Charles G. Willis

Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change

Climate change has led to major changes in the phenology (the timing of seasonal activities, such as flowering) of some species but not others. The extent to which flowering-time response to temperature is shared among closely related species might have important consequences for community-wide patterns of species loss under rapid climate change. Henry David Thoreau initiated a dataset of the Concord, Massachusetts, flora that spans ≈150 years and provides information on changes in species abundance and flowering time. When these data are analyzed in a phylogenetic context, they indicate that change in abundance is strongly correlated with flowering-time response. Species that do not respond to temperature have decreased greatly in abundance, and include among others anemones and buttercups [Ranunculaceae pro parte (p.p.)], asters and campanulas (Asterales), bluets (Rubiaceae p.p.), bladderworts (Lentibulariaceae), dogwoods (Cornaceae), lilies (Liliales), mints (Lamiaceae p.p.), orchids (Orchidaceae), roses (Rosaceae p.p.), saxifrages (Saxifragales), and violets (Malpighiales). Because flowering-time response traits are shared among closely related species, our findings suggest that climate change has affected and will likely continue to shape the phylogenetically biased pattern of species loss in Thoreaus woods.

Favorable climate change response explains non-native species' success in Thoreau's woods.

Invasive species have tremendous detrimental ecological and economic impacts. Climate change may exacerbate species invasions across communities if non-native species are better able to respond to climate changes than native species. Recent evidence indicates that species that respond to climate change by adjusting their phenology (i.e., the timing of seasonal activities, such as flowering) have historically increased in abundance. The extent to which non-native species success is similarly linked to a favorable climate change response, however, remains untested. We analyzed a dataset initiated by the conservationist Henry David Thoreau that documents the long-term phenological response of native and non-native plant species over the last 150 years from Concord, Massachusetts (USA). Our results demonstrate that non-native species, and invasive species in particular, have been far better able to respond to recent climate change by adjusting their flowering time. This demonstrates that climate change has likely played, and may continue to play, an important role in facilitating non-native species naturalization and invasion at the community level.

Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species’ phenological cueing mechanisms

PREMISE OF THE STUDY Climate change has resulted in major changes in the phenology of some species but not others. Long-term field observational records provide the best assessment of these changes, but geographic and taxonomic biases limit their utility. Plant specimens in herbaria have been hypothesized to provide a wealth of additional data for studying phenological responses to climatic change. However, no study to our knowledge has comprehensively addressed whether herbarium data are accurate measures of phenological response and thus applicable to addressing such questions. METHODS We compared flowering phenology determined from field observations (years 1852-1858, 1875, 1878-1908, 2003-2006, 2011-2013) and herbarium records (1852-2013) of 20 species from New England, United States. KEY RESULTS Earliest flowering date estimated from herbarium records faithfully reflected field observations of first flowering date and substantially increased the sampling range across climatic conditions. Additionally, although most species demonstrated a response to interannual temperature variation, long-term temporal changes in phenological response were not detectable. CONCLUSIONS Our findings support the use of herbarium records for understanding plant phenological responses to changes in temperature, and also importantly establish a new use of herbarium collections: inferring primary phenological cueing mechanisms of individual species (e.g., temperature, winter chilling, photoperiod). These latter data are lacking from most investigations of phenological change, but are vital for understanding differential responses of individual species to ongoing climate change.

Old Plants, New Tricks: Phenological Research Using Herbarium Specimens

The timing of phenological events, such as leaf-out and flowering, strongly influence plant success and their study is vital to understanding how plants will respond to climate change. Phenological research, however, is often limited by the temporal, geographic, or phylogenetic scope of available data. Hundreds of millions of plant specimens in herbaria worldwide offer a potential solution to this problem, especially as digitization efforts drastically improve access to collections. Herbarium specimens represent snapshots of phenological events and have been reliably used to characterize phenological responses to climate. We review the current state of herbarium-based phenological research, identify potential biases and limitations in the collection, digitization, and interpretation of specimen data, and discuss future opportunities for phenological investigations using herbarium specimens.

Genetic variation in tolerance of competition and neighbour suppression in Arabidopsis thaliana.

Intraspecific competitive interactions can profoundly influence phenotypic evolution. However, prior studies have rarely evaluated the evolutionary potential of the two components of competitive ability, tolerance of competition and suppression of neighbours. Here, we grow a set of 20 Arabidopsis thaliana recombinant inbred lines in three competitive treatments (noncompetitive, intra‐genotypic competition and inter‐genotypic competition) to examine if there is genetic variation for the components of competitive ability and whether neighbour relatedness has an effect on fitness. We find evidence for genetic variation in tolerance of competition and neighbour suppression and that these two competitive strategies are correlated, such that genotypes that tolerate competition will also strongly suppress neighbours. We further observe that the effect of neighbour relatedness on fitness of target individuals depends on neighbour identity, i.e. whether target individuals perform better when competing against self vs. nonself individuals depends on the genotypic identity of the nonself neighbour. The results are particularly relevant to evolutionary responses under multi‐level selection.

Diversification and the evolution of dispersal ability in the tribe Brassiceae (Brassicaceae)

BACKGROUND AND AIMS Dispersal and establishment ability can influence evolutionary processes such as geographic isolation, adaptive divergence and extinction probability. Through these population-level dynamics, dispersal ability may also influence macro-evolutionary processes such as species distributions and diversification. This study examined patterns of evolution of dispersal-related fruit traits, and how the evolution of these traits is correlated with shifts in geographic range size, habitat and diversification rates in the tribe Brassiceae (Brassicaceae). METHODS The phylogenetic analysis included 72 taxa sampled from across the Brassiceae and included both nuclear and chloroplast markers. Dispersal-related fruit characters were scored and climate information for each taxon was retrieved from a database. Correlations between fruit traits, seed characters, habitat, range and climate were determined, together with trait-dependent diversification rates. KEY RESULTS It was found that the evolution of traits associated with limited dispersal evolved only in association with compensatory traits that increase dispersal ability. The evolution of increased dispersal ability occurred in multiple ways through the correlated evolution of different combinations of fruit traits. The evolution of traits that increase dispersal ability was in turn associated with larger seed size, increased geographic range size and higher diversification rates. CONCLUSIONS This study provides evidence that the evolution of increased dispersal ability and larger seed size, which may increase establishment ability, can also influence macro-evolutionary processes, possibly by increasing the propensity for long-distance dispersal. In particular, it may increase speciation and consequent diversification rates by increasing the likelihood of geographic and thereby reproductive isolation.

The community‐level effect of light on germination timing in relation to seed mass: a source of regeneration niche differentiation

Within a community, species may germinate at different times so as to mitigate competition and to take advantage of different aspects of the seasonal environment (temporal niche differentiation). We illustrated a hypothesis of the combined effects of abiotic and biotic competitive factors on germination timing and the subsequent upscale effects on community assembly. We estimated the germination timing (GT) for 476 angiosperm species of the eastern Tibetan Plateau grasslands under two light treatments in the field: high (i.e. natural) light and low light. We also measured the shift in germination timing (SGT) across treatments for all species. Furthermore, we used phylogenetic comparative methods to test if GT and SGT were associated with seed mass, an important factor in competitive interactions. We found a significant positive correlation between GT and seed mass in both light treatments. Additionally, small seeds (early germinating seeds) tended to germinate later and large seeds (late germinating seeds) tended to germinate earlier under low light vs high light conditions. Low light availability can reduce temporal niche differentiation by increasing the overlap in germination time between small and large seeds. In turn, reduced temporal niche differentiation may increase competition in the process of community assembly.

CrowdCurio: an online crowdsourcing platform to facilitate climate change studies using herbarium specimens

Phenology is a key aspect of plant success. Recent research has demonstrated that herbarium specimens can provide important information on plant phenology. Massive digitization efforts have the potential to greatly expand herbarium-based phenological research, but also pose a serious challenge regarding efficient data collection. Here, we introduce CrowdCurio, a crowdsourcing tool for the collection of phenological data from herbarium specimens. We test its utility by having workers collect phenological data (number of flower buds, open flowers and fruits) from specimens of two common New England (USA) species: Chelidonium majus and Vaccinium angustifolium. We assess the reliability of using nonexpert workers (i.e. Amazon Mechanical Turk) against expert workers. We also use these data to estimate the phenological sensitivity to temperature for both species across multiple phenophases. We found no difference in the data quality of nonexperts and experts. Nonexperts, however, were a more efficient way of collecting more data at lower cost. We also found that phenological sensitivity varied across both species and phenophases. Our study demonstrates the utility of CrowdCurio as a crowdsourcing tool for the collection of phenological data from herbarium specimens. Furthermore, our results highlight the insight gained from collecting large amounts of phenological data to estimate multiple phenophases.

The establishment of Central American migratory corridors and the biogeographic origins of seasonally dry tropical forests in Mexico.

Biogeography and community ecology can mutually illuminate the formation of a regional species pool or biome. Here, we apply phylogenetic methods to a large and diverse plant clade, Malpighiaceae, to characterize the formation of its species pool in Mexico, and its occupancy of the seasonally dry tropical forest (SDTF) biome that occurs there. We find that the ~162 species of Mexican Malpighiaceae represent ~33 dispersals from South America beginning in the Eocene and continuing until the Pliocene (~46.4–3.8 Myr). Furthermore, dispersal rates between South America and Mexico show a significant six-fold increase during the mid-Miocene (~23.9 Myr). We hypothesize that this increase marked the availability of Central America as an important corridor for Neotropical plant migration. We additionally demonstrate that this high rate of dispersal contributed substantially more to the phylogenetic diversity of Malpighiaceae in Mexico than in situ diversification. Finally, we show that most lineages arrived in Mexico pre-adapted with regard to one key SDTF trait, total annual precipitation. In contrast, these lineages adapted to a second key trait, precipitation seasonality, in situ as mountain building in the region gave rise to the abiotic parameters of extant SDTF. The timing of this in situ adaptation to seasonal precipitation suggests that SDTF likely originated its modern characteristics by the late Oligocene, but was geographically more restricted until its expansion in the mid-Miocene. These results highlight the complex interplay of dispersal, adaptation, and in situ diversification in the formation of tropical biomes. Our results additionally demonstrate that these processes are not static, and their relevance can change markedly over evolutionary time. This has important implications for understanding the origin of SDTF in Mexico, but also for understanding the temporal and spatial origin of biomes and regional species pools more broadly.

WALDEN: multi-surface multi-touch simulation of climate change and species loss in thoreau's woods

We present a case study of an interactive, multiple heterogeneous-display, multi-touch visualization for informal science education. Our visual simulation application, called WALDEN, has been developed using a Microsoft Surface and a large data wall. Multiple displays offer users the opportunity to interact with large visual datasets and observe complex visual simulations. We discuss the design of our system, findings from our case study, the shortcomings it revealed and how we plan to address them.