European phenological response to climate change matches the warming pattern

TL;DR: In this article, the authors 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) and concluded that previously published results of phenological changes were not biased by reporting or publication predisposition.

Abstract: 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

Summary

Introduction

• Many studies examining the impacts of global warming on terrestrial ecosystems reveal a consistent pattern of change, the response to warming by phenological change across the northern hemisphere seems to be especially well documented (IPCC, 2001; Sparks & Menzel, 2002; Walther et al., 2002; Parmesan & Yohe, 2003; Root et al., 2003).
• Here, it is extremely important to keep track of the entirety of changes in order to properly address the questions of evidence of no change, change opposite to the direction expected, change not matching climate/ temperature change, and to discuss the questions of resilience and thresholds.
• The average spring advance revealed by the latter was higher (5.1 compared with 2.3 days decade 1).
• Thus, the goal of the present study was an exhaustive Europe-wide analysis of all observed changes in phenology (plants/ animals) in the period 1971–2000.

Material and methods

• An extremely abundant data set of trends in European phenological phases was systematically collected within the COST action 725 ‘Establishing a European phenological data platform for climatological applications’ (http://www.cost725.org) comprising all phenological records digitally available at present.
• If applicable, agricultural and natural phases were treated separately.
• Annual mean onset dates for nine countries (Austria, Belarus/northern Russia, Estonia, Czech Republic, Germany, Poland, Slovenia, Switzerland, Ukraine/ southern Russia), comprising 254 records (phenophases countries) of 10 1 years, however, mostly covering the total period 1951–1999, were available for the quantitative assessment of temperature responses.
• Each of the COST725 team member states contributed a countrywide trend analysis (1971–2000) including mean onset dates and their standard deviation, linear regressions of the onset dates against year including slope of the regression, standard error of the slope and significance of the regression by F-test.
• In the subsequent meta-analysis (103 199 records of 15 1 years) these trends were analysed for Europe by four phenophase groups (b0, farmers’ activities; b1, flowering and leaf unfolding; b2, fruiting; b3, leaf colouring), for countries by phenophase groups, and for countries and species.

Results

• The authors found that phenological changes were a clear reaction to temperature.
• Most phases correlated significantly with mean monthly temperatures of the month of onset and the two preceding months.
• In general, for farmers’ activities and especially spring, summer, as well as fruit ripening phases, there were more negative than positive trends (i.e. more time series revealed advancing onset), in contrast to leaf colouring and leaf fall phases where the authors had almost the same proportion of negative and positive trends (Fig. 3).

Discussion

• The authors meta-analysis comprised a huge selection of species and countries, included false phases in farming, and various phases of wild and agricultural plants covering the whole vegetation period.
• Owing to the enormous number of records included, the results are representative for Europe.
• The autumn signal was vague (delayed leaf colouring, but earlier fruit ripening because of warming, the latter more pronounced in agricultural than wild plants), thus further studies about observed climate change impacts in autumn should clearly differentiate between these phases.
• The authors would recommend further study to consider some questions arising from this study.

Figures

Fig. 3 Histograms of phenological trends in Europe. All temporal trends (1971–2000, time series 151 years) as linear regression coefficients (days yr 1) systematically reported to the COST725 meta-analysis (n5 103 199) for four different groups.

Fig. 1 Categories of system responses to observed changes and nonchanges in climate and relation to publication biases.

Fig. 4 National mean temperature trends against mean phenological trends. (a) In spring and summer (leaf unfolding, flowering – closed circles, animal phases – open circles). (b) In summer and early autumn (fruit ripening). (c) In autumn (leaf colouring and leaf fall). (d) For leaf unfolding of Fagus sylvatica and (e) for flowering of Prunus avium. Country abbreviations follow the international country codes.

Fig. 2 Temperature sensitivity and response across the year. (a) Maximum correlation coefficients of 254 mean national time series in nine European countries (see ‘Material and methods’) with mean temperatures of the previous months. Phenophases groups include farmers’ activities (b0), spring and summer with different leafing, shooting and flowering phases (b1), autumn fruit ripening (b2) and leaf colouring of deciduous trees in fall (b3). (b) Regression coefficients against mean temperature of the previous month. F, flowering; LU, leaf unfolding; LC, leaf colouring. The overall dependence of temperature sensitivity and response on mean date is high (a) R25 0.59, y5 0.0000003x3–0.0001204x21 0.0182684x 1.5823, Po0.001; (b) R25 0.47, y5 0.0000024x3 0.0011345x21 0.170218x 10.4650, Po0.001).

Table 1 Mean temperature sensitivity and response of phenological phases

Table 2 Summary of phenological trends in Europe

Frequently asked questions

Q1. What are the contributions in "European phenological response to climate change matches the warming pattern" ?

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. The authors 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. 01193. x r 2006 The Authors Journal compilation r 2006 Blackwell Publishing Ltd 1969 months ( mean advance of spring/summer by 2. 5 days 1C, delay of leaf colouring and fall by 1. 0 day 1C ). 

Q2. What are the future works in "European phenological response to climate change matches the warming pattern" ?

The autumn signal was vague ( delayed leaf colouring, but earlier fruit ripening because of warming, the latter more pronounced in agricultural than wild plants ), thus further studies about observed climate change impacts in autumn should clearly differentiate between these phases. The authors would recommend further study to consider some questions arising from this study. 

Q3. How long did the leaf colouring take?

Spring and summer phases advanced by up to 4.6 days 1C 1 warming (two outliers in summer are related to agricultural phases in Germany) and autumn leaf colouring was delayed by up to 2.4 days 1C 1. 

Q4. How many species were analysed in the study?

In total, phenological trends of 542 plant species in 21 countries (125 628 time series) and 19 animal species in three countries (301 time series) were analysed. 

Q5. What countries did warmer temperatures result in earlier leaf colouring?

Delayed leaf colouring was associated with higher temperatures ( r ¼ þ0:33); only in eastern Europe (Russia-Belarus, Russia-Ukraine and Czech Republic) did warming result in earlier leaf colouring. 

Q6. What is the importance of keeping track of the changes in the climate?

it is extremely important to keep track of theentirety of changes in order to properly address the questions of evidence of no change, change opposite to the direction expected, change not matching climate/ temperature change, and to discuss the questions of resilience and thresholds. 

Q7. Why did the earlier species show a stronger response to temperature in warmer countries?

The authors found that the earlier species were more sensitive, probably because of higher temperature variability in spring months, and they better indicated changes in temperature. 

Q8. What type of studies were included in the meta-analyses?

Parmesan & Yohe (2003) included multispecies studies from any location that reported neutral, negative and positive results and analysed a total of 677 species or species functional groups’ phenology. 

Q9. What was the frequent trend in leaf colouring?

Leaf colouring and leaf fall were less frequently observed; the majority of trends analysed were from Germany where, on average, no trend in leaf colouring was found (Fig. 4c; Menzel, 2003). 

Q10. What is the relationship between the temperature and the onset of leaf colouring?

In general, for farmers’ activities and especially spring, summer, as well as fruit ripening phases, there were more negative than positive trends (i.e. more time series revealed advancing onset), in contrast to leaf colouring and leaf fall phases where the authors had almost the same proportion of negative and positive trends (Fig. 3). 

Q11. What was the coefficient of the temperature sensitivity against the mean date of flowering?

The regression coefficients of the temperature sensitivity against mean onset date of flowering (days 1C 1 per day of the year) were 0.028 (R2 5 0.37) for Corylus avellana, 0.030 (R2 5 0.78) for Tussilago farfara, 0.047 (R2 5 0.74) for A. hippocastanum, 0.049 (R2 5 0.21)for Syringa vulgaris, 0.029 (R2 5 0.60) for Taraxacum officinalis, and, in contrast, 0.072 (R2 5 0.21) for R. pseudoacacia. 

Q12. What is the temperature response for Robinia pseudoacacia?

Phases analysed for more than six countries are highlighted in Fig. 2b: All spring phases, except Robinia pseudoacacia flowering, exhibited a stronger response to temperature in warmer than in colder countries. 

Q13. What are the results of the study?

These results strongly support previous results on a smaller number of sites and species and confirm them as being free from bias towards reporting global change impacts.