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.

Volunteer-contributed observations of flowering often correlate with airborne pollen concentrations.

Characterizing airborne pollen concentrations is crucial for supporting allergy and asthma management; however, pollen monitoring is labor intensive and, in the USA, geographically limited. The USA National Phenology Network (USA-NPN) engages thousands of volunteer observers in regularly documenting the developmental and reproductive status of plants. The reports of flower and pollen cone status contributed to the USA-NPN's platform, Nature's Notebook, have the potential to help address gaps in pollen monitoring by providing real-time, spatially explicit information from across the country. In this study, we assessed whether observations of flower and pollen cone status contributed to Nature's Notebook can serve as effective proxies for airborne pollen concentrations. We compared daily pollen concentrations from 36 National Allergy Bureau (NAB) stations in the USA with flowering and pollen cone status observations collected within 200 km of each NAB station in each year, 2009-2021, for 15 common tree taxa using Spearman's correlations. Of 350 comparisons, 58% of correlations were significant (p < 0.05). Comparisons could be made at the largest numbers of sites for Acer and Quercus. Quercus demonstrated a comparatively high proportion of tests with significant agreement (median ρ = 0.49). Juglans demonstrated the strongest overall coherence between the two datasets (median ρ = 0.79), though comparisons were made at only a small number of sites. For particular taxa, volunteer-contributed flowering status observations demonstrate promise to indicate seasonal patterns in airborne pollen concentrations. The quantity of observations, and therefore, their utility for supporting pollen alerts, could be substantially increased through a formal observation campaign.

How consistently do species leaf-out or flower in the same order? Understanding the factors that shape this characteristic of plant communities.

Plant species are frequently reported to undergo leaf-out and flowering in a consistent order from 1 year to the next; however, only a limited number of these findings arise from studies encompassing many species or sites. Here, we evaluate the consistency in the order species leafed out in the northeastern United States using observations contributed to the USA National Phenology Network's Nature's Notebook platform. We repeated this analysis for flowering, evaluating a total of 132 species across 84 sites. We documented a relatively high degree of consistency in the order of both events among individual plants, with higher consistency in flowering. A small number of species pairs exhibited very high consistency in phenological order across several sites. The majority of species pairs exhibited variability in how consistently they underwent either leaf-out or flowering from site to site, which could be the result of either plastic or locally adaptive responses. Our investigation revealed that neither functional type nor seasonal position played a major role in shaping how consistently species leafed out or flowered in the same order. Instead, we found the number of days separating the events and interannual variability in timing to be the most influential factors driving the consistency in ordering.

Updates to standardized plant and animal observation protocols of the USA National Phenology Network.

The USA National Phenology Network (USA-NPN) was established to coordinate the collection of rigorous, high-quality phenology observations to support scientific discovery and management decisions and to increase awareness of phenology, its relationship to environmental conditions and its influence on ecosystems. A cornerstone of the USA-NPN's infrastructure and data collection activities is a suite of rigorous, standardized phenology observation protocols, published in 2014 (Denny et al., Int J Biometeorol 58:591-601, 2014). In the years since, users have requested modifications and additions to the existing protocols. Here, we describe changes that have been made to the original protocols since their publication in 2014. These modifications have been made to reduce confusion in the phenophase definitions, include new taxonomic groups, and expand protocols to more fully capture certain life cycle stages. We anticipate continued expansion of the protocols and future updates can be found in the University of Arizona Research Data Repository (USA National Phenology Network 2014).

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.

COVID-19 impacts on participation in large scale biodiversity-themed community science projects in the United States.

Shutdowns associated with the COVID-19 pandemic have had extensive impacts on professional and volunteer-based biodiversity and conservation efforts. We evaluated the impact of the widespread pandemic-related closures in the spring of 2020 on participation patterns and rates on a national and a state-by-state basis in the United States in four biodiversity-themed community science programs: eBird, eButterfly, iNaturalist, and Nature's Notebook. We compared the number of participants, observations submitted, and proportion of observations collected in urban environments in spring 2020 to the expected values for these metrics based on activity in the previous five years (2015-2019), which in many cases exhibited underlying growth. At the national scale, eButterfly and Nature's Notebook exhibited declines in the number of participants and number of observations submitted during the spring of 2020 and iNaturalist and eBird showed growth in both measures. On a state-by-state basis, the patterns varied geographically and by program. The more popular programs - iNaturalist and eBird - exhibited increases in the Eastern U.S. in both the number of observations and participants and slight declines in the West. Further, there was a widespread increase in observations originating from urban areas, particularly in iNaturalist and eBird. Understanding the impacts of lockdowns on participation patterns in these programs is crucial for proper interpretation of the data. The data generated by these programs are highly valuable for documenting impacts of pandemic-related closures on wildlife and plants and may suggest patterns seen in other community science programs and in other countries.

How well do the spring indices predict phenological activity across plant species?

The spring indices, models that represent the onset of spring season biological activity, were developed using a long-term observational record from the mid-to-late twentieth century of three species of lilacs and honeysuckles contributed by volunteer observers across the nation. The USA National Phenology Network (USA-NPN) produces and freely delivers maps of spring index onset dates at fine spatial scale for the USA. These maps are used widely in natural resource planning and management applications. The extent to which the models represent activity in a broad suite of plant species is not well documented. In this study, we used a rich record of observational plant phenology data (37,819 onset records) collected in recent years (1981-2017) to evaluate how well gridded maps of the spring index models predict leaf and flowering onset dates in (a) 19 species of ecologically important, broadly distributed deciduous trees and shrubs, and (b) the lilac and honeysuckle species used to construct the models. The extent to which the spring indices predicted vegetative and reproductive phenology varied by species and with latitude, with stronger relationships revealed for shrubs than trees and with the Bloom Index compared to the Leaf Index, and reduced concordance between the indices at higher latitudes. These results allow us to use the indices as indicators of when to expect activity across widely distributed species and can serve as a yardstick to assess how future changes in the timing of spring will impact a broad array of trees and shrubs across the USA.

Creating the Urban Farmer's Almanac with Citizen Science Data.

Agriculture has long been a part of the urban landscape, from gardens to small scale farms. In recent decades, interest in producing food in cities has grown dramatically, with an estimated 30% of the global urban population engaged in some form of food production. Identifying and managing the insect biodiversity found on city farms is a complex task often requiring years of study and specialization, especially in urban landscapes which have a complicated tapestry of fragmentation, diversity, pollution, and introduced species. Supporting urban growers with relevant data informs insect management decision-making for both growers and their neighbors, yet this information can be difficult to come by. In this study, we introduced several web-based citizen science programs that can connect growers with useful data products and people to help with the who, what, where, and when of urban insects. Combining the power of citizen science volunteers with the efforts of urban farmers can result in a clearer picture of the diversity and ecosystem services in play, limited insecticide use, and enhanced non-chemical alternatives. Connecting urban farming practices with citizen science programs also demonstrates the ecosystem value of urban agriculture and engages more citizens with the topics of food production, security, and justice in their communities.

Correction: Differential changes in the onset of spring across US National Wildlife Refuges and North American migratory bird flyways.

[This corrects the article DOI: 10.1371/journal.pone.0202495.].

Differential changes in the onset of spring across US National Wildlife Refuges and North American migratory bird flyways.

Warming temperatures associated with climate change can have indirect effects on migratory birds that rely on seasonally available food resources and habitats that vary across spatial and temporal scales. We used two heat-based indices of spring onset, the First Leaf Index (FLI) and the First Bloom Index (FBI), as proxies of habitat change for the period 1901 to 2012 at three spatial scales: the US National Wildlife Refuge System; the four major bird migratory flyways in North America; and the seasonal ranges (i.e., breeding and non-breeding grounds) of two migratory bird species, Blue-winged Warbler (Vermivora cyanoptera) and Whooping Crane (Grus americana). Our results show that relative to the historical range of variability, the onset of spring is now earlier in 76% of all wildlife refuges and extremely early (i.e., exceeding 95% of historical conditions) in 49% of refuges. In all flyways but the Pacific, the rate of spring advance is generally greater at higher latitudes than at lower latitudes. This differential rate of advance in spring onset is most pronounced in the Atlantic flyway, presumably because of a "warming hole" in the southeastern US. Both FLI and FBI have advanced markedly in the breeding ranges-but not the non-breeding ranges-of the two selected bird species, albeit with considerable intra-range variation. Differences among species in terms of migratory patterns and the location and extent of seasonal habitats, as well as shifts in habitat conditions over time, may complicate predictions of the vulnerability of migratory birds to climate change effects. This study provides insight into how differential shifts in the phenology of disparate but linked habitats could inform local- to landscape-scale management strategies for the conservation of migratory bird populations.

USA National Phenology Network's volunteer-contributed observations yield predictive models of phenological transitions.

PURPOSE: In support of science and society, the USA National Phenology Network (USA-NPN) maintains a rapidly growing, continental-scale, species-rich dataset of plant and animal phenology observations that with over 10 million records is the largest such database in the United States. The aim of this study was to explore the potential that exists in the broad and rich volunteer-collected dataset maintained by the USA-NPN for constructing models predicting the timing of phenological transition across species' ranges within the continental United States. Contributed voluntarily by professional and citizen scientists, these opportunistically collected observations are characterized by spatial clustering, inconsistent spatial and temporal sampling, and short temporal depth (2009-present). Whether data exhibiting such limitations can be used to develop predictive models appropriate for use across large geographic regions has not yet been explored. METHODS: We constructed predictive models for phenophases that are the most abundant in the database and also relevant to management applications for all species with available data, regardless of plant growth habit, location, geographic extent, or temporal depth of the observations. We implemented a very basic model formulation-thermal time models with a fixed start date. RESULTS: Sufficient data were available to construct 107 individual species × phenophase models. Remarkably, given the limited temporal depth of this dataset and the simple modeling approach used, fifteen of these models (14%) met our criteria for model fit and error. The majority of these models represented the "breaking leaf buds" and "leaves" phenophases and represented shrub or tree growth forms. Accumulated growing degree day (GDD) thresholds that emerged ranged from 454 GDDs (Amelanchier canadensis-breaking leaf buds) to 1,300 GDDs (Prunus serotina-open flowers). Such candidate thermal time thresholds can be used to produce real-time and short-term forecast maps of the timing of these phenophase transition. In addition, many of the candidate models that emerged were suitable for use across the majority of the species' geographic ranges. Real-time and forecast maps of phenophase transitions could support a wide range of natural resource management applications, including invasive plant management, issuing asthma and allergy alerts, and anticipating frost damage for crops in vulnerable states. IMPLICATIONS: Our finding that several viable thermal time threshold models that work across the majority of the species ranges could be constructed from the USA-NPN database provides clear evidence that great potential exists this dataset to develop more enhanced predictive models for additional species and phenophases. Further, the candidate models that emerged have immediate utility for supporting a wide range of management applications.

Assessing accuracy in citizen science-based plant phenology monitoring.

In the USA, thousands of volunteers are engaged in tracking plant and animal phenology through a variety of citizen science programs for the purpose of amassing spatially and temporally comprehensive datasets useful to scientists and resource managers. The quality of these observations and their suitability for scientific analysis, however, remains largely unevaluated. We aimed to evaluate the accuracy of plant phenology observations collected by citizen scientist volunteers following protocols designed by the USA National Phenology Network (USA-NPN). Phenology observations made by volunteers receiving several hours of formal training were compared to those collected independently by a professional ecologist. Approximately 11,000 observations were recorded by 28 volunteers over the course of one field season. Volunteers consistently identified phenophases correctly (91% overall) for the 19 species observed. Volunteers demonstrated greatest overall accuracy identifying unfolded leaves, ripe fruits, and open flowers. Transitional accuracy decreased for some species/phenophase combinations (70% average), and accuracy varied significantly by phenophase and species (p < 0.0001). Volunteers who submitted fewer observations over the period of study did not exhibit a higher error rate than those who submitted more total observations. Overall, these results suggest that volunteers with limited training can provide reliable observations when following explicit, standardized protocols. Future studies should investigate different observation models (i.e., group/individual, online/in-person training) over subsequent seasons with multiple expert comparisons to further substantiate the ability of these monitoring programs to supply accurate broadscale datasets capable of answering pressing ecological questions about global change.

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.

Within-season flowering interruptions are common in the water-limited Sky Islands.

Within-season breaks in flowering have been reported in a wide range of highly variable ecosystems including deserts, tropical forests and high-elevation meadows. A tendency for interruptions in flowering has also been documented in southwestern US "Sky Island" plant communities, which encompass xeric to mesic conditions. Seasonal breaks in flowering have implications for plant reproductive success, population structure, and gene flow as well as resource availability for pollinators and dependent animals. Most reports of multiple within-season flowering events describe only two distinct flowering episodes. In this study, we set out to better quantify distinct within-season flowering events in highly variable Sky Islands plant communities. Across a >1,200 m elevation gradient, we documented a strong tendency for multiple within-season flowering events. In both distinct spring and summer seasons, we observed greater than two distinct within-season flowering in more than 10 % of instances. Patterns were clearly mediated by the different climate factors at work in the two seasons. The spring season, which is influenced by both temperature and precipitation, showed a mixed response, with the greatest tendency for multiple flowering events occurring at mid-elevations and functional types varying in their responses across the gradient. In the summer season, during which flowering across the gradient is limited by localized precipitation, annual plants exhibited the fewest within-season flowering events and herbaceous perennial plants showed the greatest. Additionally, more distinct events occurred at lower elevations. The patterns documented here provide a baseline for comparison of system responses to changing climate conditions.

Spring and summer patterns in flowering onset, duration, and constancy across a water-limited gradient.

PREMISE OF THE STUDY: Community-level flowering patterns can be characterized by onset, duration, and end as well as constancy, the degree to which species commence, cease, and reinitiate flowering within a season. In the mountainous Sky Islands region of the southwestern United States, flowering onset is clearly influenced by elevation in the spring, but much less so in the summer season. We evaluated whether these flowering metrics reflect these dissimilar patterns between distinct spring and summer seasons regarding the influence of the elevation and moisture gradient. • METHODS: We characterized flowering onset, end, duration, and constancy by plant functional type and their relationships to climate variables in spring and summer. We also evaluated the influence of climate on seasonal flowering patterns. • KEY RESULTS: Gaps in seasonal flowering occur frequently in this system in both seasons and among all plant functional types. In both seasons, annual plants exhibit the shortest flowering durations and highest constancies, and plants at low elevations, inhabiting environments with variable moisture conditions, show a greater tendency for longer flowering durations and lower constancy than high-elevation plants. Spring flowering characteristics are most influenced by the total amount of October-March precipitation as well as temperatures in these months, whereas summer flowering characteristics are influenced by the timing of summer-season precipitation, and next by the total amount of summer precipitation. • CONCLUSIONS: Flowering metrics, especially constancy and duration, show similar patterns in spring and summer and vary across elevation and moisture gradients. These patterns have substantial implications for plant and animal communities.

Phenological tracking enables positive species responses to climate change.

Earlier spring phenology observed in many plant species in recent decades provides compelling evidence that species are already responding to the rising global temperatures associated with anthropogenic climate change. There is great variability among species, however, in their phenological sensitivity to temperature. Species that do not phenologically "track" climate change may be at a disadvantage if their growth becomes limited by missed interactions with mutualists, or a shorter growing season relative to earlier-active competitors. Here, we set out to test the hypothesis that phenological sensitivity could be used to predict species performance in a warming climate, by synthesizing results across terrestrial warming experiments. We assembled data for 57 species across 24 studies where flowering or vegetative phenology was matched with a measure of species performance. Performance metrics included biomass, percent cover, number of flowers, or individual growth. We found that species that advanced their phenology with warming also increased their performance, whereas those that did not advance tended to decline in performance with warming. This indicates that species that cannot phenologically "track" climate may be at increased risk with future climate change, and it suggests that phenological monitoring may provide an important tool for setting future conservation priorities.

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.

Onset of summer flowering in a 'Sky Island' is driven by monsoon moisture.

Temperatures for the southwestern USA are predicted to increase in coming decades, especially during the summer season; however, little is known about how summer precipitation patterns may change. We aimed to better understand how nonsucculent plants of a water-limited gradient encompassing xeric desert to mesic mountain-top may respond to changes in summer conditions. We used a species-rich 26-yr flowering record to determine species' relationships with precipitation and temperature in months coincident with and previous to flowering. The onset of summer flowering was strongly influenced by the amount and timing of July precipitation, regardless of elevation or life form, suggesting the critical importance of soil moisture in triggering summer flowering in this region. Future changes in the timing or consistency of the early monsoon will probably impact directly on the onset of flowering for many species in this region. In addition, a key implication of predicted increasing temperatures is a decrease in available soil moisture. At all elevations, many species may be expected to flower later in the summer under the decreased soil moisture conditions associated with warmer temperatures. However, impacts on summer flowering may be greater at higher elevations, because of the greater sensitivity of mesic plants to water stress.

Monitoring plant phenology using digital repeat photography.

Repeated observations of plant phenology have been shown to be important indicators of global change. However, capturing the exact date of key events requires daily observations during the growing season, making phenologic observations relatively labor intensive and costly to collect. One alternative to daily observations for capturing the dates of key phenologic events is repeat photography. In this study, we explored the utility of repeat digital photography for monitoring phenologic events in plants. We provide an illustration of this approach and its utility by placing observations made using repeat digital imagery in context with local meteorologic and edaphic variables. We found that repeat photography provides a reliable, consistent measurement of phenophase. In addition, digital photography offers advantages in that it can be mathematically manipulated to detect and enhance patterns; it can classify objects; and digital photographs can be archived for future analysis. In this study, an estimate of greenness and counts of individual flowers were extracted by way of mathematic algorithms from the photo time series. These metrics were interpreted using meteorologic measurements collected at the study site. We conclude that repeat photography, coupled with site-specific meteorologic measurements, could greatly enhance our understanding environmental triggers of phenologic events. In addition, the methods described could easily be adopted by citizen scientists and the general public as well as professionals in the field.