic N under natural rainfall conditions and simulated rain events. Stem water δ18O values indicate that P. pallida trees in lowland plots accessed shallow groundwater, while in upland plots they relied solely on rainfall. During drought periods, P. pallida at upland plots experienced water stress, evidenced by lower stem water potentials, higher water-use efficiency, and lower predawn photosynthetic performance than at lowland plots. Prosopis pallida basal area was 5.3 times greater at lowland plots, and these plots exhibited 17 times higher carbon (C), 24 times higher N, and 35 times higher phosphorus (P) additions via litterfall, indicating that productivity of this phreatophyte was decoupled from rainfall where groundwater was present. Total N mass in soils was 4.7 times greater where groundwater was accessible, supporting the case that groundwater access increased N2 fixation at a stand level. In contrast, N mineralization and leaching losses from soils, though substantially greater in lowland relative to upland areas, were strongly controlled by rainfall. Results provide clear examples of how invasive species with particular functional attributes (i.e., N-fixing phreatophytes) exploit otherwise inaccessible resources to dramatically alter the functioning of the systems they invade and how anthropogenic changes to hydrological processes can also alter ecosystem-level impacts of biological invasions. Results also illustrate a mechanism by which regional groundwater drawdown may reduce soil nutrient accretion and availability in arid regions.

[Tropical forest restoration in Costa Rica: the effect of several strategies on litter production, accumulation and decomposition]. / Restauración ecológica de bosques tropicales en Costa Rica: efecto de varios modelos en la producción, acumulación y descomposición de hojarasca.

Tropical forest restoration strategies have the potential to accelerate the recovery of the nutrient cycles in degraded lands. Litter production and its decomposition represent the main transfer of organic material and nutrients into the soil substrate. We evaluated litter production, accumulation on the forest floor, and its decomposition under three restoration strategies: plantation (entire area planted with trees), island (trees planted in patches of three different sizes) and control (natural regeneration) plots. We also compared restoration strategies to young secondary forest (7-9 yr). Restoration treatments were established in 50 x 50m plots in June 2004 at six sites in Southern Costa Rica. Planted tree species included two native timber species (Terminalia amazonia and Vochysia guatemalensis) interplanted with two N fixers (Erythrina poeppigiana and Inga edulis). Litter was collected every 15 days between September 2008 and August 2009 in 12 0.25m2 litter traps distributed within each plot; litter that accumulated on the soil surface was collected at four locations (0.25m2 quadrats) within each plot in February and May 2009. Total litter production in plantation (6.3Mg/ha) and secondary forest (7.3Mg/ha) did not differ, but were greater than in islands (3.5Mg/ha) and control (1.4 Mg/ha). Plantation had greatest accumulation of litter on the soil surface (10.6 Mg/ha) as compared to the other treatments (SF = 7.2; I = 6.7; C = 4.9). Secondary forest was the only treatment with a greater annual production of litter than litter accumulation on the soil surface. Carbon storage in litter was similar between plantation and secondary forest, and significantly greater than the other treatments. No differences were found for carbon concentration and storage in the soil among treatments. There was also high variability in the production and accumulation of litter and carbon among sites. Active restoration treatments accelerated the production of litter and carbon storage in comparison to areas under natural recovery. However, the nutrient cycle has not necessarily been restored under these conditions, as high litter accumulation on the soil surface indicates a low decomposition rate, which slows nutrient return to the soil.