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Herbarium specimens show contrasting phenological responses to Himalayan climate

Authors:
  • N.Gene Solution of Natural Innovation

Abstract

Responses by flowering plants to climate change are complex and only beginning to be understood. Through analyses of 10,295 herbarium specimens of Himalayan Rhododendron collected by plant hunters and botanists since 1884, we were able to separate these responses into significant components. We found a lack of directional change in mean flowering time over the past 45 y of rapid warming. However, over the full 125 y of collections, mean flowering time shows a significant response to year-to-year changes in temperature, and this response varies with season of warming. Mean flowering advances with annual warming (2.27 d earlier per 1 °C warming), and also is delayed with fall warming (2.54 d later per 1 °C warming). Annual warming may advance flowering through positive effects on overwintering bud formation, whereas fall warming may delay flowering through an impact on chilling requirements. The lack of a directional response suggests that contrasting phenological responses to temperature changes may obscure temperature sensitivity in plants. By drawing on large collections from multiple herbaria, made over more than a century, we show how these data may inform studies even of remote localities, and we highlight the increasing value of these and other natural history collections in understanding long-term change.
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... Variation in flowering times due to changes in mean spring temperature has been detected among plant communities within small regions (Primack et al. 2004;Miller-Rushing et al. 2006;Panchen et al. 2012;Park and Schwartz 2014;Davis et al. 2015) and at continental scales (Calinger et al. 2013;Panchen and Gorrelick, 2016;Munson and Long 2017;Park et al. 2019;Pearson 2019). Furthermore, studies focused on select taxa across their native range have revealed shifts to earlier flowering times in warmer years (Robbirt et al. 2011;Hart et al. 2014;Matthews and Mazer 2015;Rawal et al. 2015). Considering the species diversity of any given community, flowering times can span several months, starting with early spring ephemerals extending to early fall bloomers. ...
... Today, there are almost 50 million digitized specimens in the Integrated Digitized Biocollections portal (iDigBio 2021), further enabling studies of changes to plants in recent history. Though declines in recent collections have been noted (Hart et al. 2014), verified observations from citizen science initiatives such as iNaturalist or BudBurst can also provide valuable data points to identify flowering times across the globe. ...
... Previous phenology studies have examined the relationship between changes in temperature and flowering time at the individual species level (Walkovsky 1998;Matthews and Mazer 2015), genus level (Hart et al. 2014, Rawal et al. 2015, community level (Davis et al. 2015), regional level (Park and One difference is that our study did not include species with an earliest flowering date before the end of May, but instead compared early summer with late summer flowering species. This widens the time frame for which species that bloom earlier in the growing season are affected by changing temper-FIG. ...
Article
Climate change has altered the phenological timing of plants across the globe. These changes are especially concerning for plants with small distributions and in unique ecological sites. Here, we examined changes in phenology with respect to temperature and year over a 125-yr span for 12 herbaceous species native to the lowlands of the New Jersey Pine Barrens using herbarium specimens and citizen science observations. Among early summer flowering species, flowering occurred on average 1.42 days/C earlier in the spring of the corresponding year. Early summer flowering species flowered at an average rate of 0.071 days/yr earlier over the 125-yr study period, whereas no significant change was detected in flowering times of late summer species. Exploration of a set of sister taxa with differing range sizes resulted in no detectable shifts in phenology, which may be explained by evolutionary relatedness or flowering in late summer. The variation in responses to species in the New Jersey Pine Barrens may alter the balance of this ecosystem in the future, as some species respond to changing temperatures, whereas others do not. These results add to a growing body of work suggesting that variations in temperature due to climate change are affecting plant phenology.
... Although a number of experimental phenology studies are available from the developed world (Ettinger et al. 2020), such studies are still insufficient from the developing world (Stuble et al. 2021). Very few studies reporting phenological shifts by climate warming using observational and historical data from the developing world have recently become available (Hart et al. 2014;Gaira et al. 2014;Ahmad et al. 2021;Hassan et al. 2021). As the developing world harbours a much higher proportion of the global biodiversity, conducting experimental phenology studies assumes a research priority. ...
... Recently, a few observation-based studies on the plant phenology in different parts of the Himalaya have been conducted (Hart et al. 2014;Basnett et al. 2019;Gaira et al. 2014;Ahmad et al. 2021;Hassan et al. 2021). The Kashmir Himalaya, a region located in the Himalaya global biodiversity hotspot, is recently experiencing rapid climate changes (Hassan et al. 2021), and therefore experimental phenological study from this region can help in filling the global geographical knowledge gap in phenology research. ...
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Experimental evidences in support of climate warming–driven phenological shifts are still scarce, particularly from the developing world. Here, we investigated the effect of experimental warming on flowering phenology of selected woody plants in Kashmir Himalaya. We selected the twigs of four congeneric pairs of temperate woody species (Prunus, Populus, Ulmus, Viburnum)—typical spring-flowering plants in the region. Using randomised block design, we monitored these winter dormant twigs in controlled growth chambers to study the effect of different temperature regimes (9, 17, 20 and 23 °C) and species identity on the patterns of phenological shifts. We observed a significant phenological shift in all the species showing preponement in the first flower out and senescence phases ranging from 0.56 to 3.0 and 0.77 to 4.04 days per degree increase in temperature, respectively. The duration of flowering phase in all the species showed a corresponding decrease along the gradient of increasing temperature, which was more driven by preponement of the flower senescence than the start of flower- ing. The patterns of phenological shifts were highly species-specific, and the magnitude of these shifts significantly varied in all the four pairs of congeneric species despite their phylogenetic similarity. Our study provides experimental support to the previous long-term observation and herbarium-based studies showing that the patterns of phenological shifts in response to global climate warming are likely to vary between species, even those belonging to same evolutionary stock. Our findings highlight that a one-size-fits-all strategy to manage the likely impacts of climate warming–induced phenological shifts will seldom succeed, and should instead be designed for the specific phenological responses of species and regions.
... The phenological studies and observation in modern era should involve various other strategies. Past historical patterns of plant phenology can be reconstructed from herbaria (Hart et al., 2014;Kumar and Chopra, 2018). Since phenological study of herbarium data provide distinctive insights into past responses only, therefore, longterm phenological observation becomes crucial for understanding present responses and modelling these responses in the future. ...
... associated flowering data in the Arctic. Hart (2014) analysed 10,295 herbarium specimens of Himalayan rhododendron collected by plant hunters and botanists since 1884 to show contrasting phenological responses to the Himalayan climate. However, mean flowering time showed a significant response to annual changes in temperature over the full 125 years of collections with the response varying with the season of warming. ...
... As such, they constitute a window to the evolutionary processes taking place in response to environmental change (Boakes et al. 2010, Pyke and Ehrlich 2010, Holmes et al. 2016. NHCs have provided invaluable data for studies in fields such as species distribution modelling (SDM) (Gaubert et al. 2006, Mateo et al. 2010, ecophysiology (DeLeo et al. 2019, Tseng andPari 2019), global change (Lang et al. 2019, Denney andAnderson 2020), phenology (Hart et al. 2014, Kiat et al. 2019, ecological interactions (Kido and Hood 2019), invasion biology (Crawford andHoagland 2009, Jorissen et al. 2020), conservation (Drew et al. 2017, Lughadha et al. 2019) and public health and safety (Suarez andTsutsui 2004, Komar et al. 2005). ...
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Natural history collections (NHCs) represent an enormous and largely untapped wealth of information on the Earth's biota, made available through GBIF as digital preserved specimen records. Precise knowledge of where the specimens were collected is paramount to rigorous ecological studies, especially in the field of species distribution modelling. Here, we present a first comprehensive analysis of georeferencing quality for all preserved specimen records served by GBIF, and illustrate the impact that coordinate uncertainty may have on predicted potential distributions. We used all GBIF preserved specimen records to analyse the availability of coordinates and associated spatial uncertainty across geography, spatial resolution, taxonomy, publishing institutions and collection time. We used three plant species across their native ranges in different parts of the world to show the impact of uncertainty on predicted potential distributions. We found that 38% of the 180+ million records provide coordinates only and 18% coordinates and uncertainty. Georeferencing quality is determined more by country of collection and publishing than by taxonomic group. Distinct georeferencing practices are more determinant than implicit characteristics and georeferencing difficulty of specimens. Availability and quality of records contrasts across world regions. Uncertainty values are not normally distributed but peak at very distinct values, which can be traced back to specific regions of the world. Uncertainty leads to a wide spectrum of range sizes when modelling species distributions, potentially affecting conclusions in biogeographical and climate change studies. In summary, the digitised fraction of the world's NHCs are far from optimal in terms of georeferencing and quality mainly depends on where the collections are hosted. A collective effort between communities around NHC institutions, ecological research and data infrastructure is needed to bring the data on a par with its importance and relevance for ecological research.
... In Europe, land temperatures have increased c. 1.5°C since 1900 (Luterbacher et al., 2004;Harris et al., 2014;European Environmental Agency, 2020), so the magnitude of overall phenological changes we observed is similar to what would be expected based on climate change and the observed temperature sensitivities (1.5°C × 3.6 d/°C = 5.4 d, vs our observed average shift of c. 6 d). Previous herbarium studies from the temperate zone estimated similar flowering-time advancements of −2.4 to −6.3 d per 1°C temperature increase (Primack et al., 2004;Miller-Rushing et al., 2006;Panchen et al., 2012;Calinger et al., 2013;Hart et al., 2014;Bertin, 2015;Davis et al., 2015;Bertin et al., 2017). Again, most of these studies were from the northeastern USA, and they were often geographically very restricted. ...
Article
Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long‐term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large‐scale analyses of herbarium data are prone to pseudoreplication and geographical biases. We studied over 6000 herbarium specimens of 20 spring‐flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account. On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor. Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long‐term phenology trends across large spatial scales.
... According to Figures 5 and 6, the years with high spring (FMA) temperature led to an early initiation of springwood (earlywood) formation by increasing the rate of stomatal conductance, allowing more uptake of soilmoisture by the roots. There are records of winter-spring temperature warming inducing early initiation of springwood in conifer [73] and phonological changes [74] from different regions. The transpiration process modulates the isotopic composition of leaf water by preferential loss of the lighter isotope ( 16 O) through the stomata, enriching the 18 O in leaf water [35]. ...
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... However, owing to the high data requirement of phenological studies, previous researchers have been limited in their ability to assess phenological questions which are spatially and temporally explicit in tandem (Wolkovich et al., 2014). Studies that assess a large temporal period of phenology, such as those that utilize historic herbarium records of phenology, are typically spatially limited to the local-scale or to a defined number of sites across a larger region (Primack et al., 2004;Cook et al., 2012;Hart et al., 2014;Park and Schwartz, 2015;Reeb et al., 2020). By contrast, studies that assess a large spatial area (such as at continental scales), are typically restricted to a short frame in time or phenological observations are aggregated across years (Li et al., 2019, but see Templ et al., 2018). ...
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