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Abstract

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.

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... To overcome the sparsity of long-term and spatially widespread phenology datasets, scientists have been developing innovative new methods (Cleland et al. 2007). For example, herbarium specimens are increasingly used to recreate long-term phenology observations of flowering, leaf out, and fruiting over the past 100-150 years and over broad geographical regions (Primack et al. 2004;Willis et al. 2017). Meanwhile, directed citizen science initiatives and community biodiversity data repositories such as iNaturalist are providing new sources of phenology data covering broad geographic regions (iNaturalist, 2021). ...
... These various phenology data sources come along with advantages and limitations for climate change research (Davis et al., 2015;Willis et al. 2017;Taylor et al. 2019;Funk 2018;Belitz et al. 2020). Most notably, herbarium specimens and citizen science networks include biases in sampling locations, taxonomic groups, and gaps in sampling years over time (Delisle et al. 2003;Daru et al. 2018;Panchen et al. 2019). ...
... Citizen science networks, in particular, have the potential to provide enormous numbers of phenological observations over huge geographic areas, filling in gaps not covered by herbarium specimens (Willis et al. 2017). With limited training, citizen scientists of a wide range of backgrounds can provide reliable phenology observations (Fuccillo Battle et al. 2014;Bison et al. 2019), including observations on private lands which would otherwise be inaccessible to researchers (Putman et al. 2021). ...
Article
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Phenology has emerged as a key metric to measure how species respond to changes in climate. Innovative means have been developed to extend the temporal and spatial range of phenological data by obtaining data from herbarium specimens, citizen science programs, and biodiversity data repositories. These different data types have seldom been compared for their effectiveness in detecting environmental impacts on phenology. To address this, we compare three separate phenology datasets from Denmark: (i) herbarium specimen data spanning 145 years, (ii) data collected from a citizen science phenology program over a single year observing first flowering, and (iii) data derived from incidental biodiversity observations in iNaturalist over a single year. Each dataset includes flowering day of year observed for three common spring-flowering plant species: Allium ursinum (ramsons), Aesculus hippocastanum (horse chestnut), and Sambucus nigra (black elderberry). The incidental iNaturalist dataset provided the most extensive geographic coverage across Denmark and the largest sample size and recorded peak flowering in a way comparable to herbarium specimens. The directed citizen science dataset recorded much earlier flowering dates because the program objective was to report the first flowering, and so was less compared to the other two datasets. Herbarium data demonstrated the strongest effect of spring temperature on flowering in Denmark, possibly because it was the only dataset measuring temporal variation in phenology, while the other datasets measured spatial variation. Herbarium data predicted the mean flowering day of year recorded in our iNaturalist dataset for all three species. Combining herbarium data with iNaturalist data provides an even more effective method for detecting climatic effects on phenology. Phenology observations from directed and incidental citizen science initiatives will increase in value for climate change research in the coming years with the addition of data capturing the inter-annual variation in phenology.
... Plant phenology mediates complex species interactions (e.g., plant-plant, plant-herbivore, plant-pollinator; [3][4][5]); therefore, climate change-induced disruptions to plant phenology may have cascading effects on the functions and persistence of ecosystems. While previous studies have documented a wide range of phenological responses to climate and climate change [6,7], our understanding of these responses in many taxa and ecosystems remains incomplete. This gap limits our ability to make broad scale predictions of the ecosystem-wide impacts from climate change [8,9]. ...
... Natural history collections, such as herbarium specimens, provide a long temporal record of phenology for hundreds of thousands of taxa globally and offer a data-rich resource with which to fill this gap [6]. Moreover, herbarium specimens can be used to track phenological responses to climate and climate change [10][11][12]. ...
... Herbarium specimens have recently emerged as reliable sources with which to detect and track phenological change through time [6,7,11]. As such, older specimens, specifically those collected before the onset of contemporary climate change, are critical for these types of studies. ...
Article
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Machine learning (ML) can accelerate the extraction of phenological data from herbarium specimens; however, no studies have assessed whether ML-derived phenological data can be used reliably to evaluate ecological patterns. In this study, 709 herbarium specimens representing a widespread annual herb, Streptanthus tortuosus, were scored both manually by human observers and by a mask R-CNN object detection model to (1) evaluate the concordance between ML and manually-derived phenological data and (2) determine whether ML-derived data can be used to reliably assess phenological patterns. The ML model generally underestimated the number of reproductive structures present on each specimen; however, when these counts were used to provide a quantitative estimate of the phenological stage of plants on a given sheet (i.e., the phenological index or PI), the ML and manually-derived PI’s were highly concordant. Moreover, herbarium specimen age had no effect on the estimated PI of a given sheet. Finally, including ML-derived PIs as predictor variables in phenological models produced estimates of the phenological sensitivity of this species to climate, temporal shifts in flowering time, and the rate of phenological progression that are indistinguishable from those produced by models based on data provided by human observers. This study demonstrates that phenological data extracted using machine learning can be used reliably to estimate the phenological stage of herbarium specimens and to detect phenological patterns.
... Plant phenology (i.e. the seasonal timing of life-history events such as flowering and leaf-out) is a key determinant of plant success and ecosystem productivity (Willis et al. 2017). Changes in the timing of phenological events are among the most important indicators of global warming (Parmesan and Yohe 2003). ...
... For plants, altered phenology may result in temporal mismatch and reduced complementarity between species, modifying interspecific competition for resources or plant pollination success (Smith et al. 2012). Failure in pollination reduces fruit set and causes great alterations in trophic chains (Amano et al. 2010) causing a decay at the community level, and the lost, in the worst scenario, of ecological niche for many species (Willis et al. 2017). ...
Chapter
Sierra NevadaSierra Nevada, comprising 2348 vascular floraFlora taxa (including 95 endemic taxa) is considered one of the most important plant hotspotsHot-spot within the Mediterranean region. Sierra NevadaSierra Nevada presents 362 taxa inhabiting the alpine area (ca. 242 km2), 75 endemic species (62 endemic plus 13 sub-endemic) among them, constituting ca. 79% of the endemismEndemism of the entire area. This high-mountain has preserved many species, allowing the current presence of many artic-alpine species, including twelve cold-adapted species with their southernmost limit here. There are 23 nano-hotspotsHot-spot, most of them occurring at the highest altitude, at the coldest parts. Altogether, they host 30% of the Baetic endemic floraFlora in just 0.07% of the area. Plant communities are also original, and they are composed of a mixture of Alpine and Mediterranean species. Climate changeClimate changeisClimate strongly impacting alpine biota leading to an adaptationAdaptation to the new conditions. When this adaptationAdaptation capacity is overcome species are forced to migrate to avoid extinction. Some responses are already noticeable in alpine areas, such as: phenological changes, altitudinal movements, increasing competitionCompetitionand hybridizationHybridization, and changes in plant assemblages. Direct impact related to human activities such as livestock grazing, use of fire to manage alpine pasturelands, mountain agriculture, outdoor activities, and infrastructure construction have additive effects toClimateclimate changeClimate change, and altogether they can exacerbate negative changes. Monitoring, evaluating, and understanding the effect of global changeGlobal change in the Mediterranean mountains is a top priority. We offer guidelines to orient the conservationConservation agenda at Sierra NevadaSierra Nevada: To (i) establish an early warning indicators system, (ii) preserve plant species and habitats, (iii) preserve threatened plant species ex situ, (iv) promote adaptive managementAdaptive management measures, (v) evaluate outdoor recreation activities, and (vi) control and regulate activities.
... Museum specimens represent another source of quantitative natural history data. Such specimens generally include information about the dates and locations where they were collected, although the location information can vary in its resolution (e.g., latitude and longitude, town, or county; Willis et al. 2017). The presence of physical specimens largely eliminates uncertainty around species identification and preserves morphological, phenological, and other traits that naturalists may not typically note when making field observations. ...
... The presence of physical specimens largely eliminates uncertainty around species identification and preserves morphological, phenological, and other traits that naturalists may not typically note when making field observations. Museum collections, however, frequently contain certain sampling biases-for example, overrepresentation of particular species, locations, seasons, and years preferred by the most active collectors (Daru et al. 2018, Willis et al. 2017). These biases can reduce the utility of museum specimens for answering certain questions that require more precision or other information (e.g., fine-scale shifts in ranges or changes in population sizes), but the abundance of herbarium specimens and the strengths of their rigor and accuracy, for example, make them excellent tools for assessing changes in plant anatomy and flowering, leafing, and fruiting phenology. ...
Article
Ecologists are increasingly combining historical observations made by naturalists with modern observations to detect the ecological effects of climate change. This use of historical observations raises the following question: How do we know that historical data are appropriate to use to answer current ecological questions? In the present article, we address this question for environmental philosopher Henry David Thoreau, author of Walden. Should we trust his observations? We qualitatively and quantitatively evaluate Thoreau's observations using a three-step framework: We assess the rigor, accuracy, and utility of his observations to investigate changes in plants and animals over time. We conclude that Thoreau was an accurate observer of nature and a reliable scientist. More importantly, we describe how this simple three-step approach could be used to assess the accuracy of other scientists and naturalists.
... Herbaria contain plant specimens that have been collected, preserved, and documented for future use. They are the foundation of systematic botanical research and are essential for various studies, including those on plant taxonomy, species variability, extinction risk, and phenology (Bebber et al., 2010;Besnard et al., 2018;Willis et al., 2017). The current estimate of specimens in natural history collections (NHCs) is 2-3 billion (Carranza-Rojas et al., 2017a). ...
... Despite its importance in phenological studies (Willis et al., 2017), segmentation of specimen organs such as seeds, fruits, flowers, and leaves, is still a challenging task Goëau et al., 2020). Due to the pressing and drying process, these organs have lost their natural structures and appearance and therefore present a challenge even for the current state-of-the-art deep learning models (Pearson et al., 2020). ...
Article
Herbaria contain the treasure of millions of specimens that have been preserved for several years for scientific studies. To increase the rate of scientific discoveries, digitization of these specimens is currently ongoing to facilitate the easy access and sharing of data to a wider scientific community. Online digital repositories such as Integrated Digitized Biocollection and the Global Biodiversity Information Facility have already accumulated millions of specimen images yet to be explored. This presents the perfect time to take advantage of the opportunity to automate the identification process and increase the rate of novel discoveries using computer vision (CV) and machine learning (ML) techniques. In this study, a systematic literature review of more than 70 peer-reviewed publications was conducted focusing on the application of computer vision and machine learning techniques to digitized herbarium specimens. The study categorizes the different techniques and applications that are commonly used for digitized herbarium specimens and highlights existing challenges together with their potential solutions. We hope this study will serve as a firm foundation for new researchers in the relevant disciplines and will also be enlightening to both computer science and ecology experts.
... To explore the mechanisms underlying regional and global patterns of vegetative and reproductive phenology, findings from remote sensing should be supported by speciesspecific observations. Herbarium specimens, collected around the world and increasingly accessible online, can add information about the timing of many plant phenological events, including leaf-out, flowering, fruiting, and leaf senescence, across time and phylogeny (Willis et al., 2017a;Meineke et al., 2019). Information from this geographical perspective, combined with physiological and growth chamber studies, can be used to develop mechanistic models to better understand the processes underlying these patterns (Chuine, 2000;Gauzere et al., 2017;Asse et al., 2020). ...
... Funds, research efforts, and the expansion of existing networks should aim to fill these geographical gaps. At the same time, digitized herbarium specimens from around the world are increasingly allowing researchers to expand global coverage of species-specific phenology observations, especially in the tropics (Willis et al., 2017a). ...
Article
Plant phenology research has surged in recent decades, in part due to interest in phenological sensitivity to climate change and the vital role phenology plays in ecology. Many local‐scale studies have generated important findings regarding the physiology, responses, and risks associated with shifts in plant phenology. By comparison, our understanding of regional‐ and global‐scale phenology has been largely limited to remote sensing of green‐up without the ability to differentiate among plant species. However, a new generation of analytical tools and data sources—including enhanced remote sensing products, digitized herbarium specimen data, and public participation in science—now permits investigating patterns and drivers of phenology across extensive taxonomic, temporal, and spatial scales, in an emerging field that we call macrophenology. Recent studies have highlighted how phenology affects dynamics at broad scales, including species interactions and ranges, carbon fluxes, and climate. At the cusp of this developing field of study, we review the theoretical and practical advances in four primary areas of plant macrophenology: (1) global patterns and shifts in plant phenology, (2) within‐species changes in phenology as they mediate species' range limits and invasions at the regional scale, (3) broad‐scale variation in phenology among species leading to ecological mismatches, and (4) interactions between phenology and global ecosystem processes. To stimulate future research, we describe opportunities for macrophenology to address grand challenges in each of these research areas, as well as recently available data sources that enhance and enable macrophenology research.
... Dyrmann et al., 2021;Kotowska et al., 2021). Photos are a type of legacy remote sensing data that allow scientists to test for global environmental change effects (sensu Vellend et al., 2013), just as herbarium specimens, resurveyed vegetation plots and land survey records (De Frenne, 2015; reviewed by Vellend et al., 2013;Willis et al., 2017). ...
Article
Global change is causing ecosystems to change at unprecedented rates and the urgency to quantify ecological change is high. We therefore need all possible sources of ecological data to address key knowledge gaps. Ground‐based photos are a form of remote sensing and an unconventional data source with a high potential to improve our understanding of ecological change. They can provide invaluable information on ecological conditions in the past and present at relevant spatiotemporal scales that is very difficult to obtain with other approaches. Here we review the use of ground‐based photos in a set of relevant ecological research topics, such as biodiversity and community ecology, phenology, global change ecology and landscape ecology. We highlight three main photo‐based methods in ecological research (repeat photography, time‐lapse photography and public archives), alongside which we discuss three case studies to demonstrate novel applications of these methods, to answer fundamental ecological questions. Synthesis: Photos can significantly support ecological research to improve our understanding of biotic responses in a rapidly changing world. Photos cover relatively large temporal and spatial scales, and can provide large amounts of information with limited time investment. To exploit their full potential, we need to invest not only in technological advances to compile, process and analyze images but also in proper data management.
... Image processing in combination with artificial intelligence methods has been proposed to address different issues of natural history digitization projects, such as: identification of nomenclatural type specimens [33], morphological analysis [11,37], specimen identification [6,13], identification of the elements present in a specimen image [35,36], automated information extraction [16], phenological research [38] and phenotype studies [19,30]. Some methods are specifically designed to take advantage of the large quantities of image Fig. 1a, from NHM Data Portal [22]. ...
Article
Full-text available
Semantic segmentation has been proposed as a tool to accelerate the processing of natural history collection images. However, developing a flexible and resilient segmentation network requires an approach for adaptation which allows processing different datasets with minimal training and validation. This paper presents a cross-validation approach designed to determine whether a semantic segmentation network possesses the flexibility required for application across different collections and institutions. Consequently, the specific objectives of cross-validating the semantic segmentation network are to (a) evaluate the effectiveness of the network for segmenting image sets derived from collections different from the one in which the network was initially trained on; and (b) test the adaptability of the segmentation network for use in other types of collections. The resilience to data variations from different institutions and the portability of the network across different types of collections are required to confirm its general applicability. The proposed validation method is tested on the Natural History Museum semantic segmentation network, designed to process entomological microscope slides. The proposed semantic segmentation network is evaluated through a series of cross-validation experiments designed to test using data from two types of collections: microscope slides (from three institutions) and herbarium sheets (from seven institutions). The main contribution of this work is the method, software and ground truth sets created for this cross-validation as they can be reused in testing similar segmentation proposals in the context of digitization of natural history collections. The cross-validation of segmentation methods should be a required step in the integration of such methods into image processing workflows for natural history collections.
... The recent and massive digitization of natural history collections, particularly of herbaria, offers new material available for many research activities [16][17][18] such as the analysis of plant species morphology and diversity [19,20]. Because most of the collections are dated and geolocated, they constitute a valuable source of information for (i) determining the proven or potential distribution areas of species [21][22][23], whether native or exotic (dynamics of biological invasions), with direct applications in conservation biology [24], and for (ii) determining the reproductive phenological patterns of species (e.g., date and duration of flowering and fruiting periods) [25][26][27][28]. ...
Article
Full-text available
A better knowledge of tree vegetative growth phenology and its relationship to environmental variables is crucial to understanding forest growth dynamics and how climate change may affect it. Less studied than reproductive structures, vegetative growth phenology focuses primarily on the analysis of growing shoots, from buds to leaf fall. In temperate regions, low winter temperatures impose a cessation of vegetative growth shoots and lead to a well-known annual growth cycle pattern for most species. The humid tropics, on the other hand, have less seasonality and contain many more tree species, leading to a diversity of patterns that is still poorly known and understood. The work in this study aims to advance knowledge in this area, focusing specifically on herbarium scans, as herbariums offer the promise of tracking phenology over long periods of time. However, such a study requires a large number of shoots to be able to draw statistically relevant conclusions. We propose to investigate the extent to which the use of deep learning can help detect and type-classify these relatively rare vegetative structures in herbarium collections. Our results demonstrate the relevance of using herbarium data in vegetative phenology research as well as the potential of deep learning approaches for growing shoot detection.
... Over the past decade, several types of research applied to DHS images have concentrated on an individual phenological event, most generally the flowering time, to study climate change [23]. However, few researchers have simultaneously studied various reproductive organs (such as counting flower buds, young fruits, and mature fruits) and determining how different phenological events are related [24]. ...
Chapter
Full-text available
Phenology is an important factor in studying climate change’s effect on plant growth. Recent studies on herbarium specimens have afforded valuable information on plant phenology. The initiatives of herbaria to digitize their collections can extend plant phenological research rapidly by providing online access to significant collections of digitized specimen images. However, they present a major outstanding challenge when extracting reliable data from the specimen sheets. To effectively detect the presence/absence of the reproductive organs such as buds, flowers, and fruits from the specimen images, we developed PhenoDeep, a deep learning approach based on the refined Mask Scoring R-CNN approach. The Mask Scoring R-CNN backbone network was modified by exploiting the advantages of combining ResNet and DenseNet architectures. The experimental results indicate that PhenoDeep can segment the reproductive organs within different specimens, where the precision of PhenoDeep reached 94.1% and recall 94.3%.
... With many herbaria dating back to some 200 yr, and hundreds of millions of specimens worldwide, herbaria are a tremendous treasure for studying phenology changes both long term and large scale. Previous studies have indeed found strong patterns of long-term phenology changes in herbarium data (Primack et al., 2004;Miller-Rushing et al., 2006;Davis et al., 2015;Willis et al., 2017;Lang et al., 2019;Park et al., 2019;reviewed by Jones & Daehler, 2018), and they have also demonstrated that phenology trends estimated from herbarium data are comparable to those from field observations (Davis et al., 2015;Jones & Daehler, 2018;Miller et al., 2021). However, almost all previous studies have been carried out in the USA, and there has been little work so far on herbaria and plant phenology in Europe (but please refer to Robbirt et al., 2011;Diskin et al., 2012;Molnar et al., 2012). ...
Article
Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long‐term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large‐scale analyses of herbarium data are prone to pseudoreplication and geographical biases. We studied over 6000 herbarium specimens of 20 spring‐flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account. On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor. Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long‐term phenology trends across large spatial scales.
... The diverse alien plant species and near-continental spatial scale of China can provide more general findings of global significance in exploring MRT-IR relationships (Huang et al., 2012). Furthermore, the long history of herbarium collections provides us with invaluable information on and insight into a range of problems regarding climate change, biodiversity, conservation and the subject of this study, the distribution and introduction history of alien plant species (e.g., Aikio et al., 2010b;Crawford & Hoagland, 2009;Pyke & Erlich, 2010;Willis et al., 2017). given that the information could be unreliable (Ma, 2014). ...
Article
Full-text available
Plant invasions threaten many native species and change the functioning of ecosystems worldwide. This study finds that the invasion processes of multiple species include lag, acceleration and stable phases. This three‐phase relationship between minimum residence times (the time since the alien species was first recorded) and invasion ranges should be considered when modelling species invasion risks in the future, and we should control the population sizes of these species before they reach a tipping point to minimise the potential environmental impacts. This research also highlights the importance of natural history collections in helping us to understand invasion dynamics. Plant invasions threaten many native species and change the functioning of ecosystems worldwide. This study finds that the invasion processes of multiple species include lag, acceleration and stable phases. This three‐phase relationship between minimum residence times (the time since the alien species was first recorded) and invasion ranges should be considered when modelling species invasion risks in the future, and we should control the population sizes of these species before they reach a tipping point to minimise the potential environmental impacts. This research also highlights the importance of natural history collections in helping us to understand invasion dynamics.
... Each specimen contains a wealth of information including geographic occurrence data, phenotype, genotype, phenological status, and biotic interactions (Funk, 2003;Heberling and Burke, 2019). Collectively herbarium specimens are analyzed for studies in taxonomy, systematics, floristics, ecology, phenology, conservation, and global environmental change (Funk, 2003;Calinger et al., 2013;Willis et al., 2017;Lang et al., 2019;Albani Rocchetti et al., 2021). ...
Article
Full-text available
Herbarium sheets present a unique view of the world's botanical history, evolution, and biodiversity. This makes them an all–important data source for botanical research. With the increased digitization of herbaria worldwide and advances in the domain of fine–grained visual classification which can facilitate automatic identification of herbarium specimen images, there are many opportunities for supporting and expanding research in this field. However, existing datasets are either too small, or not diverse enough, in terms of represented taxa, geographic distribution, and imaging protocols. Furthermore, aggregating datasets is difficult as taxa are recognized under a multitude of names and must be aligned to a common reference. We introduce the Herbarium 2021 Half–Earth dataset: the largest and most diverse dataset of herbarium specimen images, to date, for automatic taxon recognition. We also present the results of the Herbarium 2021 Half–Earth challenge, a competition that was part of the Eighth Workshop on Fine-Grained Visual Categorization (FGVC8) and hosted by Kaggle to encourage the development of models to automatically identify taxa from herbarium sheet images.
... However, due to visual noise, it is particularly challenging to automate information extraction from DHS images. For more refined localization of the relevant objects, several methods based on semantic and instance segmentation methods were developed (Park et al., 2018(Park et al., ) (et al., 2019 (Göeau et al., 2020) (Willis et al., 2017b) (Hussein et al., 2021). However, these techniques come with a cost since they require pixel-level annotation of training data, which is timeconsuming and labor-intensive to generate. ...
Article
Full-text available
Herbarium specimens are excellent sources of botanical information to facilitate understanding and monitoring the evolution of plants and their effects on global climate change. Globally, many herbaria have undertaken digitization projects of herbarium specimens to preserve them and make them accessible in online repositories to botanists and ecologists. Automated detection of plant organs such as plant leaves, buds, flowers, and fruits on the digitized herbarium specimen images provides valuable information in various scientific contexts. We developed a deep learning approach based on the refined YOLO-V3 approach to detect plant organs within the digitized herbarium specimen images effectively. The proposed approach combines ResNet and DenseNet architectures to improve feature extraction capabilities. Also, a new scale of feature map is added to the existing scales to address the problem of YOLO-V3's low performance in detecting small plant organs. The experimental results demonstrate that our proposed approach can detect organs of different sizes within different specimens, where the precision and recall reached 94.2% and 95.5%, respectively.
... Numerous studies using digitized herbarium specimen (DHS) images have focused on a single phenological event such as the flowering period to investigate climate change. Only a few studies have investigated several reproductive organs at the same time (such as measuring the fruit area) and determined how different phenological events are linked [5]. ...
... Much work has been published in recent years (Davis et al. 2015;Park and Schwartz 2015;Willis et al. 2017a;Park et al. 2018) that has confirmed the value of herbaria in characterizing phenological changes. A synthesis of methods and applications of these has been published recently. ...
... Much work has been published in recent years (Davis et al. 2015;Park and Schwartz 2015;Willis et al. 2017a;Park et al. 2018) that has confirmed the value of herbaria in characterizing phenological changes. A synthesis of methods and applications of these has been published recently. ...
Chapter
Herbaria can contribute to the evaluation of the floristic knowledge of territories and to the identification of “hotspots” of plant biodiversity; to the characterization of floristic regressions of certain species; and to the study of the history of introductions and expansion of invasive exotic species or of symbionts collected unintentionally with the plant samples. Herbarium specimens can also be used to characterize environmental changes in territories such as air, water and soil quality, as well as the impacts of climate change on the phenology and possibly the morphology of plant species. This chapter repeats, completes and updates a first note on the use of herbaria in highlighting environmental change presented at the international conference Botanists of the Twenty‐first Century Roles, Challenges and Opportunities, organized by UNESCO in September 2014 and published in the proceedings of this conference.
... Much work has been published in recent years (Davis et al. 2015;Park and Schwartz 2015;Willis et al. 2017a;Park et al. 2018) that has confirmed the value of herbaria in characterizing phenological changes. A synthesis of methods and applications of these has been published recently. ...
Chapter
This chapter assesses the feasibility of using natural history collections to trace temporal changes in species distribution and community composition using the example of macroalgae that are preserved as herbaria. The preservation of plants in herbaria began during the Renaissance. This technique required paper and became widespread in the 18th century thanks to technical advances in paper production. Plant classifications have been developed on the basis of the diversity of forms of reproductive organs. The algal herbarium of the Dinard maritime laboratory has been recently transferred to the Herbier national du Muséum national d'Histoire naturelle de Paris in the cryptogamy section. It is possible to explore temporal changes in species distribution from collections under certain conditions, either by using only the observations or by using those observations to model species distribution. Algal community composition and species distribution are being impacted by global change and in particular by increasing seawater temperatures and heat waves.
... De nombreux travaux ont été publiés au cours des dernières années (Davis et al. 2015 ;Park et Schwartz 2015 ;Willis et al. 2017a ;Park et al. 2018) qui ont confirmé l'intérêt des herbiers pour caractériser les modifications phénologiques. Une synthèse des méthodes et applications en a été publiée tout récemment. ...
Chapter
The “cyanobacteria and microalgae” collection of the Muséum national d'Histoire naturelle includes, respectively, 870 and 890 living strains maintained in the laboratory. This collection supports fundamental research, particularly in taxonomy and ecophysiology, but also numerous activities for the development of bioactive molecules and expertise in environmental diagnosis. These different activities benefit from the emergence of high‐throughput “‐omics” approaches, which now offer new possibilities to enable such a collection to respond to the current challenges of both fundamental and targeted research, and of the conservation of biological resources. The conservation of organisms in living collections allows us to explore their biological properties. Among these, the production of bioactive metabolites is a rapidly developing theme. The “cyanobacteria and microalgae” collection is a reference collection for environmental diagnosis.
... To avoid the potential confounding effect of supplemental watering of specimens on Museum grounds, we used phenological observations only from the unmanaged King Canyon site. Although herbarium specimens are increasingly used in phenological research (Willis et al. 2017;Jones and Daehler 2018;Pearson et al. 2021), these observations are only associated with a single date, and are highly left censored (meaning that it is only known that flowering occurred some time before the observation date), ultimately containing much less information than direct and regular observations of phenological transitions, such as the weekly observations made by Desert Museum staff. Because of this issue, in combination with a low number of flowering herbarium specimens from the Desert Museum grounds, we limit our phenological observations to the direct and regular observations of live, naturally occurring plants by Desert Museum staff. ...
... Herbarium specimens are helping to break this impasse and offer compelling snapshots of phenological events (e.g., flowering and fruiting) at specific places and in specific times and climates (see Figure IA,B in Box 1). Herbarium specimens have greatly expanded the temporal, spatial, and taxonomic depth of phenological data in the temperate zone [14,[45][46][47][48][49] while faithfully reflecting directly observed phenological sensitivity to local climate and climatic change [50]. ...
Article
Earth's most speciose biomes are in the tropics, yet tropical plant phenology remains poorly understood. Tropical phenological data are comparatively scarce and viewed through the lens of a 'temperate phenological paradigm' expecting phenological traits to respond to strong, predictably annual shifts in climate (e.g., between subfreezing and frost-free periods). Digitized herbarium data greatly expand existing phenological data for tropical plants; and circular data, statistics, and models are more appropriate for analyzing tropical (and temperate) phenological datasets. Phylogenetic information, which remains seldom applied in phenological investigations, provides new insights into phenological responses of large groups of related species to climate. Consistent combined use of herbarium data, circular statistical distributions, and robust phylogenies will rapidly advance our understanding of tropical - and temperate - phenology.
... The limitation of these approaches is that there are very few such long-term phenological observation datasets available, that too only in some countries from the developed world (Aono and Saito 2010). Although the use of herbarium and old photographic approaches is advantageous in providing the temporal depth, these datasets are beset with large temporal data gaps (Willis et al. 2017). In addition, these approaches limit our ability to distinguish the independent influence of climatic variables on phenology from other confounding factors like photoperiod, light intensity and relative humidity (Chuine et al. 2010;Ko¨rner and Basler 2010). ...
Article
Experimental evidences in support of climate warming–driven phenological shifts are still scarce, particularly from the developing world. Here, we investigated the effect of experimental warming on flowering phenology of selected woody plants in Kashmir Himalaya. We selected the twigs of four congeneric pairs of temperate woody species (Prunus, Populus, Ulmus, Viburnum)—typical spring-flowering plants in the region. Using randomised block design, we monitored these winter dormant twigs in controlled growth chambers to study the effect of different temperature regimes (9, 17, 20 and 23 °C) and species identity on the patterns of phenological shifts. We observed a significant phenological shift in all the species showing preponement in the first flower out and senescence phases ranging from 0.56 to 3.0 and 0.77 to 4.04 days per degree increase in temperature, respectively. The duration of flowering phase in all the species showed a corresponding decrease along the gradient of increasing temperature, which was more driven by preponement of the flower senescence than the start of flower- ing. The patterns of phenological shifts were highly species-specific, and the magnitude of these shifts significantly varied in all the four pairs of congeneric species despite their phylogenetic similarity. Our study provides experimental support to the previous long-term observation and herbarium-based studies showing that the patterns of phenological shifts in response to global climate warming are likely to vary between species, even those belonging to same evolutionary stock. Our findings highlight that a one-size-fits-all strategy to manage the likely impacts of climate warming–induced phenological shifts will seldom succeed, and should instead be designed for the specific phenological responses of species and regions.
... The diversity of leaf forms is a result of multiple factors, including genetic sequence, the regulated expression of specific molecular pathways, developmental patterns, and the environment (Nicotra et al., 2011;Dkhar and Pareek, 2014;Ichihashi et al., 2014;Chitwood and Sinha, 2016;Edwards et al., 2016). To fully understand the variation in leaf forms, it is important to perform an accurate analysis of the different leaf landmarks (Page et al., 2015;Soltis, 2017;Willis et al., 2017). ...
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Premise: Plant leaves are one of the most important organs for plant identification due to their variability across different taxonomic groups. While traditional morphometrics has contributed tremendously to reducing the problems accompanying plant identification and morphology-based species delimitation, image-analysis digital solutions have made it easy to detect more characters to complement existing leaf data sets. Methods: Here, we apply MorphoLeaf to generate a morphometric data set from 140 leaf specimens of seven Cucurbitaceae species via landmark extraction, the reparameterization of leaf contours, and data quantification and normalization. A statistical analysis was performed on the resulting data set. Results: A principal component analysis revealed that leaf blade area, blade perimeter, tooth area, tooth perimeter, the measure of the distance from tooth position to the tip, and the measure of the distance from tooth position to the base are important and informative landmarks that contribute to the variation within the species studied. Discussion: MorphoLeaf can be applied to quantitatively track leaf diversity, thereby functionally integrating morphometrics and shape visualization into the digital identification of plants. The success of digital morphometrics in leaf outline analyses presents researchers with opportunities to carry out more accurate image-based research in areas such as plant development, evolution, and phenotyping.
... They have been used to study the history of colonization by exotic species, patterns of invasiveness, and climate change (Nualart et al. 2017). Fuentes et al. (2008) traced the spread of invasive species to colonization and periods of intense agriculture in Chile using herbarium collections, and changes in Boston flora induced by climate change were revealed using herbarium records dating back to 1885 (Primack et al. 2004), as well as in other parts of the world (Willis et al. 2017). There is much untapped potential in collections for global change biology (Meineke et al. 2018). ...
... In contrast, herbarium specimens capture snapshots of the reproductive status of individual plants in space and time, and with hundreds of millions of records worldwide increasingly available digitally, provide unique opportunities to expand the taxonomic and spatiotemporal coverage of phenoclimatic studies (Willis et al. 2017, Meineke et al. 2018. In recent years, researchers have leveraged specimens to study phenology-climate relationships (Jones andDaehler 2018, Heberling et al. 2019), estimating phenological responsiveness for thousands of species (Park and Mazer 2018) and generating results qualitatively consistent with those from field studies (Calinger et al. 2013). ...
Article
Understanding the effects of climate change on the phenological structure of plant communities will require measuring variation in sensitivity among thousands of co‐occurring species across regions. Herbarium collections provide vast resources with which to do this, but may also exhibit biases as sources of phenological data. Despite general recognition of these caveats, validation of herbarium‐based estimates of phenological sensitivity against estimates obtained using field observations remains rare and limited in scope. Here, we leveraged extensive datasets of herbarium specimens and of field observations from the USA National Phenology Network for 21 species in the United States and, for each species, compared herbarium‐ and field‐based estimates of peak flowering dates expected under standardized temperature conditions, and of sensitivity of peak flowering time to geographic and interannual variation in mean minimum temperatures (TMIN). We found strong agreement between herbarium‐ and field‐based estimates for standardized peak flowering time (r = 0.91, p < 0.001) and for the direction and magnitude of sensitivity to both geographic TMIN variation (r = 0.88, p < 0.001) and interannual TMIN variation (r = 0.82, p < 0.001). This agreement was robust to substantial differences between datasets in 1) the long‐term TMIN conditions observed among collection and phenological monitoring sites and 2) the interannual TMIN conditions observed in the time periods encompassed by both datasets for most species. Our results show that herbarium‐based sensitivity estimates are reliable among species spanning a wide diversity of life histories and biomes, demonstrating their utility in a broad range of ecological contexts, and underscoring the potential of herbarium collections to enable phenoclimatic analysis at taxonomic and spatiotemporal scales not yet captured by observational data.
... Our dataset, despite high quantity of observations, similarly to herbarium records, still do not fully cover the geographic ranges of A. nemorosa in terms of number of grid cells with ≥10 observations (177 of 2409 grid cells). It is similar to many other species species where such limitation does not allow accurate estimation of variability of the timing of phenological phases Taylor and Guralnick, 2019;Willis et al., 2017). The distribution and density of A. nemorosa records were related to the varying availability and activity of volunteers in collecting data in individual countries and human population density than to the actual distribution of this species (Di Cecco et al., 2021;Feldman et al., 2021). ...
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Rapidly increasing resources of citizen science databases (CS) collecting information on species occurrence are increasingly useful as a data source for global biodiversity research. The photos attached to records allow to verify the species identification and identify its phenological phase. We assessed CS data's usefulness in large-scale phenological research on temperate forest understory species, using a common and widely distributed in Europe: Anemone nemorosa. We analyzed 9804 photos from CS databases. We found 177 15' grid cells with ≥10 observations of flowering plants for bootstrap estimation of flowering onset and offset. We predicted flowering dates for the present and future climate according to Shared Socioeconomic Pathways averaged over four global circulation models for 2040-60 and 2060-80 across A. nemorosa natural range. The estimated magnitude of change in the flowering phenology for both future periods is comparable. The estimated flowering onset median was 24-41 days earlier while flowering offset median was 19-34 days earlier than predicted for the current climate. We estimated a flowering length median of up to 7 days longer than for current climatic conditions. The predicted changes in the phenology of flowering will not significantly change the duration of flowering but will accelerate onset of this phenophase by about one month. Our study showed that CS might provide a valuable dataset that allows for developing reliable models of plant phenology. It was possible due to a large sample size, resulting from species characteristics: flowering when wider audience is interested in searching spring indicators, easy identification and abundant occurrence. We demonstrated that using dataset of such spatiotemporal extent can cautiously be used for development of future predictions. Such approach allows for evaluating flowering phenology in the understory and to improve understanding the consequences of climate change for biodiversity and functioning of temperate ecosystems.
... Consistent with climate change predictions, temperature changes have been correlated with shifts in plant phenophases (Parmesan and Yohe 2003, Calinger et al 2013, Willis et al 2017, Chmura et al 2019. But exploring additional variables, such as precipitation, may be especially important in water-limited systems where climate change is predicted to result in more frequent droughts (Crimmins et al 2010, McLaughlin et al 2017. ...
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Consistent with a warming climate, the timing of key phenological phases (i.e. phenophases) for many plant species is shifting, but the direction and extent of these shifts remain unclear. For large herbivores such as ungulates, altered plant phenology can have important nutritional and demographic consequences. We used two multi-year datasets collected during 1992–1996 and 2015–2019 of understory plant phenology in semi-arid forested rangelands in northeastern Oregon, United States, to test whether the duration of phenophases for forage species has changed over time for three plant functional groups (forbs, graminoids, and shrubs). Duration of spring green-up was approximately 2 weeks shorter in the later years for forbs (19 ± 3.8 d) and graminoids (13.2 ± 2.8 d), and senescence was 3 weeks longer for graminoids (25.1 ± 5.1) and shrubs (22.0 ± 4.6). Average peak flowering date was 3.1 ± 0.2 d earlier per decade for understory forage species with approximately 1/3 of the species (35%) exhibiting earlier peak flowering dates over time. Variation in late-winter precipitation had the greatest effect on the duration of understory green-up, whereas variation in summer precipitation had a greater effect on duration of the senescent period. Collectively, these results indicate climate-related progression towards shorter periods of peak plant productivity, and earlier and longer periods of plant senescence, the combination of which substantially reduces the temporal window of forage available in growing forms most usable to herbivores. This work adds a needed component to the climate change literature, by describing links between shifting climate variables, multiple phases of understory plant phenology, and possible nutritional consequences for herbivores under a warming climate.
... Natural history collections (NHCs) have been instrumental in understanding temporal trends in changes to the timing of seasonal events. In particular, herbarium specimens have been reliably used to characterize phenological responses to changing climate (reviewed in Willis et al., 2017). More recently, researchers are attempting to move beyond simply documenting changes in phenology and are examining more complex phenological responses such as determining phenological cueing mechanisms (Davis et al., 2015;Park & Mazer, 2018) and determining if changes in bird migration phenology are related to changes in body size (Zimova et al., 2021). ...
Article
Natural history collections (NHCs) have been indispensable to understanding longer‐term trends of the timing of seasonal events. Massive‐scale digitization of specimens promises to further enable phenological research, especially the ability to move towards a deeper understanding of drivers of change and how trait‐environment interactions shape phenological sensitivity. Despite the promise of NHCs to answer fundamental phenology questions, use of these data resources present unique and often overlooked challenges requiring specialized workflow steps, such as assembling multisource data, accounting for date imprecision, and making decisions about trade‐offs between data density and spatial resolution. We provide a set of key best practice recommendations and showcase these via a case study that utilizes NHC data to test hypotheses about spatiotemporal trends in adult Lepidoptera (i.e., butterflies and moths) flight timing across North America. Our case study is a worked example of these best practices, helping practitioners recognize and overcome potential pitfalls at each step, from data acquisition and cleaning, to delineating spatial units and proper estimation of phenological metrics and associated uncertainty, to building appropriate models. We confirm and extend the critical importance of voltinism and diapause strategy, but less‐so daily activity patterns, for predicting Lepidoptera phenology spatiotemporal trends. Our case study also showcases the unique power of NHC data to test existing hypotheses and generate new insights about temporal phenological trends. Specifically, migratory species and species that enter diapause as adults are advancing the start of flight periods in more recent years, even after accounting for climate context. These results highlight the physiological and adaptive differences between species with different overwintering strategies. We close by noting the value of partnerships between data scientists, museum experts, and ecological modelers to fully harness the power of digital data resources to address pressing global change challenges. These partnerships can extend approaches for integrating multiple data types to fully unlock our understanding of the tempo, mode, drivers, and outcomes of phenological changes at greater spatial, temporal, and taxonomic scales.
Article
The results of the analysis of Quercus L. species stored in the herbarium of the Department of Botany and Plant Physiology of Federal State Budget Educational Institution of Higher Education VSUFT (Voronezh) are presented. This herbarium of historical plant collections of the genus Quercus L. is critical for tracking changes in the genus, including the introduction and distribution of species. We examined the belonging of the species to systematic units – subgenus, section, subsection, row, using the traditional classification and the updated intrageneric classification of oaks. Information about the life form, plant height, date and place of collection of the specimen was recorded. We entered information into the database, which will further simplify the work on registration, revision of the herbarium fund and when replenishing herbarium specimens. Conclusions were drawn based on the results of the workabout changes in the taxonomic nature and phylogenetic relationships of species in Quercus L. genus
Article
Phenology is an ecologically critical attribute that commonly is coordinated with other plant traits. Phenological shifts may be the result of evolutionary adjustments to persistently new conditions, or transitory, varying with annual flux in abiotic conditions. In summer-dry, fire-prone Mediterranean-climates, for example, many plant lineages have historically migrated from forests to more arid shrublands resulting in adaptive trait changes. These shifts in habitat abiotic conditions and biotic interactions influence morphology of flowers and fruits and will interact with phenological timing. The Arbutoideae (Ericaceae) is one lineage that illustrates such modifications, with fruit characters evolving among genera from fleshy to dry fruit, thin to stony endocarps, and bird to rodent dispersal, among other changes. We scored herbarium collections and used ancestral trait analysis to determine phenological shifts among the five Arbutoid genera found in semi-arid climates. Our objective was to determine if phenology shifts with the phylogenetic transition to different reproductive characters. Our results indicate that phenological shifts began with some traits, like the development of a stony endocarp or dry fruits, but not with all significant trait changes. We conclude that early phenological shifts correlating with some reproductive traits were permissive for the transition to other later character changes.
Article
To date, most herbarium-based studies of phenological sensitivity to climate and of climate-driven phenological shifts fall into two categories: detailed species-specific studies vs. multi-species investigations designed to explain inter-specific variation in sensitivity to climate and/or the magnitude and direction of their long-term phenological shifts. Few herbarium-based studies, however, have compared the phenological responses of closely related taxa to detect: (1) phenological divergence, which may result from selection for the avoidance of heterospecific pollen transfer or competition for pollinators, or (2) phenological similarity, which may result from phylogenetic niche conservatism, parallel or convergent adaptive evolution, or genetic constraints that prevent divergence. Here, we compare two widespread Clarkia species in California with respect to: the climates that they occupy; mean flowering date, controlling for local climate; the degree and direction of climate change to which they have been exposed over the last 115 yr; the sensitivity of flowering date to inter-annual and to long-term mean maximum spring temperature and annual precipitation across their ranges; and their phenological change over time. Specimens of C. cylindrica were sampled from sites that were chronically cooler and drier than those of C. unguiculata, although their climate envelopes broadly overlapped. Clarkia cylindrica flowers 3.5 d earlier than C. unguiculata when controlling for the effects of local climatic conditions and for quantitative variation in the phenological status of specimens. However, the congeners did not differ in their sensitivities to the climatic variables examined here; cumulative annual precipitation delayed flowering and higher spring temperatures advanced flowering. In spite of significant spring warming over the sampling period, neither species exhibited a long-term phenological shift. Precipitation and spring temperature interacted to influence flowering date: the advancing effect on flowering date of high spring temperatures was greater in dry than in mesic regions, and the delaying effect of high precipitation was greater in warm than in cool regions. The similarities between these species in their phenological sensitivity and behavior are consistent with the interpretation that facilitation by pollinators and/or shared environmental conditions generate similar patterns of selection, or that limited genetic variation in flowering time prevents evolutionary divergence between these species.
Article
Weather and climate may influence the phenology of Dirca occidentalis A.Gray (Thymelaeaceae) in ways that impact reproductive success. Dirca occidentalis blooms during winter, when the likelihood of entomophily may be low. Based on preliminary observations that the timing of dormancy release and growth resumption varies over years and among shrubs within years, we quantified fruit set among flowers that formed at different times and examined whether annual variation in autumnal precipitation and temperature during autumn and winter are associated with phenology. Fruit set was determined during 20072008 through 20112012 by tracking 37,461 flowers near or at anthesis early, midway, and late within the blooming period of D. occidentalis. In addition, measures of phenology of 18 individual shrubs were made each December 29, January 26, and February 23 of the five blooming periods, and fruit set of these shrubs was determined. Fruit set was low (<5%) among flowers present early (December 26January 2), but increased significantly in all blooming periods, to as high as nearly 30%, among flowers at anthesis later. Phenology ratings, and lengths of newly formed stems and leaves, on December 29 increased linearly as the amount of precipitation from October 1December 15 of the same year increased. Phenology ratings on February 23 increased linearly with increasing air temperature from November 1February 23. Rankings of phenology of the 18 shrubs were highly correlated over years, and fruit set of individual shrubs over years was 1% to 52% and increased linearly as growth resumption and flowering became later. Our results demonstrate that low autumnal precipitation is associated with delayed growth resumption and flowering, which corresponds with increased fruit set of this rare species.
Article
Flowering time in plants is a highly variable trait that influences species' resource use and exchange of pollen with con- and heterospecifics. Levin (2009) suggested that habitat shifts within species might cause plastic shifts in flowering phenology, reducing pollen exchange across habitats. Coupled with divergent selection across habitats, diverged flowering time might thus pave the way towards ecological speciation. Some of these ideas may apply across species as well. If close heterospecific relatives share phylogenetically conserved flowering times and negatively affect each other's fitness, habitat shifts to microallopatry might provide a means for local coexistence by close relatives by reducing resource competition, shared enemies, or negative interactions via pollination. Habitat shifts might also select for diverged flowering time, or cause flowering time divergence, if phylogenetically conserved cues arrive at different times across habitats. Here, we ask if flowering phenology is phylogenetically conserved for 208 species at our coastal field site in northern California, whether flowering phenology differs systematically across habitat types, and whether habitat shifts are associated with phenological separation, especially in congeners. Because annuality and perenniality have been shown to be associated with habitat traits and flowering time, we included life history in our analyses as well. We also explore the frequency of habitat shifts between congener and noncongener pairs. We use both field observations and data from Jepson eFlora/Jepson Manual 2 (Baldwin et al. 2012) to explore patterns in flowering phenology. The two data sources were well-correlated across 59 species. Phylogeny, habitat, and life history all influenced flowering time, and habitat and life history were also phylogenetically conserved across 208 spp. Congeners differed in habitat more often than noncongener pairs, and also overlapped more in flowering time. Habitat shifts were not associated with shifts in flowering time in congeners, despite mean peak flowering time differences across habitats, and phylogenetic conservatism in habitat use. Congeners that differed in both habitat use and life history, however, did have the greatest difference in peak flowering dates. Habitat shifts likely play a role in local coexistence of close relatives, but our data do not support habitat-mediated changes in phenology as a possible mechanism. Experimental approaches may elucidate the role of phenology, resource competition, pollinators, and other associates in mediating coexistence of congeners at our coastal California field site.
Article
Herbarium specimens provide a critical source of phenological data that can be used to identify the direct and indirect drivers of variation in flowering date within and among species. Specimen-based phenological research in California has been accelerated by digitization efforts such as the California Phenology Network, which has scored and archived the phenological status of over 1.4 million specimens to date. Using this new data source in the Consortium of California Herbaria's CCH2 data portal, we obtained data from 993 specimens of the iconic California Poppy, Eschscholzia californica Cham., along with climate data representing all collection sites. Our goal was to determine how long-term and interannual climate variation affect flowering dates, and whether the magnitude of phenological sensitivity to climate varies across the species' range. We found that specimens collected from chronically warm or dry sites flowered relatively early, and flowering date was more sensitive to long-term mean temperature than to long-term mean precipitation. Independent of these effects of long-term conditions, flowering date in E. californica was sensitive to interannual variation in seasonal precipitation, but the direction of this effect depended on the season in which the precipitation occurred. Specimens sampled from sites experiencing warmer-than-average springs in the year of collection flowered 2.73.3 days earlier for every 1C increase in spring temperature relative to long-term mean spring temperature. The magnitude of these effects, however, varied across the range of E. californica, with greater sensitivity to temperature in relatively cooler regions and no discernible sensitivity in relatively warm regions. Consistently, California Poppies exhibited significant phenological advancement over the last 120 years, but this advancement was restricted to the cooler portions of its range. Our results provide one of the first accounts of intraspecific variation in both phenological sensitivity to climate and the magnitude of phenological shifts over time, and demonstrate that, for a single species, location- or population-specific estimates of phenological sensitivity or of temporal trends in phenology might not accurately predict phenological responses to climate change in other locations throughout its range. In this study, we highlight the utility and promise of herbarium specimens for addressing novel questions about the phenological responses of plants to climate trends.
Article
Flowering phenology in five chaparral species was investigated using more than a century of data obtained from herbarium collections. Three species examined were from the genus Arctostaphylos (Ericaceae) and two from Ceanothus (Rhamnaceae). Collections of these species were examined relative to climate change data during the same time period. For all the species, no change in average flowering time occurred during the past century. Considerable variability was found in flowering phenology and this variability was explored using generalized linear (GLM) and generalized linear mixed models (GLMM) and different dimensions of temperature and precipitation timing. While the genera performed differently, both required combinations of precipitation, temperature, and their interactions to predict flowering date. Arctostaphylos responded the most to precipitation interactions, while Ceanothus responded the most to temperature interactions and the previous growing season's precipitation. In both genera, regression coefficients were combinations of both positive and negative variables, indicating that flowering dates are complex interactions among the different dimensions of precipitation and temperature.
Article
Changes in climate can alter the phenology of organisms, potentially decoupling partners within mutualisms. Previous studies have shown that plant and pollinator phenologies are shifting over time, but these shifts have primarily been documented for generalists and within small geographic regions, and the specific climatic cues regulating these shifts are not well‐understood. We examined phenological shifts in a specialist pollinator and its host plant species over a 117‐year study period using a digitized dataset of over 4000 unique collection records. We assess how climatic cues regulate these organisms' phenologies using PRISM weather data associated with each record. We tested the hypothesis that rates of phenological change would be greater at northern latitudes. We found that the phenology of the specialist bee pollinator Habropoda laboriosa is changing over time, but at different rates across its range. Specifically, phenology is advancing to a greater degree in more northern populations, with increasing phenological advances of 0.04 days/year with each degree of latitude, and with a delay in phenology in more southern populations. In contrast, only one species in the host plant genus Vaccinium is experiencing phenological change over time. For this plant, rates of change are also variable across latitudes, but in a pattern opposite that of the bee; while phenology is advancing across its range, rates of advance are highest in more southern populations, with decreasing phenological advances of 0.01 days/year with each degree of latitude. The phenologies of both the bee and three of four Vaccinium spp. were regulated primarily by spring temperature, with phenologies overall advancing with increasing temperature, and with the strongest responses shown by the bee in northern populations. Our study provides partial support for the hypothesis that phenologies advance most at northern latitudes, but demonstrates that pollinators and plants do not adhere similarly to this prediction. Additionally, we illustrate the potential for phenological mismatch between a specialist pollinator and its host plants by showing that plants and pollinators are advancing their phenologies at different rates across space and time and with differing responses to changing climatic cues.
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Climate change represents one of the most critical threats to biodiversity with far-reaching consequences for species interactions, the functioning of ecosystems, or the assembly of biotic communities. Plant phenology research has gained increasing attention as the timing of periodic events in plants is strongly affected by seasonal and interannual climate variation. Recent technological development allowed us to gather invaluable data at a variety of spatial and ecological scales. The feasibility of phenological monitoring today and in the future depends heavily on developing tools capable of efficiently analyzing these enormous amounts of data. Deep Neural Networks learn representations from data with impressive accuracy and lead to significant breakthroughs in, e.g., image processing. This article is the first systematic literature review aiming to thoroughly analyze all primary studies on deep learning approaches in plant phenology research. In a multi-stage process, we selected 24 peer-reviewed studies published in the last five years (2016–2021). After carefully analyzing these studies, we describe the applied methods categorized according to the studied phenological stages, vegetation type, spatial scale, data acquisition- and deep learning methods. Furthermore, we identify and discuss research trends and highlight promising future directions. We present a systematic overview of previously applied methods on different tasks that can guide this emerging complex research field.
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Significance Adaptive evolution can help species to persist and spread in new environments, but it is unclear how the rate and duration of adaptive evolution vary throughout species ranges and on the decadal timescales most relevant to managing biodiversity for the 21st century. Using herbarium records, we reconstruct 150 y of evolution in an invasive plant as it spread across North America. Flowering phenology evolves to adapt to local growing seasons throughout the range but stalls after about a century. This punctuated, convergent evolution recapitulates long-term dynamics in the fossil record, implicating limits to evolutionary rates that are not evident for the first century of spread.
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1. Understanding the breadth and complexity of changes in phenology is limited by the availability of long‐term historical datasets with broad geographic range. 2. We compare a recently discovered historical dataset of plant phenology observations collected across the state of New York (1826‐1872) to contemporary volunteer‐contributed observations (2009‐2017) to evaluate changes in plant phenology between time periods. These multi‐site, multi‐taxa phenology data matched with temperature data uniquely extend historical observations back in time prior to the major atmospheric effects of the Industrial Revolution. 3. The majority of the 36 trees, shrubs and forbs that comprised our analyzable dataset flowered and leafed out earlier in contemporary years than in the early‐to‐mid 19th century. This shift is associated with a warming trend in mean January‐to‐April temperatures, with flowering and leafing advancing on average 3 days/°C earlier. On average, plants flowered 10.5 days earlier and leafed out 19 days earlier in the contemporary period. Urban areas exhibit more advanced phenology than their rural counterparts overall, insect‐pollinated trees show more advanced phenology than wind‐pollinated trees and seasonality and growth form explain significant variation in flowering phenology. The greatest rates of temperature sensitivity and change between time periods for flowering are seen in early‐season species, particularly trees. Changes in the timing of leaf out are the most advanced for trees and shrubs in urban areas. 4. Synthesis: Citizen science observations across two centuries reveal a dramatic, climate‐driven shift to earlier leaf out and flowering. The magnitude of advancement varies across settings, species and functional groups, and illustrates how long‐term monitoring and citizen science efforts are invaluable for ecological forecasting and discovery.
Article
Premise: The study of phenotypic divergence of, and selection on, functional traits in closely related taxa provides the opportunity to detect the role of natural selection in driving diversification. When selection in field populations differs between taxa in a pattern that is consistent with the phenotypic difference between them, this provides evidence that natural selection reinforces the divergence. Few studies have sought evidence for such concordance for physiological traits. Methods: Herbarium specimen records were used to detect phenological differences between sister taxa independent of the effects on flowering time of long-term variation in the climate across collection sites. In the field, physiological divergence in photosynthetic rate, transpiration rate, and instantaneous water use efficiency were recorded during vegetative growth and flowering in 13 field populations of two taxon pairs of Clarkia, each comprised of a self-pollinating and a outcrossing taxon. Results: Historically, each selfing taxon flowered earlier than its outcrossing sister taxon, independent of the effects of local long-term climatic conditions. Sister taxa differed in all focal traits, but the degree and (in one case) the direction of divergence depended on life stage. In general, self-pollinating taxa exhibited higher gas exchange rates, consistent with their earlier maturation. In 6 of 18 comparisons, patterns of selection were concordant with the phenotypic divergence (or lack thereof) between sister taxa. Conclusions: Patterns of selection on physiological traits measured in heterogeneous conditions do not reliably reflect divergence between sister taxa, underscoring the need for replicated studies of the direction of selection within and among taxa. This article is protected by copyright. All rights reserved.
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In response to the worldwide coronavirus outbreak, which effectively shut down fieldwork, laboratory and herbarium‐based studies, an evaluation was made of the effectiveness and limitations of undertaking a virtual taxonomic study using only online herbarium specimen resources related to the genus Madhuca (Sapotaceae) for the Flora of Singapore. The study demonstrated the immense value of digital images to basic taxonomic research but also found that diagnostic micro‐morphological characters, often critical in defining species boundaries, cannot be seen in many digital images, even at high resolution. Several recommendations are made on how to maximise the utility of online herbarium specimen images to help facilitate future taxonomic research, though it is clear that physical access to herbarium specimens remains essential.
Article
Consistent with a warming climate, the timing of key phenological phases (i.e., phenophases) for many plant species is shifting, but the direction and extent of these shifts remain unclear. For large herbivores such as ungulates, altered plant phenology can have important nutritional and demographic consequences. We used two multi-year datasets collected during 1992-1996 and 2015-2019 of understory plant phenology in semi-arid forested rangelands in northeastern Oregon, United States, to test whether the duration of phenophases for forage species has changed over time for three plant functional groups (forbs, graminoids, and shrubs). Duration of spring green-up was approximately two weeks shorter in the later years for forbs (19 ± 3.8 d) and graminoids (13.2 ± 2.8 d), and senescence was three weeks longer for graminoids (25.1 ± 5.1) and shrubs (22.0 ± 4.6). Average peak flowering date was 3.1 ± 0.2 d earlier per decade for understory forage species with approximately 1/3 of the species (35%) exhibiting earlier peak flowering dates over time. Variation in late-winter precipitation had the greatest effect on the duration of understory green-up, whereas variation in summer precipitation had a greater effect on duration of the senescent period. Collectively, these results indicate climate-related progression towards shorter periods of peak plant productivity, and earlier and longer periods of plant senescence, the combination of which substantially reduces the temporal window of forage available in growing forms most usable to herbivores. This work adds a needed component to the climate change literature, by describing links between shifting climate variables, multiple phases of understory plant phenology, and possible nutritional consequences for herbivores under a warming climate.
Chapter
Cyberecoethnopharmacolomics (CEEPO) reflects an integrated, holistic, evidence-based approach for the patient-centered investigation of the acquired and analyzed information on the sustainable natural products, especially those used traditionally for health purposes. This chapter discusses the morphemes of CEEPO, the relationship to ongoing botanical, chemical, biological, technological, and societal transitions in the Fourth Industrial Revolution, and the application of these advances to the quality control of traditional medicines for the benefit of the patient. Included in the discussion are the compilation of large, globally available datasets for in-field and laboratory information, the introduction of artificial intelligence to evaluate research directions, robotics to facilitate chemical and biological processing, blockchain technology to enhance trust and traceability, and the promotion of ecopharmacognosy practices with respect to the use of natural resources and laboratory practices. In addition, the importance of five “-omics,” taxonomics, metabolomics, genomics, agronomics, and economics, is discussed.
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Herbarium records provide a broad spatial and temporal range with which to investigate plant responses to environmental change. Research on plant phenology and its sensitivity to climate has advanced with the increasing availability of digitized herbarium specimens, but limitations of specimen‐derived data can undermine the inferences derived from such research. One issue that has received little attention is collection site uncertainty (i.e. error distance), a measure of confidence in the location from which a specimen was collected. We conducted comparative analyses of phenoclimatic models to determine whether spatial deviations of 2, 5, 15 or 25 km between recorded and simulated collection sites, as well as the error distance reported in digitized records, affect estimates of the phenological sensitivity of flowering time to annual temperature and precipitation in a widespread annual California wildflower. In this approach, we considered both spatial and interannual variation in climatic conditions. Simulated site displacements led to increasingly weak estimates of phenological sensitivity to temperature and precipitation anomalies with increasing distances. However, we found no significant effect of reported error distance magnitude on estimates of phenological sensitivity to climate normals or anomalies. These findings suggest that the spatial uncertainty of collection sites among specimens of widely collected plant species may not adversely affect estimates of phenological sensitivity to climate, even though real discrepancies and georeferencing inaccuracy can negatively impact such estimates. Collection site uncertainty merits further attention as a potential source of noise in herbarium data, especially for research on how plant traits respond to spatial and interannual climatic variation.
Article
Herbarium specimens are being used as reliable sources for estimating phenological behavior for plant species. Flowering and fruiting periodicity of 520 herbarium specimens, collected between 1948 and 2007 and deposited at the National Herbarium of Ethiopia, were investigated. Scientific names, collection date and locality of specimens were documented to assess the periodicity of phenological events. For the evaluation of periodicity of reproductive phenophases, the presence of flowering and fruiting were visually confirmed from each specimen. Examination of flowering periodicity of Bersama abyssinica, Brucea antidysenterica, Maytenus arbutifolia and Rosa abyssinica showed continuous flowering while Prunus africana, Lobelia rhynchopetalum, Kniphofia foliosa, Solanecio gigas, Buddleja polystachya, Dombeya torrida and Embelia schimperi exhibited seasonal flowering. Although the fruiting period is extended over several months (B. abyssinica, B. antidysenterica, E. schimperi, M. arbutifolia and R. abyssinica), seasonality in fruiting was also observed in K. foliosa, L. rhynchopetalum and P. africana. The highest number of specimens found belonged to M. arbutifolia followed by B. abyssinca and B. antidysenterica, while the highest number of specimens were collected from Shewa Upland followed by Keffa and Bale floristic regions. Surprisingly, Euryops pinifolius, a species endemic to Ethiopia, was represented by only one specimen collected from Gojjam in 1985. The results revealed that herbarium specimens can be used to study flowering and fruiting periodicity of plant species. Therefore, botanists should be encouraged to continue collecting herbarium specimens based on the distribution of species in the flora area to avoid spatial and species biases for future studies.
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The Natural History Collections of Adam Mickiewicz University (AMUNATCOLL) in Poznań contain over 2.2 million specimens. Until recently, access to the collections was limited to specialists and was challenging because of the analogue data files. Therefore, this paper presents a new approach to data sharing called the Scientific, Educational, Public, and Practical Use (SEPP) Model. Since the stakeholder group is broad, the SEPP Model assumes the following key points: full open access to the digitized collections, the structure of metadata in accordance with certain standards, and a versatile tool set for data mining or statistical and spatial analysis. The SEPP Model was implemented in the AMUNATCOLL IT system, which consists of a web portal equipped with a wide set of explorative functionalities tailored to different user groups: scientists, students, officials, and nature enthusiasts. An integral part of the system is a mobile application designed for field surveys, enabling users to conduct studies comparing their own field data and AMUNATCOLL data. The AMUNATCOLL IT database contains digital data on specimens, biological samples, bibliographic sources, and multimedia nature documents. The metadata structure was developed in accordance with ABCD 2.06 and Darwin Core standards.
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Premise: Forecasting how species will respond phenologically to future changes in climate is a major challenge. Many studies have focused on estimating species- and community-wide phenological sensitivities to climate to make such predictions, but sensitivities may vary within species, which could result in divergent phenological responses to climate change. Methods: We used 743 herbarium specimens of the mountain jewelflower (Streptanthus tortuosus, Brassicaceae) collected over 112 years to investigate whether individuals sampled from relatively warm vs. cool regions differ in their sensitivity to climate and whether this difference has resulted in divergent phenological shifts in response to climate warming. Results: During the past century, individuals sampled from warm regions exhibited a 20-day advancement in flowering date; individuals in cool regions showed no evidence of a shift. We evaluated two potential drivers of these divergent responses: differences between regions in (1) the degree of phenological sensitivity to climate and (2) the magnitude of climate change experienced by plants, or (3) both. Plants sampled from warm regions were more sensitive to temperature-related variables and were subjected to a greater degree of climate warming than those from cool regions; thus our results suggest that the greater temporal shift in flowering date in warm regions is driven by both of these factors. Conclusions: Our results are among the first to demonstrate that species exhibited intraspecific variation in sensitivity to climate and that this variation can contribute to divergent responses to climate change. Future studies attempting to forecast temporal shifts in phenology should consider intraspecific variation.
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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.
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The pace of climate change in the Arctic is dramatic, with temperatures rising at a rate double the global average. The timing of flowering and fruiting (phenology) is often temperature dependent and tends to advance as the climate warms. Herbarium specimens, photographs, and field observations can provide historical phenology records and have been used, on a localised scale, to predict species’ phenological sensitivity to climate change. Conducting similar localised studies in the Canadian Arctic, however, poses a challenge where the collection of herbarium specimens, photographs, and field observations have been temporally and spatially sporadic. We used flowering and seed dispersal times of 23 Arctic species from herbarium specimens, photographs, and field observations collected from across the 2.1 million km2 area of Nunavut, Canada, to determine (1) which monthly temperatures influence flowering and seed dispersal times; (2) species’ phenological sensitivity to temperature; and (3) whether flowering or seed dispersal times have advanced over the past 120 years. We tested this at different spatial scales and compared the sensitivity in different regions of Nunavut. Broadly speaking, this research serves as a proof of concept to assess whether phenology–climate change studies using historic data can be conducted at large spatial scales. Flowering times and seed dispersal time were most strongly correlated with June and July temperatures, respectively. Seed dispersal times have advanced at double the rate of flowering times over the past 120 years, reflecting greater late-summer temperature rises in Nunavut. There is great diversity in the flowering time sensitivity to temperature of Arctic plant species, suggesting climate change implications for Arctic ecological communities, including altered community composition, competition, and pollinator interactions. Intraspecific temperature sensitivity and warming trends varied markedly across Nunavut and could result in greater changes in some parts of Nunavut than in others.
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Changes in the life cycle of organisms (i.e. phenology) are one of the most widely used early-warning indicators of climate change, yet this remains poorly understood throughout the tropics. We exhaustively reviewed any published and unpublished study on fruiting phenology carried out at the community level in the American tropics and subtropics (latitudinal range: 26°N–26°S) to (1) provide a comprehensive overview of the current status of fruiting phenology research throughout the Neotropics; (2) unravel the climatic factors that have been widely reported as drivers of fruiting phenology; and (3) provide a preliminary assessment of the potential phenological responses of plants under future climatic scenarios. Despite the large number of phenological datasets uncovered (218), our review shows that their geographic distribution is very uneven and insufficient for the large surface of the Neotropics (~ 1 dataset per ~ 78,000 km²). Phenological research is concentrated in few areas with many studies (state of São Paulo, Brazil, and Costa Rica), whereas vast regions elsewhere entirely unstudied. Sampling effort in fruiting phenology studies was generally low: the majority of datasets targeted fewer than 100 plant species (71%), lasted 2 years or less (72%), and only 10.4% monitored > 15 individuals per species. We uncovered only 10 sites with ten or more years of phenological monitoring. The ratio of numbers of species sampled to overall estimates of plant species richness was wholly insufficient for highly diverse vegetation types such as tropical rainforests, seasonal forest and cerrado, and only slightly more robust for less diverse vegetation types, such as deserts, arid shrublands and open grassy savannas. Most plausible drivers of phenology extracted from these datasets were environmental (78.5%), whereas biotic drivers were rare (6%). Among climatic factors, rainfall was explicitly included in 73.4% of cases, followed by air temperature (19.3%). Other environmental cues such as water level (6%), solar radiation or photoperiod (3.2%), and ENSO events (1.4%) were rarely addressed. In addition, drivers were analyzed statistically in only 38% of datasets and techniques were basically correlative, with only 4.8% of studies including any consideration of the inherently autocorrelated character of phenological time series. Fruiting peaks were significantly more often reported during the rainy season both in rainforests and cerrado woodlands, which is at odds with the relatively aseasonal character of the former vegetation type. Given that climatic models predict harsh future conditions for the tropics, we urgently need to determine the magnitude of changes in plant reproductive phenology and distinguish those from cyclical oscillations. Long-term monitoring and herbarium data are therefore key for detecting these trends. Our review shows that the unevenness in geographic distribution of studies, and diversity of sampling methods, vegetation types, and research motivation hinder the emergence of clear general phenological patterns and drivers for the Neotropics. We therefore call for prioritizing research in unexplored areas, and improving the quantitative component and statistical design of reproductive phenology studies to enhance our predictions of climate change impacts on tropical plants and animals.
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The capacity of grass species to alter their reproductive timing across space and through time can indicate their ability to cope with environmental variability and help predict their future performance under climate change. We determined the long-term (1895-2013) relationship between flowering times of grass species and climate in space and time using herbarium records across ecoregions of the western USA. There was widespread concordance of C3 grasses accelerating flowering time and general delays for C4 grasses with increasing mean annual temperature, with the largest changes for annuals and individuals occurring in more northerly, wetter ecoregions. Flowering time was delayed for most grass species with increasing mean annual precipitation across space, while phenology-precipitation relationships through time were more mixed. Our results suggest that the phenology of most grass species has the capacity to respond to increases in temperature and altered precipitation expected with climate change, but weak relationships for some species in time suggest that climate tracking via migration or adaptation may be required. Divergence in phenological responses among grass functional types, species, and ecoregions suggests that climate change will have unequal effects across the western USA.
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Social image tag refinement, which aims to improve tag quality by automatically completing the missing tags and rectifying the noise-corrupted ones, is an essential component for social image search. Conventional approaches mainly focus on exploring the visual and tag information, without considering the user information, which often reveals important hints on the (in)correct tags of social images. Towards this end, we propose a novel tri-clustered tensor completion framework to collaboratively explore these three kinds of information to improve the performance of social image tag refinement. Specifically, the inter-relations among users, images and tags are modeled by a tensor, and the intra-relations between users, images and tags are explored by three regularizations respectively. To address the challenges of the super-sparse and large-scale tensor factorization that demands expensive computing and memory cost, we propose a novel tri-clustering method to divide the tensor into some sub-tensors by simultaneously clustering users, images and tags into a bunch of tri-clusters. And then we investigate two strategies to complete these sub-tensors by considering (in)dependence between the sub-tensors. Experimental results on a real-world social image database demonstrate the superiority of the proposed method compared with the state-of-the-art methods.
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Plant phenology research has gained increasing attention because of the sensitivity of phenology to climate change and its consequences for ecosystem function. Recent technological development has made it possible to gather invaluable data at a variety of spatial and ecological scales. Despite our ability to observe phenological change at multiple scales, the mechanistic basis of phenology is still not well understood. Integration of multiple disciplines, including ecology, evolutionary biology, climate science, and remote sensing, with long-term monitoring data across multiple spatial scales is needed to advance understanding of phenology. We review the mechanisms and major drivers of plant phenology, including temperature, photoperiod, and winter chilling, as well as other factors such as competition, resource limitation, and genetics. Shifts in plant phenology have significant consequences on ecosystem productivity, carbon cycling, competition, food webs, and other ecosystem functions and services. We summarize recent advances in observation techniques across multiple spatial scales, including digital repeat photography, other complementary optical measurements, and solar-induced fluorescence, to assess our capability to address the importance of these scale-dependent drivers. Then, we review phenology models as an important component of earth system modeling. We find that the lack of species-level knowledge and observation data leads to difficulties in the development of vegetation phenology models at ecosystem or community scales. Finally, we recommend further research to advance understanding of the mechanisms governing phenology and the standardization of phenology observation methods across networks. With the opportunity for “big data” collection for plant phenology, we envision a breakthrough in process-based phenology modeling.
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One of the major challenges in ecosystem conservation is obtaining baseline data, particularly for regions that have been poorly inventoried, such as regions of the African continent. Here we use a database of African herbarium records and examples from the literature to show that, although herbarium records have traditionally been collected to build botanical reference "libraries" for taxonomic and inventory purposes, they provide valuable and useful information regarding species, their distribution in time and space, their traits, phenological characteristics, associated species and their physical environment. These data have the potential to provide invaluable information to feed into evidence-based conservation decisions.
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Plants are a hyperdiverse clade that plays a key role in maintaining ecological and evolutionary processes as well as human livelihoods. Biases, gaps and uncertainties in plant occurrence information remain a central problem in ecology and conservation, but these limitations remain largely unassessed globally. In this synthesis, we propose a conceptual framework for analysing gaps in information coverage, information uncertainties and biases in these metrics along taxonomic, geographical and temporal dimensions, and apply it to all c. 370 000 species of land plants. To this end, we integrated 120 million point-occurrence records with independent databases on plant taxonomy, distributions and conservation status. We find that different data limitations are prevalent in each dimension. Different metrics of information coverage and uncertainty are largely uncorrelated, and reducing taxonomic, spatial or temporal uncertainty by filtering out records would usually come at great costs to coverage. In light of these multidimensional data limitations, we discuss prospects for global plant ecological and biogeographical research, monitoring and conservation and outline critical next steps towards more effective information usage and mobilisation. Our study provides an empirical baseline for evaluating and improving global floristic knowledge, along with a conceptual framework that can be applied to study other hyperdiverse clades.
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We analysed plant collecting in Germany between 1826 and 2014 by counting specimens of common, rare, and invasive species deposited in the herbaria of Munich during that period. Plant collecting increased in the late 1940s and continued until the mid-1980s, but has since declined to levels similar to 1900. In spite of the decline in collecting, the number of specimens of invasive species has strongly increased. The only other attempt to analyse botanical collecting in a large European region, an analysis of botanical recording in the British Isles 1836 to 1988, did not find a decline by the mid-1980s. For the United States, an analysis of collecting between the 1890s and 1999 found that it peaked in the 1930s. Museum time-series (representing the same species collected at different times) have been integral to identifying temporal responses to environmental change, for example, changed flowering times in response to an earlier onset of spring and the change of a region's floristic composition. A possible way to combat the likely loss of time-series in European herbaria is for collection personal to engage with biology teachers at high schools and universities to encourage the collecting of local plants as part of courses in the life sciences. Citation: Renner S. S. & Rockinger A. 2016: Is plant collecting in Germany coming to an end? — Willdenowia 46: 93–97. doi: http://dx.doi.org/10.3372/wi.46.46106 Version of record first published online on 25 March 2016 ahead of inclusion in April 2016 issue.
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Understanding the extremely variable, complex shape and venation characters of angiosperm leaves is one of the most challenging problems in botany. Machine learning offers opportunities to analyze large numbers of specimens, to discover novel leaf features of angiosperm clades that may have phylogenetic significance, and to use those characters to classify unknowns. Previous computer vision approaches have primarily focused on leaf identification at the species level. It remains an open question whether learning and classification are possible among major evolutionary groups such as families and orders, which usually contain hundreds to thousands of species each and exhibit many times the foliar variation of individual species. Here, we tested whether a computer vision algorithm could use a database of 7,597 leaf images from 2,001 genera to learn features of botanical families and orders, then classify novel images. The images are of cleared leaves, specimens that are chemically bleached, then stained to reveal venation. Machine learning was used to learn a codebook of visual elements representing leaf shape and venation patterns. The resulting automated system learned to classify images into families and orders with a success rate many times greater than chance. Of direct botanical interest, the responses of diagnostic features can be visualized on leaf images as heat maps, which are likely to prompt recognition and evolutionary interpretation of a wealth of novel morphological characters. With assistance from computer vision, leaves are poised to make numerous new contributions to systematic and paleobotanical studies.
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Rapid changes to the biosphere are altering ecological processes worldwide. Developing informed policies for mitigating the impacts of environmental change requires an exponential increase in the quantity, diversity, and resolution of field-collected data, which, in turn, necessitates greater reliance on innovative technologies to monitor ecological processes across local to global scales. Automated digital time-lapse cameras – “phenocams” – can monitor vegetation status and environmental changes over long periods of time. Phenocams are ideal for documenting changes in phenology, snow cover, fire frequency, and other disturbance events. However, effective monitoring of global environmental change with phenocams requires adoption of data standards. New continental-scale ecological research networks, such as the US National Ecological Observatory Network (NEON) and the European Union's Integrated Carbon Observation System (ICOS), can serve as templates for developing rigorous data standards and extending the utility of phenocam data through standardized ground-truthing. Open-source tools for analysis, visualization, and collaboration will make phenocam data more widely usable.
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Context Just as the timing of the vegetative growing season affects a host of ecological processes, the seasonality of floral availability impacts ecological processes from nectar availability and allergen production to competition for pollinator attention. However, no existing methodology is capable of evaluating multi-species bloom phenology in a standardized fashion across multiple ecosystems or compositionally distinct local flora. Thus, the manner in which the onset of the bloom season (during which the majority of species flower) differs along climate gradients and among distinct local flora remains largely unknown. Objectives This study evaluates differences in the timing of the bloom season throughout the western United States, and the relationship of the bloom season to the vegetative growing season and to local climate conditions. Methods This study estimated the season during which all but the earliest and latest 5 % of local species flower (the bloom season) using digital herbarium records. Bloom season timing was compared to land surface phenology, SI-x phenoclimate metrics, and PRISM climate normals. Results Local differences in mean temperature of the coldest month explained 76 % of observed variation in bloom season onset. Variation in land surface phenology explained 50 % of observed variation, while SI-x Bloom estimates explained 64 % of observed variation in bloom season onset. Conclusions These results confirm that bloom season phenology is distinct from the vegetative growing season, and that local temperature is a good predictor of bloom season onset. This work represents a new modality for studying multi-taxa flowering phenology at landscape and regional scales.
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Phenology has achieved a prominent position in current scenarios of global change research given its role in monitoring and predicting the timing of recurrent life cycle events. However, the implications of phenology to environmental conservation and management remain poorly explored. Here, we present the first explicit appraisal of how phenology — a multidisciplinary science encompassing biometeorology, ecology, and evolutionary biology — can make a key contribution to contemporary conservation biology. We focus on shifts in plant phenology induced by global change, their impacts on species diversity and plant–animal interactions in the tropics, and how conservation efforts could be enhanced in relation to plant resource organization. We identify the effects of phenological changes and mismatches in the maintenance and conservation of mutualistic interactions, and examine how phenological research can contribute to evaluate, manage and mitigate the consequences of land-use change and other natural and anthropogenic disturbances, such as fire, exotic and invasive species. We also identify cutting-edge tools that can improve the spatial and temporal coverage of phenological monitoring, from satellites to drones and digital cameras. We highlight the role of historical information in recovering long-term phenological time series, and track climate-related shifts in tropical systems. Finally, we propose a set of measures to boost the contribution of phenology to conservation science. We advocate the inclusion of phenology into predictive models integrating evolutionary history to identify species groups that are either resilient or sensitive to future climate-change scenarios, and understand how phenological mismatches can affect community dynamics, ecosystem services, and conservation over time.
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For most species, a precise understanding of how climatic parameters determine the timing of seasonal life cycle stages is constrained by limited long-term data. Further, most long-term studies of plant phenology that have examined relationships between phenological timing and climate have been local in scale or have focused on single climatic parameters. Herbarium specimens, however, can expand the temporal and spatial coverage of phenological datasets. Using Trillium ovatum specimens collected over > 100 yr across its native range, we analyzed how seasonal climatic conditions (mean minimum temperature (Tmin ), mean maximum temperature and total precipitation (PPT)) affect flowering phenology. We then examined long-term changes in climatic conditions and in the timing of flowering across T. ovatum's range. Warmer Tmin advanced flowering, whereas higher PPT delayed flowering. However, Tmin and PPT were shown to interact: the advancing effect of warmer Tmin was strongest where PPT was highest, and the delaying effect of higher PPT was strongest where Tmin was coldest. The direction of temporal change in climatic parameters and in the timing of flowering was dependent on geographic location. Tmin , for example, decreased across the observation period in coastal regions, but increased in inland areas. Our results highlight the complex effects of climate and geographic location on phenology.
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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.
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Recent herbarium-based phenology assessments of many plant species have found significant responses to global climate change over the previous century. In this study, we investigate how the flowering phenology of three alpine ginger Roscoea species responses to climate change over the century from 1913 to 2011, by comparing between herbarium-based phenology records and direct flowering observations. According to the observations, flowering onset of the three alpine ginger species occurred either 22 days earlier or was delayed by 8-30 days when comparing the mean peak flowering date between herbarium-based phenology records and direct flowering observations. It is likely that this significant change in flowering onset is due to increased annual minimum and maximum temperatures and mean annual temperature by about 0.053 C per year. Our results also show that flowering time changes occurred due to an increasing winter spring minimum temperature and monsoon minimum temperature, suggesting that these Roscoea species respond greatly to climate warming resulting in changes on flowering times.
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Recent herbarium-based phenology assessments of many plant species have found significant responses to global climate change over the previous century. In this study, we investigate how the flowering phenology of three alpine ginger Roscoea species responses to climate change over the century from 1913 to 2011, by comparing between herbarium-based phenology records and direct flowering observations. According to the observations, flowering onset of the three alpine ginger species occurred either 22 days earlier or was delayed by 8e30 days when comparing the mean peak flowering date between herbarium-based phenology records and direct flowering observations. It is likely that this significant change in flowering onset is due to increased annual minimum and maximum temperatures and mean annual temperature by about 0.053�C per year. Our results also show that flowering time changes occurred due to an increasing winter spring minimum temperature and monsoon minimum temperature, suggesting that these Roscoea species respond greatly to climate warming resulting in changes on flowering times.
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Earlier spring leaf unfolding is a frequently observed response of plants to climate warming. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in chilling may counteract the advance of leaf unfolding in response to warming. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C(-1) during 1980-1994 to 2.3 ± 1.6 days °C(-1) during 1999-2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24-30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as 'photoperiod limitation' mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.
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To access a full text version of this paper plus supplementary materials, navigate to: http://www.bioone.org/toc/apps/3/9 Effective workflows are essential components in the digitization of biodiversity specimen collections. To date, no comprehensive, community-vetted workflows have been published for digitizing flat sheets and packets of plants, algae, and fungi, even though latest estimates suggest that only 33% of herbarium specimens have been digitally transcribed, 54% of herbaria use a specimen database, and 24% are imaging specimens. In 2012, iDigBio, the U.S. National Science Foundation’s (NSF) coordinating center and national resource for the digitization of public, nonfederal U.S. collections, launched several working groups to address this deficiency. Here, we report the development of 14 workflow modules with 7–36 tasks each. These workflows represent the combined work of approximately 35 curators, directors, and collections managers representing more than 30 herbaria, including 15 NSF-supported plant-related Thematic Collections Networks and collaboratives. The workflows are provided for download as Portable Document Format (PDF) and Microsoft Word files. Customization of these workflows for specific institutional implementation is encouraged.
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The growth stages of development of many cultivated plants have been described by numerous scientists according to the principles of the extended BBCH scale within the last 19 years. The BBCH scales are now well- known worldwide and are used by research, administration and practise in agriculture and horticulture, as in the phenology as an integrative science in environment, meteorology and climatology. This fact indicates that the basic objectives and hope have been reached, justifying the practical approach taken by the authors of this scale. The BBCH scale is a contribution to improve the communication between different groups of scientists and to allow the interchange of data and scientific results in a transparent way. The BBCH scales have turned out helpful and practical. The aim to cause the harmonisation in the application of decimal codes for the description of the phenological growth stages of plants and weeds was reached. They also fulfilled the hope of the initiators to contribute with it to the improvement of the international agrarian-scientific and interdisciplinary communication. This paper will describe the history and background of the BBCH scales. The original publications are described and explained with reference of the original literature sources. The paper will describe the different area of use of the scales and list the different scientific disciplines using them. The worldwide success of the BBCH scales is the work of many scientists around the globe.
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• Mountainous regions support high plant productivity, diversity, and endemism, yet are highly vulnerable to climate change. Historical records and model predictions show increasing temperatures across high elevation regions including the Southern Rocky Mountains, which can have a strong influence on the performance and distribution of montane plant species. Rare plant species can be particularly vulnerable to climate change because of their limited abundance and distribution.• We tracked the phenology of rare and endemic species, which are identified as imperiled, across three different habitat types with herbarium records to determine if flowering time has changed over the last century, and if phenological change was related to shifts in climate.• We found that the flowering date of rare species has accelerated 3.1 d every decade (42 d total) since the late 1800s, with plants in sagebrush interbasins showing the strongest accelerations in phenology. High winter temperatures were associated with the acceleration of phenology in low elevation sagebrush and barren river habitats, whereas high spring temperatures explained accelerated phenology in the high elevation alpine habitat. In contrast, high spring temperatures delayed the phenology of plant species in the two low-elevation habitats and precipitation had mixed effects depending on the season.• These results provide evidence for large shifts in the phenology of rare Rocky Mountain plants related to climate, which can have strong effects on plant fitness, the abundance of associated wildlife, and the future of plant conservation in mountainous regions. © 2015 Botanical Society of America, Inc.
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We investigate the utility of using historical data sources to track changes in flowering time of coastal species in south-eastern Australia in response to recent climate warming. Studies of this nature in the southern hemisphere are rare, mainly because of a paucity of long-term data sources. Despite this, we found there is considerable potential to utilise existing data sourced from herbaria collections and field naturalists' notes and diaries to identify native plant species suitable as biological indicators of climate change. Of 101 candidate species investigated in the present study, eight were identified as showing a general trend towards earlier flowering over time, indicating a correlation with increasing temperatures. There was some evidence to suggest that species which flower in spring and summer may be more sensitive to changes in temperature. There was a high level of uncertainty regarding the detection of trends, which was a function of the accessibility, abundance and accuracy of the various data sources. However, this uncertainty could be resolved in future studies by combining the datasets from the present study with field monitoring of phenological cycles in climatically different locations. Data held by community groups could be made more accessible if there was a concerted effort to fund collation and digitisation of these records. This might best be achieved by working with community groups, and facilitated through the recent establishment of a community phenological observation database in Australia.
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A goal of the biodiversity research community is to digitize the majority of the one billion specimens in US collections by 2020. Meeting this ambitious goal requires increased collaboration and technological innovation and broader engagement beyond the walls of universities and museums. Engaging the public in digitization promises to both serve the digitizing institutions and further the public understanding of biodiversity science. We discuss three broad areas accessible to public participants that will accelerate research progress: label and ledger transcription, georeferencing from locality descriptions, and specimen annotation from images. We illustrate each activity, compare useful tools, present best practices and standards, and identify gaps in our knowledge and areas for improvement. The field of public participation in digitization of biodiversity research specimens is in a growth phase with many emerging opportunities for scientists, educators, and the public, as well as broader communication with complementary projects in other areas (e.g., the digital humanities).
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