Ten best practices for effective phenological research.

The number and diversity of phenological studies has increased rapidly in recent years. Innovative experiments, field studies, citizen science projects, and analyses of newly available historical data are contributing insights that advance our understanding of ecological and evolutionary responses to the environment, particularly climate change. However, many phenological data sets have peculiarities that are not immediately obvious and can lead to mistakes in analyses and interpretation of results. This paper aims to help researchers, especially those new to the field of phenology, understand challenges and practices that are crucial for effective studies. For example, researchers may fail to account for sampling biases in phenological data, struggle to choose or design a volunteer data collection strategy that adequately fits their project's needs, or combine data sets in inappropriate ways. We describe ten best practices for designing studies of plant and animal phenology, evaluating data quality, and analyzing data. Practices include accounting for common biases in data, using effective citizen or community science methods, and employing appropriate data when investigating phenological mismatches. We present these best practices to help researchers entering the field take full advantage of the wealth of available data and approaches to advance our understanding of phenology and its implications for ecology.

Functional traits influence patterns in vegetative and reproductive plant phenology - a multi-botanical garden study.

Phenology has emerged as key indicator of the biological impacts of climate change, yet the role of functional traits constraining variation in herbaceous species' phenology has received little attention. Botanical gardens are ideal places in which to investigate large numbers of species growing under common climate conditions. We ask whether interspecific variation in plant phenology is influenced by differences in functional traits. We recorded onset, end, duration and intensity of initial growth, leafing out, leaf senescence, flowering and fruiting for 212 species across five botanical gardens in Germany. We measured functional traits, including plant height, absolute and specific leaf area, leaf dry matter content, leaf carbon and nitrogen content and seed mass and accounted for species' relatedness. Closely related species showed greater similarities in timing of phenological events than expected by chance, but species' traits had a high degree of explanatory power, pointing to paramount importance of species' life-history strategies. Taller plants showed later timing of initial growth, and flowered, fruited and underwent leaf senescence later. Large-leaved species had shorter flowering and fruiting durations. Taller, large-leaved species differ in their phenology and are more competitive than smaller, small-leaved species. We assume climate warming will change plant communities' competitive hierarchies with consequences for biodiversity.

Conservation ethics in the time of the pandemic: Does increasing remote access advance social justice?

The COVID-19 pandemic is stimulating improvements in remote access and use of technology in conservation-related programs and research. In many cases, organizations have intended for remote engagement to benefit groups that have been marginalized in the sciences. But are they? It is important to consider how remote access affects social justice in conservation biology-i.e., the principle that all people should be equally respected and valued in conservation organizations, programs, projects, and practices. To support such consideration, we describe a typology of justice-oriented principles that can be used to examine social justice in a range of conservation activities. We apply this typology to three conservation areas: (1) remote access to US national park educational programs and data; (2) digitization of natural history specimens and their use in conservation research; and (3) remote engagement in conservation-oriented citizen science. We then address the questions: Which justice-oriented principles are salient in which conservation contexts or activities? How can those principles be best realized in those contexts or activities? In each of the three areas we examined, remote access increased participation, but access and benefits were not equally distributed and unanticipated consequences have not been adequately addressed. We identify steps that can and are being taken to advance social justice in conservation, such as assessing programs to determine if they are achieving their stated social justice-oriented aims and revising initiatives as needed. The framework that we present could be used to assess the social justice dimensions of many conservation programs, institutions, practices, and policies.

A comparison of herbarium and citizen science phenology datasets for detecting response of flowering time to climate change in Denmark.

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.

The growing and vital role of botanical gardens in climate change research.

Botanical gardens make unique contributions to climate change research, conservation, and public engagement. They host unique resources, including diverse collections of plant species growing in natural conditions, historical records, and expert staff, and attract large numbers of visitors and volunteers. Networks of botanical gardens spanning biomes and continents can expand the value of these resources. Over the past decade, research at botanical gardens has advanced our understanding of climate change impacts on plant phenology, physiology, anatomy, and conservation. For example, researchers have utilized botanical garden networks to assess anatomical and functional traits associated with phenological responses to climate change. New methods have enhanced the pace and impact of this research, including phylogenetic and comparative methods, and online databases of herbarium specimens and photographs that allow studies to expand geographically, temporally, and taxonomically in scope. Botanical gardens have grown their community and citizen science programs, informing the public about climate change and monitoring plants more intensively than is possible with garden staff alone. Despite these advances, botanical gardens are still underutilized in climate change research. To address this, we review recent progress and describe promising future directions for research and public engagement at botanical gardens.

Siberian plants shift their phenology in response to climate change.

Siberia has undergone dramatic climatic changes due to global warming in recent decades. Yet, the ecological responses to these climatic changes are still poorly understood due to a lack of data. Here, we use a unique data set from the Russian 'Chronicles of Nature' network to analyse the long-term (1976-2018) phenological shifts in leaf out, flowering, fruiting and senescence of 67 common Siberian plant species. We find that Siberian boreal forest plants advanced their early season (leaf out and flowering) and mid-season (fruiting) phenology by -2.2, -0.7 and -1.6 days/decade, and delayed the onset of senescence by 1.6 days/decade during this period. These mean values, however, are subject to substantial intraspecific variability, which is partly explained by the plants' growth forms. Trees and shrubs advanced leaf out and flowering (-3.1 and -3.3. days/decade) faster than herbs (-1 day/decade), presumably due to the more direct exposure of leaf and flower buds to ambient air for the woody vegetation. For senescence, we detected a reverse pattern: stronger delays in herbs (2.1 days/decade) than in woody plants (1.0-1.2 days/decade), presumably due to the stronger effects of autumn frosts on the leaves of herbs. Interestingly, the timing of fruiting in all four growth forms advanced at similar paces, from 1.4 days/decade in shrubs to 1.7 days/decade in trees and herbs. Our findings point to a strong, yet heterogeneous, response of Siberian plant phenology to recent global warming. Furthermore, the results highlight that species- and growth form-specific differences among study species could be used to identify plants particularly at risk of decline due to their low adaptive capacity or a loss of synchronization with important interaction partners.

Comparing fruiting phenology across two historical datasets: Thoreau's observations and herbarium specimens.

BACKGROUND AND AIMS: Fruiting remains under-represented in long-term phenology records, relative to leaf and flower phenology. Herbarium specimens and historical field notes can fill this gap, but selecting and synthesizing these records for modern-day comparison requires an understanding of whether different historical data sources contain similar information, and whether similar, but not equivalent, fruiting metrics are comparable with one another. METHODS: For 67 fleshy-fruited plant species, we compared observations of fruiting phenology made by Henry David Thoreau in Concord, Massachusetts (1850s), with phenology data gathered from herbarium specimens collected across New England (mid-1800s to 2000s). To identify whether fruiting times and the order of fruiting among species are similar between datasets, we compared dates of first, peak and last observed fruiting (recorded by Thoreau), and earliest, mean and latest specimen (collected from herbarium records), as well as fruiting durations. KEY RESULTS: On average, earliest herbarium specimen dates were earlier than first fruiting dates observed by Thoreau; mean specimen dates were similar to Thoreau's peak fruiting dates; latest specimen dates were later than Thoreau's last fruiting dates; and durations of fruiting captured by herbarium specimens were longer than durations of fruiting observed by Thoreau. All metrics of fruiting phenology except duration were significantly, positively correlated within (r: 0.69-0.88) and between (r: 0.59-0.85) datasets. CONCLUSIONS: Strong correlations in fruiting phenology between Thoreau's observations and data from herbaria suggest that field and herbarium methods capture similar broad-scale phenological information, including relative fruiting times among plant species in New England. Differences in the timing of first, last and duration of fruiting suggest that historical datasets collected with different methods, scales and metrics may not be comparable when exact timing is important. Researchers should strongly consider matching methodology when selecting historical records of fruiting phenology for present-day comparisons.

Macrophenology: insights into the broad-scale patterns, drivers, and consequences of phenology.

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.

New social trails made during the pandemic increase fragmentation of an urban protected area.

Urban protected areas are an important resource to people and wildlife, providing many ecosystem services. During the initial phase of the COVID-19 pandemic lockdown during March-June 2020, there was a major increase in the number of hikers and bicyclists in urban protected areas, including the Webster Woods in Newton, Massachusetts (USA), an 82.5-ha protected area. The Webster Woods is one of the largest protected areas near the center of Boston and is widely used in conservation textbooks as an example of the effects of habitat fragmentation on the amount of undisturbed habitat. Prior to the pandemic, the Webster Woods had been extensively fragmented by paved roads, dirt roads, and trails, with little interior habitat remaining. During the first four months of the pandemic, hikers and bicyclists made 4.9 km of new social (or informal) trails, an increase of 36%. This recent fragmentation represents a dramatic increase in the level of human impact on the area, reducing the amount of interior habitat from 3.2 to 2.1 ha. Levels of human activity returned to pre-pandemic levels in autumn 2020 and city officials have started closing access to some of the new trails, allowing vegetation to regrow. It is possible that similar increases in social trails and associated fragmentation have occurred in other protected areas (especially those in urban areas) around the world due to the pandemic, and these disturbances should be evaluated for their effects on plant and animal populations.

Effects of the COVID-19 pandemic on noise pollution in three protected areas in metropolitan Boston (USA).

Noise pollution can reduce the ability of urban protected areas to provide a refuge for people and habitat for wildlife. Amidst an unprecedented global pandemic, it is unknown if the changes in human activity have significantly impacted noise pollution in metropolitan parks. We tested the hypothesis that reduced human activity associated with the COVID-19 pandemic lockdowns would lead to reduced sound levels in protected areas compared with non-pandemic times. We measured sound levels in three urban protected areas in metropolitan Boston, MA (USA) at three time periods: in the fall and summer before the pandemic, immediately after the government-imposed lockdown in March 2020 when the trees were leafless, and during the beginning of reopening in early June 2020 when the trees had leaves. At all time periods, sound levels were highest near major roads and demonstrated a logarithmic decrease further from roads. At the two protected areas closest to the city center, sound levels averaged 1-3 dB lower during the time of the pandemic lockdown. In contrast, at the third protected area, which is transected by a major highway, sound levels were 4-6 dB higher during the time of the pandemic, likely because reduced traffic allowed vehicles to travel faster and create more noise. This study demonstrates that altered human levels of activity, in this case associated with the COVID-19 pandemic, can have major, and in some cases unexpected, effects on the levels of noise pollution in protected areas.

COVID-19 pandemic impacts on conservation research, management, and public engagement in US national parks.

The COVID-19 pandemic has disrupted the timing and substance of conservation research, management, and public engagement in protected areas around the world. This disruption is evident in US national parks, which play a key role in protecting natural and cultural resources and providing outdoor experiences for the public. Collectively, US national parks protect 34 million ha, host more than 300 million visits annually, and serve as one of the world's largest informal education organizations. The pandemic has altered park conditions and operations in a variety of ways. Shifts in operational conditions related to safety issues, reduced staffing, and decreased park revenues have forced managers to make difficult trade-offs among competing priorities. Long-term research and monitoring of the health of ecosystems and wildlife populations have been interrupted. Time-sensitive management practices, such as control of invasive plants and restoration of degraded habitat, have been delayed. And public engagement has largely shifted from in-person experiences to virtual engagement through social media and other online interactions. These changes pose challenges for accomplishing important science, management, and public engagement goals, but they also create opportunities for developing more flexible monitoring programs and inclusive methods of public engagement. The COVID-19 pandemic reinforces the need for strategic science, management planning, flexible operations, and online public engagement to help managers address rapid and unpredictable challenges.

Global COVID-19 lockdown highlights humans as both threats and custodians of the environment.

The global lockdown to mitigate COVID-19 pandemic health risks has altered human interactions with nature. Here, we report immediate impacts of changes in human activities on wildlife and environmental threats during the early lockdown months of 2020, based on 877 qualitative reports and 332 quantitative assessments from 89 different studies. Hundreds of reports of unusual species observations from around the world suggest that animals quickly responded to the reductions in human presence. However, negative effects of lockdown on conservation also emerged, as confinement resulted in some park officials being unable to perform conservation, restoration and enforcement tasks, resulting in local increases in illegal activities such as hunting. Overall, there is a complex mixture of positive and negative effects of the pandemic lockdown on nature, all of which have the potential to lead to cascading responses which in turn impact wildlife and nature conservation. While the net effect of the lockdown will need to be assessed over years as data becomes available and persistent effects emerge, immediate responses were detected across the world. Thus, initial qualitative and quantitative data arising from this serendipitous global quasi-experimental perturbation highlights the dual role that humans play in threatening and protecting species and ecosystems. Pathways to favorably tilt this delicate balance include reducing impacts and increasing conservation effectiveness.

COVID-19 pandemic and associated lockdown as a "Global Human Confinement Experiment" to investigate biodiversity conservation.

Efforts to curtail the spread of the novel coronavirus (SARS-CoV2) have led to the unprecedented concurrent confinement of nearly two-thirds of the global population. The large human lockdown and its eventual relaxation can be viewed as a Global Human Confinement Experiment. This experiment is a unique opportunity to identify positive and negative effects of human presence and mobility on a range of natural systems, including wildlife, and protected areas, and to study processes regulating biodiversity and ecosystems. We encourage ecologists, environmental scientists, and resource managers to contribute their observations to efforts aiming to build comprehensive global understanding based on multiple data streams, including anecdotal observations, systematic assessments and quantitative monitoring. We argue that the collective power of combining diverse data will transcend the limited value of the individual data sets and produce unexpected insights. We can also consider the confinement experiment as a "stress test" to evaluate the strengths and weaknesses in the adequacy of existing networks to detect human impacts on natural systems. Doing so will provide evidence for the value of the conservation strategies that are presently in place, and create future networks, observatories and policies that are more adept in protecting biological diversity across the world.

Phenological mismatch with trees reduces wildflower carbon budgets.

Interacting species can respond differently to climate change, causing unexpected consequences. Many understorey wildflowers in deciduous forests leaf out and flower in the spring when light availability is the highest before overstorey canopy closure. Therefore, different phenological responses by understorey and overstorey species to increased spring temperature could have significant ecological implications. Pairing contemporary data with historical observations initiated by Henry David Thoreau (1850s), we found that overstorey tree leaf out is more responsive to increased spring temperature than understorey wildflower phenology, resulting in shorter periods of high light in the understorey before wildflowers are shaded by tree canopies. Because of this overstorey-understorey mismatch, we estimate that wildflower spring carbon budgets in the northeastern United States were 12-26% larger during Thoreau's era and project a 10-48% reduction during this century. This underappreciated phenomenon may have already reduced wildflower fitness and could lead to future population declines in these ecologically important species.

Leaf longevity in temperate evergreen species is related to phylogeny and leaf size.

Leaf longevity (LL), the amount of time a photosynthetically active leaf remains on a plant, is an important trait of evergreen species, affecting physiological ecology and ecosystem processes. A long LL gives leaves more time to fix carbon but carries higher construction costs, while a short LL allows plants to respond more rapidly to changing environmental conditions. For many evergreen taxa, LL data are not readily available, and it is not known if LL is phylogenetically conserved. To address this gap, we measured LL for 169 temperate and boreal evergreen woody species at the Arnold Arboretum, a botanical garden in Boston, Massachusetts, along with metrics of leaf size and number known to be related to LL. We hypothesized that LL is phylogenetically conserved, and that longer LL is associated with a greater numbers of leaves, smaller leaves, and a colder hardiness zone of the species' native range. We found that average LL ranged from 1.4 years in Rhododendron tomentosum to 10.5 years in Abies cilicia. LL was phylogenetically conserved, with some genera, such as Abies and Picea, exhibiting long LL (> 3 years) and others, such as Ilex and Rhododendron, exhibiting short LL (< 3 years). Leaf length was negatively correlated with LL in conifers, due to differences between Pinus and other genera; however, there was no correlation between LL and number of leaves. This study highlights the considerable variation and phylogenetic pattern in LL among temperate evergreen species, which has implications for carbon budgets and ecosystem models.

Drivers of vegetative dormancy across herbaceous perennial plant species.

Vegetative dormancy, that is the temporary absence of aboveground growth for ≥ 1 year, is paradoxical, because plants cannot photosynthesise or flower during dormant periods. We test ecological and evolutionary hypotheses for its widespread persistence. We show that dormancy has evolved numerous times. Most species displaying dormancy exhibit life-history costs of sprouting, and of dormancy. Short-lived and mycoheterotrophic species have higher proportions of dormant plants than long-lived species and species with other nutritional modes. Foliage loss is associated with higher future dormancy levels, suggesting that carbon limitation promotes dormancy. Maximum dormancy duration is shorter under higher precipitation and at higher latitudes, the latter suggesting an important role for competition or herbivory. Study length affects estimates of some demographic parameters. Our results identify life historical and environmental drivers of dormancy. We also highlight the evolutionary importance of the little understood costs of sprouting and growth, latitudinal stress gradients and mixed nutritional modes.

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

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

Local environment, not local adaptation, drives leaf-out phenology in common gardens along an elevational gradient in Acadia National Park, Maine.

PREMISE OF THE STUDY: Climate-driven changes in phenology are substantially affecting ecological relationships and ecosystem processes. The role of variation among species has received particular attention; for example, variation among species' phenological responses to climate can disrupt trophic interactions and can influence plant performance. Variation within species in phenological responses to climate, however, has received much less attention, despite its potential role in ecological interactions and local adaptation to climate change. METHODS: We constructed three common gardens across an elevation gradient on Cadillac Mountain in Acadia National Park, Maine, to test population-level responses in leaf-out phenology in a reciprocal transplant experiment. The experiment included three native species: low bush blueberry (Vaccinium angustifolium), sheep's laurel (Kalmia angustifolia), and three-toothed cinquefoil (Sibbaldiopsis tridentata). KEY RESULTS: Evidence for local adaptation of phenological response to temperature varied among the species, but was weak for all three. Rather, variation in phenological response to temperature appeared to be driven by local microclimate at each garden site and year-to-year variation in temperature. CONCLUSIONS: Population-level adaptations in leaf-out phenology appear to be relatively unimportant for these species in Acadia National Park, perhaps a reflection of strong genetic mixing across elevations, or weak differences in selection on phenological response to spring temperatures at different elevations. These results concur with other observational data in Acadia and highlight the utility of experimental approaches to understand the importance of annual and local site variation in affecting phenology both among and within plant species.

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

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