Phenological Research using Herbarium Specimens
This page tabulates published phenological research that has used herbarium specimen data.
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- Last updated July 26, 2021 -
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- Last updated July 26, 2021 -
A primer on herbarium-based phenological research
Brian Haggerty, Alisa Hove, Susan Mazer
This document provides a straightforward overview of phenological research using herbaria. It was developed as part of the Phenological Literacy: Understanding Through Science and Stewardship (PLUSS) Program.
Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species' phenological cueing mechanisms | 2015 | American Journal of Botany
Charles C. Davis, Charles G. Willis, Bryan Connolly, Courtland Kelly, Aaron M. Ellison
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. 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. 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. 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.
Herbarium specimens demonstrate earlier flowering times in response to warming in Boston | 2004 | Ecology
Daniel Primack, Carolyn Imbres, Richard B. Primack, Abraham J. Miller‐Rushing, Peter Del Tredici
Museum specimens collected in the past may be a valuable source of information on the response of species to climate change. This idea was tested by comparing the flowering times during the year 2003 of 229 living plants growing at the Arnold Arboretum in Boston, Massachusetts, USA, with 372 records of flowering times from 1885 to 2002 using herbarium specimens of the same individual plants. During this period, Boston experienced a 1.5°C increase in mean annual temperature. Flowering times became progressively earlier; plants flowered 8 d earlier from 1980 to 2002 than they did from 1900 to 1920. Most of this shift toward earlier flowering times is explained by the influence of temperature, especially temperatures in the months of February, March, April, and May, on flowering time. Plants with a long flowering duration appear to be as useful for detecting responses to changing temperatures as plants with a short flowering duration. Additional studies using herbarium specimens to detect responses to climate change could examine specimens from specific, intensively collected localities, such as mountain peaks, islands, and unique habitats.
Old plants, new tricks: Phenological research using herbarium specimens | 2017 | Trends in Ecology and Evolution
Charles G. Willis, Elizabeth R. Ellwood, Richard B. Primack, Charles C. Davis, Katelin D. Pearson, Amanda S. Gallinat, Jenn M. Yost, Gil Nelson, Susan J. Mazer, Natalie L. Rossington, Tim H. Sparks, Pamela S. Soltis
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.
Herbarium specimens can reveal impacts of climate change on plant phenology; a review of methods and applications | 2018 | PeerJ
Casey A. Jones, Curtis C. Daehler
Studies in plant phenology have provided some of the best evidence for large-scale responses to recent climate change. Over the last decade, more than thirty studies have used herbarium specimens to analyze changes in flowering phenology over time, although studies from tropical environments are thus far generally lacking. In this review, we summarize the approaches and applications used to date. Reproductive plant phenology has primarily been analyzed using two summary statistics, the mean flowering day of year and first-flowering day of year, but mean flowering day has proven to be a more robust statistic. Two types of regression models have been applied to test for associations between flowering, temperature and time: flowering day regressed on year and flowering day regressed on temperature. Most studies analyzed the effect of temperature by averaging temperatures from three months prior to the date of flowering. On average, published studies have used 55 herbarium specimens per species to characterize changes in phenology over time, but in many cases fewer specimens were used. Geospatial grid data are increasingly being used for determining average temperatures at herbarium specimen collection locations, allowing testing for finer scale correspondence between phenology and climate. Multiple studies have shown that inferences from herbarium specimen data are comparable to findings from systematically collected field observations. Understanding phenological responses to climate change is a crucial step towards recognizing implications for higher trophic levels and large-scale ecosystem processes. As herbaria are increasingly being digitized worldwide, more data are becoming available for future studies. As temperatures continue to rise globally, herbarium specimens are expected to become an increasingly important resource for analyzing plant responses to climate change.
Primary Research Articles
Substantial shifts in flowering phenology of Sternbergia vernalis in the Himalaya: Supplementing decadal field records with historical and experimental evidences | 2021 | The Science of the Total Environment
Tabasum Hassan, Maroof Hamid, Sajad A. Wani, Akhtar H. Malik, Showkat A. Waza, Anzar A. Khuroo
In an age of anthropocene, shifting plant phenology is one of the most striking biological indicators of global environmental change. Majority of the studies reporting shifts in plant phenology are available from the North America and Europe and largely scarce from the developing world, including the Himalaya; and studies integrating multiple methodological approaches to investigate the climate-driven phenological shifts are too rare. Here, we report the shifts in spring flowering phenology of model plant species, Sternbergia vernalis in response to the changing climate in Kashmir Himalaya, by integrating decadal field observational records with long-term herbarium and dated-photograph data, and supported with experimental evidences. Our results revealed a significant increasing trend of 0.038, 0.016 and 0.023 °C/year in the annual mean maximum temperature (Tmax), mean minimum temperature (Tmin) and diurnal temperature range (DTR) respectively; but an insignificant decreasing trend in annual precipitation of -1.24 mm/year over the last four decades (1980-2019) in this Himalayan region. The flowering phenology of S. vernalis has significantly advanced by 11.8 days/°C and 27.8 days/°C increase in Tmax and Tmin respectively, indicating that the climate warming has led to substantial shifts in flowering phenology of the model plant species. We also observed a strong association of seasonal Tmax (December-February) and DTR on the early onset of spring flowering, however precipitation had no significant effect on the timing of flowering. The greenhouse experiment results further supported a significant effect of temperature in triggering the phenological shifts, wherein the model plant grown under different temperature treatments flowered 9-20 days earlier compared to the control. Our study showcases the integrated use of multiple methodological approaches for unravelling the long-term phenological shifts in response to climate change, and contributes in filling the knowledge gaps in the phenological research from the developing world in general and the Himalaya in particular.
Surprising roles of climate in regulating flowering phenology in a subtropical ecosystem | 2021 | Ecography
Zhuqiu Song, Yanjun Du, Richard Primack, Abraham Miller-Rushing, Wanhui Ye, Zhongliang Huang
Climate-driven changes in phenology have widespread effects on ecological interactions and species' abundances. Most predictions of changes in phenology and the consequences for ecology and conservation are based on research in temperate systems. Climate-driven changes in phenology are largely undocumented in subtropical regions, which host much of the world's biodiversity. Factors important to regulating phenology in temperate systems (e.g. winter chilling requirements) are likely weak or absent in subtropical ecosystems; plant phenology in these regions could respond to climate differently than in the temperate zone. Here we examine flowering phenology data for 105 plant species based on herbarium specimens and photographs from 1911 to 2015 in the southern subtropical Nanling region in south China. Temperatures in this region warmed 0.3 degrees C over the 105-year study period, and most plant species flowered earlier over time, although species varied substantially in the magnitude of phenological response to warming temperatures. Spring flowering times advanced in response to warming temperatures in late summer and early autumn and in early spring, with late summer and early autumn temperatures having almost twice as strong an effect on spring flowering times as early spring temperatures (-4.7 versus -2.5 days degrees C-1). This strong effect of late summer and early autumn temperatures is very different from temperate systems and has substantial implications for anticipating future changes in phenology. The temperatures in late summer and early autumn may affect spring phenology by accelerating bud formation or initial growth. Warming January temperature delayed summer flowering and advanced winter flowering. Increases in precipitation during April to June also tended to delay summer flowering. Autumn flowering species showed inconsistent responses to warming. These results highlight important differences between climate-driven changes in phenology in temperate and subtropical areas. Understanding these differences will be important in understanding the effects of climate change on vegetation phenology and ecosystem processes.
Accounting for imperfect detection in data from museums and herbaria when modeling species distributions: combining and contrasting data-level versus model-level bias correction | 2021 | Ecography
Kelley D. Erickson, Adam B. Smith
The digitization of museum collections as well as an explosion in citizen science initiatives has resulted in a wealth of data that can be useful for understanding the global distribution of biodiversity, provided that the well-documented biases inherent in unstructured opportunistic data are accounted for. While traditionally used to model imperfect detection using structured data from systematic surveys of wildlife, occupancy models provide a framework for modelling the imperfect collection process that results in digital specimen data. In this study, we explore methods for adapting occupancy models for use with biased opportunistic occurrence data from museum specimens and citizen science platforms using seven species of Anacardiaceae in Florida as a case study. We explored two methods of incorporating information about collection effort to inform our uncertainty around species presence: 1) filtering the data to exclude collectors unlikely to collect the focal species and 2) incorporating collection covariates (collection type, time of collection and history of previous detections) into a model of collection probability. We found that the best models incorporated both the background data filtration step as well as collector covariates. Month, method of collection and whether a collector had previously collected the focal species were important predictors of collection probability. Efforts to standardize meta-data associated with data collection will improve efforts for modeling the spatial distribution of a variety of species.
Historical floras reflect broad shifts in flowering phenology in response to a warming climate | 2021 | Ecosphere
Alistair G. Auffret
Organisms across the globe are experiencing shifts in phenological events as a result of ongoing climate change. Recently, a variety of novel methods have been applied in order to fill gaps in the phenological data set, in which records often have a patchy temporal, spatial, and/or taxonomic resolution. Here, I tested whether changes in flowering phenology could be detected through the months of flowering stated in 11 guides to the Swedish flora published over a period of 220 yr (1798-2018), focussing on 241 plant species (approximately 8% of the Swedish flora), and accounting for the large increase in herbarium records that have occurred over the same period. Despite the coarse, monthly scale of flowering times reported, historical floras and wildflower guides may hold potential to fill temporal and taxonomic gaps in the plant phenological data set. However, factors other than climate may also influence any apparent phenological shifts over time. Here, flowering was found to start earlier (0.49 d/decade), end later (0.71 d/decade), and carry on longer (1.19 d/decade), with flowering length also associated with increases in the regional temperature anomaly during the 20th century (0.11 months/degrees C). First flowering occurring earlier in 71% of species (14% showing a significant negative trend), 68% of species ceased flowering later (20%), and 80% flowered for longer (29%). Detected phenological shifts also appeared to be related to species' flowering seasonality. Later-flowering species were found to flower later and for longer, while increasing temperatures appeared to drive stronger responses both in flowering onset in early-flowering species and in flowering cessation in later-flowering species. Although potential issues exist regarding the largely unknown ways by which authors have determined flowering times and the coarseness of the data, historical floras may be a useful resource in phenological and climate change research, with the potential to both identify and compare the broad climatic responses of a region's entire flora over long time periods, as well as filling gaps in an otherwise patchy data set.
Extirpated prairie species demonstrate more variable phenological responses to warming than extant congeners | 2021 | American Journal of Botany
Meredith A. Zettlemoyer, Katarina Renaldi, Michael D. Muzyka
Shifting phenology in response to climate is one mechanism that can promote population persistence and geographic spread; therefore, species with limited ability to phenologically track changing environmental conditions may be more susceptible to population declines. Alternatively, apparently nonresponding species may demonstrate divergent responses to multiple environmental conditions experienced across seasons.
Capitalizing on herbarium records from across the midwestern United States and on detailed botanical surveys documenting local extinctions over the past century, we investigated whether extirpated and extant taxa differ in their phenological responses to temperature and precipitation during winter and spring (during flowering and the growing season before flowering) or in the magnitude of their flowering time shift over the past century.
Although warmer temperatures across seasons advanced flowering, extirpated and extant species differed in the magnitude of their phenological responses to winter and spring warming. Extirpated species demonstrated inconsistent phenological responses to warmer spring temperatures, whereas extant species consistently advanced flowering in response to warmer spring temperatures. In contrast, extirpated species advanced flowering more than extant species in response to warmer winter temperatures. Greater spring precipitation tended to delay flowering for both extirpated and extant taxa. Finally, both extirpated and extant taxa delayed flowering over time.
This study highlights the importance of understanding phenological responses to seasonal warming and indicates that extirpated species may demonstrate more variable phenological responses to temperature than extant congeners, a finding consistent with the hypothesis that appropriate phenological responses may reduce species' likelihood of extinction.
Phenological responses to climate change based on a hundred years of herbarium collections of tropical Melastomataceae | 2021 | PLoS ONE
Duane F. Lima, Jose H.F. Mello, Isadora T. Lopez, Rafaela C. Forzza, Renato Goldenberg, Leandro Freitas
Changes in phenological events have been vastly documented in face of recent global climate change. These studies are concentrated on temperate plants, and the responses of tropical species are still little understood, likely due to the lack of long-term phenological records in the tropics. In this case, the use of herbarium specimens to gather phenological data over long periods and wide geographic areas has emerged as a powerful tool. Here, we used four Melastomataceae species endemic to the Brazilian Atlantic Forest to evaluate phenological patterns and alterations as responses to recent climate changes. Phenological data were gathered from Reflora Virtual Herbarium specimens collected between 1920 and 2018, and analyzed with circular statistics applied to the intervals 1920-1979, 1980-1999, and 2000-2018. The effects of temperature range, average temperature, precipitation, and photoperiod on flowering and fruiting of each species were tested using multiple linear regressions. Through circular statistics, we detected changes, mostly delays, in the flowering of Miconia quinquedentata, Pleroma clavatum and P. trichopodum, and in the fruiting of M. acutiflora, P. clavatum and P. trichopodum. We also found that flowering and fruiting occurrence were related to local climatic conditions from months prior to the collections. We found marked phenological variations over the decades and also that these variations are associated to global climate change, adding up to the large body of evidence from higher latitudes. Our results also support herbarium collections as an important source for long-term tropical phenological studies. The lack of consistent patterns of responses among the four species (e.g. fruiting delayed two months in P. clavatum and advanced one month in M. acutiflora) suggests that climate change has unequal effects across tropical forests. This highlights the urgent need for further research to understand and forecast the ecological implications of these changes in global ecosystems processes.
Macroevolutionary history predicts flowering time but not phenological sensitivity to temperature in grasses | 2021 | American Journal of Botany
Barbara M. Neto-Bradley, Jeannette Whitton, Linda P.J. Lipsen, Matthew W. Pennell
Long-term observations show that flowering phenology has shifted in many lineages in response to climate change. However, it remains unclear whether these results can be generalized to predict the presence, direction, or magnitude of responses in lineages for which we lack long time-series data. If phenological responses are phylogenetically conserved, we can extrapolate from species for which we have data to predict the responses of close relatives. While several studies have found that closely related species flower at similar times, fewer have evaluated whether phylogenetically proximal species respond to environmental change similarly.
We paired flowering time data from 3161 manually scored herbarium specimens of 72 species of grasses (Poaceae) with historical climate data and analyzed the phylogenetic signal and phylogenetic half-life of phenological sensitivity. We also ran these analyses on a subset of species showing statistically significant sensitivities, in order to assess the role of sampling bias on phylogenetic signal.
Closely related grass species tend to flower at similar times, but flowering times respond to temperature changes in species-specific ways. We also show that only including species for which there is strong evidence of phenological shifts results in overestimating phylogenetic signal.
In agreement with other recent studies, our results suggest caution in extrapolating from evidence of phylogenetic similarity to predicting shared responses in this ecologically relevant trait. Future work is needed to better understand the discrepancy between the phylogenetic signal in observed phenological shifts and absence of such signal in sensitivity.
Comparing fruiting phenology across two historical datasets: Thoreau's observations and herbarium specimens | 2021 | Annals of Botany
Tara K. Miller, Amanda S. Gallinat, Linnea C. Smith, Richard B. Primack
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.
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.
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.
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.
Phenological sensitivity to temperature mediates herbivory | 2021 | Global Change Biology
Emily K. Meineke, Charles C. Davis, T. Jonathan Davies
Species interactions drive ecosystem processes and are a major focus of global change research. Among the most consequential interactions expected to shift with climate change are those between insect herbivores and plants, both of which are highly sensitive to temperature. Insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change, yet empirical data on changes in synchrony are lacking. Using evidence of herbivory on herbarium specimens collected from the northeastern United States and France from 1900 to 2015, we provide evidence that plant species with temperature-sensitive phenologies experience higher levels of insect damage in warmer years, while less temperature-sensitive, co-occurring species do not. While herbivory might be mediated by interactions between warming and phenology through multiple pathways, we suggest that warming might lengthen growing seasons for phenologically sensitive plant species, exposing their leaves to herbivores for longer periods of time in warm years. We propose that elevated herbivory in warm years may represent a previously underappreciated cost to phenological tracking of climate change over longer timescales.
Tracking biological footprints of climate change using flowering phenology of the geophytes: Pancratium tenuifolium and Scadoxus multiflorus | 2021 | International Journal of Biometeorology
Drought-adapted geophytes are responding to the effects of climate change in arid and semi-arid environments. In this study, herbarium and historical rainfall data were used to examine the impact of rainfall changes on flowering trends of Pancratium tenuifolium Hochst. ex A.Rich and Scadoxus multiflorus (Martyn) Raf. subsp. multiflorus. Flowering was delayed by approximately 7 days per decade for P. tenuifolium during the period 1930 to 2018 and by approximately 14 days per decade for S. multiflorus subsp. multiflorus during the period 1924 to 2008. Scadoxus multiflorus subsp. multiflorus delayed the day of flowering by approximately 0.3 days per millimetre increase of rainfall, with Pancratium tenuifolium showing a non-significant response to summer rainfall during the same period. Overall, a linear mixed-effects model revealed that the day of flowering was delayed by approximately 8 days per degree rise in latitude and advanced by approximately 9 days per degree rise in longitude. Additionally, summer rainfall had significant effects on the day of flowering with a 1-mm increase in summer rainfall delaying the day of flowering by approximately 0.16 days. These changes in flowering times may ultimately alter the distribution of geophytes in Namibia.
Seasonality and the Relationships Between Reproductive and Leaf Phenophases In Myrtaceae Using Field and Herbarium Data | 2021 | Floresta e Ambiente
Jonathan Tejeda Orellana, Jociene Oliveira Vitoria Nascimento, Jorge Grilo, Samia Paula Santos Neves, Lia D'Afonseca Pedreira de Miranda, Ligia Silveira Funch
Phenological studies are considerably complemented through field data and herbarium collection databases. We examined the seasonality and relationships between leafing and reproductive phenophases using field observations and herbarium data of Campomanesia eugenioides var. desertorum, Eugenia punicifolia, and Psidium schenckianum, all native species of Myrtaceae. Field observations were performed in a caatinga remnant in Bahia State, Brazil; HUEFS herbarium collections were examined. In general, all species showed seasonal reproductive phases and aseasonal leaf phases, and Spearman correlations were observed between those phases. Field observations and herbarium collections were similar and complementary, providing clues about seasonality and the relationship between leaf and reproductive phases of Myrtaceae species.
Phenological change modelling for selected Himalayan medicinal herbs using herbarium records: A case study | 2021 | Ecological Informatics
Kailash S Gaira, Uppeandra Dhar
Regarding the effects of warming on phenology, essentially that climate warming is advancing vegetation phenology around the globe, and case studies of specific species/regions work to gauge this impact. Thus, we attempted to demonstrate phenological patterns of selected 4 alpine/sub-alpine and 4 temperate medicinal herbs based on higher medicinal value of Indian Himalayan Region (IHR) using total 654 herbarium records and applied Generalized Additive Model (GAM) as non-normal and non-linear application. The GAM demonstrated an advancement in the flowering time for alpine/sub-alpine species (Arnebia benthamii, Meconopsis aculeata, Podophyllum hexandrum) and temperate species (Delphinium denudatum and Dioscorea deltoidea), while delayed flowering for Swertia cordata (p < 0.001). Combining the herbarium records, the model significantly projected advancement in flowering time (21-25 days) over the last 100 years only for alpine/sub-alpine species (p < 0.0001). However, the relationship between flowering time and warming winter temperature was predicted advancement in flowering time for alpine/sub-alpine species (6-10 days per 1 degrees C) and temperate species (8-11 days per 1 degrees C). The results reveal that long-term herbarium records may be considered as a useful tool for predicting the possible impact of climate change on plant phenology in the IHR using GAM approach.
Precipitation contributes to plant height, but not reproductive effort, for western prairie fringed orchid (Platanthera praeclara Sheviak & Bowles): Evidence from herbarium records | 2020 | Ecology and Evolution
Lori A. Biederman, Sydney M. Weldon, Derek S. Anderson, Mark J. Leoschke
The western fringed prairie orchid (WFPO) is a rare plant found in mesic to wet tallgrass prairies in the Great Plains and Midwest regions of the United States. The size of WFPO populations varies considerably from year to year, and studies have suggested that population size is dependent on precipitation during critical periods in the plant's annual development. We hypothesized that plant height and reproductive effort would also be controlled by precipitation, either during these periods or over a broader period. We acquired available images of WFPO from 21 herbaria, and of these 141 individual plants had information adequate for analysis, although some population/year combinations were represented multiple times. For each specimen, we measured plant height (cm) and reproductive effort (as measured by total flower and bud count). We used bootstrapped linear regression, randomly selecting one individual from each population/year combination, to compare precipitation models, both during critical periods and the various summaries. We found that precipitation during the phenologically critical periods was a poor predictor of plant height and reproductive effort. Of the broader precipitation variables, accumulated precipitation from January 1 to collection date best described plant height. We also used correlations to detect a relationship among the variables WFPO height, reproductive effort, precipitation, latitude, and year of collection. Year of specimen collection was negatively correlated with WFPO plant height and accumulated precipitation, suggesting that both have declined in more recent years. Negative correlations with latitude also suggest height and precipitation decrease in the northern part of WFPO's range. Reproductive effort was not related to tested precipitation variables; however, it was weakly correlated with plant height. Although the results are limited, this study leverages available data and makes inferences on WFPO biology over broad ranges of time (1894-2012) and latitude (37.5 degrees-49.9 degrees).
A new method for counting reproductive structures in digitized herbarium specimens using Mask R-CNN | 2020 | Frontiers in Plant Science
Charles C. Davis, Julien Champ, Daniel S. Park, Ian Breckheimer, Goia M. Lyra, Junxi Xie, Alexis Joly, Dharmesh Tarapore, Aaron M. Ellison, Pierre Bonnet
Phenology-the timing of life-history events-is a key trait for understanding responses of organisms to climate. The digitization and online mobilization of herbarium specimens is rapidly advancing our understanding of plant phenological response to climate and climatic change. The current practice of manually harvesting data from individual specimens, however, greatly restricts our ability to scale-up data collection. Recent investigations have demonstrated that machine-learning approaches can facilitate this effort. However, present attempts have focused largely on simplistic binary coding of reproductive phenology (e.g., presence/absence of flowers). Here, we use crowd-sourced phenological data of buds, flowers, and fruits from >3,000 specimens of six common wildflower species of the eastern United States (Anemone canadensisL.,A. hepaticaL.,A. quinquefoliaL.,Trillium erectumL.,T. grandiflorum(Michx.) Salisb., andT. undulatumWild.) to train models using Mask R-CNN to segment and count phenological features. A single global model was able to automate the binary coding of each of the three reproductive stages with >87% accuracy. We also successfully estimated the relative abundance of each reproductive structure on a specimen with >= 90% accuracy. Precise counting of features was also successful, but accuracy varied with phenological stage and taxon. Specifically, counting flowers was significantly less accurate than buds or fruits likely due to their morphological variability on pressed specimens. Moreover, our Mask R-CNN model provided more reliable data than non-expert crowd-sourcers but not botanical experts, highlighting the importance of high-quality human training data. Finally, we also demonstrated the transferability of our model to automated phenophase detection and counting of the threeTrilliumspecies, which have large and conspicuously-shaped reproductive organs. These results highlight the promise of our two-phase crowd-sourcing and machine-learning pipeline to segment and count reproductive features of herbarium specimens, thus providing high-quality data with which to investigate plant responses to ongoing climatic change.
Flowering phenology of a widespread perennial herb shows contrasting responses to global warming between humid and non‐humid regions | 2020 | Functional Ecology
Zhuqui Song, Yongshuo H. Fu, Yanjun Du, Lin Li, Xuejun Ouyang, Wanhui Ye, Zhongliang Huang
Plant phenology was assessed as one of the most key Essential Biodiversity Variables on species functional traits, which underpins a variety of aspects of ecosystem function and is a vital determinant of species distribution. Flowering phenology is one of the most sensitive indicators of the effects of recent climatic change. Understanding of intraspecific variation in phenological responses to climate change can contribute to the accurate prediction of phenology and the assessment of potential impacts of climate change on organisms. However, this intraspecific variation in phenological sensitivity in natural systems is still unclear, especially at large spatial scales.
Using the widespread perennial herb Spiranthes sinensis, we quantified intraspecific variation in phenological responses to warming among groups located along climatic gradients. Phenological data were derived from 1,681 collections of herbarium specimens and photographs across eastern Asia and southeastern Australia over the period 1902–2017 and spans eight humid and eight non‐humid regions.
We found that peak flowering dates of Spiranthe sinensis (FLss) showed substantial intraspecific variation in temperature sensitivity, ranging from −5.16 ± 1.13 to 4.16 ± 0.90 days/°C. Across all 16 regions, FLss exhibited the strongest delayed response to warming in southeastern Australia. Temperature sensitivity of the FLss was significantly correlated with annual precipitation and aridity index of a region, suggesting a possible role of declined water availability in reducing temperature sensitivity. Notably, contrasting phenological responses to warming were found between collections with different humidity regimes: humid regions generally flowered earlier (M: −3.57 days/°C) and non‐humid regions exhibited slightly delayed flowering (M: 1.25 days/°C).
These findings provide empirical evidence of substantial intraspecific variation in phenological sensitivity across large spatial scales, and highlights that soil water availability may play a key role in a warming planet, especially in non‐humid regions.
Herbarium records indicate variation in bloom-time sensitivity to temperature across a geographically diverse region | 2020 | International Journal of Biometeorology
Christopher W. Kopp, Barbara M. Neto-Bradley, Linda P.J. Lipsen, Jas Sandhar, Siena Smith
Anthropogenic warming’s effects on phenology across environmental and temporal gradients are well recognized. Long-term phenological monitoring data are often limited in duration and geographic scope, but recent efforts to digitize herbaria collections make it possible to reliably reconstruct historic flowering phenology across broad geographic scales and multiple species, lending to an increased understanding of community response to climate change. In this study, we examined collection dates (1901 to 2015) of 8540 flowering specimens from 39 native species in the Pacific Northwest (PNW) region of North America. We hypothesized that flowering phenology would be sensitive to temperature but that sensitivity would vary depending on blooming season and geographic range position. As expected, we found that early-season bloomers are more sensitive to temperature than later-season bloomers. Sensitivity to temperature was significantly greater at low elevations and in the maritime (western) portion of the PNW than at higher elevations and in the eastern interior, respectively. The elevational and longitudinal effects on flowering sensitivity reflect spring “arriving” earlier at low elevations and in the maritime portion of the PNW. These results demonstrate that phenological responses to warming vary substantially across climatically diverse regions, warranting careful and nuanced consideration of climate warming’s effects on plant phenology.
The changing flowering phenology of Crinum lilies in arid and semi-arid regions: implications for phenological responses to climate change | 2019 | Biologia
Ezekiel G. Kwenbeya, Lillian Pazvakawambwa
Herbarium data have availed the much-needed long-term data that have constrained long-termand real-time phenological studies. Using herbarium specimens from the National Herbarium of Namibia, species, region, rainfall, latitude and longitude were regressed against the day of flowering to determine the effect of each variable on the day of flowering. This study used parameter estimates and the odds ratios from ordinal regression analysis to interpret the influence of the explanatory variables on the day of flowering. The results revealed that flowering dates of C. lugardiae have advanced by six days/decade during the period 1950 to 2010. Average summer rainfall decreased by approximately 3 mm per year from 1960 to 2015 in Namibia. Consequently, significant rainfall effects were recorded on the day of flowering for C. buphanoides, C. stuhlmannii subsp. delagoense and C. paludosum which have advanced by approximately 1 day/decade/mm, 1 day/decade/mm and 2 day/decade/mm during the period studied, respectively. Increase in latitude delayed day of flowering whilst an advancement of the day of flowering with an increase in longitude was observed. Substantial interaction effects among the explanatory variables were demonstrated. Combined effects of rainfall and latitude had a negative effect on the day of flowering whereas interaction effects of average summer rainfall and longitude had a positive combined effect on day of flowering. Our results, therefore, reveal the complex effects of rainfall and geographical location on flowering phenology of different Crinum species. The potential impacts of the phenological responses of different Crinum species on other organisms are discussed.
Changes in flowering phenology of Cardamine concatenata and Erythronium americanum over 111 years in the Central Appalachians | 2019 | Plant Ecology
Lori Petrauski, Sheldon F. Owen, George D. Constantz, James T. Anderson
Spring ephemerals in the Central Appalachians are a key component of deciduous forest communities and can be indicators of shifting phenology due to climate changes in this ecosystem. The objectives of this study were to (1) determine if there have been any changes in date of flowering for the Cutleaf Toothwort (Cardamine concatenata) and Yellow Trout Lily (Erythronium americanum) in West Virginia over the last 111 years; (2) determine which climatic factors affect the blooming date of these perennial, spring ephemeral wildflowers; and (3) evaluate the effect of elevation on changing blooming dates using herbarium specimens and photographs from 1904 to 2015. Both species are widespread throughout the woodlands of eastern North America. Both species have significantly advanced their spring flowering over the last century Spring temperature was the strongest predictor of blooming date (2.91 and 3.44 days earlier/1 degrees C increase in spring temperature, respectively). Flowers at < 500 m elevation bloomed earlier and demonstrated a stronger shift in flowering date over time than flowers at > 1000 m elevations. Lower elevations, higher spring and winter temperatures, and low amounts of precipitation were associated with earlier spring flowering. This research demonstrates the plasticity of phenological response to a variety of climatic variables, the usefulness of using herbarium specimens to reconstruct flowering dates over a topographically variable area, and the contrasting effects of climate change on high elevation regions of West Virginia.
An examination of climate-driven flowering-time shifts at large spatial scales over 153 years in a common weedy annual | 2019 | American Journal of Botany
Colette S. Berg, Jason L. Brown, Jennifer J. Weber
Understanding species' responses to climate change is a critical challenge facing biologists today. Though many species are widespread, few studies of climate-driven shifts in flowering time have examined large continuous spatial scales for individual species. And even fewer studies have examined these shifts at time scales greater than a few decades.
We used digitized herbarium specimens and PRISM climate data to produce the spatially and temporally broadest-scale study of flowering time in a single species to date, spanning the contiguous United States and 153 years (1863-2016) for a widespread weedy annual, Triodanis perfoliata (Campanulaceae). We examined factors driving phenological shifts as well as the roles of geographic and temporal scale in understanding these trends.
Year was a significant factor in both geospatial and climatic analyses, revealing that flowering time has advanced by similar to 9 days over the past similar to 150 years. We found that temperature as well as vapor pressure deficit, an understudied climatic parameter associated with evapotranspiration and water stress, were strongly associated with peak flowering. We also examined how sampling at different spatiotemporal scales influences the power to detect flowering-time shifts, finding that relatively large spatial and temporal scales are ideal for detecting flowering-time shifts in this widespread species.
Our results emphasize the importance of understanding the interplay of geospatial factors at different scales to examine how species respond to climate change.
A new phenological metric for use in pheno-climatic models: A case study using herbarium specimens of Streptanthus tortuosus | 2019 | Applications in Plant Sciences
Natalie L. Rossington Love, Isaac W. Park, Susan J. Mazer
Herbarium specimens have been used to detect climate‐induced shifts in flowering time by using the day of year of collection (DOY) as a proxy for first or peak flowering date. Variation among herbarium sheets in their phenological status, however, undermines the assumption that DOY accurately represents any particular phenophase. Ignoring this variation can reduce the explanatory power of pheno‐climatic models (PCMs) designed to predict the effects of climate on flowering date.
Here we present a protocol for the phenological scoring of imaged herbarium specimens using an ImageJ plugin, and we introduce a quantitative metric of a specimen's phenological status, the phenological index (PI), which we use in PCMs to control for phenological variation among specimens of Streptanthus tortuosus (Brassicaceeae) when testing for the effects of climate on DOY. We demonstrate that including PI as an independent variable improves model fit.
Including PI in PCMs increased the model R 2 relative to PCMs that excluded PI; regression coefficients for climatic parameters, however, remained constant.
Our protocol provides a simple, quantitative phenological metric for any observed plant. Including PI in PCMs increases R 2 and enables predictions of the DOY of any phenophase under any specified climatic conditions.
Reproductive phenology of Leptolobium dasycarpum and L. elegans across the Brazilian savanna based on herbarium records | 2019 | Flora
Wellington Santos Fava, Nicolay Leme da Cunha, Aline Pedroso Lorenz
Changes in phenological events have a prominent position in current global change research. Phenological studies for the Brazilian savannah plants are geographically restricted and long-term variation is still unclear. Thus the use of herbarium data can provide long-term phenological evaluation and it is important to understand the phenology-climate dynamics on broader scales. We used climatic data and 252 herbarium specimens collected between 1961 and 2012 to examine the phenological trends in Leptolobium dasycarpum and L. elegans (Leguminosae, Papilionoideae). We tested the effect of average temperature and rainfall of each specimen's month of flowering and/or fruiting and the three months prior using generalized least squares models. The species presented similar flowering and fruiting seasons, peaking in the wet season. Across this hotspot of biodiversity characterized by extraordinary environmental variations between the wet and dry seasons, L. dasycarpum and L. elegans tend to delay their phenophases with increasing temperature and precipitation. However, we did not find a significant alteration of the phenophase dates over the 52 years. In addition, although the temperature in Cerrado has increased during the period investigated, these two species were not affected by the climatic changes, indicating that additional factors or even the interaction of multiple drivers may have determined their flowering/fruiting control.
Shifts in the timing of the early flowering in plants from a semi-arid ecoregion under climate change | 2019 | Biologica
Climate change has been significantly changing ecosystems. Regarding angiosperms, elevated temperature has affected the flowering time of plants across habitats, where earlier flowering was induced. The impacts of climate change on vegetation are expected to be more pronounced in dry regions because of the high irregularity in precipitation and temperature. Assessment of the effects of the long-term climate change on plants is recently possible due to the increased digitization of historical herbarium specimens. For instance, these herbarium specimens can be used to detect changes in flowering time. In this study, the shifts in flowering time of plant species collected from a semi-arid region in the western USA (the Trans-Pecos ecoregion, Texas, USA) was analyzed using a herbarium database. A total of 7163 herbarium records from 172 species were examined. Statistically significant shifts were detected in the flowering day for the early flowering stage of 19 species in the semi-arid region from 1900 to 2017. According to t-test results, 9 species delayed flowering ranging between 17 and 50days, whereas 10 species flowering started flowering ranging from 31 to 55days earlier (p <= 0.05). Overall, these results contribute to a better understanding of the expression of plant reproductive strategies by revealing the plant responses to warming, and the ability of plants to respond climate change.
Spring- and fall-flowering species show diverging phenological responses to climate in the Southeast USA | 2019 | International Journal of Biometeorology
Katelin D. Pearson
Plant phenological shifts (e.g., earlier flowering dates) are known consequences of climate change that may alter ecosystem functioning, productivity, and ecological interactions across trophic levels. Temperate, subalpine, and alpine regions have largely experienced advancement of spring phenology with climate warming, but the effects of climate change in warm, humid regions and on autumn phenology are less well understood. In this study, nearly 10,000 digitized herbarium specimen records were used to examine the phenological sensitivities of fall- and spring-flowering asteraceous plants to temperature and precipitation in the US Southeastern Coastal Plain. Climate data reveal warming trends in this already warm climate, and spring- and fall-flowering species responded differently to this change. Spring-flowering species flowered earlier at a rate of 1.8-2.3days per 1 degrees C increase in spring temperature, showing remarkable congruence with studies of northern temperate species. Fall-flowering species flowered slightly earlier with warmer spring temperatures, but flowering was significantly later with warmer summer temperatures at a rate of 0.8-1.2days per 1 degrees C. Spring-flowering species exhibited slightly later flowering times with increased spring precipitation. Fall phenology was less clearly influenced by precipitation. These results suggest that even warm, humid regions may experience phenological shifts and thus be susceptible to potentially detrimental effects such as plant-pollinator asynchrony.
Temperature controls phenology in continuously flowering Protea species of subtropical Africa | 2019 | Applications in Plant Sciences
Barnabas H. Daru, Matthew M. Kling, Emily K. Meineke, Abraham E. van Wyk
Herbarium specimens are increasingly used as records of plant flowering phenology. However, most herbarium‐based studies on plant phenology focus on taxa from temperate regions. Here, we explore flowering phenologic responses to climate in the subtropical plant genus Protea (Proteaceae), an iconic group of plants that flower year‐round and are endemic to subtropical Africa.
We present a novel, circular sliding window approach to investigate phenological patterns developed for species with year‐round flowering. We employ our method to evaluate the extent to which site‐to‐site and year‐to‐year variation in temperature and precipitation affect flowering dates using a database of 1727 herbarium records of 25 Protea species. We also explore phylogenetic conservatism in flowering phenology.
We show that herbarium data combined with our sliding window approach successfully captured independently reported flowering phenology patterns (r = 0.93). Both warmer sites and warmer years were associated with earlier flowering of 3–5 days/°C, whereas precipitation variation had no significant effect on flowering phenology. Although species vary widely in phenological responsiveness, responses are phylogenetically conserved, with closely related species tending to shift flowering similarly with increasing temperature.
Our results point to climate‐responsive phenology for this important plant genus and indicate that the subtropical, aseasonally flowering genus Protea has temperature‐driven flowering responses that are remarkably similar to those of better‐studied northern temperate plant species, suggesting a generality across biomes that has not been described elsewhere.
Patterns and biases in an Arctic herbarium specimen collection: Implications for phenological research | 2019 | Applications in Plant Sciences
Zoe A. Panchen, Jennifer Doubt, Heather M. Kharouba, Mark O. Johnston
Herbarium specimens are increasingly used in phenological studies. However, natural history collections can have biases that influence the analysis of phenological events. Arctic environments, where remoteness and cold climate govern collection logistics, may give rise to unique or pronounced biases.
We assessed the presence of biases in time, space, phenological events, collectors, taxonomy, and plant traits across Nunavut using herbarium specimens accessioned at the National Herbarium of Canada (CAN).
We found periods of high and low collection that corresponded to societal and institutional events; greater collection density close to common points of air and sea access; and preferences to collect plants at the flowering phase and in peak flower, and to collect particular taxa, flower colours, growth forms, and plant heights. One‐quarter of collectors contributed 90% of the collection.
Collections influenced by temporal and spatial biases have the potential to misrepresent phenology across space and time, whereas those shaped by the interests of collectors or the tendency to favour particular phenological stages, taxa, and plant traits could give rise to imbalanced phenological comparisons. Underlying collection patterns may vary among regions and institutions. To guide phenological analyses, we recommend routine assessment of any herbarium data set prior to its use.
Phenology models using herbarium specimens are only slightly improved by using finer‐scale stages of reproduction | 2019 | Applications in Plant Sciences
Elizabeth R. Ellwood, Richard B. Primack, Charles G. Willis, Janneke HilleRisLambers
Herbarium specimens are increasingly used to study reproductive phenology. Here, we ask whether classifying reproduction into progressively finer‐scale stages improves our understanding of the relationship between climate and reproductive phenology.
We evaluated Acer rubrum herbarium specimens across eastern North America, classifying them into eight reproductive phenophases and four stages of leaf development. We fit models with different reproductive phenology categorization schemes (from detailed to broad) and compared model fits and coefficients describing temperature, elevation, and year effects. We fit similar models to leaf phenology data to compare reproductive to leafing phenology.
Finer‐scale reproductive phenophases improved model fits and provided more precise estimates of reproductive phenology. However, models with fewer reproductive phenophases led to similar qualitative conclusions, demonstrating that A. rubrum reproduces earlier in warmer locations, lower elevations, and in recent years, as well as that leafing phenology is less strongly influenced by temperature than is reproductive phenology.
Our study suggests that detailed information on reproductive phenology provides a fuller understanding of potential climate change effects on flowering, fruiting, and leaf‐out. However, classification schemes with fewer reproductive phenophases provided many similar insights and may be preferable in cases where resources are limited.
A new method and insights for estimating phenological events from herbarium specimens | 2019 | Applications in Plant Sciences
Katelin D. Pearson
A novel method of estimating phenology of herbarium specimens was developed to facilitate more precise determination of plant phenological responses to explanatory variables (e.g., climate).
Simulated specimen data sets were used to compare the precision of phenological models using the new method and two common, alternative methods (flower presence/absence and ≥50% flowers present). The new “estimated phenophase” method was more precise and extracted a greater number of significant species‐level relationships; however, this method only slightly outperformed the simple “binary” (e.g., flowers present/absent) method.
The new method enables estimation of phenological trends with greater precision. However, when time and resources are limited, a presence/absence method may offer comparable results at lower cost. Using a more restrictive approach, such as only including specimens in a certain phenophase, is not advised given the detrimental effect of decreased sample size on resulting models.
Toward a large‐scale and deep phenological stage annotation of herbarium specimens: Case studies from temperate, tropical, and equatorial floras | 2019 | Applications in Plant Sciences
Titouan Lorieul, Katelin D. Pearson, Elizabeth R. Ellwood, Hervé Goëau, Jean‐Francois Molino, Patrick W. Sweeney, Jenn M. Yost, Joel Sachs, Erick Mata‐Montero, Gil Nelson, Pamela S. Soltis, Pierre Bonnet, Alexis Joly
Phenological annotation models computed on large‐scale herbarium data sets were developed and tested in this study.
Herbarium specimens represent a significant resource with which to study plant phenology. Nevertheless, phenological annotation of herbarium specimens is time‐consuming, requires substantial human investment, and is difficult to mobilize at large taxonomic scales. We created and evaluated new methods based on deep learning techniques to automate annotation of phenological stages and tested these methods on four herbarium data sets representing temperate, tropical, and equatorial American floras.
Deep learning allowed correct detection of fertile material with an accuracy of 96.3%. Accuracy was slightly decreased for finer‐scale information (84.3% for flower and 80.5% for fruit detection).
The method described has the potential to allow fine‐grained phenological annotation of herbarium specimens at large ecological scales. Deeper investigation regarding the taxonomic scalability of this approach is needed.
Herbarium specimens reveal substantial and unexpected variation in phenological sensitivity across the eastern United States | 2019 | Philosophical Transactions of the Royal Society B-Biological Sciences
Daniel S. Park, Ian Breckheimer, Alex C. Williams, Edith Law, Aaron M. Ellison, Charles C. Davis
Phenology is a key biological trait that can determine an organism's survival and provides one of the clearest indicators of the effects of recent climatic change. Long time-series observations of plant phenology collected at continental scales could clarify latitudinal and regional patterns of plant responses and illuminate drivers of that variation, but few such datasets exist. Here, we use the web tool CrowdCurio to crowdsource phenological data from over 7000 herbarium specimens representing 30 diverse flowering plant species distributed across the eastern United States. Our results, spanning 120 years and generated from over 2000 crowdsourcers, illustrate numerous aspects of continental-scale plant reproductive phenology. First, they support prior studies that found plant reproductive phenology significantly advances in response to warming, especially for early-flowering species. Second, they reveal that fruiting in populations from warmer, lower latitudes is significantly more phenologically sensitive to temperature than that for populations from colder, higher-latitude regions. Last, we found that variation in phenological sensitivities to climate within species between regions was of similar magnitude to variation between species. Overall, our results suggest that phenological responses to anthropogenic climate change will be heterogeneous within communities and across regions, with large amounts of regional variability driven by local adaptation, phenotypic plasticity and differences in species assemblages. As millions of imaged herbarium specimens become available online, they will play an increasingly critical role in revealing large-scale patterns within assemblages and across continents that ultimately can improve forecasts of the impacts of climatic change on the structure and function of ecosystems.
Overlooked climate parameters best predict flowering onset: Assessing phenological models using the elastic net 2018 | Global Change Biology
Isaac W. Park, Susan J. Mazer
Determining the manner in which plant species shift their flowering times in response to climatic conditions is essential to understanding and forecasting the impacts of climate change on the world's flora. The limited taxonomic diversity and duration of most phenological datasets, however, have impeded a comprehensive, systematic determination of the best predictors of flowering phenology. Additionally, many studies of the relationship between climate conditions and plant phenology have included only a limited set of climate parameters that are often chosen a priori and may therefore overlook those parameters to which plants are most phenologically sensitive. This study harnesses 894,392 digital herbarium records and 1,959 in situ observations to produce the first assessment of the effects of a large number (25) of climate parameters on the flowering time of a very large number (2,468) of angiosperm taxa throughout North America. In addition, we compare the predictive capacity of phenological models constructed from the collection dates of herbarium specimens vs. repeated in situ observations of individual plants using a regression approach-elastic net regularization-that has not previously been used in phenological modeling, but exhibits several advantages over ordinary least squares and stepwise regression. When herbarium-derived data and in situ phenological observations were used to predict flowering onset, the multivariate models based on each of these data sources had similar predictive capacity (R-2 = 0.27). Further, apart from mean maximum temperature (TMAX), the two best predictors of flowering time have not commonly been included in phenological models: the number of frost-free days (NFFD) and the quantity of precipitation as snow (PAS) in the seasons preceding flowering. By vetting these models across an unprecedented number of taxa, this work demonstrates a new approach to phenological modeling.
Using herbarium specimens to select indicator species for climate change monitoring | 2018 | Biodiversity and Conservation
Rebecca A. Hufft, Michelle E. DePrenger-Levin, Richard A. Levy, Melissa B. Islam
Phenology is one of the best indicators to observe plant responses to climate change and predict future changes in plant communities. Choosing indicator species to monitor biological responses to climate change may be improved if herbarium specimens are combined with ongoing monitoring efforts to understand phenological responses over longer periods. We analyzed herbarium specimen data from Colorado’s alpine region, as alpine areas are predicted to be especially sensitive to climate change. We assessed phenological patterns in relation to temperature and precipitation for 287 species and growing degree days (GDD) for 235 species. Average low temperature, maximum GDD, and average precipitation increased over the study period. As temperature and GDD increased, phenology advanced, but as precipitation increased, phenology was delayed. Even with this variability of environmental responses, a significant trend of earlier flowering appeared when all species were analyzed together. Of the species that showed significantly earlier flowering dates, they advanced on average more than 39 days over the 61 years of the study. When assessing only specimens of species monitored in a national program (USA National Phenology Network), we found that these species showed similar trends to the entire dataset. When selecting species for ongoing monitoring efforts, herbarium specimens are an important resource to incorporate historical patterns into assessments of climate change and phenological drivers.
Prediction of Arctic plant phenological sensitivity to climate change from historical records | 2017 | Ecology and Evolution
Zoe A. Panchen, Root Gorelick
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.
Climate drives shifts in grass reproductive phenology across the western USA | 2017 | New Phytologist
Seth M. Munson, A. Lexine Long
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.
Validating Herbarium-Based Phenology Models Using Citizen-Science Data | 2016 | BioScience
Katie V. Spellman, Christa P. H. Mulder
Both herbarium specimens and citizen-science observations have become increasingly accessible but underutilized sources of data for phenology research. We developed and tested a novel technique that uses high-quality citizen-science observations to provide an independent validation of phenology models derived from herbarium specimens. Using this approach, we were able to evaluate the strengths and weaknesses of the herbarium data set. We found that our models were valid for understanding the relative shifts in the phenology of the focal species across a large geographic area but needed further calibration to provide accurate predictions for specific dates and locations. As herbarium specimens become increasingly digitized and citizen science becomes more frequently used as a research methodology, the potential application of the technique we present here will grow.
Timing the bloom season: a novel approach to evaluating reproductive phenology across distinct regional flora
2016 | Landscape Ecology
Isaac W. Park
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.
Historical changes in flowering phenology are governed by temperature × precipitation interactions in a widespread perennial herb in western North America | 2016 | New Phytologist
Elizabeth R. Matthews, Susan J. Mazer
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.
Realising the potential of herbarium records for conservation biology | 2016 | South African Journal of Botany
M. Greve, A.M. Lykke, C.W. Fagg, R.E. Gereau, G.P. Lewis, R. Marchant, A.R. Marshall, J. Ndayishimiye, J. Bogaert, J.-C. Svenning
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.
Long-term herbarium records reveal temperature-dependent changes in flowering phenology in the southeastern USA | 2015| International Journal of Biometeorology
Isaac W. Park, Mark D. Schwartz
In recent years, a growing body of evidence has emerged indicating that the relationship between flowering phenology and climate may differ throughout various portions of the growing season. These differences have resulted in long-term changes in flowering synchrony that may alter the quantity and diversity of pollinator attention to many species, as well as altering food availability to pollenivorous and nectarivorous animal species. However, long-term multi-season records of past flowering timing have primarily focused on temperate environments. In contrast, changes in flowering phenology within humid subtropical environments such as the southeastern USA remain poorly documented. This research uses herbarium-based methods to examine changes in flowering time across 19,328 samples of spring-, summer-, and autumn-flowering plants in the southeastern USA from the years 1951 to 2009. In this study, species that flower near the onset of the growing season were found to advance under increasing mean March temperatures (−3.391 days/°C, p = 0.022). No long-term advances in early spring flowering or spring temperature were detected during this period, corroborating previous phenological assessments for the southeastern USA. However, late spring through mid-summer flowering exhibited delays in response to higher February temperatures (over 0.1.85 days/°C, p ≤ 0.041 in all cases). Thus, it appears that flowering synchrony may undergo significant restructuring in response to warming spring temperatures, even in humid subtropical environments.
Long-term shifts in the phenology of rare and endemic Rocky Mountain plants | 2015 | American Journal of Botany
Seth M. Munson, Anna A. Sher
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.
Herbarium records identify sensitivity of flowering phenology of eucalypts to climate: Implications for species response to climate change | 2014| Austral Ecology
Deepa S. Rawal, Sabine Kasel, Marie R. Keatley, Craig R. Nitschke
Flowering phenology is very sensitive to climate and with increasing global warming the flowering time of plants is shifting to earlier or later dates. Changes in flowering times may affect species reproductive success, associated phenological events, species synchrony, and community composition. Long‐term data on phenological events can provide key insights into the impacts of climate on phenology. For Australia, however, limited data availability restricts our ability to assess the impacts of climate change on plant phenology. To address this limitation other data sources must be explored such as the use of herbarium specimens to conduct studies on flowering phenology. This study uses herbarium specimens for investigating the flowering phenology of five dominant and commercially important Eucalyptus species of south‐eastern Australia and the consequences of climate variability and change on flowering phenology. Relative to precipitation and air humidity, mean temperature of the preceding 3 months was the most influential factor on the flowering time for all species. In response to a temperature increment of 1°C, a shift in the timing of flowering of 14.1–14.9 days was predicted for E. microcarpa and E. tricarpa while delays in flowering of 11.3–15.5 days were found for E. obliqua, E. radiata and E. polyanthemos. Eucalyptus polyanthemos exhibited the greatest sensitivity to climatic variables. The study demonstrates that herbarium data can be used to detect climatic signals on flowering phenology for species with a long flowering duration, such as eucalypts. The robust relationship identified between temperature and flowering phenology indicates that shifts in flowering times will occur under predicted climate change which may affect reproductive success, fitness, plant communities and ecosystems.
Phylogenetic and climatic constraints drive flowering phenological patterns in a subtropical nature reserve | 2014 | Journal of Plant Ecology
Nan-Cai Pei, W. John Kress, Bu-Feng Chen, David L. Erickson, Khoon Meng Wong. Jin-Long Zhang, Wan-Hui Ye, Zhong-Liang Huang, Dian-Xiang Zhang
Aims: Exploring flowering patterns and detecting processes are essential when probing into the nature of reproductive traits during the life history and the interactions among different evolutionary clades. Such patterns are believed to be influenced by many factors, but quantifying these impacts at the community-level remains poorly understood.
Methods: We investigated the flowering patterns based on long-term herbarium records in a given area from subtropical forest regions in southern China. We obtained 5258 herbarium voucher specimens collected from the Dinghushan National Nature Reserve (DNNR) belonging to 166 families, 943 genera and 2059 species and examined the month when each species was flowering during the period 1920–2007.
Important Findings: The results showed that plants flowered sequentially almost throughout the whole year, showing the characteristics of subtropical evergreen broad-leaved forests. Flowering spectrums of the entire flora and the four life forms exhibited a clear unimodality that is probably typical of subtropical forest communities. Flowering patterns of the DNNR were positively correlated with mean rainfall, mean air temperature and mean sunshine duration. Median flowering dates of the 38 large species-rich families ranged from early April to late August; 25 families exhibited significant unimodal distribution patterns, whereas the remaining families were unclear or bimodal. Median flowering dates of the 10 most species-rich genera ranged from middle May to later July. While the results are consistent with climatic factors playing a general role in flowering patterns, median flowering dates varied significantly among species-rich families and genera, suggesting that phylogenies could provide specific constraints in subtropical forests.
Increasing temperature causes flowering onset time changes of alpine ginger Roscoea in the Central Himalayas2015 | Journal of Asia-Pacific Biodiversity
Dharmalingam Mohandass, Jian-Li Zhao, Yong-Mei Xia, Mason J.Campbell, Qing-Jun Li
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.
Climate Change and Flowering Phenology in Worcester County, Massachusetts | 2014 | International Journal of Plant Sciences
Robert I. Bertin
Flowering times are sensitive indicators of climate change. This study explores important methodological issues in the use of samples of phenological records, quantifies change in flowering times, and examines causes of variability among species. I used Monte Carlo simulations to explore effects of sample size on estimates of phenological statistics. I documented 60 yr of change in temperature and flowering times of forbs in Worcester County, Massachusetts, a largely nonurban area, using a combination of herbarium specimens and observations, and I tested several hypotheses using these data. I also compared changes in flowering times in eastern North America from several published studies. Average spring temperatures increased 1.4°C (0.24°C/decade) during the last 60 yr. Mean and median flowering dates were most robust for small sample sizes, while early and late flowering dates and ranges were least stable. Mean flowering time advanced 2.9 d (0.4°C/decade), with greatest advances in early-flowering species. The predicted advance for a spring-flowering species was 4–10 d (0.6°–1.5°C/decade) using different models, corresponding to 2.5–6.3 d/°C of springtime warming. Flowering advanced more in species with shorter blooming periods than in species with longer blooming periods. Flowering advance was unaffected by a species’ native status and by whether it was locally increasing or declining. Phenological advances reported for the same species in different studies showed no significant correlation. Advances in flowering times were comparable to those in other north temperate studies, as was the large change in spring-flowering species. Contrary to other studies, phenological changes were unrelated to a species’ native status and to changes in species frequency. Results of simulations and comparisons across studies suggest that sampling error may contribute substantially to reported variation among species.
Common garden comparison of the leaf‐out phenology of woody species from different native climates, combined with herbarium records, forecasts long‐term change | 2014 | Ecology Letters
Constantin M. Zohner, Susanne S. Renner
A well‐timed phenology is essential for plant growth and reproduction, but species‐specific phenological strategies are still poorly understood. Here, we use a common garden approach to compare biannual leaf‐out data for 495 woody species growing outdoors in Munich, 90% of them not native to that climate regime. For three species, data were augmented by herbarium dates for 140‐year‐long time series. We further meta‐analysed 107 temperate‐zone woody species in which leaf‐out cues have been studied, half of them also monitored here. Southern climate–adapted species flushed significantly later than natives, and photoperiod‐ and chilling‐ sensitive species all flushed late. The herbarium method revealed the extent of species‐specific climate tracking. Our results forecast that: (1) a northward expansion of southern species due to climate warming will increase the number of late flushers in the north, counteracting documented and expected flushing time advances; and (2) photoperiod‐ and chilling‐sensitive woody species cannot rapidly track climate warming.
Impacts of differing community composition on flowering phenology throughout warm temperate, cool temperate and xeric environments | 2014 | Global Ecology and Biogeography
Isaac W. Park
Aims: Flowering phenology is well documented to restrict the distribution of many plant species. However, community‐level shifts in flowering time may occur either through exclusion of species with unsuitably early or late flowering for local conditions (composition‐derived phenological shifts) or through intraspecific phenological responses to climate variations over space. Although these mechanisms have quite different ecological implications, the relative contribution of composition‐derived phenological shifts remains largely unknown. Therefore, determining the magnitude of composition‐derived phenological variation is crucial for understanding the relationship between phenology and community assemblage over space, and for predicting the impacts of future climate change. This study will evaluate the contributions of compositional differences to spatial variation in community‐level flowering times throughout the early, mid and late portions of the growing season and across a variety of temperate environments.
Location: Continental United States.
Methods: This study develops novel herbarium‐based methods to separate intraspecific phenological variations over space from changes in flowering time derived from differences in community composition.
Results: Although typically smaller than intraspecific variations, composition‐derived shifts in flowering time explained up to 49.3% of overall phenological variation. Composition‐derived changes in flowering time among late‐flowering species also explained the greatest proportion of overall variation and were the most responsive to differing climate conditions. Xeric regions also exhibited composition‐derived phenological shifts that were stronger and more closely tied to climate conditions (R2 up to 0.553) than other regions.
Main conclusions: These results indicate that interspecific differences in flowering time play a significant role in determining the composition of the plant community over space. However, the impact of flowering phenology on community assemblage varies considerably among seasons and climate regions, and appears to be strongest among xeric regions and among late‐flowering species.
Herbarium specimens show contrasting phenological responses to Himalayan climate | 2014 | PNAS
Robbie Hart, Jan Salick, Sailesh Ranjitkar, Jianchu Xu
Responses by flowering plants to climate change are complex and only beginning to be understood. Through analyses of 10,295 herbarium specimens of Himalayan Rhododendron collected by plant hunters and botanists since 1884, we were able to separate these responses into significant components. We found a lack of directional change in mean flowering time over the past 45 y of rapid warming. However, over the full 125 y of collections, mean flowering time shows a significant response to year-to-year changes in temperature, and this response varies with season of warming. Mean flowering advances with annual warming (2.27 d earlier per 1 °C warming), and also is delayed with fall warming (2.54 d later per 1 °C warming). Annual warming may advance flowering through positive effects on overwintering bud formation, whereas fall warming may delay flowering through an impact on chilling requirements. The lack of a directional response suggests that contrasting phenological responses to temperature changes may obscure temperature sensitivity in plants. By drawing on large collections from multiple herbaria, made over more than a century, we show how these data may inform studies even of remote localities, and we highlight the increasing value of these and other natural history collections in understanding long-term change.
Flowering cycles of woody bamboos native to southern South America | 2014 | Journal of Plant Research
Neotropical woody bamboos range from northern Mexico to southern Argentina and Chile. The most interesting aspect of bamboo biology is their flowering habit. The species that are the most intriguing are those that manifest a cyclic pattern of gregarious flowering after long vegetative periods. The flowering cycle has been described in very few species. The goal was to identify mass flowering events of woody bamboo species native to Argentina and neighboring areas, and to estimate the flowering cycle of each species. Sixteen species were surveyed: Chusquea culeou, C. deficiens, C. lorentziana, C. montana, C. quila, C. ramosissima, C. tenella, C. valdiviensis; Colanthelia rhizantha; Guadua chacoensis, G. paraguayana, G. trinii; Merostachys clausenii, M. multiramea, Rhipidocladum neumannii and R. racemiflorum. To reconstruct flowering dates, information from literature and herbarium collections was consulted and more than 990 records were gathered. Flowering cycles were estimated by recording the intervals between reported flowering events. Evidence of regular flowering cycles of ca. 30 years was found for most of the species considered. There is a remarkable concentration of flowering cycles about multiples of 15–16 years. Flowering synchrony among different species of woody bamboos was recorded for the first time in South America.
Determining past leaf‐out times of New England's deciduous forests from herbarium specimens | 2014 | American Journal of Botany
Peter H. Everill, Richard B. Primack, Elizabeth R. Ellwood, Eli K. Melaas
There is great interest in studying leaf‐out times of temperate forests because of the importance of leaf‐out in controlling ecosystem processes, especially in the face of a changing climate. Remote sensing and modeling, combined with weather records and field observations, are increasing our knowledge of factors affecting variation in leaf‐out times. Herbarium specimens represent a potential new source of information to determine whether the variation in leaf‐out times observed in recent decades is comparable to longer time frames over past centuries. Here we introduce the use of herbarium specimens as a method for studying long‐term changes in leaf‐out times of deciduous trees. We collected historical leaf‐out data for the years 1834–2008 from common deciduous trees in New England using 1599 dated herbarium specimens with young leaves. We found that leaf‐out dates are strongly affected by spring temperature, with trees leafing out 2.70 d earlier for each degree C increase in mean April temperature. For each degree C increase in local temperature, trees leafed out 2.06 d earlier. Additionally, the mean response of leaf‐out dates across all species and sites over time was 0.4 d earlier per decade. Our results are of comparable magnitude to results from studies using remote sensing and direct field observations. Across New England, mean leaf‐out dates varied geographically in close correspondence with those observed in studies using satellite data. This study demonstrates that herbarium specimens can be a valuable source of data on past leaf‐out times of deciduous trees.
Species-level phenological responses to ‘global warming’ as evidenced by herbarium collections in the Tibetan Autonomous Region | 2013 | Biodiversity and Conservation
Zhongrong Li, Ning Wu, Xinfen Gao, Yan Wu, Krishna P. Oli
In recent years attention has been given to assess the impacts of warming on the plant flowering phenology. There is a growing realization that herbarium-based collections could offer a reliable and relatively time-saving baseline data source to identify these effects. This article examines the magnitude and trends of warming effects on the average flowering timing (AFT) of plants in Tibet Autonomous Region using analysis of herbarium specimens collected for 4 decades. Mixed model with randomized blocks was used to analyze a set of 41 species (total 909 specimens) which were collected during the period of 1961–2000. Results showed that an earlier AFT emerged within 40 years period in comparison to the recorded data of the year of 2000 (0.5 days per year), and that 7.5 days early flowering was contributed by mean summer (i.e., June–August) temperature. It is proposed that temporary shifts in flowering phenology responding to continuing temperature rise could quantify the extent to which climate affects plant species. Analysis of well recorded herbarium specimens could provide a reasonable indication on the impacts of rising temperature on plant phenology. The result of this study could also facilitate a bridge between the scientific knowledge and indigenous knowledge of Tibetan communities.
Herbarium specimens reveal the footprint of climate change on flowering trends across north‐central North America | 2013 | Ecology Letters
Kellen M. Calinger, Simon Queenborough, Peter S. Curtis
Shifting flowering phenology with rising temperatures is occurring worldwide, but the rarity of co‐occurring long‐term observational and temperature records has hindered the evaluation of phenological responsiveness in many species and across large spatial scales. We used herbarium specimens combined with historic temperature data to examine the impact of climate change on flowering trends in 141 species collected across 116,000 km2 in north‐central North America. On average, date of maximum flowering advanced 2.4 days °C−1, although species‐specific responses varied from − 13.5 to + 7.3 days °C−1. Plant functional types exhibited distinct patterns of phenological responsiveness with significant differences between native and introduced species, among flowering seasons, and between wind‐ and biotically pollinated species. This study is the first to assess large‐scale patterns of phenological responsiveness with broad species representation and is an important step towards understanding current and future impacts of climate change on species performance and biodiversity.
Phenological Predictability Index in BRAHMS: a tool for herbarium‐based phenological studies | 2012 | Ecography
Carolyn E. B. Proença, Denis L. Filer, Eddie Lenza, Juliana S. Silva, Stephen A. Harris
Phenological Predictability Index (PPI) is a tool for analysing phenological patterns incorporating herbarium data within BRAHMS (Botanical Research and Herbarium Management System). PPI produces a maximum‐activity period and associated event predictability index between ∼0 and 1. Simple, monthly random sampling showed the ideal number of unique records (event/month/year) is > 50. PPI correctly predicted the maximum‐activity flowering month for seven out of eight species studied in the field, and was positively correlated (R2= 0.610, p = 0.02) with phenophase length, even using suboptimum numbers of unique records.
Digital herbarium archives as a spatially extensive, taxonomically discriminate phenological record; a comparison to MODIS satellite imagery | 2012 | International Journal of Biometeorology
Isaac W. Park
This study demonstrates that phenological information included in digital herbarium archives can produce annual phenological estimates correlated to satellite-derived green wave phenology at a regional scale (R = 0.183, P = 0.03). Thus, such records may be utilized in a fashion similar to other annual phenological records and, due to their longer duration and ability to discriminate among the various components of the plant community, hold significant potential for use in future research to supplement the deficiencies of other data sources as well as address a wide array of important issues in ecology and bioclimatology that cannot be addressed easily using more traditional methods.
Herbarium specimens, photographs, and field observations show Philadelphia area plants are responding to climate change | 2012 | American Journal of Botany
Zoe A. Panchen, Richard B. Primack, Tomasz Aniśko, Robert E. Lyons
The global climate is changing rapidly and is expected to continue changing in coming decades. Studying changes in plant flowering times during a historical period of warming temperatures gives us a way to examine the impacts of climate change and allows us to predict further changes in coming decades. The Greater Philadelphia region has a long and rich history of botanical study and documentation, with abundant herbarium specimens, field observations, and botanical photographs from the mid‐1800s onward. These extensive records also provide an opportunity to validate methodologies employed by other climate change researchers at a different biogeographical area and with a different group of species. Data for 2539 flowering records from 1840 to 2010 were assessed to examine changes in flowering response over time and in relation to monthly minimum temperatures of 28 Piedmont species native to the Greater Philadelphia region. Regression analysis of the date of flowering with year or with temperature showed that, on average, the Greater Philadelphia species studied are flowering 16 d earlier over the 170‐yr period and 2.7 d earlier per 1°C rise in monthly minimum temperature. Of the species studied, woody plants with short flowering duration are the best indicators of a warming climate. For monthly minimum temperatures, temperatures 1 or 2 mo prior to flowering are most significantly correlated with flowering time. Studies combining herbarium specimens, photographs, and field observations are an effective method for detecting the effects of climate change on flowering times.
Pollination mode predicts phenological response to climate change in terrestrial orchids: a case study from central Europe | 2012 | Journal of Ecology
Attila Molnár V, Jácint Tökölyi, Zsolt Végvári, Gábor Sramkó, József Sulyok, Zoltán Barta
Herbarium collections contain long‐term data for a wide range of taxa and provide unique opportunities to evaluate the importance of life‐history components in driving species‐specific responses to climate change. In this paper, we analyse the relationships between change in flowering dates and life‐history traits within a phylogenetic framework. The study is based on an extensive data set of herbarium specimens of orchids collected in Hungary between 1837 and 2009, supplemented by recent field observations (1980–2011). Of the 39 taxa investigated, 31 (79%) showed apparent advancement in mean flowering time. Among these, advancement was statistically significant in nine taxa. The rest (eight taxa) showed non‐significant delays in flowering. Averaging across all taxa, flowering time advanced by 3 days (3.8% of flowering period) during the last 50 years compared with the period before 1960. In taxa showing significant advancement, flowering times advanced by 7.7 days (8.6% of the flowering period). The most extreme advancement was 13.9 days. Multivariate models were used to evaluate ways in which life history may affect phenological responses to climate change. Pollination mode (i.e. deceptive vs. rewarding vs. autogamous), life span (i.e. short‐lived vs. long‐lived), biogeographical distribution type (i.e. Mediterranean vs. non‐Mediterranean) and flowering time (i.e. mean date of blooming) emerged as important factors that influence changes in flowering through time. Phylogenetic relatedness did not predict phenological response. The strongest response was observed in orchids that flower relatively early in spring, exhibit an autogamous or deceptive pollination mechanism, have a long life span and possess a Mediterranean centre of distribution. Our investigation demonstrates that the majority of Hungarian orchids have shifted their yearly mean flowering to earlier dates during the past 50 years. Certain life‐history traits, but not phylogenetic relatedness, were found to be important in predicting climatic responsiveness in European terrestrial orchids.
The phenology of Rubus fruticosus in Ireland: herbarium specimens provide evidence for the response of phenophases to temperature, with implications for climate warming | 2012 | International Journal of Biometeorology
E. Diskin, H. Proctor, M. Jebb, T. Sparks, A. Donnelly
To date, phenological research has provided evidence that climate warming is impacting both animals and plants, evidenced by the altered timing of phenophases. Much of the evidence supporting these findings has been provided by analysis of historic records and present-day fieldwork; herbaria have been identified recently as an alternative source of phenological data. Here, we used Rubus specimens to evaluate herbaria as potential sources of phenological data for use in climate change research and to develop the methodology for using herbaria specimens in phenological studies. Data relevant to phenology (collection date) were recorded from the information cards of over 600 herbarium specimens at Ireland’s National Herbarium in Dublin. Each specimen was assigned a score (0–5) corresponding to its phenophase. Temperature data for the study period (1852 – 2007) were obtained from the University of East Anglia’s Climate Research Unit (CRU); relationships between temperature and the dates of first flower, full flower, first fruit and full fruit were assessed using weighted linear regression. Of the five species of Rubus examined in this study, specimens of only one (R. fruticosus) were sufficiently abundant to yield statistically significant relationships with temperature. The results revealed a trend towards earlier dates of first flower, full flower and first fruit phenophases with increasing temperature. Through its multi-phenophase approach, this research serves to extend the most recent work—which validated the use of herbaria through use of a single phenophase—to confirm herbarium-based research as a robust methodology for use in future phenological studies.
Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens | 2011 | Proceedings of the Royal Society B Biological Sciences
Paul-Camilo Zalamea, François Munoz, Pablo R. Stevenson, C. E. Timothy Paine, Carolina Sarmiento, Daniel Sabatier, Patrick Heuret
Plant phenology is concerned with the timing of recurring biological events. Though phenology has traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale dataset of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns within and among climatic regions. Although previous studies have suggested that pioneer species generally produce flowers continually throughout the year, we found that at least one third of Cecropia species are characterized by clear annual flowering behaviour. We further investigated the relationships between phenology and climate seasonality, showing strong associations between phenology and seasonal variations in precipitation and temperature. We also verified our results against field survey data gathered from the literature. Our findings indicate that herbarium material is a reliable resource for use in the investigation of large-scale patterns in plant phenology, offering a promising complement to local intensive field studies.
Potential of herbarium records to sequence phenological pattern: a case study of Aconitum heterophyllum in the Himalaya | 2011 | Biodiversity and Conservation
Kailash S. Gaira, Uppeandra Dhar, O. K. Belwal
Several pieces of evidence indicate that global climate change is affecting biological systems all across the world. Phenology is one of the tools that may indicate changing patterns. The paper focuses on the phenological pattern of alpine/sub-alpine species Aconitum heterophyllum, a high-value medicinal herb of the Indian Himalayan Region (IHR), a global hotspot and known to be sensitive to climatic change. In all 117 herbarium specimens of the species collected from three provinces (Western Himalaya, North West Himalaya and Trans Himalaya) of the region were recorded. Historic herbarium records (1848–2003) were analyzed to predict the flowering patterns using Generalized Additive Model (GAM) in view of complexity in the herbarium-based data structure. GAM indicated that the flowering time responded significantly, 26 days earlier per 1,000 m (P < 0.02). Likewise, the model showed significantly earlier flowering (17–25 days) during the last 100 years (P < 0.01). Moreover, maximum temperature of winter (December–February) explained increasing trends at both elevations (lower and mid) and mean winter temperature influenced the early flowering time (19–27 days) with an increase of 1°C. The overall early flowering of A. heterophyllum may perhaps be considered as indicator of climate change; however, more datasets of herbarium records are required to further strengthen this premise. This study was undertaken to show that herbarium records could be utilized as a potential resource for assessing climate change using GAM.
Validation of biological collections as a source of phenological data for use in climate change studies: a case study with the orchid Ophrys sphegodes | 2010 | Journal of Ecology
Karen M. Robbirt, Anthony J. Davy, Michael J. Hutchings, David L. Roberts
The scarcity of reliable long‐term phenological data has severely hindered the study of the responses of species to climate change. Biological collections in herbaria and museums are potential sources of long‐term data for such study, but their use for this purpose needs independent validation. Here we report a rigorous test of the validity of using herbarium specimens for phenological studies, by comparing relationships between climate and time of peak flowering derived from herbarium records and from direct field‐based observations, for the terrestrial orchid Ophrys sphegodes. We examined herbarium specimens of O. sphegodes collected between 1848 and 1958, and recorded peak flowering time directly in one population of O. sphegodes between 1975 and 2006. The response of flowering time to variation in mean spring temperature (March–May) was virtually identical in both sets of data, even though they covered different periods of time which differ in extent of anthropogenic temperature change. In both cases flowering was advanced by c. 6 days per °C rise in average spring temperature. The proportion of variation in flowering time explained by spring temperature was lower in the herbarium record than in direct field observations. It is likely that some of the additional variation was due to geographical variation in collection site, as flowering was significantly earlier at more westerly sites, which have had warmer springs, over their range of 3.44° of longitude. Predictions of peak flowering time based on the herbarium data corresponded closely with observed peak flowering times in the field, indicating that flowering response to temperature had not altered between the two separate periods over which the herbarium and field data were collected. These results provide the first direct validation of the use of herbarium collections to examine the relationships between phenology and climate when field‐based observational data are not available.
Biological indicators of climate change: evidence from long-term flowering records of plants along the Victorian coast, Australia | 2010 | Australian Journal of Botany
Libby Rumpff, Fiona Coates, John W. Morgan
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.
Effects of urbanization on flowering phenology in the metropolitan phoenix region of USA: Findings from herbarium records| 2010 | Journal of Arid Environments
Kaesha L.Neil, Leslie Landrum, Jianguo Wu
Phenological studies have become more prominent recently because of rising interests in understanding how plants, communities, and ecosystems respond to global climate change and urban climate modifications. Herbarium records of plants can be a particularly useful source of information for studying historical trends in phenology in areas where long-term phenological records do not exist. In this study, we used herbarium records to examine the historical patterns of flowering phenology of 87 shrubs and ephemerals in the Phoenix metropolitan region in the southwestern United States from 1902 through 2006. We found that 19% of plant species examined either advanced or delayed their flowering. Also, the flowering responses of 28% of the species examined showed significant differences between urban and non-urban areas: 24% advanced in urban areas and 5% delayed. Our study indicates that urbanization may have a significant effect on the flowering phenology of a small but substantial proportion of plants, which will likely affect native biological diversity and ecosystem services due to potential changes in population and community dynamics.
Effects of small-scale disturbances and elevation on the morphology, phenology and reproduction of a successful geophyte | 2009 | Journal of Plant Ecology
Daniel Gómez-García, José Azorín, A. Javier Aguirre
Aims: We aimed to find out how a geophyte, Merendera montana, occupies a wide ecological, elevational and climatic range. This occurrence in that environmental array is outstanding not only among geophytes but also in the whole flora of the Iberian Peninsula, where only a very few plants show such an apparent success. Specifically, we compared morphological and reproductive traits, and frequency of different types of reproduction in disturbed and undisturbed grasslands. Furthermore, we have analyzed the phenology of this plant by trying to understand how it manages to spread in an exceptional elevational gradient of 2000 m, with contrasting climatic regimes between the mediterranean and the alpine regions.
Methods: We measured the plant density of M.montana populations in different types of Pyrenean grasslands either with or without small-scale disturbances at seven sites from the basal to the alpine belt (400–2300 m a.s.l.). In each one of these populations, 100 individuals—1200 in total—were uprooted to measure their morphological features as well as type and occurrence of reproduction. Phenology (flowering and fruiting dates and leaf lifespan) was estimated using 5 years of records in the studied areas and >200 herbarium sheets from the whole altitudinal rank and collected in the last 30 years. Differences in plant densities were analyzed with non-parametric Mann–Whitney U-test; differences in morphological traits, fruit and seed production associated with disturbance, with one-way analysis of covariance test (general linear model). Finally, linear regression analyses were used to determine the relationships between clonal reproduction and elevation and those between flowering, fruiting and senescence and date and elevation.
Important Findings: In all cases, plant density in disturbed grasslands was significantly higher than in undisturbed grasslands. Plant height and weight, bulb depth, leaf width and bulb and root weight were higher in disturbed plots. Disturbed and undisturbed plots were similar in most aspects of sexual reproduction, including fruiting percentage and seed production, but average seed weight was higher in the disturbed plots. Clonal reproduction and the synchrony of both types of reproduction were significantly higher in disturbed plots. Flowering and leaf emergence dates were not affected by disturbance but at the lowest elevations, they happened at least 2 months later than at the highest elevations. Summarizing, clonal reproduction, advantage in seedling establishment and an unusual but favorable phenology are the main factors in explaining the success of this geophyte colonizing disturbed soils that, in consequence, allow M.montana to settle in a wide range of climatic and ecological conditions.
Phenological trends among Australian alpine species: using herbarium records to identify climate-change indicators | 2009 | Australian Journal of Botany
R. V. Gallagher, L. Hughes, M. R. Leishman
Global temperatures are increasing at an unprecedented rate and the analysis of long-term phenological records has provided some of the most compelling evidence for the effect of these changes on species. In regions where systematically collected data on the timing of life-cycle events is scarce, such as Australia, researchers must seek alternative sources of information from which climate-change signals can be identified. In the present paper, we explore the limitations and strengths of using herbarium specimens to detect changes in flowering phenology, to select potential indicator species, and to pinpoint locations for potential monitoring schemes of native plants in Australia’s subalpine and alpine zone. We selected 20 species on the basis of a range of selection criteria, including a flowering duration of 3 months or less and the number of herbarium records available in the areas above 1500 m. By the use of gridded temperature data within the study region, we identified an increase in mean annual temperature of 0.74°C between 1950 and 2007. We then matched the spatial locations of the herbarium specimens to these temperature data and, by using linear regression models, identified five species whose flowering response may be sensitive to temperature. Higher mean annual temperatures at the point of collection were negatively associated with earlier flowering in each of these species (α = 0.05). We also found a significant (P = 0.02) negative relationship between year and flowering observation for Alpine groundsel, Senecio pectinatus var. major. This species is potentially a suitable candidate for monitoring responses of species to future climate change, owing to the accessibility of populations and its conspicuous flowers. It is also likely that with ongoing warming the other four species identified (Colobanthus affinis, Ewartia nubigena, Prasophyllum tadgellianum and Wahlenbergia ceracea) in the present study may show the same response.
Declining insolation induces synchronous flowering of Montanoa and Simsia (Asteraceae) between Mexico and the Equator | 2009 | Trees
Zoraida Calle, Alan H. Strahler, Rolf Borchert
We analyze the latitudinal shift in the onset of synchronous flowering in the woody genera Montanoa and Simsia (Asteraceae) between Mexico (28° N) and the Equator, where it cannot be caused by declining day length. Synchronous flowering of >100 Montanoa quadrangularis trees was observed during two consecutive years near Cali, Colombia (4° N). Analysis of herbarium specimens yielded flowering periods for 21 Montanoa species and 18 Simsia species between 4 and 28° N. Daily insolation is a function of day length and the angle at which the sun’s rays strike the earth. Between Mexico and Colombia (4° N), the maximum of insolation gradually shifts from the summer solstice to the autumn equinox. In parallel, flowering of Montanoa and Simsia starts progressively later between July and November, during the period of declining insolation. Near the Equator, there are two periods of declining insolation, and correspondingly, two flowering periods. Thus, at all tropical latitudes, flowering time of Montanoa and Simsia is highly correlated with declining insolation. The seasonal decline in daily insolation, rather than in photoperiod, apparently induces synchronous flowering of Montanoa and Simsia at the same time each year.
Mushroom fruiting and climate change | 2008 | PNAS
Håvard Kauserud, Leif Christian Stige, Jon Olav Vik, Rune H. Økland, Klaus Høiland, Nils Chr. Stenseth
Many species of fungi produce ephemeral autumnal fruiting bodies to spread and multiply. Despite their attraction for mushroom pickers and their economic importance, little is known about the phenology of fruiting bodies. Using ≈34,500 dated herbarium records we analyzed changes in the autumnal fruiting date of mushrooms in Norway over the period 1940–2006. We show that the time of fruiting has changed considerably over this time period, with an average delay in fruiting since 1980 of 12.9 days. The changes differ strongly between species and groups of species. Early-fruiting species have experienced a stronger delay than late fruiters, resulting in a more compressed fruiting season. There is also a geographic trend of earlier fruiting in the northern and more continental parts of Norway than in more southern and oceanic parts. Incorporating monthly precipitation and temperature variables into the analyses provides indications that increasing temperatures during autumn and winter months bring about significant delay of fruiting both in the same year and in the subsequent year. The recent changes in autumnal mushroom phenology coincide with the extension of the growing season caused by global climate change and are likely to continue under the current climate change scenario.
Has climatic warming altered spring flowering date of Sonoran desert shrubs? | 2007 | The Southwestern Naturalist
Janice E. Bowers
With global warming, flowering at many locations has shifted toward earlier dates of bloom. A steady increase in average annual temperature since the late 1890s makes it likely that flowering also has advanced in the northern Sonoran Desert of the southwestern United States and northwestern Mexico. In this study, phenological models were used to predict annual date of spring bloom in the northern Sonoran Desert from 1894 to 2004; then, herbarium specimens were assessed for objective evidence of the predicted shift in flowering time. The phenological models were derived from known flowering requirements (triggers and heat sums) of Sonoran Desert shrubs. According to the models, flowering might have advanced by 20–41 d from 1894 to 2004. Analysis of herbarium specimens collected during the 20th century supported the model predictions. Over time, there was a significant increase in the proportion of shrub specimens collected in flower in March and a significant decrease in the proportion collected in May. Thus, the flowering curve – the proportion of individuals in flower in each spring month – shifted toward the start of the calendar year between 1900 and 1999. This shift could not be explained by collection activity: collectors showed no tendency to be active earlier in the year as time went on, nor did activity toward the end of spring decline in recent decades. Earlier bloom eventually could have substantial impacts on plant and animal communities in the Sonoran Desert, especially on migratory hummingbirds and population dynamics of shrubs.
Photographs and herbarium specimens as tools to document phenological changes in response to global warming | 2006 | American Journal of Botany
Abraham J. Miller‐Rushing, Richard B. Primack, Daniel Primack, Sharda Mukunda
Global warming is affecting natural systems across the world. Of the biological responses to warming, changes in the timing of phenological events such as flowering are among the most sensitive. Despite the recognized importance of phenological changes, the limited number of long‐term records of phenological events has restricted research on the topic in most areas of the world. In a previous study in Boston (American Journal of Botany 91: 1260–1264), we used herbarium specimens and one season of field observations to show that plants flowered earlier as the climate warmed over the past 100 yr. In our new study, we found that two extra years of data did not strengthen the explanatory power of the analysis. Analysis of herbarium specimens without any field data yielded results similar to analyses that included field observations. In addition, we found that photographs of cultivated and wild plants in Massachusetts, data similar to that contained in herbarium specimens, show changes in flowering times that closely match independent data on the same species in the same locations. Dated photographs of plants in flower represent a new resource to extend the range of species and localities addressed in global‐warming research.
A new herbarium‐based method for reconstructing the phenology of plant species across large areas | 2006 | American Journal of Botany
Claude Lavoie, Daniel Lachance
Phenological data have recently emerged as particularly effective tools for studying the impact of climate change on plants, but long phenological records are rare. The lack of phenological observations can nevertheless be filled by herbarium specimens as long as some correction procedures are applied to take into account the different climatic conditions associated with sampling locations. In this study, we propose a new herbarium‐based method for reconstructing the flowering dates of plant species that have been collected across large areas. Coltsfoot (Tussilago farfara L.) specimens from southern Quebec were used to test the method. Flowering dates for coltsfoot herbarium specimens were adjusted according to the date of disappearance of snow cover in the region where they were collected and compared using a reference point (the date of earliest snowmelt). In southern Quebec, coltsfoot blooms earlier at present (15–31 d) than during the first part of the 20th century. This phenomenon is likely associated with the climate warming trends recorded in this region in the last century, especially during the last three decades when the month of April became warmer, thereby favoring very early‐flowering cases. The earlier flowering of coltsfoot is, however, only noticeable in large urban areas (Montreal, Quebec City), suggesting a strong urban heat island effect on the flowering of this plant. Herbarium specimens are useful phenological indicators; however, the databases should be carefully examined prior to analysis to detect biases or trends associated with sampling locations.
Family, visitors and the weather: patterns of flowering in tropical rain forests of northern Australia | 2005 | Journal of Ecology
S. L. Boulter, R. L. Kitching, B. G. Howlett
A data base on the flowering phenology of the Wet Tropics bioregion of far northern Queensland, Australia, has been constructed, based upon over 36 774 records from two Queensland‐based herbaria. Flowering patterns have been analysed against the predictions of three overlapping hypotheses based on climatic, biotic and phylogenetic explanations. No one hypothesis is supported to the exclusion of the others. Patterns of flowering in the Wet Tropics show marked seasonal increases and decreases, except in the northern lowlands. In general this seasonality correlates with rainfall and temperature and is exacerbated by increasing latitude and altitude. There is little or no statistical evidence for the over‐dispersion of flowering times that would indicate a competition‐avoidance mechanism: flowering within taxa or morphological groups tends to be clumped (and if not, is random). That clumping of flowering within taxa does not coincide with a single season provides support for a mass action hypothesis based on the minimization of generalist predation and/or the avoidance of flower predation. Timing of flowering did show some consistency among species within genera and within families, but there was little consistency at higher taxonomic levels. Clear separation of the biotic and phylogenetic hypotheses requires greater knowledge of pollination ecology and phylogeny of this large and diverse flora. Understanding of flowering patterns and their underlying determining mechanisms is a key to assessing the ecosystem health of the forest. Our results highlight the importance of competitive interactions and of physical and evolutionary factors as determinants of flowering time, intensity and co‐occurrence in tropical forests.
El Niño and displays of spring-flowering annuals in the Mojave and Sonoran deserts | 2004 | The Journal of the Torrey Botanical Society
Janice E. Bowers
Although popular and scientific literature frequently assumes a strong connection between El Niño-Southern Oscillation (ENSO) and good displays of spring-flowering annuals in the southwestern United States, such assumptions are based on anecdotal, short-term evidence. The goals of this study were to identify good wildflower years as objectively as possible, to assess the correlation between El Niño and good displays of spring-flowering annuals, and to examine the influence of rainfall amounts on good wildflower years. The terms “good displays” and “good wildflower years” refer to times or places when populations of showy spring-flowering annuals (often called winter annuals) are abundant, robust, and diverse. In the deserts of southeastern California and southern Arizona, good wildflower years occurred about once every 5 to 7 years in the 20th century. The connection between good wildflower years and traditionally defined El Niño episodes was weak, but when El Niño was redefined in a phenologically meaningful way as any calendar year in which the average Southern Oscillation Index (SOI) between July and December was negative, 21 of 27 good wildflower years in the combined deserts were associated with El Niño. Good wildflower years were 3.6 times more likely after redefined El Niño years than after other years. Rain in the months before good wildflower years was at least 30% greater than the long-term average in the Mojave Desert and at least 50% greater in the Sonoran Desert. A diverse flora of spring-flowering annuals occurred in the region during the late Wisconsin and early Holocene, which was a period of wetter, milder winters and cooler summers. Perhaps some species of spring-flowering annuals persist today in the arid southwestern United States only because frequent El Niño conditions recreate the cool, moist conditions of the late Pleistocene.
Herbarium data reveal an association between fleshy fruit type and earlier flowering time | 2005 | International Journal of Plant Sciences
Kjell Bolmgren, Karin Lönnberg
Herbarium phenology data were evaluated and then applied in a phylogenetically independent contrast study in which flowering times were compared between fleshy and nonfleshy‐fruited plants growing in the north‐temperate provinces of Uppland and Södermanland, southeastern Sweden (59°–60°N). To evaluate herbarium phenology data, flowering‐time information taken from herbarium specimens in the Swedish Natural History Museum (S) was compared with two independent field phenology data sets. Herbarium collections and the field studies were restricted to the province of Uppland. Flowering times derived from herbarium specimens correlated equally well with each of the two field‐phenology data sets as the field phenology data sets did to each other. Differences between flowering times derived from field and herbarium collections were not affected by the number of herbarium specimens used. However, these differences in flowering times were affected by flowering season such that herbarium‐derived flowering times were later for early spring‐flowering species and earlier for late summer‐flowering species when compared with flowering times derived from field data. In the phylogenetically independent contrast study of mean flowering times in fleshy‐ compared with nonfleshy‐fruited plants, herbarium data were compiled for 77 species in 17 phylogenetically independent contrasts. Flowering time was found to be earlier for fleshy‐fruited taxa, illustrating the evolutionary interdependence between flowering and fruiting phases and the constraining effects of a north‐temperate climate on phenology evolution. This study shows that herbaria are reliable and time‐saving data sources for comparative phenology studies and allow for studies at large phylogenetic and geographic scales that would otherwise be impossible.
Photoperiodic control of seasonal development and dormancy in tropical stem-succulent trees | 2001 | Tree Physiology
R. Borchert, G. Rivera
Museum specimens collected in the past may be a valuable source of information on the response of species to climate change. This idea was tested by comparing the flowering times during the year 2003 of 229 living plants growing at the Arnold Arboretum in Boston, Massachusetts, USA, with 372 records of flowering times from 1885 to 2002 using herbarium specimens of the same individual plants. During this period, Boston experienced a 1.5°C increase in mean annual temperature. Flowering times became progressively earlier; plants flowered 8 d earlier from 1980 to 2002 than they did from 1900 to 1920. Most of this shift toward earlier flowering times is explained by the influence of temperature, especially temperatures in the months of February, March, April, and May, on flowering time. Plants with a long flowering duration appear to be as useful for detecting responses to changing temperatures as plants with a short flowering duration. Additional studies using herbarium specimens to detect responses to climate change could examine specimens from specific, intensively collected localities, such as mountain peaks, islands, and unique habitats.
Trends in the phenology of flowering in the orchidaceae of Western Mexico | 1996 | Biotropica
Phenology and flowering periodicity of Neotropical dry forest species: evidence from herbarium collections | 1996 | Journal of Tropical Ecology
To examine the potential contribution of herbarium material to the description and analysis of tropical tree phenology, flowering times and geographical distribution were graphed for 1673 flowering collections from 18 species native to Neotropical dry forests and phenological differences between species were analysed. These include the timing and duration of flowering as well as morphological differences such as flowering on leafless twigs vs flowering on shoots bearing old or new foliage. Species-specific flowering periods of herbarium collections are similar to those observed in phenological field studies, but are often longer because of the larger geographical and temporal sampling range. Conspecific collections of different geographical origin show distinct differences in flowering periodicity, which are correlated with differences in the timing and intensity of the dry season. Interspecific differences in the timing of phenology relative to the dry season indicate differences in the control of phenology by seasonal drought. Herbaria thus represent a large potential source of phenological information which can either supplement and extend phenological field studies or provide phenological information for dry forest species not studied in the field but well represented in herbarium collections.
The Ruby-throated Hummingbird and its major food plants: ranges, flowering phenology, and migration | 1982 | Canadian Journal of Zoology
Robert I. Bertin
The Ruby-throated Hummingbird (or rubythroat, Archilochus colubris) and several of its major food plants were examined to assess the importance of rubythroat versus insect pollination, the overlap of geographical ranges, and the synchrony between migration and flowering times. Seed set of Impatiens biflora was increased 8–17% by rubythroat and insect visitation over the level achieved by insects alone. The rubythroat's range is not contiguous with that of any of 22 putative food plants examined, but is nearly coincident with the range of certain forest types, perhaps reflecting the importance of sap for food. A new method was developed to estimate peak flowering times of plants from herbarium data. Based on these data and field observations, only one rubythroat food plant (Impatiens biflora) had peak flowering times close to peak rubythroat migration times throughout their shared range. Rubythroats and their North American food plants are facultative mutualists, with the plants apparently having been evolutionarily more labile.