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.

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.

Plant and bird phenology and plant occurrence from 1851 to 2020 (non-continuous) in Thoreau's Concord, Massachusetts.

Concord, Massachusetts, USA has served as an active location for phenological observations since philosopher and naturalist Henry David Thoreau began recording plant and animal occurrence and phenology in 1851. Since that time, numerous naturalists, scientists, and researchers have continued this tradition, creating an invaluable time series of 758 species in a single location. In total, 13,441 phenological records, spanning 118 years, now exist, with observations of many species ongoing. Relative abundance data for an additional 200 plant species is also provided. Thoreau's published journals and records in Special Collections libraries at the Concord Free Public Library, Harvard University, Peabody Essex Museum, and Morgan Library and Museum provide insight into his methods of routinely walking around Walden Pond, through natural areas, and within the town of Concord, seeking the first leaf or flower on plants, seasonal observations of migratory birds, and fruit maturation times. Several amateur naturalists, and most recently the present research group, have followed this method of regularly searching Concord for the earliest signs of seasonal events, visiting many of the same locations including Walden Pond, the site made famous by Thoreau. While Thoreau's observations were initially made out of a curious desire to document the natural world, these data have led to dozens to contemporary studies, addressing timely issues such as climate change, conservation, ecology, and invasive species. This time series of data, initiated by Thoreau and continued by others, has resulted in dozens of peer-reviewed publications, a popular science book, and numerous educational and outreach opportunities. These data grow increasingly valuable with time and as new and creative studies are undertaken with Thoreau's historic records. No copyright restrictions apply to the use of this data set other than citing this publication.

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.

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.

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.

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.

Science in Places of Grandeur: Communication and Engagement in National Parks.

The USA has set aside over 400 national parks and other protected areas to be managed by the National Park Service (NPS). Collectively, these sites attract over 300 million visits per year which makes the NPS one of the largest informal education institutions in the country. Because the NPS supports and facilitates scientific studies in parks, the national park system provides abundant opportunity for biologists and other scientists to engage global audiences in learning, exploring, and even conducting science. Those opportunities are best pursued through collaborations among scientists and the professional communication staff (interpreters, educators, media specialists, etc.) of parks and their partner organizations. This article describes unique opportunities and rationale for such collaborations, presents several examples that highlight the range of activities and lessons drawn from them, and invites scientists to conduct studies in parks and bring their science into the public eye.

How training citizen scientists affects the accuracy and precision of phenological data.

Monitoring plant and animal phenology is a critical step to anticipating and predicting changes in species interactions and biodiversity. Because phenology necessarily involves frequent and repeated observations over time, citizen scientists have become a vital part of collecting phenological data. However, there is still concern over the accuracy and precision of citizen science data. It is possible that training citizen scientists can improve data quality though there are few comparisons of trained and untrained citizen scientists in the ability of each to accurately and precisely measure phenology. We assessed how three types of observers-experts, trained citizen scientists that make repeated observations, and untrained citizen scientists making once-per-year observations-differ in quantifying temporal change in flower and fruit abundance of American mountain ash trees (Sorbus americana Marsh.) and arthropods in Acadia National Park, Maine, USA. We found that trained more so than untrained citizen science observers over- or under-estimated abundances leading to precise but inaccurate characterizations of phenological patterns. Our results suggest a new type of bias induced by repeated observations: A type of learning takes place that reduces the independence of observations taken on different trees or different dates. Thus, in this and many other cases, having individuals make one-off observations of marked plants may produce data as good if not better than individuals making repeated observations. For citizen science programs related to phenology, our results underscore the importance of (a) attracting the most number of observers possible even if they only make one observation, (b) producing easy-to-use and informative data sheets, and

Phenology research for natural resource management in the United States.

Natural resource professionals in the United States recognize that climate-induced changes in phenology can substantially affect resource management. This is reflected in national climate change response plans recently released by major resource agencies. However, managers on-the-ground are often unclear about how to use phenological information to inform their management practices. Until recently, this was at least partially due to the lack of broad-based, standardized phenology data collection across taxa and geographic regions. Such efforts are now underway, albeit in very early stages. Nonetheless, a major hurdle still exists: phenology-linked climate change research has focused more on describing broad ecological changes rather than making direct connections to local to regional management concerns. To help researchers better design relevant research for use in conservation and management decision-making processes, we describe phenology-related research topics that facilitate "actionable" science. Examples include research on evolution and phenotypic plasticity related to vulnerability, the demographic consequences of trophic mismatch, the role of invasive species, and building robust ecological forecast models. Such efforts will increase phenology literacy among on-the-ground resource managers and provide information relevant for short- and long-term decision-making, particularly as related to climate response planning and implementing climate-informed monitoring in the context of adaptive management. In sum, we argue that phenological information is a crucial component of the resource management toolbox that facilitates identification and evaluation of strategies that will reduce the vulnerability of natural systems to climate change. Management-savvy researchers can play an important role in reaching this goal.

Standardized phenology monitoring methods to track plant and animal activity for science and resource management applications.

Phenology offers critical insights into the responses of species to climate change; shifts in species' phenologies can result in disruptions to the ecosystem processes and services upon which human livelihood depends. To better detect such shifts, scientists need long-term phenological records covering many taxa and across a broad geographic distribution. To date, phenological observation efforts across the USA have been geographically limited and have used different methods, making comparisons across sites and species difficult. To facilitate coordinated cross-site, cross-species, and geographically extensive phenological monitoring across the nation, the USA National Phenology Network has developed in situ monitoring protocols standardized across taxonomic groups and ecosystem types for terrestrial, freshwater, and marine plant and animal taxa. The protocols include elements that allow enhanced detection and description of phenological responses, including assessment of phenological "status", or the ability to track presence-absence of a particular phenophase, as well as standards for documenting the degree to which phenological activity is expressed in terms of intensity or abundance. Data collected by this method can be integrated with historical phenology data sets, enabling the development of databases for spatial and temporal assessment of changes in status and trends of disparate organisms. To build a common, spatially, and temporally extensive multi-taxa phenological data set available for a variety of research and science applications, we encourage scientists, resources managers, and others conducting ecological monitoring or research to consider utilization of these standardized protocols for tracking the seasonal activity of plants and animals.

Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate.

Variation in species' responses to abiotic phenological cues under climate change may cause changes in temporal overlap among interacting taxa, with potential demographic consequences. Here, we examine associations between the abiotic environment and plant-pollinator phenological synchrony using a long-term syrphid fly-flowering phenology dataset (1992-2011). Degree-days above freezing, precipitation, and timing of snow melt were investigated as predictors of phenology. Syrphids generally emerge after flowering onset and end their activity before the end of flowering. Neither flowering nor syrphid phenology has changed significantly over our 20-year record, consistent with a lack of directional change in climate variables over the same time frame. Instead we document interannual variability in the abiotic environment and phenology. Timing of snow melt was the best predictor of flowering onset and syrphid emergence. Snow melt and degree-days were the best predictors of the end of flowering, whereas degree-days and precipitation best predicted the end of the syrphid period. Flowering advanced at a faster rate than syrphids in response to both advancing snow melt and increasing temperature. Different rates of phenological advancements resulted in more days of temporal overlap between the flower-syrphid community in years of early snow melt because of extended activity periods. Phenological synchrony at the community level is therefore likely to be maintained for some time, even under advancing snow melt conditions that are evident over longer term records at our site. These results show that interacting taxa may respond to different phenological cues and to the same cues at different rates but still maintain phenological synchrony over a range of abiotic conditions. However, our results also indicate that some individual plant species may overlap with the syrphid community for fewer days under continued climate change. This highlights the role of interannual variation in these flower-syrphid interactions and shows that species-level responses can differ from community-level responses in nonintuitive ways.

Effects of warming temperatures on winning times in the Boston marathon.

It is not known whether global warming will affect winning times in endurance events, and counterbalance improvements in race performances that have occurred over the past century. We examined a time series (1933-2004) from the Boston Marathon to test for an effect of warming on winning times by men and women. We found that warmer temperatures and headwinds on the day of the race slow winning times. However, 1.6°C warming in annual temperatures in Boston between 1933 and 2004 did not consistently slow winning times because of high variability in temperatures on race day. Starting times for the race changed to earlier in the day beginning in 2006, making it difficult to anticipate effects of future warming on winning times. However, our models indicate that if race starting times had not changed and average race day temperatures had warmed by 0.058°C/yr, a high-end estimate, we would have had a 95% chance of detecting a consistent slowing of winning marathon times by 2100. If average race day temperatures had warmed by 0.028°C/yr, a mid-range estimate, we would have had a 64% chance of detecting a consistent slowing of winning times by 2100.

Forecasting phenology: from species variability to community patterns.

Shifts in species' phenology in response to climate change have wide-ranging consequences for ecological systems. However, significant variability in species' responses, together with limited data, frustrates efforts to forecast the consequences of ongoing phenological changes. Herein, we use a case study of three North American plant communities to explore the implications of variability across levels of organisation (within and among species, and among communities) for forecasting responses to climate change. We show how despite significant variation among species in sensitivities to climate, comparable patterns emerge at the community level once regional climate drivers are accounted for. However, communities differ with respect to projected patterns of divergence and overlap among their species' phenological distributions in response to climate change. These analyses and a review of hypotheses suggest how explicit consideration of spatial scale and levels of biological organisation may help to understand and forecast phenological responses to climate change.

Moving forward in global-change ecology: capitalizing on natural variability.

Natural resources managers are being asked to follow practices that accommodate for the impact of climate change on the ecosystems they manage, while global-ecosystems modelers aim to forecast future responses under different climate scenarios. However, the lack of scientific knowledge about short-term ecosystem responses to climate change has made it difficult to define set conservation practices or to realistically inform ecosystem models. Until recently, the main goal for ecologists was to study the composition and structure of communities and their implications for ecosystem function, but due to the probable magnitude and irreversibility of climate-change effects (species extinctions and loss of ecosystem function), a shorter term focus on responses of ecosystems to climate change is needed. We highlight several underutilized approaches for studying the ecological consequences of climate change that capitalize on the natural variability of the climate system at different temporal and spatial scales. For example, studying organismal responses to extreme climatic events can inform about the resilience of populations to global warming and contribute to the assessment of local extinctions. Translocation experiments and gene expression are particular useful to quantitate a species' acclimation potential to global warming. And studies along environmental gradients can guide habitat restoration and protection programs by identifying vulnerable species and sites. These approaches identify the processes and mechanisms underlying species acclimation to changing conditions, combine different analytical approaches, and can be used to improve forecasts of the short-term impacts of climate change and thus inform conservation practices and ecosystem models in a meaningful way.

Toward a synthetic understanding of the role of phenology in ecology and evolution.

Phenology affects nearly all aspects of ecology and evolution. Virtually all biological phenomena-from individual physiology to interspecific relationships to global nutrient fluxes-have annual cycles and are influenced by the timing of abiotic events. Recent years have seen a surge of interest in this topic, as an increasing number of studies document phenological responses to climate change. Much recent research has addressed the genetic controls on phenology, modelling techniques and ecosystem-level and evolutionary consequences of phenological change. To date, however, these efforts have tended to proceed independently. Here, we bring together some of these disparate lines of inquiry to clarify vocabulary, facilitate comparisons among habitat types and promote the integration of ideas and methodologies across different disciplines and scales. We discuss the relationship between phenology and life history, the distinction between organismal- and population-level perspectives on phenology and the influence of phenology on evolutionary processes, communities and ecosystems. Future work should focus on linking ecological and physiological aspects of phenology, understanding the demographic effects of phenological change and explicitly accounting for seasonality and phenology in forecasts of ecological and evolutionary responses to climate change.

The effects of phenological mismatches on demography.

Climate change is altering the phenology of species across the world, but what are the consequences of these phenological changes for the demography and population dynamics of species? Time-sensitive relationships, such as migration, breeding and predation, may be disrupted or altered, which may in turn alter the rates of reproduction and survival, leading some populations to decline and others to increase in abundance. However, finding evidence for disrupted relationships, or lack thereof, and their demographic effects, is difficult because the necessary detailed observational data are rare. Moreover, we do not know how sensitive species will generally be to phenological mismatches when they occur. Existing long-term studies provide preliminary data for analysing the phenology and demography of species in several locations. In many instances, though, observational protocols may need to be optimized to characterize timing-based multi-trophic interactions. As a basis for future research, we outline some of the key questions and approaches to improving our understanding of the relationships among phenology, demography and climate in a multi-trophic context. There are many challenges associated with this line of research, not the least of which is the need for detailed, long-term data on many organisms in a single system. However, we identify key questions that can be addressed with data that already exist and propose approaches that could guide future research.