Divergent responses of leaf phenology to ... - Wiley Online Library

Divergent responses of leaf phenology to changing temperature among plant species and geographical regions HAICHENG ZHANG,1 WENPING YUAN,1, SHUGUANG LIU,2

AND

WENJIE DONG1

1

State Key Laboratory of Earth Surface Processes and Resource Ecology, Beijing Normal University, Beijing 100875/Zhuhai 519087 China 2 State Engineering Laboratory of Southern Forestry Applied Ecology and Technology, Central South University of Forestry and Technology, Changsha, Hunan 410004 China Citation: Zhang, H., W. Yuan, S. Liu, and W. Dong. 2015. Divergent responses of leaf phenology to changing temperature among plant species and geographical regions. Ecosphere 6(12):250. http://dx.doi.org/10.1890/ES15-00223.1

Abstract. Shifts in plants’ phenophases caused by climate change can strongly affect the ecosystem structure and function. Temperature sensitivity, which is expressed as the date of phenological event change for per degree Celsius change of temperature (days 8C1), has been widely used to characterize the plants’ responses to changed temperature. In this study, we analyzed the temperature sensitivity of leaf phenology (leaf unfolding date, LUD; leaf falling date, LFD) for more than 700 plant species based on the phenological observations at 56 sites in China from 1963 to 1988. Our results suggested significant spatial and interspecific variations in the responses of leaf phenology to changing temperature. Approximately 48.8% cases of LUD advanced significantly (p , 0.1) with the increasing spring temperature and 33.9% cases of LFD delayed significantly with increasing autumn temperature. The spring events were overall more sensitive to temperature than autumn events. Although the LUD of plants in warmer regions was more sensitive to changing temperature, the temperature sensitivities of LFD for plants in warmer regions were not significantly different from that for plants in cooler regions. Moreover, for spring phenology, many sites suggested higher temperature sensitivity for species that unfold their leaves earlier. For autumn phenology, species with later leaf-falling dates were generally more sensitive to temperature. Differences in species’ responses to temperature that caused the discrepant changes in species’ growing season can strongly impact vegetation dynamic and ecosystem function, and thus should be considered more when predicting the effects of climate warming on the biosphere. Key words: climate warming; interspecific variation; leaf falling date; leaf phenology; leaf unfolding date; spatial variation; temperature sensitivity. Received 15 April 2015; accepted 3 June 2015; published 8 December 2015. Corresponding Editor: J. Weltzin. Copyright: Ó 2015 Zhang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected]

INTRODUCTION

inconsistent conclusions on the magnitude and even direction of the changes in spring and autumn phenophases, which have been found to vary across within-species populations (Menzel et al. 2006), species (Miller-Rushing and Primack 2008, Dunnell and Travers 2011, Bock et al. 2014) and regions (Primack et al. 2009, Shen et al. 2014). This large variation can be attributed their

Numerous observations have shown that climate change, especially increased air temperature, profoundly impacts plant phenological events (Menzel et al. 2006, Cook et al. 2012, Diez et al. 2012, Wolkovich et al. 2012, CaraDonna et al. 2014). However, recent studies revealed v www.esajournals.org

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discrepancies in plants’ temperature sensitivity (Menzel et al. 2006, Bertin 2008, Diez et al. 2012), which is expressed as the date of phenological event change for per degree Celsius change of temperature (days 8C1). The difference in temperature sensitivities of phenophases among plant species strongly impacts ecosystem properties, such as species composition and ecosystem productivity (Fitter and Fitter 2002, Cong et al. 2012, Ge et al. 2014). Divergent responses of species’ phenology to climate change can lead to new patterns of species coexistence during reproduction, potentially affecting competitive interactions and, ultimately, the species composition of the community (Chuine and Beaubien 2001, Post et al. 2001, Sherry et al. 2007). For example, experimental warming advanced the flowering and fruiting phenology for species that began to flower before the peak of summer heat but delayed reproduction in species that started flowering after the peak temperature in a tall grass prairie in North America, this may reduce competition by spreading primary resource use over different temporal pools (Sherry et al. 2007). Moreover, in a fluctuating climate system, if spring phenology in trees has an instantaneous response to an external temperature increase, there could be fatal consequences due to the elevated probability of the tree’s exposure to frost (Inouye 2008, Lessard-Therrien et al. 2014). Many studies have investigated the temperature sensitivity of plant phenophases, and there are still many inconsistent conclusions. Menzel et al. (2006) suggested that the phenological responses of plants to temperature in warmer countries were stronger than those in colder countries of Europe. However, Root et al. (2003) analyzed global patterns of phenological responses to recent climate changes and suggested that the mean phenological shifts between latitudes 508 and 728 N were larger than those between 328 and 508 N. Moreover, several studies (Chuine et al. 2000, Berg et al. 2005, Vitasse et al. 2010) noticed stable temperature sensitivity among populations within a species, which is contrary to the diversified pattern found by others (Baliuckas and Pliura 2003, Lu et al. 2006). Generally, previous conclusions on plants’ temperature sensitivity are based on observations at local areas (Vitasse et al. 2010) and only v www.esajournals.org

involved limited species (Chuine et al. 2000). Several widely used datasets (i.e., Pan European Phenology Database; PEP725) have a mean climate typical of the temperate mid-latitudes and are mostly obtained from Europe and North America, but have a poor sampling in other regions of the world especially the relatively cold climates, and warm and dry climates (Wang et al. 2014a). Moreover, phenological datasets derived from satellite observations cannot describe the phenology of individual plants, but rather the integrative phenology at the ecosystem level (Sto¨ckli and Vidale 2004, Garonna et al. 2014). Using the long-term phenology observations in China, we aimed to quantify the temperature sensitivity of spring and autumn leaf phenophases for multiple species, and tested the following hypotheses (1) increasing temperature will induce advancement in spring phenophases and delay in autumn phenophases; (2) leaf phenology of plants in warmer regions is more sensitive to changing temperature; (3) species that unfold leaf earlier or fall leaf later are more sensitive to changing temperature.

MATERIAL

AND

METHODS

Phenological data from 1963 to 1988 were obtained from the Plant and Animal Phenology Observation Annals in China. The dataset includes phenology observations for more than 700 woody plant species from 91 families over 56 sites locating mainly in the middle and east China within latitudes 21–498 N (Fig. 1). Phenological observations were generally conducted in ecosystem study stations or botanical gardens. Most of the stations were built according to the standard principle for ecosystem studies. Topography, soil and meteorological conditions of the observational sites generally could represent local environments. The observed plant species were chosen from the common and representative species of local plant communities. Several widely growing species can be found in many different observation sites. The time series of phenology observations at most sites were more than 10 years (Appendix: Table A1). Overall, this study included 25,943 observations for the leaf unfolding date (LUD) and 17,098 observations for the leaf falling date (LFD). Daily air temperature observations from 1963 to 1988 for all sites 2


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Fig. 1. Locations of the 56 phonological observation sites included in present study.

were provided by China Meteorological Data Sharing Service System (http://www.cma.gov.cn/ 2011qxfw/2011qsjgx/). Most of the phenological observation sites have a meteorological station within 50 km. Temperature sensitivity of plant phenology is expressed as the date of phenological event change for per degree Celsius change of temperature (days 8C1). Similar with previous studies (Menzel et al. 2006, Wang et al. 2014a, Wolkovich et al. 2012), the temperature sensitivity was calculated as the slope coefficient of linear regression equations between phenological records and mean preseason temperature as shown below: LUD ¼ kLUD ðMSTÞ þ e1

ð1Þ

LFD ¼ kLFD ðMAuTÞ þ e2

ð2Þ

temperature (Fig. 2a). On average, a 18C increase in mean spring temperature induced an earlier shift of four days for leaf unfolding over all of investigated sites. Responses of leaf unfolding to air temperature (kLUD, days 8C1) varied drastically among plant species and geographical regions. Approximately 48.8% cases of leaf unfolding date showed significant advancement (p , 0.1) with the increasing mean spring temperature, while 50.9% cases showed insignificant (p . 0.1) changes and the residual 0.3% showed significant (p , 0.1) delays. Generally, the temperature sensitivity of plants in warm regions showed larger interspecific variances compared to those in cool regions (Appendix: Fig. A1a). Meanwhile, for plants with significant (p , 0.1) temperature sensitivity, the strength of the temperature sensitivity increased significantly with increasing local temperature (Fig. 2a). For example, in regions with a mean annual temperature lower than 108C, the kLUD overall ranged from 5 to 2 days 8C1; in regions with a mean annual temperature of approximately 208C, the magnitudes of kLUD were mostly larger than five days 8C1. The temperature sensitivity of leaf falling to the mean autumn temperature (kLFD, days 8C1) also varied substantially among plant species (Fig. 2b). On average, a 18C increase in mean autumn temperature induced a delay of 2.1 days for leaf falling. A large proportion of LFD records (62.9%) showed an insignificant correlation of

where kLUD is the sensitivity of leaf unfolding date (LUD) to mean spring (February, March and April) temperature (MST); kLFD is the sensitivity of leaf falling date (LFD) to mean autumn (August, September and October) temperature (MAuT); and e1 and e2 are the regression errors. In this analysis, only the plant species with at least seven-years of observations were included.

RESULTS Leaf unfolding at the majority of the sites showed a negative response to mean spring v www.esajournals.org

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Fig. 3. Mean sensitivity of leaf unfolding date (LUD) to mean spring temperature (kLUD, a) and mean sensitivity of leaf falling date (LFD) to mean autumn temperature (kLFD, b) for primary plant families. Error bar denotes the standard deviation of sensitivities for plant species belonging to the same family. Only the significant (p , 0.1) sensitivities were included in the calculation.

Fig. 2. Temperature sensitivity of the leaf unfolding date (LUD) to mean spring temperature (kLUD) (a), and the leaf falling date (LFD) to mean autumn temperature (kLFD) (b) for plant species at different sites. The inserted pie charts present the percentages of plant species that show insignificant (black, p . 0.1), significantly negative (red, p , 0.1) and significantly positive (green, p , 0.1) temperature responses.

times that of Lauraceae (2.8 days 8C1). The considerable standard deviations of kLUD and kLFD for each plant family highlighted that kLUD or kLFD for different species belonging to the same family could be quite different. Further analysis suggested that, at some sites (10 of 30 investigated sites), plant species with earlier leaf unfolding dates showed higher temperature sensitivities (Fig. 4a). At six of 13 investigated sites, the temperature sensitivity of leaf falling was higher for the plant species with later leaf falling dates (Fig. 4c).

leaf falling with mean autumn temperature, and approximately 33.9% records were positively correlated to autumn temperature, with kLFD ranging from 2 to 15 days 8C1. The residual 3.2% suggested significant advances in LFD with increased autumn temperature. Different from the leaf unfolding date, the temperature sensitivity of leaf falling date did not show a significant trend over the geographical areas (Fig. 2b). Temperature sensitivity of leaf unfolding and falling dates (kLUD and kLFD) also varied obviously among plant families (Fig. 3). For example, the mean kLUD for Euphorbiaceae was 7.6 days 8C1, and it was about two times the mean kLUD for Betulaceae (4.0 days 8C1). The mean kLFD for Betulaceae (7.6 days 8C1) was nearly three v www.esajournals.org

DISCUSSION Changes in temperature can strongly alter leaf phenophases; however, the responses of phenophases to preseason temperature vary drastically 4


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among plant species and geographical locations. Our results suggested that leaf phenophases of many plants respond significantly to the changes in spring and autumn temperature. On average, the temperature sensitivities of leaf unfolding (kLUD, 4 days 8C1) are stronger than those of leaf falling (LFD, 2.1 days 8C1). Temperature sensitivities for plants in China are overall comparable to observations in Europe and North America (Menzel et al. 2006, Miller-Rushing and Primack 2008, Wolkovich et al. 2012). Although considerable plant species showed significant advances in LUD with increasing spring temperature and delays in LFD with increasing autumn temperature, a sizable proportion of the observations still do not confirm to these two change trends. Previous studies have also reported the divergent temperature sensitivities of plant phenology (Estrella and Menzel 2006, Parmesan 2007, Shen et al. 2011). The responses of leaf unfolding to spring temperature were found to be stronger in warm regions than in cold regions (Fig. 2a). Other lines of evidence also support this result (Menzel et al. 2006, Doi and Takahashi 2008, Shen et al. 2014). One of the potential causes is that temperature variance in cold regions was larger than that in warm regions (Appendix: Fig. A2). Plants growing in cold regions may have adapted to the unstable temperature conditions (Pau et al. 2011, Wang et al. 2014a), thus showing low temperature sensitivity. For example, Lapenis et al. (2014) found that the temperature sensitivity of flowering phenology showed a negative spatial correlation with the seasonal temperature range. Furthermore, Shen et al. (2014) suggested that temperature increases in winter and early spring tended to be larger at higher latitudes, and thus are more frequent to delay the fulfillment of the chilling requirement for spring phenophases. In this way, the advance in LUD caused by increasing spring temperature will be relatively small for plants in high latitudes. There is still no recognized explanation for the higher temperature sensitivity of the species with earlier leaf-unfolding and later falling dates (Fig. 4). Leaves generally unfold when previous accumulated heat fulfills a threshold (Yu et al. 2010, Zhao et al. 2013). As the early leaf-out species require less thermal forcing, the same amount of temperature increase (assumed to be

Fig. 4. Temperature sensitivity of LUD (or LFD) for plant species unfolding (or falling) their leaves at different times of the year. kLUD is the temperature sensitivity of the leaf unfolding date (LUD) to mean spring temperature; kLFD is the temperature sensitivity of the leaf falling date (LFD) to mean autumn temperature. The * indicates a significant trend (p , 0.05), and the ** indicates a very significant trend (p , 0.01). Only sites with at least seven plant species showing significant (p , 0.1) kLUD or kLFD were included in this analysis. Only sites with a significant (p , 0.05) relationship between the temperature sensitivities of LUD (or LFD) and species’ unfolding (falling) dates were presented in this Fig. In total, 14 of 30 tested sites were analyzed for LUD and six of 13 sites for LFD.

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even over the spring season) may be more effective to these species. Moreover, a previous study suggested that the thermal forcing required for leaf unfolding increased steeply with decreasing winter chilling for late leaf-out species, but increased slowly for early leaf-out species (Murray et al. 1989). With the rising temperature, the winter chilling decrease, and the thermal requirements for late leaf-out species will increase more compared to early leaf-out species. In this way, advances in leaf unfolding dates caused by spring warming will be smaller for late leaf-out species, and the late leaf-out species will show lower temperature sensitivities. Furthermore, it is still difficult to explain why species that fall leaves earlier in autumn show lower temperature sensitivities. It is possible that some other environmental factors or species’ intrinsic properties have induced differences in plants’ response to temperature. The temperature sensitivity derived from historical phenology observations from 1963 to 1988 may not be able to fully represent the current conditions. Although temperature has been widely regarded as the dominant factor of plant phenology, the high interannual variation related to circulation patterns, solar cycles, and oscillation (e.g., the EI Nino Southern Oscillation [ENSO] and the North Atlantic Oscillation [NAO]) can also strongly impact phenophases (Badeck et al. 2004). Previous studies proved that the global climate system has changed drastically since the end of the 1980s (the end of our study period) (Walther et al. 2002, Fischlin et al. 2007). Thus, plants’ temperature sensitivity may have also changed. Several observations have already suggested significant temporal changes in the plants’ responses to changed temperature (Rutishauser et al. 2008, Wang et al. 2014b). Overall, a longer-term observation, especially with the observations in recent decades, will be helpful to quantify the temperature sensitivity of current plants and explore the impacts of systematic climate change on plants’ temperature sensitivity. The divergent responses of leaf phenology to temperature among plant species and geographical locations may have ecological significance, and should be incorporated into the phenology model for predicting the impacts of global warming on ecosystem functions. Plant species with earlier leaf unfolding dates show the higher v www.esajournals.org

temperature sensitivity, and they will therefore start their growing season earlier with increasing spring temperature compared to other species, resulting in greater superiority for interspecific competition. Different temperature sensitivities also caused compression and expansion of the growing season for different species (Sherry et al. 2007), which may further induce changes in species composition and ecosystem production. The suite of changes in phenology caused by climate change will likely create powerful selection pressure not only on plant species themselves but also possibly on species at higher trophic levels that depend on these plants (Tilman et al. 1997, Hooper 1998, Stevens and Carson 2001). Previous studies also highlighted that the phenology of growth, including the timing of leaf emergence and senescence, determines the seasonal cycle of leaf function. This will impact ecosystem carbon and water cycle (Schaber and Badeck 2003, Cong et al. 2012, Fridley 2012). Overall, the divergent temperature responses of leaf phenology can induce changes in many ecological processes, and thus should be considered seriously when simulating the ecosystem carbon cycle or assessing the impacts of climate warming on terrestrial ecosystems.

ACKNOWLEDGMENTS This study was supported by the National Natural Science Foundation of China (41201078), National Science Foundation for Excellent Young Scholars of China (41322005) and Program for New Century Excellent Talents in University (NCET-12-0060).

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SUPPLEMENTAL MATERIAL ECOLOGICAL ARCHIVES The Appendix is available online: http://dx.doi.org/10.1890/ES15-00223.1.sm


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