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.

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

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

Machine learning predicts large scale declines in native plant phylogenetic diversity.

Though substantial effort has gone into predicting how global climate change will impact biodiversity patterns, the scarcity of taxon-specific information has hampered the efficacy of these endeavors. Further, most studies analyzing spatiotemporal patterns of biodiversity focus narrowly on species richness. We apply machine learning approaches to a comprehensive vascular plant database for the United States and generate predictive models of regional plant taxonomic and phylogenetic diversity in response to a wide range of environmental variables. We demonstrate differences in predicted patterns and potential drivers of native vs nonnative biodiversity. In particular, native phylogenetic diversity is likely to decrease over the next half century despite increases in species richness. We also identify that patterns of taxonomic diversity can be incongruent with those of phylogenetic diversity. The combination of macro-environmental factors that determine diversity likely varies at continental scales; thus, as climate change alters the combinations of these factors across the landscape, the collective effect on regional diversity will also vary. Our study represents one of the most comprehensive examinations of plant diversity patterns to date and demonstrates that our ability to predict future diversity may benefit tremendously from the application of machine learning.

Widespread sampling biases in herbaria revealed from large-scale digitization.

Nonrandom collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras online offer a timely opportunity to assess commonalities and differences in herbarium sampling biases. We determined spatial, temporal, trait, phylogenetic, and collector biases in c. 5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England, USA (NE). We identified numerous shared and unique biases among these regions. Shared biases included specimens collected close to roads and herbaria; specimens collected more frequently during biological spring and summer; specimens of threatened species collected less frequently; and specimens of close relatives collected in similar numbers. Regional differences included overrepresentation of graminoids in SA and AU and of annuals in AU; and peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by very few individuals. We hypothesize that these mega-collectors, with their associated preferences and idiosyncrasies, shaped patterns of collection bias via 'founder effects'. Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.

Herbarium specimens show patterns of fruiting phenology in native and invasive plant species across New England.

PREMISE OF THE STUDY: Patterns of fruiting phenology in temperate ecosystems are poorly understood, despite the ecological importance of fruiting for animal nutrition and seed dispersal. Herbarium specimens represent an under-utilized resource for investigating geographical and climatic factors affecting fruiting times within species, patterns in fruiting times among species, and differences between native and non-native invasive species. METHODS: We examined over 15,000 herbarium specimens, collected and housed across New England, and found 3159 specimens with ripe fruits, collected from 1849-2013. We examined patterns in fruiting phenology among 37 native and 18 invasive woody plant species common to New England. We compared fruiting dates between native and invasive species, and analyzed how fruiting phenology varies with temperature, space, and time. KEY RESULTS: Spring temperature and year explained a small but significant amount of the variation in fruiting dates. Accounting for the moderate phylogenetic signal in fruiting phenology, invasive species fruited 26 days later on average than native species, with significantly greater standard deviations. CONCLUSIONS: Herbarium specimens can be used to detect patterns in fruiting times among species. However, the amount of intraspecific variation in fruiting times explained by temporal, geographic, and climatic predictors is small, due to a combination of low temporal resolution of fruiting specimens and the protracted nature of fruiting. Later fruiting times in invasive species, combined with delays in autumn bird migrations in New England, may increase the likelihood that migratory birds will consume and disperse invasive seeds in New England later into the year.

Patterns and predictors of fleshy fruit phenology at five international botanical gardens.

PREMISE OF THE STUDY: To improve our understanding of the patterns and drivers of fleshy fruit phenology, we examined the sequence, patterns across years and locations, and drivers of fruiting times at five botanical gardens on three continents. METHODS: We monitored four stages of fruit phenology for 406 temperate, fleshy-fruited, woody plant species in 2014 and 2015. KEY RESULTS: Across all gardens, ripe fruits were present from May to March of the following year, with peak fruiting durations ranging from under 1 week to over 150 days. Species-level first fruiting and onset of peak fruiting dates were strongly associated with one another within sites and were more consistent between years and sites than the end of peak fruiting and last fruiting date. The order of fruiting among species between years and gardens was moderately consistent, and both peak fruiting times and fruiting durations were found to be phylogenetically conserved. CONCLUSIONS: The consistent order of fruiting among species between years and locations indicates species-specific phenological responses to environmental conditions. Wide variation in fruiting times across species and in the duration of peak fruiting reinforces the importance of understanding how plant phenology impacts dispersers and monitoring the health and consistency of these interactions.

Global biogeography of seed dormancy is determined by seasonality and seed size: a case study in the legumes.

Seed dormancy is expected to provide ecological advantages by adjusting germination to the favorable growth period. However, many species produce nondormant seeds, particularly in wet tropical forests, a biogeographic pattern that is not well accounted for in current models. We hypothesized that the global distribution of dormant seeds derives from their adaptive value in predictably fluctuating (i.e. seasonal) environments. However, the advantage conferred by dormancy might ultimately depend on other seed attributes, particularly size. This general model was tested within a phylogenetically informed framework using a data set comprising > 216 000 world-wide observations of Fabaceae, spanning three orders of magnitude in seed size and including both dormant and nondormant seeds. Our results confirmed our hypothesis: nondormant seeds can only evolve in climates with long growing seasons and/or in lineages that produce larger seeds. Conversely, dormancy should be evolutionarily stable in temperate lineages with small seeds. When the favorable season is fleeting, seed dormancy is the only adaptive strategy. Based on these results, we predict that, within a given lineage, taxa producing larger, nondormant seeds will necessarily predominate in aseasonal environments, while plants bearing small, dormant seeds will be dominant under short growing seasons.

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.

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.

The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants.

Seed dormancy, by controlling the timing of germination, can strongly affect plant survival. The kind of seed dormancy, therefore, can influence both population and species-level processes such as colonization, adaptation, speciation, and extinction. We used a dataset comprising over 14,000 taxa in 318 families across the seed plants to test hypotheses on the evolution of different kinds of seed dormancy and their association with lineage diversification. We found morphophysiological dormancy to be the most likely ancestral state of seed plants, suggesting that physiologically regulated dormancy in response to environmental cues was present at the origin of seed plants. Additionally, we found that physiological dormancy (PD), once disassociated from morphological dormancy, acted as an 'evolutionary hub' from which other dormancy classes evolved, and that it was associated with higher rates of lineage diversification via higher speciation rates. The environmental sensitivity provided by dormancy in general, and by PD in particular, appears to be a key trait in the diversification of seed plants.

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.

Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy.

Leaf out phenology affects a wide variety of ecosystem processes and ecological interactions and will take on added significance as leaf out times increasingly shift in response to warming temperatures associated with climate change. There is, however, relatively little information available on the factors affecting species differences in leaf out phenology. An international team of researchers from eight Northern Hemisphere temperate botanical gardens recorded leaf out dates of c. 1600 woody species in 2011 and 2012. Leaf out dates in woody species differed by as much as 3 months at a single site and exhibited strong phylogenetic and anatomical relationships. On average, angiosperms leafed out earlier than gymnosperms, deciduous species earlier than evergreen species, shrubs earlier than trees, diffuse and semi-ring porous species earlier than ring porous species, and species with smaller diameter xylem vessels earlier than species with larger diameter vessels. The order of species leaf out was generally consistent between years and among sites. As species distribution and abundance shift due to climate change, interspecific differences in leaf out phenology may affect ecosystem processes such as carbon, water, and nutrient cycling. Our open access leaf out data provide a critical framework for monitoring and modelling such changes going forward.

Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change.

PREMISE OF THE STUDY: The study of how phenology may contribute to the assembly of plant communities has a long history in ecology. Climate change has brought renewed interest in this area, with many studies examining how phenology may contribute to the success of exotic species. In particular, there is increasing evidence that exotic species occupy unique phenological niches and track climate change more closely than native species. METHODS: Here, we use long-term records of species' first flowering dates from fi ve northern hemisphere temperate sites (Chinnor, UK and in the United States, Concord, Massachusetts; Fargo, North Dakota; Konza Prairie, Kansas; and Washington,D.C.) to examine whether invaders have distinct phenologies. Using a broad phylogenetic framework, we tested for differences between exotic and native species in mean annual flowering time, phenological changes in response to temperature and precipitation,and longer-term shifts in first flowering dates during recent pronounced climate change ("flowering time shifts"). KEY RESULTS: Across North American sites, exotic species have shifted flowering with climate change while native species, on average, have not. In the three mesic systems, exotic species exhibited higher tracking of interannual variation in temperature,such that flowering advances more with warming, than native species. Across the two grassland systems, however, exotic species differed from native species primarily in responses to precipitation and soil moisture, not temperature. CONCLUSIONS: Our findings provide cross-site support for the role of phenology and climate change in explaining species' invasions.Further, they support recent evidence that exotic species may be important drivers of extended growing seasons observed with climate change in North America.

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 approximately 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 Thoreau's woods.

Widespread homogenization of plant communities in the Anthropocene.

Native biodiversity decline and non-native species spread are major features of the Anthropocene. Both processes can drive biotic homogenization by reducing trait and phylogenetic differences in species assemblages between regions, thus diminishing the regional distinctiveness of biotas and likely have negative impacts on key ecosystem functions. However, a global assessment of this phenomenon is lacking. Here, using a dataset of >200,000 plant species, we demonstrate widespread and temporal decreases in species and phylogenetic turnover across grain sizes and spatial extents. The extent of homogenization within major biomes is pronounced and is overwhelmingly explained by non-native species naturalizations. Asia and North America are major sources of non-native species; however, the species they export tend to be phylogenetically close to recipient floras. Australia, the Pacific and Europe, in contrast, contribute fewer species to the global pool of non-natives, but represent a disproportionate amount of phylogenetic diversity. The timeline of most naturalisations coincides with widespread human migration within the last ~500 years, and demonstrates the profound influence humans exert on regional biotas beyond changes in species richness.

Phenology models using herbarium specimens are only slightly improved by using finer-scale stages of reproduction.

PREMISE OF THE STUDY: Herbarium specimens are increasingly used to study reproductive phenology. Here, we ask whether classifying reproduction into progressively finer-scale stages improves our understanding of the relationship between climate and reproductive phenology. METHODS: We evaluated Acer rubrum herbarium specimens across eastern North America, classifying them into eight reproductive phenophases and four stages of leaf development. We fit models with different reproductive phenology categorization schemes (from detailed to broad) and compared model fits and coefficients describing temperature, elevation, and year effects. We fit similar models to leaf phenology data to compare reproductive to leafing phenology. RESULTS: Finer-scale reproductive phenophases improved model fits and provided more precise estimates of reproductive phenology. However, models with fewer reproductive phenophases led to similar qualitative conclusions, demonstrating that A. rubrum reproduces earlier in warmer locations, lower elevations, and in recent years, as well as that leafing phenology is less strongly influenced by temperature than is reproductive phenology. DISCUSSION: Our study suggests that detailed information on reproductive phenology provides a fuller understanding of potential climate change effects on flowering, fruiting, and leaf-out. However, classification schemes with fewer reproductive phenophases provided many similar insights and may be preferable in cases where resources are limited.

Digitization protocol for scoring reproductive phenology from herbarium specimens of seed plants.

PREMISE OF THE STUDY: Herbarium specimens provide a robust record of historical plant phenology (the timing of seasonal events such as flowering or fruiting). However, the difficulty of aggregating phenological data from specimens arises from a lack of standardized scoring methods and definitions for phenological states across the collections community. METHODS AND RESULTS: To address this problem, we report on a consensus reached by an iDigBio working group of curators, researchers, and data standards experts regarding an efficient scoring protocol and a data-sharing protocol for reproductive traits available from herbarium specimens of seed plants. The phenological data sets generated can be shared via Darwin Core Archives using the Extended MeasurementOrFact extension. CONCLUSIONS: Our hope is that curators and others interested in collecting phenological trait data from specimens will use the recommendations presented here in current and future scoring efforts. New tools for scoring specimens are reviewed.

Antagonistic multilevel selection on size and architecture in variable density settings.

In some ecological settings, an individual's fitness depends on both its own phenotype (individual-level selection) as well as the phenotype of the individuals with which it interacts (group-level selection). Using contextual analysis to measure multilevel selection in experimental stands of Arabidopsis thaliana, we detected significant linear selection that reversed across individual versus group levels for two composite phenotypic traits, "size" and "elongation." In both cases, selection at the individual level acted to increase values of these traits, presumably due to their positive effect on resource acquisition. Group selection favored decreased values of the same traits. Nonlinear selection was weak but significant in several cases, including stabilizing selection on developmental rate; individuals with very rapid development likely had lower than average fitness due to their reduced resource level at reproduction, while very delayed reproduction may have resulted in lower fitness if prolonged competition for resources reduced overall environmental quality and fitness of all individuals in a group. Under this scenario, stabilizing selection on individual traits is evidence of selection at the group level. Significant density-dependent selection suggests that a threshold density must be reached before group selection acts. Below this threshold, selection at the individual level affects phenotypic evolution more strongly than group selection. A second experiment measured multilevel selection in progeny stands of the original experimental plants. Multilevel selection again acted antagonistically on a composite trait that included size and elongation as well as on an architectural trait, branch production. The magnitude of individual versus group selection was relatively similar in the progeny generation, and the observed balance of individual versus group selection across densities is generally consistent with the hypotheses that multilevel selection can contribute to phenotypic evolution and to important demographic phenomena, including soft selection and the "law of constant yield."

Phylogenetic conservatism and trait correlates of spring phenological responses to climate change in northeast China.

Climate change has resulted in major changes in plant phenology across the globe that includes leaf-out date and flowering time. The ability of species to respond to climate change, in part, depends on their response to climate as a phenological cue in general. Species that are not phenologically responsive may suffer in the face of continued climate change. Comparative studies of phenology have found phylogeny to be a reliable predictor of mean leaf-out date and flowering time at both the local and global scales. This is less true for flowering time response (i.e., the correlation between phenological timing and climate factors), while no study to date has explored whether the response of leaf-out date to climate factors exhibits phylogenetic signal. We used a 52-year observational phenological dataset for 52 woody species from the Forest Botanical Garden of Heilongjiang Province, China, to test phylogenetic signal in leaf-out date and flowering time, as well as, the response of these two phenological traits to both temperature and winter precipitation. Leaf-out date and flowering time were significantly responsive to temperature for most species, advancing, on average, 3.11 and 2.87 day/°C, respectively. Both leaf-out and flowering, and their responses to temperature exhibited significant phylogenetic signals. The response of leaf-out date to precipitation exhibited no phylogenetic signal, while flowering time response to precipitation did. Native species tended to have a weaker flowering response to temperature than non-native species. Earlier leaf-out species tended to have a greater response to winter precipitation. This study is the first to assess phylogenetic signal of leaf-out response to climate change, which suggests, that climate change has the potential to shape the plant communities, not only through flowering sensitivity, but also through leaf-out sensitivity.

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.