Plant phenological records in northern Finland since the 18th century as retrieved from databases, archives and diaries for biometeorological research

Plant phenological data from northern Finland, compiled from several sources, were examined as potential biometeorological indicators of climate change since the 18th century. A common feature of individual series was their sporadic nature. In addition to waning enthusiasm, wartime hardships and crop failures had caused gaps in recording observations during the 18th and 19th centuries. The present study’s challenge was to combine separate records, as retrieved from several historical archives and personal diaries, into a single continuous series. To avoid possible biases due to the variability of data availability each year, each phenomenon-specific mean series was transformed into normalized site-specific index series. These series were compared to each other and to a regional instrumental temperature series (years 1802–2011). The inter-phenomena correlations were high. Moreover, a strong biometeorological response of the phenological series, most especially to monthly mean temperature in May, and seasonally to the April through June temperatures, was identified. This response focused on slightly later spring months compared to the responses in an earlier study conducted for southern Finland. The findings encouraged us to compute a total phenological index series as an average of all available phenomenon-specific index series for northern Finland. The earliest phenological springs were found as a cluster in the recent end of the record, whereas the anomalously-late phenological spring could be found through the centuries. This finding could indicate that potential future warming could result in an earlier onset of phenological springs (i.e. as experienced by the plants), with a remaining possibility of late phenological springs. To conclude, it was shown that the indices are reliable biometeorological indicators of the April through June temperature variations and thus of the climate variability in the region.     

西安木本植物物候与气候要素的关系

根据1963–2007年中国物候观测网西安观测站的物候和气温、降水资料,分析了西安站34种木本植物春季展叶始期、展叶盛期、始花期和盛花期等4个关键物候期的变化趋势、对气候变化的阶段响应特点及其与气温、降水变化的关系。结果表明,1963年以来,西安地区气温呈显著上升趋势,特别是1994年前后,气温发生明显突变,上升趋势更加明显;西安春季物候变化主要呈现提前趋势。在45年中,观测到的34种植物的展叶始期平均提前1天,展叶盛期平均提前1.4天,始花期平均提前9天,盛花期平均提前12天;以突变点为界,34个物种1995–2007年的4种物候期比1963–1994年平均提前了4.34±0.77天;春季物候期的早晚主要受春季气温的影响,特别是春季物候期发生当月和上一月的平均气温对物候期的影响最为显著。叶物候和物候发生期前一月的降水量有较为明显的相关关系,花物候期和降水的关系不明显。     

Remote sensing of larch phenological cycle and analysis of relationships with climate in the Alpine region

This research aims at developing a remote sensing technique for monitoring the interannual variability of the European larch phenological cycle in the Alpine region of Aosta Valley (Northern Italy) and to evaluate its relationships with climatic factors. Phenological field observations were conducted in eight test sites from 2005 to 2007 to determine the dates of completion of different phenological phases. MODerate Resolution Imaging Spectrometer (MODIS) 250 m 16‐days normalized difference vegetation index (NDVI) time series were fitted with double logistic curves and the dates corresponding to different features of the curves were determined. Comparison with field data showed that the features of the fitted NDVI curve that allowed the best estimate of the start and end of the growing season were the zeroes of its third derivative (MAE of 6 and 4 days, respectively). The start and end of season were also estimated with the spring warming (SW) and growing season index (GSI) phenological models. MODIS start and end of season dates generally agreed with those obtained by the SW and GSI climate‐driven phenological models. However, phenological models provided erroneous results when applied in years with anomalous meteorological conditions. The relationships between interannual variability of the larch phenological cycle and climate were investigated by comparing the mean start and end of season yearly anomalies with air temperature anomalies. A strong linear relationship (R²=0.91) was found between mean spring temperatures and mean start of season dates, with an increase of 1 °C in mean spring temperature leading to a 7‐day anticipation of mean larch bud‐burst date. Leaf coloring dates were found to be best related with mean September temperature (R²=0.77), but with higher spring temperatures appearing to lead to earlier leaf coloring.     

Phenological responses of plants to climate change in an urban environment

Global climate change is likely to alter the phenological patterns of plants due to the controlling effects of climate on plant ontogeny, especially in an urbanized environment. We studied relationships between various phenophases (i.e., seasonal biological events) and interannual variations of air temperature in three woody plant species (Prunus davidiana, Hibiscus syriacus, and Cercis chinensis) in the Beijing Metropolis, China, based on phenological data for the period 1962–2004 and meteorological data for the period 1951–2004. Analysis of phenology and climate data indicated significant changes in spring and autumn phenophases and temperatures. Changes in phenophases were observed for all the three species, consistent with patterns of rising air temperatures in the Beijing Metropolis. The changing phenology in the three plant species was reflected mainly as advances of the spring phenophases and delays in the autumn phenophases, but with strong variations among species and phenophases in response to different temperature indices. Most phenophases (both spring and autumn phenophases) had significant relationships with temperatures of the preceding months. There existed large inter- and intra-specific variations, however, in the responses of phenology to climate change. It is clear that the urban heat island effect from 1978 onwards is a dominant cause of the observed phenological changes. Differences in phenological responses to climate change may cause uncertain ecological consequences, with implications for ecosystem stability and function in urban environments.     

Does flower phenology mirror the slowdown of global warming?

Although recent global warming trends in air temperature are not as pronounced as those observed only one decade ago, global mean temperature is still at a very high level. Does plant phenology – which is believed to be a suitable indicator of climate change – respond in a similar way, that is, does it still mirror recent temperature variations? We explored in detail long-term flowering onset dates of snowdrop, cherry, and lime tree and relevant spring temperatures at three sites in Germany (1901–2012) using the Bayesian multiple change-point approach. We investigated whether mean spring temperature changes were amplified or slowed down in the past decade and how plant phenology responded to the most recent temperature changes. Incorporating records with different end points (i.e., 2002 and 2012), we compared differences in trends and inferred possible differences caused by extrapolating phenological and meteorological data. The new multiple-change point approach is characterized by an enhanced structure and greater flexibility compared to the one change point model. However, the highest model probabilities for phenological (meteorological) records were still obtained for the one change point (linear) model. Marked warming trends in the recent decade were only revealed for mean temperatures of March to May, here better described with one or two change point models. In the majority of cases analyzed, changes in temperatures were well mirrored by phenological changes. However, temperatures in March to May were linked to less strongly advancing onset dates for lime tree flowering during the period 1901-2012, pointing to the likely influence of photoperiodic constraints or unfulfilled chilling requirements. Due to the slowdown of temperature increase, analyses conducted on records ending in 2002 demonstrated distinct differences when compared with records ending in 2012. Extrapolation of trends could therefore (along with the choice of the statistical method) lead to distinctly different results and most recent data should be integrated in order not to over- or underestimate future phenological changes.     

Interannual phenological variability in two North-East Atlantic populations of Calanus finmarchicus

Phenological variations of the marine copepod Calanus finmarchicus were studied in Svalbard and northern Iceland, where samples were collected in summer and spring, respectively, over two decades. Four phenological indices, developed for copepodite stage-structured data, were used: the proportion of CV to total abundance (CVT), the population development index (PDI), the average weighted stage (AWS), and the average age in days (AAD). The variation of these indices was compared within and between locations to evaluate their suitability for the analysis of phenological effects. For both populations, phenology was related to local temperature and spring bloom dynamics, influenced by Atlantic water inflow. Large-scale climate was related to phenological variation only in the Svalbard population. C. finmarchicus phenology advanced under warmer conditions in both locations. We conclude that vertical phenological indices, i.e. based on interannual changes in copepodite stage structure, are useful to investigate zooplankton phenology, especially when data series covering the whole life cycle are unavailable. We suggest that AWS and AAD can be applied irrespective of sampling time, while PDI and CVT should be applied for early and late sampling seasons, respectively. When multiple phenological indices are needed, AAD in combination with either CVT or PDI should be preferred.     

中国东部温带植被生长季节的空间外推估计

利用地面植物物候和遥感归一化差值植被指数（NDVI）数据,以及一种物候-遥感外推方法,实现植被生长季节从少数站点到较多站点的空间外推。结果表明：（1）在1982～1993年期间,中国东部温带地区植被生长季节多年平均起讫日期的空间格局与春季和秋季平均气温的空间格局相关显著;（2）在不同纬度带和整个研究区域,植被生长季节结束日期呈显著推迟的趋势,而开始日期则呈不显著提前的趋势,这与欧洲和北美地区植被生长季节开始日期显著提前而结束日期不显著推迟的变化趋势完全不同;（3）北部纬度带的植被生长季节平均每年延长1．4～3．6d,全区的植被生长季节平均每年延长1．4d,与同期北半球和欧亚大陆植被生长季节延长的趋势数值相近;（4）植被生长季节结束日期的显著推迟与晚春至夏季的区域性降温有关,而植被生长季节开始日期的不显著提前则与晚冬至春季气温趋势的不稳定变化有关;（5）在年际变化方面,植被生长季节开始和结束日期分别与2～4月份平均气温和5～6月份平均气温呈负相关关系。     

内蒙古中西部优势植物春季返青对降水的非线性响应

长期以来,研究植被物候变化与气候因子的关系多基于线性模型,事实上植被物候对气候变化的响应可能是非线性的。以1984-2017年内蒙古中西部温性典型草原和温性草原化荒漠长时间序列植被物候观测资料为基础,分析了近40年来气候变化背景下不同草地类型优势植物返青期变化特征及其对春季降水的非线性响应。结果表明：（1）温性典型草原冷蒿返青期主要受水分控制,与春季降水量表现为开口向下的二次函数关系。气候暖干化导致的水分亏缺是冷蒿返青期呈极显著延迟趋势（1.32 d/a）的主要原因;春季降水量超过60 mm时,冷蒿返青期表现出由延迟转变为提前的趋势。（2）温性草原化荒漠猫头刺返青期主要受热量控制。受春季显著升温影响,猫头刺返青期呈极显著提前趋势（0.63 d/a）。春季降水增多利于猫头刺提早返青,二者表现为开口向上的二次函数关系;春季降水量超过40 mm时,猫头刺返青期对降水的响应程度逐渐降低,这可能与荒漠植物本身的生理特性有关。     

Phenological changes and reduced seasonal synchrony in western Poland

Botanical gardens offer continuity for phenological recording in observers, protocols and plant specimens that may not be achievable from other sources. Here, we examine phenological change and synchrony from one such garden in western Poland. We analysed 66 botanical phenophases and 18 interphase intervals recorded between 1977 and 2007 from the Poznań Botanical Garden. These were examined for trends through time and responsiveness to temperature. Furthermore, we derived measures of synchrony for start of spring and end of autumn events to assess if these had changed over time. All 39 events with a mean date before mid-July demonstrated a significant negative relationship with temperature. Where autumn events were significantly related to temperature, they indicated a positive relationship. Typically, spring events showed an advance over time and autumn events a delay. Interphase intervals tended to lengthen over the study period. The measures of synchrony changed significantly over time suggesting less synchrony among spring events and also among autumn events. In combination, these results suggest increases in growing season length. However, responses to a changing climate were species-specific. Thus, the transitions from winter into spring and from autumn into winter are becoming less clearly defined.     

Phenological models for blooming of apple in a mountainous region

Six phenological series were available for ‘Golden Delicious’ apple blooming at six sites in Trentino, an alpine fruit-growing region. Several models were tested to predict flowering dates, all involving a “chilling and forcing” approach. In many cases, application of the models to different climatic conditions results in low accuracy of prediction of flowering date. The aim of this work is to develop a model with more general validity, starting from the six available series, and to test it against five other phenological series outside the original area of model development. A modified version of the “Utah” model was the approach that performed best. In fact, an algorithm using “chill units” for rest completion and a thermal sum for growing-degree-hours (GDH), whose efficiency changes over time depending on the fraction of forcing attained, yielded a very good prediction of flowering. Results were good even if hourly temperatures were reconstructed from daily minimum and maximum values. Errors resulting from prediction of flowering data were relatively small, and root mean square errors were in the range of 1–6 days, being <2 days for the longest phenological series. In the most general form of the model, the summation of GDH required for flowering is not a fixed value, but a function of topoclimatic variables for a particular site: slope, aspect and spring mean temperature. This approach allows extension of application of the model to sites with different climatic features outside the test area.     

Phytophenological trends in Switzerland

Nation-wide phenological observations have been made in Switzerland since 1951. In addition to these observation programmes, there are two very long phenological series in Switzerland: leaf bud burst of horse-chestnut trees has been observed in Geneva since 1808 and full flowering of cherry trees in Liestal since 1894. In addition to the presentation of these two long phenological series, trends for 896 phenological time series have been calculated with national data from 1951 to 1998. The earlier bud burst of horse-chestnut trees in Geneva can be attributed mainly to the city effect (warmth island). This phenomenon was not observed with the cherry tree flowering in Liestal. A clear trend towards earlier appearance dates in spring and a weak tendency towards later appearance dates in autumn could be shown with data from the national observation network. It must be noted that different phenophases and plant species react differently to various environmental influences. Received: 25 October 2000 / Revised: 9 May 2001 / Accepted: 4 June 2001     

基于数字相机图像的西藏当雄高寒草地群落物候模拟

物候现象是环境条件季节和年际变化最直观、敏感的综合指示器, 其发生时间不仅反映了陆地生态系统短期的动态特征, 其微小的变化还会对陆地生态系统产生重要的反馈作用。高寒草地是青藏高原分布广泛、极具代表性的植被类型, 准确地获取高寒草地群落的物候特征, 对于理解和预测气候变化对青藏高原生态系统的影响具有重要意义。该文以西藏当雄高寒草地为研究对象, 探讨了近地面数字相机图像在高寒草地群落季相监测中的作用, 结果如下: 1)通过比较不同绿度指数的差别, 确定了准确表征高寒草地植被群落季相变化的绿度指数——绝对绿度指数(2G_RB); 2)结合土壤含水量数据, 通过线性回归分析得知高寒草地植被群落生长过程与表层(≤10 cm)土壤含水量的变化较为一致(R ² > 0.70); 3)通过对比分析, 发现降水在高寒草地群落季相“变绿”过程中具有“触发”作用。研究表明, 数字相机技术可作为物候监测手段, 实现高寒草地植被群落季相的实时、连续获取, 为更好地揭示气候变化影响下景观尺度季相演变特征, 诊断地方、区域和全球尺度上生态系统对气候变化的快速响应提供了有效的手段。     

Advances in first bloom dates and increased occurrences of yearly second blooms in eastern China since the 1960s: further phenological evidence of climate warming

Confirming the results of previous regional studies on changes in first bloom dates (FBD) in China, this study provides evidence that complements conclusions drawn from studies of phenological changes in other dynamic climate systems in the Northern Hemisphere. Furthermore, increased occurrences of yearly second blooms (YSB) further reinforce results derived from other studies indicating a recent trend of generalized climate warming across China. Additionally, ascertaining changes in FBD and YSB against a recent background not only provides a hitherto poorly formulated autumnal equivalent to the well-studied shifts in FBD, but also formulates both spring and autumn flowering changes in recent years. Data in this study are derived from observations made from 1963 to 2006 by the Chinese Phenological Observation Network (CPON)—a nationwide system of monitoring stations that has made observations of over 173 species from across China since 1963. At each site, the mean value of each species’ annual deviation and spring mean surface temperatures were calculated. For each species, years and locations were also recorded for species in which second blooms (YSB) occurred. Of the 46 FBD samples, 31 showed advances from the mean, blooming earlier over the course of the study period. Notably, although only 8 of the 46 FBD samples showed significance levels of 0.1 or better, the average FBD did advance by 5.3 days. After the 1980s, the frequency of YSB occurrence remained steady, declining a little from the peak in the 1980s, but still exhibiting occurrences far more than were observed earlier. The data from this study clearly indicate that both the phenological advance of FBD in spring and the increased occurrence of YSB are consistent with climate warming.     

A 250-year index of first flowering dates and its response to temperature changes

Widespread concerns about global biodiversity loss have led to a growing demand for indices of biodiversity status. Today, climate change is among the most serious threats to global biodiversity. Although many studies have revealed phenological responses to climate change, no long-term community-level indices have been developed. We derived a 250-year index of first flowering dates for 405 plant species in the UK for assessing the impact of climate change on plant communities. The estimated community-level index in the most recent 25 years was 2.2–12.7 days earlier than any other consecutive 25-year period since 1760. The index was closely correlated with February–April mean Central England Temperature, with flowering 5.0 days earlier for every 1°C increase in temperature. The index was relatively sensitive to the number of species, not records per species, included in the model. Our results demonstrate how multi-species, multiple-site phenological events can be integrated to obtain indices showing trends for each species and across species. This index should play an important role in monitoring the impact of climate change on biodiversity. Furthermore, this approach can be extended to incorporate data from other taxa and countries for evaluating cross-taxa and cross-country phenological responses to climate change.     

European phenological response to climate change matches the warming pattern

Global climate change impacts can already be tracked in many physical and biological systems; in particular, terrestrial ecosystems provide a consistent picture of observed changes. One of the preferred indicators is phenology, the science of natural recurring events, as their recorded dates provide a high-temporal resolution of ongoing changes. Thus, numerous analyses have demonstrated an earlier onset of spring events for mid and higher latitudes and a lengthening of the growing season. However, published single-site or single-species studies are particularly open to suspicion of being biased towards predominantly reporting climate change-induced impacts. No comprehensive study or meta-analysis has so far examined the possible lack of evidence for changes or shifts at sites where no temperature change is observed. We used an enormous systematic phenological network data set of more than 125 000 observational series of 542 plant and 19 animal species in 21 European countries (1971–2000). Our results showed that 78% of all leafing, flowering and fruiting records advanced (30% significantly) and only 3% were significantly delayed, whereas the signal of leaf colouring/fall is ambiguous. We conclude that previously published results of phenological changes were not biased by reporting or publication predisposition: the average advance of spring/summer was 2.5 days decade⁻¹ in Europe. Our analysis of 254 mean national time series undoubtedly demonstrates that species' phenology is responsive to temperature of the preceding months (mean advance of spring/summer by 2.5 days°C⁻¹, delay of leaf colouring and fall by 1.0 day°C⁻¹). The pattern of observed change in spring efficiently matches measured national warming across 19 European countries (correlation coefficient r =−0.69, P <0.001).     

Natural history museum collections provide information on phenological change in British butterflies since the late-nineteenth century

Museum collections have the potential to provide valuable information on the phenological response of organisms to climate change. This is particularly useful for those species for which few data otherwise exist, but also to extend time series to the period before other observational data are available. To test this potential, we analysed data from 2,630 specimens of four species of British butterflies (Anthocharis cardamines, Hamearis lucina, Polyommatus bellargus and Pyrgus malvae), collected from 1876 to 1999 and stored in the Natural History Museum, London, UK (NHM). In A. cardamines, first-generation P. bellargus and P. malvae, we found that there was a strong significant negative relationship between spring temperature and 10th percentile collection dates, which approximates mean first appearance date, and median collection date, which approximates mean flight date. In all four species, there was a significant negative relationship between the 10th percentile collection date and the length of the collection period, which approximates flight period. In second-generation P. bellargus, these phenological measurements were correlated with summer temperature. We found that the rates of phenological response to temperature, based on NHM data, were similar to, or somewhat greater than, those reported for other organisms based on observational data covering the last 40 years. The lower rate of phenological response, and the significant influence of February rather than March or April temperatures, in recent decades compared with data from earlier in the twentieth century may indicate that early emerging British butterfly species are currently approaching the limits of phenological advancement in response to recent climate warming.     

Greater phenological sensitivity to temperature on higher Scottish mountains: new insights from remote sensing

Mountain plants are considered among the species most vulnerable to climate change, especially at high latitudes where there is little potential for poleward or uphill dispersal. Satellite monitoring can reveal spatiotemporal variation in vegetation activity, offering a largely unexploited potential for studying responses of montane ecosystems to temperature and predicting phenological shifts driven by climate change. Here, a novel remote‐sensing phenology approach is developed that advances existing techniques by considering variation in vegetation activity across the whole year, rather than just focusing on event dates (e.g. start and end of season). Time series of two vegetation indices (VI), normalized difference VI (NDVI) and enhanced VI (EVI) were obtained from the moderate resolution imaging spectroradiometer MODIS satellite for 2786 Scottish mountain summits (600–1344 m elevation) in the years 2000–2011. NDVI and EVI time series were temporally interpolated to derive values on the first day of each month, for comparison with gridded monthly temperatures from the preceding period. These were regressed against temperature in the previous months, elevation and their interaction, showing significant variation in temperature sensitivity between months. Warm years were associated with high NDVI and EVI in spring and summer, whereas there was little effect of temperature in autumn and a negative effect in winter. Elevation was shown to mediate phenological change via a magnification of temperature responses on the highest mountains. Together, these predict that climate change will drive substantial changes in mountain summit phenology, especially by advancing spring growth at high elevations. The phenological plasticity underlying these temperature responses may allow long‐lived alpine plants to acclimate to warmer temperatures. Conversely, longer growing seasons may facilitate colonization and competitive exclusion by species currently restricted to lower elevations. In either case, these results show previously unreported seasonal and elevational variation in the temperature sensitivity of mountain vegetation activity.     

Detecting nonlinear response of spring phenology to climate change by Bayesian analysis

The impact of climate change on the advancement of plant phenological events has been heavily studied in the last decade. Although the majority of spring plant phenological events have been trending earlier, this is not universally true. Recent work has suggested that species that are not advancing in their spring phenological behavior are responding more to lack of winter chill than increased spring heat. One way to test this hypothesis is by evaluating the behavior of a species known to have a moderate to high chilling requirement and examining how it is responding to increased warming. This study used a 60‐year data set for timing of leaf‐out and male flowering of walnut (Juglans regia) cultivar ‘Payne’ to examine this issue. The spring phenological behavior of ‘Payne’ walnut differed depending on bud type. The vegetative buds, which have a higher chilling requirement, trended toward earlier leaf‐out until about 1994, when they shifted to later leaf‐out. The date of male bud pollen shedding advanced over the course of the whole record. Our findings suggest that many species which have exhibited earlier bud break are responding to warmer spring temperatures, but may shift into responding more to winter temperatures (lack of adequate chilling) as warming continues.     

East versus West: contrasts in phenological patterns?

Aim To examine whether change in the timing of a large number of phenological events and their response to temperature differs between trophic levels during the period 1988–2008. Location In the vicinity of Kazan, Tatarstan Republic, Russia (55°45′ N, 49°08′ E). Methods Observations of the dates of first events of 22 plant phases, 8 insect phases, 3 herpetofauna phases and 26 migrant bird phases were examined using regression to assess changes over time and response to temperature. Differences between trophic levels were assessed using ANOVA. Results In comparison to studies from western Europe, relatively few phenological series (15) revealed a significant advance over time, but a much larger number (37), including all the herpetofauna and nearly all the plants, showed a response to temperature. Trends in birds were, on average, twice as great as those for plants, but plants had a significantly greater temperature response. Over the study period local temperatures had not risen significantly but some phenological change was still evident. Main conclusions Phenological change has been less marked in the eastern edge of Europe than in western and central Europe. This is compatible with a lack of significant local warming during the study period. A large number of species show strong responses to temperature so will be expected to advance if/when local temperatures do increase. In contrast to results from elsewhere in Europe, early events were not the most temperature responsive, suggesting local adaptation preventing precocious behaviour and the consequent dangers of sub‐zero temperatures.     

Phenological response to climate change in China: a meta‐analysis

The change in the phenology of plants or animals reflects the response of living systems to climate change. Numerous studies have reported a consistent earlier spring phenophases in many parts of middle and high latitudes reflecting increasing temperatures with the exception of China. A systematic analysis of Chinese phenological response could complement the assessment of climate change impact for the whole Northern Hemisphere. Here, we analyze 1263 phenological time series (1960–2011, with 20+ years data) of 112 species extracted from 48 studies across 145 sites in China. Taxonomic groups include trees, shrubs, herbs, birds, amphibians and insects. Results demonstrate that 90.8% of the spring/summer phenophases time series show earlier trends and 69.0% of the autumn phenophases records show later trends. For spring/summer phenophases, the mean advance across all the taxonomic groups was 2.75 days decade^?1 ranging between 2.11 and 6.11 days decade^?1 for insects and amphibians, respectively. Herbs and amphibians show significantly stronger advancement than trees, shrubs and insect. The response of phenophases of different taxonomic groups in autumn is more complex: trees, shrubs, herbs and insects show a delay between 1.93 and 4.84 days decade^?1, while other groups reveal an advancement ranging from 1.10 to 2.11 days decade^?1. For woody plants (including trees and shrubs), the stronger shifts toward earlier spring/summer were detected from the data series starting from more recent decades (1980s–2000s). The geographic factors (latitude, longitude and altitude) could only explain 9% and 3% of the overall variance in spring/summer and autumn phenological trends, respectively. The rate of change in spring/summer phenophase of woody plants (1960s–2000s) generally matches measured local warming across 49 sites in China (R = ?0.33, P < 0.05).