Stephanie Pau

Warming experiments underpredict plant phenological responses to climate change

Warming experiments are increasingly relied on to estimate plant responses to global climate change. For experiments to provide meaningful predictions of future responses, they should reflect the empirical record of responses to temperature variability and recent warming, including advances in the timing of flowering and leafing. We compared phenology (the timing of recurring life history events) in observational studies and warming experiments spanning four continents and 1,634 plant species using a common measure of temperature sensitivity (change in days per degree Celsius). We show that warming experiments underpredict advances in the timing of flowering and leafing by 8.5-fold and 4.0-fold, respectively, compared with long-term observations. For species that were common to both study types, the experimental results did not match the observational data in sign or magnitude. The observational data also showed that species that flower earliest in the spring have the highest temperature sensitivities, but this trend was not reflected in the experimental data. These significant mismatches seem to be unrelated to the study length or to the degree of manipulated warming in experiments. The discrepancy between experiments and observations, however, could arise from complex interactions among multiple drivers in the observational data, or it could arise from remediable artefacts in the experiments that result in lower irradiance and drier soils, thus dampening the phenological responses to manipulated warming. Our results introduce uncertainty into ecosystem models that are informed solely by experiments and suggest that responses to climate change that are predicted using such models should be re-evaluated.

Phylogenetic conservatism in plant phenology

Summary 1. Phenological events – defined points in the life cycle of a plant or animal – have been regarded as highly plastic traits, reflecting flexible responses to various environmental cues. 2. The ability of a species to track, via shifts in phenological events, the abiotic environment through time might dictate its vulnerability to future climate change. Understanding the predictors and drivers of phenological change is therefore critical. 3. Here, we evaluated evidence for phylogenetic conservatism – the tendency for closely related species to share similar ecological and biological attributes – in phenological traits across flowering plants. We aggregated published and unpublished data on timing of first flower and first leaf, encompassing ~4000 species at 23 sites across the Northern Hemisphere. We reconstructed the phylogeny for the set of included species, first, using the software program Phylomatic, and second, from DNA data. We then quantified phylogenetic conservatism in plant phenology within and across sites. 4. We show that more closely related species tend to flower and leaf at similar times. By contrasting mean flowering times within and across sites, however, we illustrate that it is not the time of year that is conserved, but rather the phenological responses to a common set of abiotic cues. 5. Our findings suggest that species cannot be treated as statistically independent when modelling phenological responses. 6. Synthesis. Closely related species tend to resemble each other in the timing of their life-history events, a likely product of evolutionarily conserved responses to environmental cues. The search for the underlying drivers of phenology must therefore account for species’ shared evolutionary histories.

Sensitivity of Spring Phenology to Warming Across Temporal and Spatial Climate Gradients in Two Independent Databases

Disparate ecological datasets are often organized into databases post hoc and then analyzed and interpreted in ways that may diverge from the purposes of the original data collections. Few studies, however, have attempted to quantify how biases inherent in these data (for example, species richness, replication, climate) affect their suitability for addressing broad scientific questions, especially in under-represented systems (for example, deserts, tropical forests) and wild communities. Here, we quantitatively compare the sensitivity of species first flowering and leafing dates to spring warmth in two phenological databases from the Northern Hemisphere. One—PEP725—has high replication within and across sites, but has low species diversity and spans a limited climate gradient. The other—NECTAR—includes many more species and a wider range of climates, but has fewer sites and low replication of species across sites. PEP725, despite low species diversity and relatively low seasonality, accurately captures the magnitude and seasonality of warming responses at climatically similar NECTAR sites, with most species showing earlier phenological events in response to warming. In NECTAR, the prevalence of temperature responders significantly declines with increasing mean annual temperature, a pattern that cannot be detected across the limited climate gradient spanned by the PEP725 flowering and leafing data. Our results showcase broad areas of agreement between the two databases, despite significant differences in species richness and geographic coverage, while also noting areas where including data across broader climate gradients may provide added value. Such comparisons help to identify gaps in our observations and knowledge base that can be addressed by ongoing monitoring and research efforts. Resolving these issues will be critical for improving predictions in understudied and under-sampled systems outside of the temperature seasonal mid-latitudes.

Natural history, biogeography, and endangerment of Hawaiian dry forest trees

We describe the floristic composition of Hawaiian dry forest trees and identify natural history characteristics and biogeographic variables that are associated with risk of endangerment. Hawaiian dry forests are comprised of 109 tree species in 29 families, with 90% of all species endemic, 10% indigenous, and 37% single-island endemics. Forty-five percent of Hawaiian dry forest taxa are at risk of endangerment. Dry forest taxa at risk have a significantly larger range size compared to taxa from other Hawaiian forest types. Dispersal mechanism was a significant predictor of a species occurrence in dry forest compared to other forest types based on logistic regressions clustered by lineage. Among dry forest taxa, hermaphroditic breeding systems, autochorous dispersal mechanisms, conspicuous flowers, and dry fruit were all more likely to be at risk of endangerment. When analyses were clustered by lineage using logistic regressions, only dispersal mechanism and flower size were significant predictors of risk and taxa with autochorous dispersal and conspicuous flowers were more likely to be at risk. The Big Island, Maui, Oahu, and Kauai all have remarkably similar numbers of dry forest taxa (63–65 species) and dry forest taxa at risk of endangerment. However, Big Island and Kauai have the highest number and percentage of single-island endemics. These results demonstrate patterns of endangerment specific to Hawaiian dry forests, the high levels of endangerment in this forest type, and the importance of prioritizing conservation in dry forest regions.

A Global Assessment of Long-Term Greening and Browning Trends in Pasture Lands Using the GIMMS LAI3g Dataset

Pasture ecosystems may be particularly vulnerable to land degradation due to the high risk of human disturbance (e.g., overgrazing, burning, etc.), especially when compared with natural ecosystems (non-pasture, non-cultivated) where direct human impacts are minimal. Using maximum annual leaf area index (LAImax) as a proxy for standing biomass and peak annual aboveground productivity, we analyze greening and browning trends in pasture areas from 1982–2008. Inter-annual variability in pasture productivity is strongly controlled by precipitation (positive correlation) and, to a lesser extent, temperature (negative correlation). Linear temporal trends are significant in 23% of pasture cells, with the vast majority of these areas showing positive LAImax trends. Spatially extensive productivity declines are only found in a few regions, most notably central Asia, southwest North America, and southeast Australia. Statistically removing the influence of precipitation reduces LAImax trends by only 13%, suggesting that precipitation trends are only a minor contributor to long-term greening and browning of pasture lands. No significant global relationship was found between LAImax and pasture intensity, although the magnitude of trends did vary between cells classified as natural versus pasture. In the tropics and Southern Hemisphere, the median rate of greening in pasture cells is significantly higher than for cells dominated by natural vegetation. In the Northern Hemisphere extra-tropics, conversely, greening of natural areas is 2–4 times the magnitude of greening in pasture areas. This analysis presents one of the first global assessments of greening and browning trends in global pasture lands, including a comparison with vegetation trends in regions dominated by natural ecosystems. Our results suggest that degradation of pasture lands is not a globally widespread phenomenon and, consistent with much of the terrestrial biosphere, there have been widespread increases in pasture productivity over the last 30 years.

Asynchronous response of tropical forest leaf phenology to seasonal and el Niño-driven drought.

The Hawaiian Islands are an ideal location to study the response of tropical forests to climate variability because of their extreme isolation in the middle of the Pacific, which makes them especially sensitive to El Niño-Southern Oscillation (ENSO). Most research examining the response of tropical forests to drought or El Niño have focused on rainforests, however, tropical dry forests cover a large area of the tropics and may respond very differently than rainforests. We use satellite-derived Normalized Difference Vegetation Index (NDVI) from February 2000-February 2009 to show that rainforests and dry forests in the Hawaiian Islands exhibit asynchronous responses in leaf phenology to seasonal and El Niño-driven drought. Dry forest NDVI was more tightly coupled with precipitation compared to rainforest NDVI. Rainforest cloud frequency was negatively correlated with the degree of asynchronicity (ΔNDVI) between forest types, most strongly at a 1-month lag. Rainforest green-up and dry forest brown-down was particularly apparent during the 2002–003 El Niño. The spatial pattern of NDVI response to the NINO 3.4 Sea Surface Temperature (SST) index during 2002–2003 showed that the leeward side exhibited significant negative correlations to increased SSTs, whereas the windward side exhibited significant positive correlations to increased SSTs, most evident at an 8 to 9-month lag. This study demonstrates that different tropical forest types exhibit asynchronous responses to seasonal and El Niño-driven drought, and suggests that mechanisms controlling dry forest leaf phenology are related to water-limitation, whereas rainforests are more light-limited.

Prioritizing conservation of tropical dry forests in the Pacific

To identify forests of high priority for conservation in tropical dry forests of New Caledonia, Fiji, the Marquesas and Hawaii, we examined patterns of woody plant species richness (total, native and endemic) and threatened species (IUCN categorization and density) at the stand level, using Gentrys transect method. There were associations between total, native and endemic plant species richness in all four Pacific dry forest regions but we found no significant association with the presence or density of species listed on the IUCN Red List. Dry forests in New Caledonia and Hawaii merit the highest conservation priority in the Pacific, based on level of endemism and number of threatened species. The study sites that merit high conservation priority are Metzdorf, Nekoro and Pindai, in New Caledonia, Kokee and Kaupulehu, in Hawaii, and Vatia, in Fiji. New Caledonia and Fiji have a small dry forest extent and protected area extent compared with other dry forests in biodiversity hotspots. Although we identified priority areas for dry forest conservation, more comparative plot data, presence/absence data in fragments and regional geographical data are needed to adequately manage and protect dry forests in the Pacific.

A Dynamic History of Climate Change and Human Impact on the Environment from Keālia Pond, Maui, Hawaiian Islands

High-resolution palynological, charcoal, and sedimentological analysis of a sediment core from Keālia Pond, Maui, coupled with archaeological and historical records, provides a detailed chronology of vegetation and climate change since before human arrival. These records provide new evidence for human–environment linkages during the Hawaiian Polynesian period and subsequent European period. Prior to human arrival, the charcoal record indicates that native forests were subject to natural fires. A shift from dry to wet climate conditions marked the beginning of the Medieval Climate Anomaly (MCA) as evidenced by a precipitation reconstruction based on a pollen abundance index. Charcoal increases around AD 840–1140 signal the presence of Polynesians in the Keālia Pond region, but there is no evidence of rapid and extensive forest clearance immediately after Polynesian arrival. The greatest reduction in pollen diversity at Keālia Pond occurred during the European period (post 1778), at which point the pollen record indicates that montane forest taxa declined, native lowland taxa disappeared from the record, and nonnative taxa Prosopis and Batis made their first appearances. Accounts by early Europeans during the nineteenth and twentieth centuries provide a historical narrative supporting the interpretation that European impacts on vegetation were widespread, whereas in this region of Maui, Polynesian impacts on vegetation appear largely confined to the lowlands.

Phenology and Productivity of C3 and C4 Grasslands in Hawaii

Grasslands account for a large proportion of global terrestrial productivity and play a critical role in carbon and water cycling. Within grasslands, photosynthetic pathway is an important functional trait yielding different rates of productivity along environmental gradients. Recently, C3-C4 sorting along spatial environmental gradients has been reassessed by controlling for confounding traits in phylogenetically structured comparisons. C3 and C4 grasses should sort along temporal environmental gradients as well, resulting in differing phenologies and growing season lengths. Here we use 10 years of satellite data (NDVI) to examine the phenology and greenness (as a proxy for productivity) of C3 and C4 grass habitats, which reflect differences in both environment and plant physiology. We perform phylogenetically structured comparisons based on 3,595 digitized herbarium collections of 152 grass species across the Hawaiian Islands. Our results show that the clade identity of grasses captures differences in their habitats better than photosynthetic pathway. Growing season length (GSL) and associated productivity (GSP) were not significantly different when considering photosynthetic type alone, but were indeed different when considering photosynthetic type nested within clade. The relationship between GSL and GSP differed most strongly between C3 clade habitats, and not between C3-C4 habitats. Our results suggest that accounting for the interaction between phylogeny and photosynthetic pathway can help improve predictions of productivity, as commonly used C3-C4 classifications are very broad and appear to mask important diversity in grassland ecosystem functions.

Long-term increases in tropical flowering activity across growth forms in response to rising CO2 and climate change

Mounting evidence suggests that anthropogenic global change is altering plant species composition in tropical forests. Fewer studies, however, have focused on long-term trends in reproductive activity, in part because of the lack of data from tropical sites. Here, we analyze a 28-year record of tropical flower phenology in response to anthropogenic climate and atmospheric change. We show that a multidecadal increase in flower activity is most strongly associated with rising atmospheric CO2 concentrations using yearly aggregated data. Compared to significant climatic factors, CO2 had on average an approximately three-, four-, or fivefold stronger effect than rainfall, solar radiation, and the Multivariate ENSO Index, respectively. Peaks in flower activity were associated with greater solar radiation and lower rainfall during El Niño years. The effect of atmospheric CO2 on flowering has diminished over the most recent decade for lianas and canopy trees, whereas flowering of midstory trees and shrub species continued to increase with rising CO2 . Increases in flowering were accompanied by a lengthening of flowering duration for canopy and midstory trees. Understory treelets did not show increases in flowering but did show increases in duration. Given that atmospheric CO2 will likely continue to climb over the next century, a long-term increase in flowering activity may persist in some growth forms until checked by nutrient limitation or by climate change through rising temperatures, increasing drought frequency and/or increasing cloudiness and reduced insolation.