Lengthened flowering season under climate warming: Evidence from manipulative experiments
Introduction
Flowering phenology plays a critical role in plant reproductive success (Bogdziewicz et al., 2020; Elzinga et al., 2007; Waters et al., 2020), species fitness (Lázaro et al., 2020; Zhao et al., 2020), and plant-pollinator interactions (Hegland et al., 2009; Kharouba et al., 2018, 2020; Maglianesi et al., 2020), and consequently has a substantial impact on ecosystem structure and function (Burkle et al., 2013; CaraDonna et al., 2014; Cleland et al., 2007; Peñuelas and Filella, 2001). As an important component of flowering phenology, the flowering season can affect fruit production of plant species, and thus disrupt reproductive rhythms, as well as interactions between plants and pollinators (CaraDonna et al., 2014; Høye et al., 2013; Miller-Rushing and Inouye, 2009; Rafferty et al., 2016). For example, shortened flowering seasons could decrease the chance of successful pollination and threaten the propagation of certain plant species, which may accelerate biodiversity loss in the long term (Burkle et al., 2013; Høye et al., 2013; Zhao et al., 2013). In the Arctic, compressed flowering seasons could reduce flower-visitor abundance, indicating negative consequences for plant-pollinator interactions under climate warming (Høye et al., 2013). In contrast, a longer flowering season could increase the risk of pollen-related respiratory diseases (Bock et al., 2014; Ziello et al., 2012; Newnham et al., 2013). Although flowering itself is more important than flowering onset, the flowering season has received little attention (Jentsch et al., 2009; Marchin et al., 2015; Dorji et al., 2020). In addition, the global land-surface temperature is predicted to increase by 1.0–3.7 °C by the end of this century (IPCC, 2013). Because of the different sensitivities of the first and last flowering dates to elevated temperatures (Høye et al., 2013; Mo et al., 2017), climate warming may have the potential to affect the flowering season of terrestrial plants, and may subsequently impact ecosystem structure and function (CaraDonna et al., 2014; Høye et al., 2013).
Diverse response patterns of the flowering season to climate warming in various ecosystem types have been reported from long-term observational studies(Bock et al., 2014; CaraDonna et al., 2014; Prevéy et al., 2019). For example, these studies show that climate warming could extend the flowering season in a subalpine mountain plant community (CaraDonna et al., 2014), which is attributed to greater advancement in the beginning than the ending of flowering (Mo et al., 2017). In contrast, climate warming can shorten the flowering season in the Arctic and alpine tundra by elevating the temperature during flowering (Høye et al., 2013; Prevéy et al., 2019). Similarly, on the island of Guernsey in the English Channel, the flowering season for 232 species was also compressed over a long-term warming-climate scenario (Bock et al., 2014). The different impacts of climate warming on flowering seasons in previous studies may be attributed to different species compositions in diverse ecosystem types (Ge et al., 2015; Mo et al., 2017). For example, the flowering phenology of trees and forbs has weaker temperature sensitivity than that of herbs (Mo et al., 2017). In addition, herbs show greater advancements in spring phenophases than do trees and shrubs (Ge et al., 2015). Nevertheless, the general response patterns of the flowering season to climate warming and how the changing environmental factors associated with climate warming affect the flowering season in experimental systems remain poorly understood.
Manipulative experiments are critical for exploring the underlying mechanisms of flowering season responses to climate warming (Marchin et al., 2015; Meng et al., 2016; Nam and Kim, 2020; Wang et al., 2014). It has been shown that temperature alone cannot explain changes in the flowering season under experimental warming in Duke Forest (Marchin et al., 2015), which suggests that other factors (excluding temperature) should be considered to better understand variations in the flowering season under climate warming. In fact, precipitation and soil water availability have been demonstrated to affect the flowering season in different ecosystems and plant functional groups under a warming climate (Bykova et al., 2019; Meng et al., 2016; Nam and Kim, 2020). For example, precipitation could be a limiting factor for the flowering season in herb species, even if temperature requirements are fulfilled (Nam and Kim, 2020). In addition, soil water availability could also drive changes in the flowering season of alpine meadow communities by affecting flowering development (Meng et al., 2016). Nevertheless, the underlying mechanisms of warming-induced changes in the flowering season are still scarce, which poses considerable challenges to gain a better understanding and robust prediction of plant phenology under climate change (Marchin et al., 2015; Liu et al., 2020; Piao et al., 2019). Therefore, it is necessary to integrate available data to reveal the patterns of the flowering season in response to experimental warming with a unified view.
Previous synthetic analyses have been conducted to explore the general patterns of climate warming impacts on plant phenology using long-term observations or in situ experiments (Wolkovich et al., 2012; Ge et al., 2015; Mo et al., 2017; Huang et al., 2020; Collins et al., 2021). However, the response of the flowering season to elevated temperatures in experimental systems was not considered and seriously restricts the creation of a robust prediction of plant phenology under climate warming (Marchin et al., 2015). To assess and quantify the flowering season response of different ecosystems and plant functional groups to experimental warming, we conducted a meta-analysis with updated data from 26 studies (ranging from 2005 to 2020) and 168 species; the spread of locations is shown in Fig. 1. In analyzing the response patterns of the flowering season to experimental warming, we examined how latitude, temperature, and precipitation at the study site, as well as the functional group of the plant species, impacted flowering seasons of individual species to experimental warming.
Section snippets
Data collection
Peer-reviewed publications conducted with manipulative warming experiments published before October 2020 were collected by searching Web of Science (1900–2020, Thomson Reuters, New York, NY, USA) and China National Knowledge Infrastructure (CNKI) to build a database. Flowering duration, flowering season, flowering period, warming, increased temperature, elevated temperature, and rising temperature were used as keywords in the search process. In total, 208 references were identified using
Experimental warming-induced changes in flowering season with plant functional groups
Overall, compared with the control, the average flowering season was significantly lengthened by 2.08% under experimental warming across all species included in the analysis (Fig. 2). In addition, experimental warming prolonged the flowering season of herbaceous species by 2.18% but had no effect on woody species (Fig. 2). Warming-induced changes in flowering seasons of wind-pollinated species (−4.53%) and insect-pollinated species (+4.21%) were the opposite from one another. Among the woody
Overall experimental warming impacts on flowering season of terrestrial plants
The overall experimental warming-induced extension of the terrestrial plant flowering season in this study is in accordance with findings reported by a previous meta-analysis using long-term observations in China, which also revealed a prolonged flowering season under a warming climate from 1963 to 2013 (Mo et al., 2017). In contrast, our findings are inconsistent with those reported by a recent study in tundra ecosystems (Collins et al., 2021), which revealed that warming had no impact on the
Conclusions
Using a meta-analysis approach, we demonstrated that experimental warming generally prolonged the flowering season of terrestrial plants in temperate and northern ecosystems, which could alter interactions between plants and pollinators, as well as competition between species. However, the diverse responses of flowering season to experimental warming are dependent on plant functional types, geographic and climate factors (latitude and MAT, respectively), and warming magnitudes, which poses
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Sen Yang for the help for the data collection and analysis. This study was financially supported by the Postdoctoral Innovation and Practice Base of Anyang Institute of Technology (BSJ2020021, BHJ2021007), and the National Natural Science Foundation of China (42107225).
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