Skip to main content
Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Estimation of true dates of various flowering stages at a centennial scale by applying a Bayesian statistical state space model

  • Nagai Shin ,

    Contributed equally to this work with: Nagai Shin, Hakuryu Fujiwara

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing – original draft, Writing – review & editing

    nagais@jamstec.go.jp

    Affiliation Research Institute for Global Change, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan

  • Hakuryu Fujiwara ,

    Contributed equally to this work with: Nagai Shin, Hakuryu Fujiwara

    Roles Data curation, Investigation

    Affiliation Amateur Photographer, Motosu City, Japan

  • Shinjiro Sugiyama,

    Roles Data curation, Investigation

    Affiliation Neo Community Center, Motosu City, Japan

  • Hiroshi Morimoto,

    Roles Formal analysis, Methodology, Validation, Writing – review & editing

    Affiliation Emeritus Professor, Nagoya University, Nagoya, Japan

  • Taku M. Saitoh

    Roles Validation, Writing – review & editing

    Affiliation Center for Environmental and Societal Sustainability, Gifu University, Gifu, Japan

Abstract

Evaluation of long-term detailed cherry flowering phenology is required for a deep understanding of the sensitivity of spring phenology to climate change and its effect on cultural ecosystem services. Neodani Usuzumi-zakura (Cerasus itosakura) is a famous cherry tree in Gifu, Japan. On the basis of detailed decadal flowering phenology information published on the World Wide Web, we estimated the probability distributions of the year-to-year variability of the true dates of first flowering (FFL), first full bloom (FFB), last full bloom (LFB), and last flowering (LFL) from 1924 to 2024 by applying a Bayesian statistical state space model explained by air temperature data. We verified the estimated values against flowering phenology records of the tree from the literature and a private collection. The true dates of FFL and FFB could be explained by means of daily minimum air temperature from 1 December to 28/29 February and that of daily mean air temperature from 1 to 31 March, and those of LFB and LFL by means of daily mean air temperature from 1 to 10 April. Results were similar when we used air temperature data recorded at weather stations both 1 km and 29 km from the tree. These results indicated that our proposed Bayesian statistical state space model can estimate cherry flowering phenology that takes into account centennial-scale air temperature data recorded at a nearby weather station with a coarse temporal resolution.

Introduction

Long-term records or prediction of cherry flowering phenology play an important role in the evaluation of changes in the sensitivity of spring plant phenology (i.e., flowering and leaf flushing) to climate change and its effect on cultural ecosystem services. As many deciduous trees flush new leaves at the same time as or after cherry flowering in Japan [1], cherry flowering phenology can be used as a representative spring plant phenology. Japan celebrates a traditional culture of Hanami, or cherry-blossom viewing [2]. For this reason, long-term records of Hanami festivals in the Imperial Palace since the 9th century, which can be used as proxy data for cherry flowering phenology [3], can be retrieved. Old diaries written by a citizen in the 19th century (middle Edo era) also allowed us to retrieve continuous records of cherry flowering phenology [4]. Since the early 20th century (late Meiji era), weather stations throughout Japan have collected phenological observations of various animals and plants. The records of cherry flowering date back to 1903 in Miyagi Prefecture [5,6] and to 1909 in Kyoto [7]. The Japanese Meteorological Agency (JMA) standardized phenological observations in 1953 [8], but we can retrieve the records of cherry flowering phenology (mainly Yoshino cherry, Cerasus × yedoensis) before then at multiple weather stations in Japan. Analysis of these data found that: (1) the dates of first flowering (FFL) throughout Japan advanced by 1.2 days per decade from 1953 to 2022 [9]; and (2) the correlation between dates of FFL and latitude decreased from 1953 to 2020 owing to delayed release of endodormancy in low latitude regions where annual mean air temperature is high [10].

Previous studies based on the long-term continuous records of cherry flowering phenology at multiple weather stations or popular cherry blossom viewing sites in Japan predicted the dates of FFL and first full bloom (FFB) by semi-empirical statistical phenology models (so-called “degree-day models” [1113]) and machine learning algorithms (e.g., self-organizing maps [10], random forests, artificial neural networks, and gradient-boosting decision trees [14]). However, these models and algorithms have three issues. First, no model or algorithm can predict the dates of the last full bloom (LFB) and last flowering (LFL). The periods from FFL to FFB or from FFB to LFB differ among years owing to the day-to-day variability of temperature after FFL. To accurately evaluate the sensitivity of spring plant phenology to climate change [15] and thus of cultural ecosystem services generated by cherry flowering [12,13,16,17], long-term continuous records or predicted dates of LFB and LFL as well as of FFL and FFB are required. Second, in a semi-empirical statistical model [1113], it is required to optimize each parameter by using daily or hourly air temperature data. The accuracy of a general semi-empirical statistical model applied to all observation sites in Japan was remarkably poor in the south, where the annual mean air temperature is high [11]. To improve the accuracy of semi-empirical statistical models, optimization of parameters at each observation site is required, but calculation is labor-intensive. Third, although websites of weather service companies, governmental and municipal offices, and tourism associations provide dates of flowering phenology at a daily time step at famous cherry blossom viewing spots in Japan (e.g., “tenki.jp” [18], “Weather News” [19], “Neodani Usuzumi-zakura” [20], “Miharu Taki-zakura” [21]), many of those popular cherry blossom viewing sites are distant from weather stations. To develop semi-empirical statistical models for these sites, correction of air temperature data observed at a nearby weather station (e.g., by applying the temperature lapse rate with altitude) is required, but the corrected data include uncertainty due to microclimate effects.

To resolve these difficulties, we propose a Bayesian statistical state space model that takes into account temperature data recorded at nearby weather stations. A major advantage of this model is that its estimates of the actual state (i.e., true dates of FFL or FFB) are output as a probability distribution by updating the prior distribution to the posterior distribution with new observed data under conditions of ambiguity, as explained in “Material and methods”. We estimated the year-to-year variability of the true dates of FFL, FFB, LFB, and LFL of Neodani Usuzumi-zakura in Gifu, Japan, at a centennial time scale by applying a Bayesian statistical state space model. Many conventional studies have tried to predict the unique flowering dates and to minimize error. However, long-term prediction tends to be unstable. If the method is based on literal diaries, then the prediction becomes more unreliable. To bring this uncertainty under control, we predicted the distribution of flowering dates rather than unique flowering dates. The Bayesian method then enables us to evaluate the flowering dates from the probability distribution. In other words, using the probability distribution, we can estimate quantitatively the uncertainty of prediction. The concept of our proposed model based on the Bayesian statistics is definitely different from that of conventional phenology models based on the traditional statistics [3,10,12,13]. The aims of this study were (1) to develop a cherry flowering phenology model to estimate the dates of FFL, FFB, LFB, and LFL from centennial-scale coarse (i.e., monthly or weekly) temperature data recorded at a nearby weather station and (2) to discuss the utility and uncertainty of this proposed.

Materials and methods

Records of flowering phenology

Our target was the ~1500-year-old Neodani Usuzumi-zakura (Cerasus itosakura), in Motosu City, Gifu Prefecture, Japan (35°37′55.9″N, 136°36′31.7″E; 200 m a.s.l.) [20]. The Motosu City Office website has published the dates of FFL, 20%−30% and 50% flowering, FFB, and LFB since 1989, the dates of first scattering since 2001, and the dates of LFL since 2002. It provides daily flowering phenology information during the flowering season, and a live feed of the tree [20]. We used the records of the dates of FFL, FFB, LFB, and LFL.

To validate the accuracy of model estimation before 1989, we retrieved records of cherry flowering phenology from the literature in the National Diet Library, Gifu City Central Library, and Motosu City Library and a private collection (so-called “historical dark data” [22,23]). We retrieved the records of 17 years of FFL dates and 13 years of FFB dates from the literature [2432], a photograph in 1930 [33], and unpublished data of Motosu City from 1981 to 1988 (Motosu City, unpublished). The JMA literature refers to the tree as C. itosakura except in 1937. Although it is unclear whether these records (except in 1937) indicate Neodani Usuzumi-zakura, we used them. A photograph might be considered to be taken from FFB to LFB dates. We retrieved records of 48 years of FFL dates since 1977 and 64 years of FFB dates since 1955 from the private collection of Hakuryu Fujiwara, an amateur photographer and one of coauthors of this study. His definition of full bloom was that there were no unopened buds on the canopy as viewed through a telescope. Few to no flowers bloomed in several years from 1955 to around 1980 because the tree’s health was compromised, but after root surgery, the tree’s vigor recovered. Part of his data (1968−1990) is published [34]. Observation records, which were converted to the day of year (DOY) for analysis, in literature, photographs, and the private collection of Hakuryu Fujiwara are listed in the (S1 File).

Air temperature data

We used air temperature data since 1924 recorded at the Gifu weather station (35°24′02.2″N, 136°45′45.1″E, 12.7 m a.s.l.), about 29 km southeast of the Tarumi weather station (35°38′20.8″N, 136°36′11.8″E; 190 m a.s.l.), and since November 1978 recorded at the Tarumi weather station, about 1 km northeast of Neodani Usuzumi-zakura. The annual mean temperature (1991–2020) differed between Gifu and Tarumi by 3.4°C [35].

The dates of FFL, FFB, and LFB from 1989 to 2024 and that of LFL from 2002 to 2024 had means (and SDs) of (FFL) DOY 92.0 (6.2), (FFB) 96.9 (5.9), (LFB) 102.1 (5.6), and (LFL) 106.3 (6.0) (Fig 1). On this basis, we used the average daily minimum air temperature from 1 December to 28/29 February to account for the chilling requirement for release from endodormancy, the average daily mean air temperature in March to account for the heat requirement for the growth of flower buds, and the average daily mean air temperature from 1 to 10 April to account for the heat requirement for further growth of flower and leaf buds [1113,36].

thumbnail
Fig 1. Flowering phenology dates of Neodani Usuzumi-zakura from 1989 to 2024 published on the Motosu City Web site.

https://doi.org/10.1371/journal.pone.0317708.g001

Flowering phenology model

Cherry trees form flower buds during summer, which then enter endodormancy. Exposure to winter cold releases the endodormancy. The flower buds then develop as heat increases [1113,17,36]. To explain these processes, we constructed two varying coefficient regression models for the dates of FFL or FFB and of LFB or LFL, respectively. To validate the model estimation based on air temperature data recorded at the Gifu weather station during the period without data at the Tarumi weather station (1924–1978), we estimated the dates of FFL, FFB, LFB, and LFL by using air temperature data in Gifu from 1924 to 2024 and in Tarumi from 1979 to 2024 and compared the results.

The proposed Bayesian statistical state space model has three merits. First, its estimates of the actual state are output as a probability distribution and are explained as the essential variability once noise such as observation errors is removed. This merit reduces the uncertainty of observed data caused by qualitative visual inspection, individual differences among trees (i.e., resolving the issue of the representativeness of sampling data), and effects of microclimate. Second, it is not required to optimize each parameter, as in a semi-empirical statistical model [1113]. Third, cherry flowering phenology can be estimated by using explanatory factors with a coarse temporal resolution (i.e., monthly or weekly air temperatures). These two merits reduce the complicated processes and labor-intensive calculations. Two previous studies have applied the Bayesian inference to phenology models but differed from the current study that made use of a state space model to estimate true dates [17,37].

Estimation of the dates of FFL and FFB

To estimate dates of FFL and FFB, as explanatory variables we set the average daily minimum air temperature from 1 December to 28/29 February and monthly mean air temperature in March. During this period, the true date of FFL or FFB α1t is explained by a general linearized model with ex1t (average daily minimum air temperature from 1 December to 28/29 February) as explanatory variable 1, and ex2t (monthly mean temperature in March) as explanatory variable 2 in year t (Eq 4). We assumed that coefficients β1t of ex1t and γ1t of ex2t and variable μ1t as the intercept vary according to the random walk model (i.e., state space equations: Eqs 13). On the other hand, y1t as the observed value of FFL and FFB dates is explained by the sum of α1t (actual state in year t; i.e., true dates of FFL or FFB) and white noise (i.e., observation equation: Eq 5): (1) (2) (3) (4) (5) where follows a normal distribution with a mean ω1t of 0 and a variance of . Terms σω1, στ1, and συ1 are the SDs (standard deviations) of the process errors, and σφ1 is the SD of the observation error.

Estimation of the dates of LFB and LFL

To estimate dates of LFB and LFL, as an explanatory variable we set the average daily mean air temperature from 1 to 10 April. During this period, the true date of LFB or LFL, α2t, is explained by a general linearized model with ex3t (average daily mean air temperature from 1 to 10 April) as explanatory variable 3 in year t (Eq 8). We assumed that coefficient β2t of ex3t and variable μ2t as the intercept varied according to a random walk model (i.e., state space equations: Eqs 6 and 7). On the other hand, y2t as the observed value of LFB and LFL dates is explained by the sum of α2t (actual state in year t; i.e., true date of LFB or LFL) and white noise (i.e., observation equation: Eq 9): (6) (7) (8) (9) where follows a normal distribution with a mean ω2t of 0 and a variance of . Terms σω2 and στ2 are the SDs of the process errors, and σφ2 is the SD of the observation error.

When we applied the state space model (Eqs 19) to actual data, we updated the prior distribution to the posterior distribution through the use of Bayesian inference. For example, the Bayesian update rule of the observation equation (Eq 5) is explained as: (10) where , and P(α1t) are the posterior distribution, likelihood, and prior distribution, respectively. We set the prior distribution α10, α20, β10, and β20 as uniform (i.e., non-informative). We used Markov chain Monte Carlo methods for generation of the random numbers following the posterior distribution. We implemented it by embedding RStan packages [38] in R software [39,40].

We set the number of chains (number of times to generate a set of random numbers) to 4, the number of repetitions of random number generation to 100 000, 150 000, or 200 000, the burn-in period (initial data discarded) to 20 000, 30 000, or 50 000, and “thin” to 2. The model was run in R v. 4.2.2 and RStan v. 2.21.8 software on the RStudio desktop v. R2022.02.3 build 492 platform [41]. We modified the publicly available code of Baba (2019) [40,42].

Results

Estimation of flowering phenology from air temperature data recorded at the Gifu weather station

The estimated true dates of FFL, FFB, LFB, and LFL from 1924 to 2024 based on air temperature data recorded at the Gifu weather station (α1t and α2t in Eqs 4 and 8) are shown in Fig 2. Despite annual fluctuations, the median of the estimated true date of FFL advanced by 1.877 days/decade (R2 = 0.45, P < 0.001), that of FFB by 1.901 days/decade (R2 = 0.48, P < 0.001), that of LFB by 0.750 days/decade (R2 = 0.29, P < 0.001), and that of LFL by 0.953 days/decade (R2 = 0.30, P < 0.001).

thumbnail
Fig 2.

Relationship between probability distributions of estimated true dates of (a) FFL, (b) FFB, (c) LFB, and (d) LFL from 1924 to 2024 (α1t and α2t in Eqs 4 & 8) by the proposed Bayesian statistical state space model based on temperature data at Gifu weather station and observed values in records from Motosu City, the literature, and a private collection (y1t and y2t in Eqs 5 & 9).

https://doi.org/10.1371/journal.pone.0317708.g002

The median of the estimated variables μ1t and μ2t as the intercept, coefficient β1t of ex1t as explanatory variable 1, coefficient γ1t of ex2t as explanatory variable 2, and coefficient β2t of ex3t as explanatory variable 3 (μ1t, β1t, and γ1t in Eqs 13, and μ2t and β2t in Eqs 6 and 7) are summarized in Table 1. Coefficients β1t and γ1t negatively affected the estimated true dates of FFL and FFB. For example, a 1°C increase of the average daily minimum air temperature from 1 December to 28/29 February advanced FFL by 3.09 days, and a 1°C increase of the monthly mean temperature in March advanced FFL by 3.75 days. Similarly, β2t negatively affected the estimated true dates of LFB and LFL.

thumbnail
Table 1. Medians of estimated variables μ1t and μ2t as the intercept, coefficient β1t of ex1t as explanatory variable 1, coefficient γ1t of ex2t as explanatory variable 2, and coefficient β2t of ex3t as explanatory variable 3 based on air temperature data recorded at the Gifu weather station.

As an example, in the case of the estimated model for the true date of FFL, we show the probability distributions of estimated variable μ1t and coefficients β1t and γ1t in Fig 3.

https://doi.org/10.1371/journal.pone.0317708.t001

thumbnail
Fig 3.

Probability distributions of estimated (a) variable μ1t as the intercept, (b) coefficient β1t of ex1t as explanatory variable 1, and (c) coefficient γ1t of ex2t as explanatory variable 2 (μ1t, β1t, and γ1t in Eqs 13) in the case of the estimated model for the true date of FFL.

https://doi.org/10.1371/journal.pone.0317708.g003

Most of the observed values (y1t and y2t in Eqs 5 and 9) of FFL, FFB, LFB, and LFL lay within the 95% credible interval of the estimated true dates from 1924 to 2024 (α1t and α2t in Eqs 4 and 8). Almost no discrepancies were found between α1t (median of estimated true date) and observed values of FFL and FFB before 1940. In contrast, α1t (the year-to-year variability of estimated true date) was not inclined to match the dates of FFB from 1955 to 1975 recorded by Hakuryu Fujiwara (during the period when the tree’s vigor was reduced).

Estimation of flowering phenology from air temperature data recorded at the Tarumi weather station

The estimated true dates of FFL, FFB, LFB, and LFL from 1979 to 2024 based on air temperature data recorded at the Tarumi weather station (α1t and α2t in Eqs 4 and 8) are shown in Fig 4. Despite annual fluctuations, the median of the estimated true date of FFL advanced by 1.823 days/decade (R2 = 0.18, P < 0.01), that of FFB by 1.921 days/decade (R2 = 0.20, P < 0.01), that of LFB by 0.109 days/decade (R2 = 0.14, P < 0.05), and that of LFL by 0.116 days/decade (R2 = 0.11, P < 0.05).

thumbnail
Fig 4.

Relationship between probability distributions of estimated true dates of (a) FFL, (b) FFB, (c) LFB, and (d) LFL from 1979 to 2024 (α1t and α2t in Eqs 4 & 8) by our Bayesian statistical state space model based on temperature data at Tarumi weather station and observed values in records from Motosu City (y1t and y2t in Eqs 5 & 9).

https://doi.org/10.1371/journal.pone.0317708.g004

The medians of the estimated variables μ1t and μ2t and coefficients β1t, γ1t, and β2t are summarized in Table 2. Coefficients β1t and γ1t negatively affected the estimated true dates of FFL and FFB. Similarly, β2t negatively affected the estimated true dates of LFB and LFL.

thumbnail
Table 2. Medians of estimated variables μ1t and μ2t, and coefficients β1t, γ1t, and β2t based on air temperature data recorded at the Tarumi weather station.

https://doi.org/10.1371/journal.pone.0317708.t002

Most of the observed values (y1t and y2t in Eqs 5 and 9) of FFL, FFB, LFB, and LFL lay within the 95% credible interval of the estimated true dates.

Discussion

Applying a Bayesian statistical state space model allowed us to estimate the year-to-year variability of the true dates of FFL, FFB, LFB, and LFL at a centennial scale, covering the period when there were no records of the flowering phenology of Neodani Usuzumi-zakura (Fig 2). In particular, we could estimate the true dates at almost the same accuracy by models explained by air temperature data recorded at weather stations both 1 km and 29 km from Neodani Usuzumi-zakura with a coarse temporal resolution (Figs 2 and 4). The mean daily air temperatures from 1 January to 31 December from 1991 to 2020 observed at Gifu and Tarumi had a significant positive correlation (r = 1.0, P < 0.001, degree of freedom 363 [43]). Despite the effect of microclimatology on air temperature, this means that there were no extreme discrepancies in patterns of day-to-day variability of air temperature between the weather stations. For this reason, the values of the coefficients β1t, γ1t, and β2t (in Eqs 4 and 8) differed between models (Tables 1 and 2). Interestingly, the coefficient β1t of the average daily minimum air temperature from 1 December to 28/29 February, which accounts for the chilling requirement for release from endodormancy, and the coefficient γ1t of the average daily mean air temperature in March, which accounts for the heat requirement for the growth of flower buds, negatively affected the true dates of FFL and FFB (Tables 1 and 2). If sufficient exposure to winter cold is not obtained, the timing of release from endodormancy and subsequent flowering will be delayed [10,11]. However, despite the current warming climate, the average daily minimum air temperature from 1 December to 28/29 February at the Gifu and Tarumi weather stations may allow sufficient chilling for release from endodormancy, and subsequent warmer-than-average conditions during January or February would accelerate the growth of flower buds.

The probability distributions of the coefficients β1t, γ1t, and β2t (in Eqs 4 and 8) were updated through the Bayesian update of the observation equation (Eqs 5 and 9) and state space equations (Eqs 1, 2, 6 and 7) when we obtained the observed values of FFL and FFB y1t or of LFB and LFL y2t (Fig 3). The values of FFL, FFB, and LFB were first observed in 1989 and that of LFL in 2002 (Fig 1). The median of estimated coefficients β1t, γ1t, and β2t were almost constant before those years, while their credible intervals gradually widened into the past (Fig 3). However, if we obtain observed dates of FFL, FFB, LFB, and LFL y1t or y2t before 1989 or 2002, we can improve the accuracy of the estimated true dates; that is, the width of the 95% credible interval of the estimated true dates will be narrowed. This is another advantage of the proposed Bayesian statistical state space model. As an example, we estimated the true date of FFB from 1924 to 2024 both from flowering phenology records of the tree from the literature and a private collection before 1989 and from observed data published on the website since 1989 as the observed value of FFB y1t (Fig 5). Compared with the values of the true date of FFB (Fig 2B), intercept μ1t (Fig 3A), and coefficients β1t (Fig 3B) and γ1t (Fig 3C) estimated only from observed data published on the website since 1989, the width of the 95% credible intervals was narrowed except when there was no observed value of FFB y1t.

thumbnail
Fig 5.

(a) Probability distributions of the estimated true date of FFB from 1924 to 2024 (α1t in Eq 4) by the proposed Bayesian statistical state space model based on temperature data at Gifu weather station, and both flowering phenology records of the tree from the literature and a private collection before 1989 (1928−1937: Literature and photograph; 1955−1980: Private collection of Hakuryu Fujiwara; and 1981−1988: Unpublished data of Motosu City [Motosu City {Unpublished}]) and observed data published on a website since 1989 as the observed value of FFB date (y1t in Eq 5). Probability distributions of estimated (b) variable μ1t as the intercept, (c) coefficient β1t of ex1t as explanatory variable 1, and (d) coefficient γ1t of ex2t as explanatory variable 2 (μ1t, β1t, and γ1t in Eqs 13) in the case of this estimated model for the true date of FFB.

https://doi.org/10.1371/journal.pone.0317708.g005

The mean air temperature on the date of FFL was lower in a climatic region with a low annual mean air temperature than in one with a high annual mean air temperature [44]. This indicates a low cumulative heat requirement for the growth of flower buds in a climatic region where the chilling requirement for release from endodormancy can be met. In addition, in Hachijojima (33°06′44′′N, 139°47′01′′E), at the southern distribution limit of the full bloom of Yoshino cherry, in years when the chilling requirement for release from endodormancy was not met, the growth of flower buds had a greater heat requirement, and the FFL date tended to be delayed [45]. These facts indicate that the FFL date at a given site in a given year is determined by the balance between the chilling requirement for release from endodormancy and the heat requirement for the growth of flower buds. Therefore, in a region where cherry flowering phenology is strongly affected by global warming, the values of the coefficients β1t and γ1t (in Eq 4) may change on decadal to centennial time scales. Unlike conventional statistical phenology models which give time-invariant constant coefficients, the proposed Bayesian statistical state space model can evaluate temporal changes in the values of coefficients β1t and γ1t (in Eq 4). In Japan, weather stations began modern meteorological observations in the late 19th century [43], and since 1953 have recorded the dates of FFL and FFB of Yoshino cherry by standardized observations [46]. In addition, unstandardized records of the dates of FFL and FFB, which might include uncertainty due to visual inspection, can be traced back to the beginning of the 20th century at several weather stations [57]. By applying the proposed Bayesian statistical state space model to these data at multiple points across a wide area at a centennial scale, we can detect the spatiotemporal characteristic of the coefficients β1t and γ1t (in Eq 4). This analysis will provide useful evidence for an understanding of the sensitivity and resilience of cherry flowering phenology to climate change.

Conclusion

We estimated the probability distributions of the year-to-year variability of the true dates of FFL, FFB, LFB, and LFL in Neodani Usuzumi-zakura at a centennial scale, including periods without records of flowering phenology, by applying a Bayesian statistical state space model explained by air temperature data. The estimated values were validated against the retrieved flowering phenology records of the tree from the literature and a private collection. Means of daily minimum air temperature from 1 December to 28/29 February and that of daily mean air temperature from 1 to 31 March explained the true dates of FFL and FFB, while means of daily mean air temperature from 1 to 10 April explained the true dates of LFB and LFL. Results were similar when based on air temperature data recorded at weather stations both 1 km and 29 km from Neodani Usuzumi-zakura, with differences caused by microclimate. These facts indicated that the proposed Bayesian statistical state space model was useful to estimate the true dates of FFL, FFB, LFB, and LFL by using explanatory factors as air temperature with a coarse temporal resolution without the need for labor-intensive calculations for optimization of each parameter in a conventional semi-empirical statistical model. The application of the model to multiple points can successfully estimate the uncertainty of long-term predictions and will deepen our understanding of the spatio-temporal variability of the dates of FFL, FFB, LFB, and LFL at a centennial scale.

Supporting information

S1 File. Observation records, which were converted to the day of year (DOY) for analysis, in literature, photographs, and the private collection of Hakuryu Fujiwara.

https://doi.org/10.1371/journal.pone.0317708.s001

(CSV)

Acknowledgments

We are grateful to the editors and reviewers for their constructive comments.

References

  1. 1. Sato M. Long-term variations of budding and flowering in trees of the botanical garden of University of Tsukuba, Japan. Tsukuba J Agric For. 2014; 2: 41–55 (in Japanese with English summary) [cited 2024 August 10]. Available from https://farm.t-pirc.tsukuba.ac.jp/tjaf/tjaf_no2.html
  2. 2. Iwasaki F. Cultural history of the Japanese flowering cherries. Hokuryukan; 2018 (in Japanese).
  3. 3. Aono Y, Kazui K. Phenological data series of cherry tree flowering in Kyoto, Japan, and its application to reconstruction of springtime temperatures since the 9th century. Int J Climatol. 2008; 28: 905–914. https://doi.org/10.1002/joc.1594
  4. 4. Shin N, Sasai Y, Kotani A, Saitoh TM. Mining plant phenology records from Kanazawa, Japan in the 1807–1838 Kakuson Diary. Int J Biometeorol. 2024; 68: 125–131. https://doi.org/10.1007/s00484-023-02576-3 pmid:37957434
  5. 5. Ishinomaki Weather Station. Weather report in Miyagi Prefecture. 1906−1916a; 5: 31−36 [cited 2024 August 10]. Available from https://dl.ndl.go.jp/pid/2390659/1/1 (in Japanese, public access)
  6. 6. Ishinomaki Weather Station. Weather report in Miyagi Prefecture. 1906−1916b; 9: 22−28. Available from https://dl.ndl.go.jp/pid/2390665/1/1 (ditto)
  7. 7. Central Meteorological Observatory. Memoirs of industrial meteorology. 1934−1942; 4(1), 235p. (ditto)
  8. 8. JMA. Guidelines for the observation of phenology, 3rd edn. Japan Meteorological Agency, Tokyo; 1985 (in Japanese)
  9. 9. JMA. Climate change monitoring report 2022. Japan Meteorological Agency. 114p; 2023 [cited 2024 August 10]. Available from https://www.data.jma.go.jp/cpdinfo/monitor/2022/pdf/ccmr2022_all.pdf.
  10. 10. Nagai S, Morimoto H, Saitoh TM. A simpler way to predict flowering and full bloom dates of cherry blossoms by self-organizing maps. Ecol Informat. 2020a; 56: 101040. https://doi.org/10.1016/j.ecoinf.2019.101040
  11. 11. Asakura T, Sugiura H, Sakamoto D, Sugiura T, Gemma H. A universal model for predicting the full bloom date of Japanese flowering cherry. J Agric Meteorol. 2010; 66(4): 269–277 (in Japanese with English summary)
  12. 12. Chung U, Mack L, Yun JI, Kim S-H. Predicting the timing of cherry blossoms in Washington, DC and mid-Atlantic states in response to climate change. PLoS One. 2011; 6(11): e27439. pmid:22087317
  13. 13. Nagai S, Saitoh TM, Yoshitake S. Cultural ecosystem services provided by flowering of cherry trees under climate change: a case study of the relationship between the periods of flowering and festivals. Int J Biometeorol. 2019; 63: 1051–1058 pmid:31030319
  14. 14. Masago Y, Lian M. Estimating the first flowering and full blossom dates of Yoshino cherry (Cerasus × yedoensis ‘Somei-yoshino’) in Japan using machine learning algorithms. Ecol Informat. 2022; 71: 101835. https://doi.org/10.1016/j.ecoinf.2022.101835
  15. 15. Nagai S, Saitoh TM, Morimoto H. Does global warming decrease the correlation between cherry blossom flowering date and latitude in Japan?. Int J Biometeorol. 2020b; 64: 2205–2210. pmid:32892239
  16. 16. Sakurai R, Jacobson SK, Kobori H, Primack R, Oka K, Komatsu N, et al. Culture and climate change: Japanese cherry blossom festivals and stakeholders’ knowledge and attitudes about global climate change. Biol Conserv. 2011; 144: 654–658
  17. 17. Allen JM, Terres MA, Katsuki T, Iwamoto K, Kobori H, Higuchi H, et al. Modeling daily flowering probabilities: expected impact of climate change on Japanese cherry phenology. Global Change Biol. 2014; 20: 1251–1263. pmid:23966290
  18. 18. tenki.jp. Information of cherry flowering and full bloom in 2024 (in Japanese). 2024; [cited 2024 August 10]. Available from: https://tenki.jp/sakura/
  19. 19. Weather News. Sakura Ch. Web (in Japanese) 2024; [cited 2024 August 10]. Available from: https://weathernews.jp/sakura/
  20. 20. City Motosu. Information of Neodani Usuzumizakura Web (in Japanese). 2024; [cited 2024 August 10]. Available from: https://www.city.motosu.lg.jp/category/2-18-2-0-0-0-0-0-0-0.html
  21. 21. Miharu Town Development Corporation. Find! Miharu Web (in Japanese). 2024; [cited 2024 August 10]. Available from: https://miharukoma.com/
  22. 22. Easterday K, Paulson T, DasMohapatra P, Alagona P, Feirer S, Kelly M. From the field to the cloud: A review of three approaches to sharing historical data from field stations using principles from data science. Front Environ Sci. 2018; 6: 88.
  23. 23. Kelly JA, Farrell SL, Hendrickson LG, Luby J, Mastel KL. A critical literature review of historic scientific analog data: Uses, successes, and challenges. Data Sci J. 2022; 21: 14, 1–11.
  24. 24. Central Meteorological Observatory. Weather Miscellaneous. 1931a; 4(3). Tokyo (in Japanese, register to view)
  25. 25. Central Meteorological Observatory. Weather Miscellaneous. 1931b; 6(1). Tokyo (ditto)
  26. 26. JMA. Geophysical review. 1930; 368. Tokyo (in Japanese, register to view)
  27. 27. JMA. Geophysical review. 1931; 380. Tokyo (ditto)
  28. 28. JMA. Geophysical review. 1933; 404. Tokyo (ditto)
  29. 29. JMA. Geophysical review. 1934; 416. Tokyo (ditto)
  30. 30. JMA. Geophysical review. 1935; 428. Tokyo (ditto)
  31. 31. JMA. Geophysical review. 1936; 440. Tokyo (ditto)
  32. 32. JMA. Geophysical review. 1937; 452. Tokyo (ditto)
  33. 33. Miyawaki K. Emperor Keitai and Usuzumi-zakura. Solving the mysteries of ancient dynasty. Eds. Gifu Prefecture Cultural Properties Protection Association. Motosu Village (Motosu County); 1983 (in Japan).
  34. 34. Gifu Prefectural Forestry Center. Vitality and “Sakura Guardian” in Usuzumi-zakura. Mino, Japan; 1996 (in Japanese)
  35. 35. JMA. Search site for archived past weather data (in Japanese). 2024; [cited 2024 August 10]. Available from: https://www.data.jma.go.jp/stats/etrn/index.php
  36. 36. Luedeling E, Guo L, Dai J, Leslie C, Blanke MM. Differential responses of trees to temperature variation during the chilling and forcing phases. Agric For Meteorol. 2013; 181: 33–42. http://dx.doi.org/10.1016/j.agrformet.2013.06.018
  37. 37. Ibáñez I, Primack RB, Miller-Rushing AJ, Ellwood E, Higuchi H, Lee SD, et al. Forecasting phenology under global warming. Phil Trans R Soc B. 2010; 365: 3247−3260. pmid:20819816
  38. 38. RStan. RStan Web. 2024; [cited 2024 August 10]. Available from: https://mc-stan.org/rstan/
  39. 39. The R Foundation. The R project for statistical computing Web. 2024; [cited 2024 August 10]. Available from: https://www.r-project.org/
  40. 40. Baba S. Introduction to data analysis using Bayesian statistical modeling with R and Stan. Tokyo, Japan: Kodansha Scientific Co., Ltd.; 2019 (in Japanese)
  41. 41. Posit Software. RStudio desktop Web. 2024; [cited 2024 August 10]. Available from: https://posit.co/download/rstudio-desktop/
  42. 42. Logics-of-blue. Download site for sample data and code of “Introduction to data analysis using Bayesian statistical modeling with R and Stan” Web. 2019; [cited 2024 August 10]. Available from: https://github.com/logics-of-blue/book-r-stan-bayesian-model-intro
  43. 43. JMA. Download site for archived weather data (in Japanese). 2024; [cited 2024 August 10]. Available from: https://www.data.jma.go.jp/risk/obsdl/index.php
  44. 44. Nagata H, and Yurugi Y. Phenological studies in woody plants (II): Flowering in cherry trees. The bulletin of the Faculty of Agriculture, Mie University 1982; 64: 11−20. http://hdl.handle.net/10076/3125 (in Japanese with English summary)
  45. 45. Shin N, Saitoh TM, Takasu H, Morimoto H. Influence of climate change on flowering phenology of Yoshino cherry at its southern distribution limit. Int J Biometeorol 2024; pmid:39392471
  46. 46. JMA. Information of phenology Web. 2024; [cited 2024 August 10]. Available from: https://www.data.jma.go.jp/sakura/data/index.html