In the era of the Anthropocene, changes in the timing of plant life cycle events serve as prominent biological markers of global environmental shifts. Major of the studies dedicated to documenting and analyzing plant phenological changes are from North America and Europe. Although few studies are available from Himalayan regions, but there is a notable scarcity of comparable studies in the developing world, particularly in regions like the Himalaya. To fill this knowledge gap, the present study aims to attempt the reveal to attempt to unravel the vegetative and reproductive phenology of Phytolacca acinosa across Kashmir Himalaya. For this, we selected and tagged 10 healthy individuals for monitoring and documenting the onset and duration of different phenological events from sprouting to senescence. Further, flowering phenology was recorded using flowering variables such as moment, intensity and duration. Our results reveal that Phytolacca acinosa completes the entire life cycle within a period 7–8 months, and the timing of phenophases varied significantly across the selected sites. Our results also reveal that the plant populations at lower elevations exhibited a clear precedence of vegetative and reproductive phases in their life cycle as compared to those growing at higher elevations. We found that all the phenophases except senescence showed an overlap with the preceding phase. We also found that the flowering variables showed significant variation across the selected sites with the maximum values at low elevations, while minimum values at high elevations. Our study is the first attempt that provides useful insights into the phenology of P. acinosa across different habits along an elevation gradient in Kashmir Himalaya. Phenological adjustments, such as advancing or delaying reproductive phases, are crucial strategies for species to optimize reproductive success. Global climate change, characterized by rapid warming and disruptions, particularly during reproductive periods, has notably impacted species at higher elevations. Understanding phenological attributes is vital in contemporary conservation biology and the phenological data from this study will assist in formulating effective strategies for the restoration and conservation of the target species.
Research Article
From Sprouting to Senescence: Phenological Chronicles of Phytolacca acinosa Roxb. in the Himalayan Highlands
https://doi.org/10.21203/rs.3.rs-5008493/v1
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Biodiversity
Elevation
Global warming
Himalaya
Phenology
Phenology refers to the timing of natural biological events and is closely linked to the survival and reproduction of organisms (CaraDonna et al., 2014). It involves the life cycle phases/activities of plants and their temporal occurrence throughout the year (Menzel, 2002). Phenology studies the timing of biological events and their relation with varying seasonal climatic conditions (Fitchett et al., 2015). It serves as a tool to evaluate the impact of changing environmental conditions on overall plant growth and development (Cornelius et al., 2012). Generally, phenological events are happening earlier in temperate environments due to climate change but recent studies focussed on species-specific variations in the extent and direction of these changes (Cook et al., 2012; Ovaskainen et al., 2013). Phenological studies are considered a significant biological indicator, providing insights into ecosystem dynamics and their response to diverse environmental stimuli (Cosmulescu et al., 2021). A comprehensive understanding of plant phenology provides insights into the ecological and evolutionary aspects of plants. Also, it plays a pivotal role in assessing changes in species composition and determining various structural and functional attributes within a plant community (Shen et al., 2015). Various environmental (elevation, photoperiod), edaphic factors (soil structure, nutrient availability) and climatic (rainfall, temperature) factors govern and determine the trajectory of phenological events of the plants (Bhattacharya, 2022).
The phenophases are very sensitive to changing environmental conditions and thus act as effective biological indicator of climate change (Negi et al., 2012). In mountainous ecosystems, plant phenology shows an intimate relationship with elevation-dependent climatic conditions (Menzel et al., 2006; Chen et al., 2018; Stucky et al., 2018). A species responds to environmental cues such as precipitation, air and soil temperature, and humidity by either preponing or postponing its phenophases (Bhattarai et al., 2021; Hassan et al., 2022). Phenological shifts is regarded as a key strategy employed by vegetation to cope with global climate change (Zohner et al. 2017; Liu and Zhang 2020). The current climate warming is inducing notable phenological shifts, either advancing spring flowering in temperate ecosystems or delaying summer flowering phenology in various plant species and consequently affecting crucial ecological processes and biotic interactions of these plants (Cleland et al., 2012; Iler et al., 2021; Rosbakh et al., 2021). To unravel the mechanisms behind phenological shifts and to enhance predictions of future changes in phenological events, it is crucial to gain a more comprehensive understanding of the relationship between climate warming and the associated phenological changes in species (Hassan et al., 2022). The study of phenology along elevation gradients enhances our understanding of variations in plant development under diverse temperature regimes and elucidates the potential impacts of these phenological shifts on plant-pollinator interaction (Cornelius et al., 2013; Morton and Rafferty, 2017). Shifts in phenophases, indicated by early germination, prolonged vegetative and reproductive stages, variations in insect occurrence, and delayed senescence, serve as potential indicators of how plant species adapt to diverse habitats with distinct environmental and bioclimatic conditions (Fu et al., 2015; Li et al., 2016). The onset and longevity of flowering and floral evocation significantly influence the plant-pollinator interaction. Early flowering leads to pollen limitation due to the absence of pollinators, while delayed flowering often results in seed maturation failure due to a shorter growing season (Nebot et al., 2018). The knowledge of selective forces shaping the evolution of flowering time in plants is essential to understand the relationships between flowering phenology, seed set, and the extent of spatial and temporal variation in these associations (Morellato et al., 2016). Studying pollination mechanisms is crucial for understanding the breeding and mating systems of plant species and can contribute to enhancing genetic diversity within their gene pool.
In high mountainous regions, the flowering phenology varies along elevation gradients, with plants at lower elevations often flowering earlier than those of the same species at higher elevations (Ranjitkar et al., 2013; Wang et al., 2022). Habitat variability and elevation influence the plant phenophases in a species-specific manner. In the coexisting species variations in phenology may affect the survival of one or both species (Visser and Both, 2005; Yang and Rudolf, 2010). The Himalayan montane and snowy habitats exhibit diverse ecological and bioclimatic gradients, supporting rich plant diversity, including a high proportion of endemics (Singh et al., 2008). These ecosystems display significant variations in biotic and abiotic factors along elevation, resulting in a significant impact on the phenological attributes of plants (Caldwell et al., 2007; Shabir et al., 2013; Bisht and Chauhan, 2018; Wu et al., 2021). The shifts in phenological events can contribute to phenotypic plasticity and thus playing a key role in defining the geographical range and distribution of plant species (Nazir et al., 2017).
The current study aimed to investigate the phenology of Phytolacca acinosa across diverse habitats along an elevation gradient in Kashmir Himalaya. Phenological studies are vital for understanding the phenotypic and reproductive plasticity of plant species under varying environmental conditions and have broad significant conservation implications. This study was conducted to achieve the following specific objectives; a) to study the vegetative and reproductive phenology of Phytolacca acinosa across different habitats in Kashmir Himalaya b) to assess the impact of habitat variability on the start, completion, and duration of different phenophases of P. acinosa c) To investigate how flowering phenology variables like moment, intensity and duration vary across different study sites.
Methodology
Study species
Phytolacca acinosa Roxb. belonging to family Phytolaccaceae is a perennial herb widely distributed across the Himalayan regions. It is native to east and south-east Asia, and also found in the north-western Himalayan region at the elevation range of 1500–3400 m a.s.l. The stem of P. acinosa is erect, typically 0.5–1.5 m tall, leafy throughout; leaves are elliptic or lanceolate; inflorescence is densely flowered raceme; flowers bisexual ca. 8 mm in diameter; tepals 5, white and seeds are reniform, smooth, ca. 3 mm (Wyrzykiewicz-Raszewska, 2009). P. acinosa is an economically valuable medicinal herb and is widely used as a diuretic in traditional Chinese medicine system (Basnet and Kalauni, 2020; Magray et al., 2023). P. acinosa has a wide elevational range and therefore, can be used to assess the strategies of the plant species to successfully adapt and grow in varying environmental conditions along the wide elevational gradient.
Study area
This study was conducted in Kashmir Himalaya — a region falling toward the northwestern side of the Himalaya biodiversity hotspot in India (Rodgers & Panwar, 1988; Dar & Khuroo, 2020), encompassing an area of around 15,948 sq. km. (Fig. 1). The altitudinal gradient of the valley ranges from 1500 to 1800 m a.s.l., whereas the average elevation of the adjacent mountains’ ranges from 3000 to 4000 m a.s.l., with Kolahoi (5420 m a.s.l.) (Romshoo et al., 2020) being the highest peak. Climate of this region exhibits resemblance with continental-Mediterranean type found along temperate latitudes and is characterized by well-defined seasonality. The region experiences moderate variations in precipitation, with an average annual rainfall of 1005.5 ± 197.6 mm, and significant variations in mean annual temperature with mean minimum and maximum temperatures, ranging from 5.4 ± 0.4 to 17.6 ± 0.8°C (Romshoo et al., 2020). The vegetation of the area is temperate; subalpine and alpine type harbouring enormous floristic diversity. The region exhibits significant elevational and climatic variations and therefore offers an ideal system for studying the relation between elevation and functional traits and predicting the drivers of these trait variations.
Survey and sampling
To study the phenology of P. acinosa four sites namely Drung, Gogaldara, Gulmarg, and Doodhpathri were selected (Fig. 1). Geo-coordinates, elevation and habitat characteristics of the study sites are provided in Table 1. A total of 40 healthy individual plants (10 from each site) were selected and tagged for monitoring and documenting the onset and duration of different phenological events from sprouting to senescence. Data regarding initiation, completion, and duration of the phenophases viz., vegetative phase (including rhizome sprouting), sexual phase (including flower bud formation, anthesis, fruit formation, seed maturation), and senescence of aerial shoots were recorded for two consecutive growing seasons (Smitha and Thondaiman, 2016; Wani et al., 2022). Duration was calculated based on the initial and final dates of each respective phenophase. Flowering phenology was recorded using variables such as moment, intensity, and duration. Moment represents the number of days between the start of flowering and the day with the highest flower number (Dafni, 1992). Intensity refers to the maximum flower count on a census day (Herrera, 1986). Duration is the number of days between the first and last flower appearance (Dafni, 1992).
| Study sites | Latitude (N) | Longitude (E) | Elevation (m asl) | Habitat |
|---|---|---|---|---|
| Drung | 34.03783° | 74.41106° | 2250 | Shady, inside forest |
| Gulmarg | 34.04557° | 74.38441° | 2630 | Partial shady and slope |
| Gogaldara | 34.04317° | 74.51425° | 2470 | Shady slope |
| Doodhpathri | 33.88613° | 74.58712° | 2780 | Open slope |
The present study revealed that the timing (initiation and completion) and duration of all the phenophases varied significantly across the selected sites (Table 2). Plant populations at lower elevations exhibit a clear precedence of the vegetative and reproductive phases in their life cycle compared to those growing at higher elevations. All the phenophases except senescence showed an overlap with the preceding phase (Table 2). The phenology of the P. acinosa from the sprouting of buds present on the rhizome to the senescence of the aboveground shoot was monitored (Fig. 2A-E) and the data related to the different phenophases was recorded (Table 2).
|
Phenophase |
Study sites (Elevation) |
||||
|---|---|---|---|---|---|
|
Drung |
Gogaldara |
Gulmarg |
Doodhpathri |
||
|
Sprouting |
I |
1(4)* |
3(4) |
1(5) |
2(5) |
|
C |
3(5) |
4(5) |
1(6) |
2(6) |
|
|
D |
41 |
42 |
34 |
35 |
|
|
Bud formation |
I |
2(5) |
3(5) |
4(5) |
4(5) |
|
C |
2(7) |
2(7) |
2(7) |
2(7) |
|
|
D |
60 |
53 |
44 |
46 |
|
|
Anthesis |
I |
4(5) |
2(6) |
3(6) |
4(6) |
|
C |
4(7) |
1(8) |
2(8) |
3(8) |
|
|
D |
59 |
57 |
54 |
52 |
|
|
Fruit formation |
I |
2(7) |
3(7) |
4(7) |
1(8) |
|
C |
4(08) |
1(9) |
2(9) |
2(9) |
|
|
D |
50 |
48 |
43 |
38 |
|
|
Seed formation |
I |
2(8) |
2(8) |
4(8) |
1(9) |
|
C |
3(9) |
3(9) |
4(9) |
1(10) |
|
|
D |
42 |
41 |
32 |
30 |
|
|
Senescence |
I |
3(9) |
3(9) |
3(9) |
3(9) |
|
C |
1(11) |
1(11) |
4(10) |
4(10) |
|
|
D |
48 |
43 |
36 |
31 |
|
|
Duration of growth season |
216 |
199 |
179 |
167 |
|
Phytolacca acinosa, a perennial rhizomatous plant species found in the temperate to subalpine areas in Kashmir Himalaya, endures harsh winters (December to April) through rhizomes bearing dormant perennating buds which sprout into juvenile shoots upon the return of favorable conditions (Fig. 2A). The sprouting varied considerably among the sites, ranging from the Ist week of April to 2nd week of May (Table 2). In the plant population growing at the low elevation site (Drung), sprouting started early in 1st week of April and lasted up to the 3rd week of May while as those growing at high elevation site (Doodhpathri) sprouting started late in the 2nd week of May and lasted up to the 2nd week of June (Table 2). The vegetative phase (sprouting) lasts for a duration of approximately 30 to 40 days. The sexual phase follows the vegetative phase and is marked by the formation of flower buds in the leaf axils (Fig. 2B). Initially, the terminal inflorescence branch produces floral buds, followed by the development of buds on lateral inflorescence branches. The sexual phase (bud formation) also varied among sites starting in the 2nd week of May and continuing till the 2nd week of July. The duration of this phase ranged from 44 days (Gulmarg) to 60 days (Drung) and was followed by anthesis. Anthesis starts with the opening of the first flower of the terminal inflorescence axis and proceeds in an acropetal order (Fig. 2C). This phase begins in the 4th week of May and completes in the 2nd week of August. At high elevation sites, plants complete anthesis in a shorter duration than at low-elevation sites (Table 2). Flowering showed pronounced asynchrony, with the timing of flower opening varying among both individual flowers and different plants. Likewise, fruit formation in the species was also highly asynchronous across all study sites, commencing from the 2nd week of July and continuing till the 2nd week of September. The fruit, classified as a follicle, undergoes numerous morphological changes before achieving maturation. The entire process of fruit formation spans 38–50 days, resulting in a mature fruit with an oblate shape and ca. 7mm diameter (Fig. 2D). Furthermore, the species exhibits asynchronous seed formation due to the asynchronous anthesis and fruit formation at all sites. Seed formation initiates in the 2nd week of August and extends up to the 1st week of October. There is also asynchrony in the maturation of seeds between terminal and lateral inflorescence branches, with seeds on the terminal branch maturing first, followed by the maturation of seeds on lateral branches. The seed maturation takes place acropetally and Seeds were borne in purplish-back berries (Fig. 2E). Mature seeds were angulate, smooth, reniform in shape, and black-colored. Finally, the plant species undergo senescence marked by the withering of the aerial shoots (Fig. 2F). The phenophase of senescence begins in September (3rd week) and completes in October (4th week). The duration of senescence ranges from 47 days for Drung to 31 days for Doodhpathri (Table 2). P. acinosa completes the entire lifecycle within a period of 7 to 8 months (Fig. 3). The prolonged duration of aerial shoots facilitates the production of numerous reproductive units and their persistence for longer periods, contributing to its enhanced survival in natural habitats. All flowering variables (moment, intensity and duration) varied considerably across the selected sites. The values of these variables were maximum at low elevation sites and minimum at high elevation sites (Table 3). The values of flowering variables varied significantly across study sites. For instance, the maximum values for flowering variables were recorded at Drung: moment was 28 ± 1.5 days, intensity was 789.33 ± 5 flowers and duration was 59 ± 2 days. While the minimum values for flowering variables were recorded at Doodhpathri: moment was 24 ± 0.5 days, intensity was 730.67 ± 2.2 flowers and duration was 22.3 ± 1.2 days.
sites in Kashmir Himalaya.
|
Variable (in days) |
Study sites |
|||
|---|---|---|---|---|
|
Drung |
Gogaldara |
Gulmarg |
Doodhpathri |
|
|
Moment |
28 ± 1.5 |
27 ± 1 |
25 ± 1.2 |
24 ± 0.5 |
|
Intensity |
789.33 ± 5 |
750.67 ± 2.5 |
766.00 ± 3.1 |
730.67 ± 2.2 |
|
Duration |
59 ± 2 |
57 ± 1.6 |
54 ± 1 |
52 ± 0.9 |
Phenology holds a key position in the present global-change research scenarios, given its role in monitoring, understanding, and predicting the timing of recurring climate-related biological events, including sprouting, leaf formation, flowering, fruiting, and senescence (Rosenzweig et al., 2008; Morellato et al., 2016). It serves as a tool for evaluating climate change impacts on plant growth and development and ultimately determines the ecological and evolutionary success of plants in changing environmental conditions (Cornelius et al., 2012; Morellato et al., 2016). Understanding phenology, especially flowering phenology, is crucial for devising effective conservation strategies and large-scale cultivation of alpine plants that are susceptible to climate change (Bernardello et al., 2001). Our results revealed that the phenophases in P. acinosa varied significantly across selected sites along an elevation gradient. At the low elevation site (Drung) all phenological events from sprouting to senescence started much earlier than at the high elevation site (Doodhpathri). These findings are in line with Rafferty et al. (2020) who also reported advancement in phenological events at lower elevations compared to higher elevations. The potential explanation for this disparity lies in altitude-dependent variations in climatic factors, especially precipitation and temperature (Bhattarai et al., 2021). Temperature is the most important factor that governs plant phenology (Cornelius et al., 2012; Hassan et al., 2022). The early sprouting in low elevation Drung populations may be linked to advanced hormone signaling for the sprouting of juvenile rhizomes (Gordo and Sanz, 2010; Moore and Lauenroth, 2017; Dorji et al., 2020). These results conform with studies carried out on other plant species (Long-Xing et al., 2008; Julien and Sobrino, 2009). The delay in sprouting initiation at higher elevations may be attributed to extended winters, lower temperatures, and inadequate moisture content (Zettlemoyer et al., 2017; Gremer et al., 2020). Phenophases exhibit high sensitivity to ecological conditions, especially temperature, serving as reliable biological indicators of climate (Negi et al., 2012). Studies on plant phenology and phenophase patterns in alpine environments have offered vital insights into the responses of different plant species to varying climatic conditions along various elevation gradients (Chen et al., 2018; Stucky et al., 2018). Elevation influences phenological phases primarily through a temperature drop of approximately 0.6°C for every 100 meter rise in elevation (Barry, 1981). In many plant species, exposure to high temperatures successfully releases bud dormancy (Rohde and Bhalerao, 2007).
In the present study start and duration of the reproductive phase (anthesis, fruit and seed formation) and flowering variables (moment, intensity and duration) also varied from site to site with the maximum and minimum values at Drung (low elevation) and Doodhpathri (high elevation) respectively. This may be due to high temperatures and light intensity at low elevations (Van der Kooi et al., 2019). The onset and duration of the flowering phase, as well as the relative duration of the male and female phases, influence the flower visitation rate and pattern of pollinators, thereby affecting the success of the sexual cycle (Liu et al., 2021). Flowering phenology is crucial for plant community structure, management, conservation, stability of mutualistic communities, essential ecosystem services, and plant-pollinator interactions (Thébault and Fontaine, 2010; Garibaldi et al., 2013; Morellato et al., 2016). Floral evocation is an important event in flower morphogenesis and overall development (Smitha and Thondaiman, 2016). Phytolacca acinosa exhibited variations in flower longevity and highly asynchronous flower anthesis both within a population and across populations in different habitats. Similarly, asynchrony in flowering and variation in flower longevity was observed in Ferula jaeschkeana across different habitats along the elevation gradient (Yaqoob and Nawchoo, 2016). Asynchronous anthesis promotes cross-pollination and ensures prolonged availability of pollen for successful pollination and fertilization (Shabir et al., 2013). Variations in flowering phenology impact the reproductive success of the plants in alpine regions. This represents a key trait, as changes in floral evocation can result in reduced reproductive effort (Schwartz, 2003). The prolonged phenological durations including extended vegetative growth and flower longevity, early sprouting, asynchronous anthesis, and longer flowering durations are key strategies enabling plants to cope with changing environmental conditions and influence their reproductive success and distribution patterns (Morton and Rafferty, 2017; Li et al., 2016). Hence, evaluating the phenological spectrum of plant species is essential for their successful conservation and restoration. phenological data is at the core of conservation programs aimed at the restoration of plant communities and the reintroduction of threatened plant species. Phenological parameters offer crucial metrics that can be readily recorded and directly applied to an evolving conservation approach focused on preserving ecological processes, besides concentrating on endangered species or forest structures (Morellato et al., 2016; Dronova et al., 2021).
Phenology involves monitoring and predicting the timing of plant species’ biological events and is strongly linked to their growth, reproduction, and survival. Understanding phenology is crucial for devising effective conservation strategies and large-scale cultivation of alpine plants. Our study is the first attempt that provides useful insights into the phenology of P. acinosa across different habits along an elevation gradient in Kashmir Himalaya. The present study revealed significant variability in the initiation, completion, and duration of phenophases across the selected sites along the elevation gradient. At the low elevation Drung population, phenophases such as sprouting, bud formation, anthesis, and fruit formation commence earlier compared to the high elevation Doodhpathri population. All phenological variables (moment, intensity, and duration) were also highest at low elevation sites. The plasticity in the life cycle or biological events is important for the species to adapt to varying environmental pressures prevalent in these habitats. The advancing and delaying of phenophases in response to ecological conditions are essential strategies employed by the target species to maximize reproductive success. Global climate change, marked by rapid warming and climatic disruptions, especially during reproductive phases has significantly affected the reproductive output of species growing at higher elevations. The knowledge of phenological attributes is vital in contemporary conservation biology. The phenological data from this study will assist in formulating effective strategies for the restoration and conservation of the target species.
Acknowledgments
We are grateful to the research scholars of PRBGPR Laboratory, Department of Botany, University of Kashmir, for their kind assistance and support during the present study.
Author contributions
Junaid A. Magray: Conceptualization; Methodology; Data collection; Curation and analysis; Software; Visualization; Writing-Original draft. Bilal A. Wani: Data collection. Tajamul Islam: Data collection; Curation and analysis; Writing-Original draft; Writing-Review and Editing. Hanan Javid: Data collection. Aijaz Hassan Ganie: Conceptualization; Supervision; Investigation; Validation; Writing-Review and Editing. Roof Ul Qadir: Data collection. Irshad A. Nawchoo: Conceptualization; Supervision; Investigation; Validation; Writing-Review and Editing. All authors contributed to the article and approved the submitted version.
Funding
Junaid A. Magray, Bilal A. Wani and Tajamul Islam highly acknowledges the University Grants Commission, Govt. of India under MANF-201920-JKO416200268, MANF-2018-19-JAM-100111 and 924/(CSIRNET JUNE-2019) respectively for providing financial assistance as Junior Research Fellowship.
Data availability
The data used in this manuscript is available in the manuscript.
Ethics declaration
Competing interest
The authors declare they have no competing interests.
Plant ethical statement
The plant material was collected from different sites in Kashmir Himalaya. The plant specimens were identified by Akhtar H. Malik and a voucher specimens were deposited at University of Kashmir Herbarium (KASH-3797,3798,3799,3800).
Ethics approval and consent to participate
A prior permission was obtained to collect the plant material used in the present study. The authors confirm that all methods were carried out by relevant guidelines and regulations
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No competing interests reported.