Evaluating the role of phenology in managing urban invasions: A case study of Broussonetia papyrifera

Journal Pre-proof Evaluating the role of phenology in managing urban invasions: a case study of Broussonetia papyrifera Ikramjeet Maan, Amarpreet Kaur, Harminder Pal Singh, Daizy R. Batish, Ravinder Kumar Kohli

PII:

S1618-8667(19)30718-6

DOI:

https://doi.org/10.1016/j.ufug.2020.126583

Reference:

UFUG 126583

To appear in:

Urban Forestry & Urban Greening

Received Date:

18 September 2019

Revised Date:

2 January 2020

Accepted Date:

2 January 2020

Please cite this article as: Maan I, Kaur A, Singh HP, Batish DR, Kohli RK, Evaluating the role of phenology in managing urban invasions: a case study of Broussonetia papyrifera, Urban Forestry and amp; Urban Greening (2020), doi: https://doi.org/10.1016/j.ufug.2020.126583

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Evaluating the role of phenology in managing urban invasions: a case study of Broussonetia papyrifera

Ikramjeet Maana, Amarpreet Kaurb, Harminder Pal Singha,*, Daizy R. Batishb,*, Ravinder Kumar Kohlib,c

Department of Environment Studies, Panjab University, Chandigarh 160014, India

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Department of Botany, Panjab University, Chandigarh 160 014, India

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Central University of Punjab, Mansa Road, Bathinda 160014, India

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Running head: Phenology of invasive tree Broussonetia papyrifera

Corresponding author: Harminder Pal Singh, Daizy R. Batish; Tel.: +91 172 253 4005,

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4095; Fax: +91-172-2783817; E-mail: [email protected]; [email protected]

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Graphical abstract

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Abstract

Multidisciplinary approaches are required for the management of invasive woody species in urban areas. In this context, phenological studies are a useful tool to understand tree

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development and devise suitable management strategies under urban forestry conditions. The significant role of phenology in attributing competitive advantages to invasive alien species

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has also been long recognized by community ecologists. Therefore, phenological calendars of

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invasive species may help in their detection, management and mitigation. In the present study, an attempt has been made to understand the invasive potential of an emerging invasive tree of urban landscapes, Broussonetia papyrifera (paper mulberry; Moraceae), through its phenological assessment by using a standardized numerical scale, BBCH (Biologische Bundesanstalt, Bundessortenamt, CHemische Industrie). The tree is native to southeastern and eastern Asia and the Pacific Islands, and is rapidly spreading across various tropical and

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subtropical regions. The phenology of B. papyrifera was described in eight principal growth stages (PGSs) with two developmental cycles in a year, presented as primary (January-June) and secondary (June-November) flushes. The observations were further supported by the corresponding dates, photographs, meteorological data (air temperature, precipitation and photoperiod) and climatic water balance of the study area. Results suggest that the occurrence of two developmental cycles, a prolonged reproductive period, strategy to attract frugivores with brightly colored pulpy fruits, and ability to survive under a wide temperature range help

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in the spread of B. papyrifera. The phenological scale provided in this study describes accurate and precise developmental stages of the tree that can be used to devise efficient

management strategies for its control in urban areas. The information can also be exploited

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for assessing the climatic conditions required for its prevalence, predicting its future

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geographic range, and further research.

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Keywords: developmental cycle; paper mulberry; plant invasion; reproductive growth stages;

Abbreviations

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urban forest interfaces; vegetative growth stages

BBCH: Biologische Bundesantalt, Bundessortenamt and CHemische Industrie

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PGS: Principal Growth Stage

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SGS: Secondary Growth Stage F: Female tree M: Male tree

T: Temperature P: Precipitation PE: Potential evapotranspiration

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AE: Actual evapotranspiration WD: Water deficit

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WS: Water surplus

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1. Introduction Since the mid-20th century, urban ecosystems have been facing significant environmental threats from invasive alien species due to the increased urbanization, overexploitation, and habitat fragmentation (Alston and Richardson, 2006; Wang et al., 2018). Residential communities and landscape managers of urban areas may further aggravate this process by propagating invasive, exotic plant species for horticultural applications (Bañuelas et al., 2019). Such species escape their cultivated zones and spread in nearby areas, especially the

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highly disturbed regions of urban forest interfaces (Alston and Richardson, 2006; Bañuelas et al., 2019). Multidisciplinary approaches are required for the management of invasive woody species in urbanized areas. In this context, phenological studies can help us

forestry conditions (Ramírez and Davenport, 2016).

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understand invasive tree development and devise suitable management strategies under urban

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Phenology is a scientific discipline addressing the timing and duration of various periodic

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events in a species’ life cycle (Lieth, 1976). From the time plant invasion has received due attention from ecologists, phenology has been acknowledged for its significance in structuring the invasion paradigm (Crawley et al., 1996; Fridley, 2012). Community ecology

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theory put forward by Wolkovich and Cleland (2011) emphasizes the phenological disparities between exotic and native species and their consequent implications. Martín-Forés et al.

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(2018) suggested that along with other performance traits, unique phenological characteristics

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are vital for invasiveness in exotic plant species. Pertinent phenological attributes in invasive plants include extended leaf phenology (Fridley, 2012), altered life span (Marushia et al., 2010), early leaf-out (Polgar et al., 2014), and advanced flowering phenology (Lloret et al., 2005). Thus, phenological research may assist in the detection, evaluation, management and mitigation of invasive species (Bradley, 2014; Morellato et al., 2016). Exhaustive knowledge about the life-cycle events of an invasive species may generate novel and creative

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management ideas or may supplement the efficacy of ongoing management approaches (Marushia et al., 2010). Development of phenological growth guides for different invasive species may, therefore, be useful in assessing their invasive tendencies, predicting their responses towards changing environmental conditions and, more importantly, in devising suitable strategies for their management (Jaryan et al., 2014; Kaur et al., 2017). For standardised phenological descriptions of plant species, the BBCH (Biologische Bundesantalt, Bundessortenamt and CHemische Industrie) scale has been used for decades

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(Bleiholder et al., 1989; Hack et al., 1992). The BBCH scale explains the life cycle of a plant species in a two-digit code, its first digit reflecting the principal growth stage (PGS) and the

second digit signifying the secondary growth stage (SGS). Both PGS and SGS are described

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using ordinal numbers (0 to 9), with each principal growth stage defining the major phases and the associated SGS precisely specifying minor growth characteristics within particular

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PGS. This scale has been advantageous in studying the vegetative and reproductive stages of

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annual, biennial and perennial plants, in a simplified and systematic manner. It has often been used to describe growth stages of agricultural and horticultural species (Meier et al., 2009; Alcaraz et al., 2013; Pham et al., 2015; Tejera and Heaton, 2017). Recently, such studies have

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also been conducted for invasive alien species, such as Chinese tallow tree, (Sapium sebiferum; Jaryan et al., 2014) and parthenium weed (Parthenium hysterophorus; Kaur et al.,

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2017), highlighting their most competitive growth stages. Ramírez and Davenport (2016) also

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recommended that the scale be appropriately applied to phenological studies pertaining to urban forestry.

Broussonetia papyrifera (L.) Hert. ex Vent. (paper mulberry; Moraceae) is a dioecious

deciduous tree, native to southeastern and eastern Asia, and the Pacific Islands (Huston, 2004; Gonzalez-Lorca et al., 2015). It has been popular in various parts of the world, specifically in Asia, having been utilized for almost 1,500 years for silviculture, the

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manufacture of paper and tapa cloth, and ornamental purposes. Apart from that, the tree is used in Chinese traditional medicine, as it possesses anti-inflammatory, antinociceptive, antihepatotoxic, antimicrobial, cytotoxic, and antioxidant activities (Ko et al., 2008; Wu, 2012). Due to its high economic, aesthetic and medicinal value, B. papyrifera has been intentionally dispersed across the globe. The tree has been widely planted in urban forests and has become naturalized in different parts of India, Ghana, southern Europe and the USA (Gonzalez-Lorca et al., 2015). The tree is designated as an invasive species in many

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countries, including Argentina (Ghersa et al., 2002), USA (Morgan et al., 2019), Philippines (Florece and Coladilla, 2006), Pakistan (Malik and Hussain, 2007) and Ghana (Bosu et al., 2013). In India, although the history of introduction of B. papyrifera is difficult to trace,

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reports from the 1950s described its utilization in silviculture (Krishnaswamy, 1957) and its

B. papyrifera as an invasive alien in India.

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naturalization in the sub-Himalayan region (Parker, 1973). Later, Khuroo et al. (2012) listed

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High reproductive potential, by means of both sexual and vegetative propagation, is reported to be the major reason for its fast spread (Morgan et al., 2019). Due to vigorous growth, the tree forms monocultures in wastelands, degraded forest areas, and along

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roadsides. Moreover, its large and dense canopy does not allow the understory to proliferate. This results in exclusion of many other useful indigenous plant species, including broad-

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leaved trees (Bosu et al., 2013). Therefore, the areas invaded by B. papyrifera are reported to

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have lower floristic diversity and species richness (Malik and Husain, 2007; Bosu et al., 2013). Continuous spread of the tree is, therefore, a matter of serious concern and implies a need for effective management strategies. Considering the invasion potential of B. papyrifera and its ecological impacts, the current study was conducted to document its life cycle, aiming to assess the phenological characteristics facilitating its invasion and associated management implications.

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2. Materials and Methods 2.1. Research area The study was conducted on the campus of Panjab University, Chandigarh, India (30º45ʹN; 76º45′E; 348 m above sea level) for two consecutive years, 2015 and 2016. The study area is in a well-developed city located in the lowest belt of the Shivalik ranges of the Himalayas. It has a humid subtropical climate with absolute air temperature (as recorded in 2017-18)

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ranging from a minimum of ~3°C during winters (November to February) to a maximum of ~45°C during summers (April to July). Average annual rainfall (as recorded in 2017) is reported to be ~974 mm, most of which is recorded during the monsoon period (July to

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September) (Chandigarh Administration, 2019). The soil is a sandy loam (Psammentic

hapludalf; Batish et al., 2009). The well-planned design of Chandigarh has resulted in the

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expansion of nearby suburban townships and industrial areas. Therefore, the natural forest

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ranges surrounding the city (e.g., Kansal forests, Nepali forests, Patiali ki Rao) have faced various kinds of pressures including landscape fragmentation, deforestation, and overexploitation. Formal records of the introduction of B. papyrifera in the city are not

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available, but city forestry officials indicated that it had been intentionally planted in parks, along roadsides and within educational campuses (personal communication). Thereafter, the

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tree escaped and spread throughout wastelands, urban and sub-urban areas, and into urban-

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forest interfaces.

2.2. Research methodology 2.2.1. Data collection Six trees of B. papyrifera (three male and three female) located on the campus of Panjab University were selected for collecting phenological data. Panjab University has an area of

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550 acres (2.2 km2). The campus is landscaped with various avenue and ornamental trees planted in the parks, botanical garden and along the roadsides (Panjab University, 2019). Winds are generally light blowing from the northwest to southeast direction with the speed up to 5.144 ms‒1 (Chandigarh Administration, 2019). The trees selected for the study were mature, 12-15 m in height and 70-85 cm in circumference (measured at breast height [1.4 m above the ground]). A sample of the tree along with male and female reproductive parts has been deposited in the herbarium of the Department of Botany, Panjab University, Chandigarh

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(plant accession number: PAN21500). Five random branches (n=30), with the minimum height of 1.5 m above the ground level, were tagged in each tree. The selection was random, but care was taken so the

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observations could be conveniently made. The two-digit BBCH coding system was used to describe the phenological growth stages of the tree on the basis of observed/measured

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morphological traits, following Hack et al. (1992) and Finn et al. (2007). Two nodes per

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branch were monitored in all the trees for documenting the vegetative and reproductive stages. Most of the phenophases were slow enough to allow for observations twice a week. However, fast developing phenophases were studied on a daily basis. The date corresponding

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to a particular growth stage was noted when at least one node in all the tagged branches reached that particular stage, and the total number of days taken for the completion of each

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PGS was calculated. Since B. papyrifera is a dioecious plant, the reproductive development

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in the female and male trees are described in the results by F and M, respectively. In addition, the growth stages were digitally photographed (Olympus SZ-15, Tokyo, Japan), and the most suitable photograph was chosen from the camera’s image database for pictorial representation. To relate observed phenological data with microclimatic conditions, the meteorological data for daily air temperature (T [°C]) and precipitation (P [mm]), prevailing

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during the observation period, were obtained from the India Meteorological Department, Chandigarh, located within 5 km of the study area. In addition to that, data for daily photoperiod (hours) were collected from a local, daily newspaper (Chandigarh Tribune).

2.2.2. Data analysis In the two consecutive years of study (2015 and 2016), no major differences were observed in meteorological conditions. Average monthly air temperature and precipitation did not vary

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significantly between the two years. Consequently, no significant variations in the duration of growth stages of B. papyrifera were noticed during the two years of study, and the average data have been presented. Further, considering the importance of moisture in woody plant

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survival and adaptation, potential evapotranspiration (PE), actual evapotranspiration (AE), water deficit (WD) and water surplus (WS) were estimated for the study area and study

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(2010) by using local meteorological data.

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species following Thornthwaite (1948), Mather and Yoshioka (1968) and Dourado-Neto et al.

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PE (mm) was calculated by expression:

where, T is the average monthly air temperature (°C)

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I is the summation of monthly index (i) for twelve months, obtained by equation

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a is an exponent calculated using equation

AE (mm) was calculated by expression: For wet season (when P-PE≥0)

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For dry season (when P-PE<0)

where S is the soil water storage change between two consecutive months (mm) Soil water storage (S; mm) was calculated using following equation

where SWHC is the soil water holding capacity (mm) calculated by equation

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where θf is the field capacity (cm3 cm-3); θw is the wilting capacity (cm3 cm-3); z is the effective root depth (mm) of B. papyrifera

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AWL is the accumulated potential water loss (mm) calculated as

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where i is an index of number of chosen period (For January, February, ..... December, i = 1,

WD (mm) was calculated as

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WS (mm) was calculated as

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2, ..... 12)

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For wet season (when P‒PE≥0)

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For dry season (when P‒PE<0)

3. Results The study revealed the occurrence of two developmental cycles in B. papyrifera within a single calendar year, presented as primary flush (JanuaryJune) and secondary flush

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(JuneNovember). The persistence of two developmental cycles can play a significant role in successful invasion of this tree. The primary flush was observed in the spring, whereas the secondary flush commenced during the summer monsoon season. Eight of the ten principal growth stages (PGSs) were identified in B. papyrifera according to the extended BBCH scale. The vegetative growth stages were described by bud development (PGS 0), leaf development (PGS 1), and shoot elongation (PGS 3); the reproductive growth stages included inflorescence emergence (PGS 5), flowering (PGS 6), fruit development (PGS 7) and

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maturity (PGS 8); and the post-reproductive stage was marked as senescence (PGS 9) (Table 1; Fig. 1; Fig. 2). Most of the developmental stages occurred simultaneously, and thus, the duration of various growth stages often overlapped (Table 1). The minimum temperature

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during the entire study period (Jan 2015- Dec 2016) was observed to be 2.1°C (on Jan 24, 2016), and the maximum was observed to be 43.4°C (on May 24, 2015).

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The phenological cycle commenced with the development of a small bud, covered with a

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brown scale, at the nodal regions of the branches (Two-digit code, 00). Later on, the bud began to swell, as determined by its enlarged size and the scale’s altered color (01). At the

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end of the bud swelling, the dark purplish scale began to separate, slightly disclosing the green color of the bud (03). By the end of bud break, green leaf tips were clearly visible above the scale (09) (Table 1; Fig. 1a). These events are described by PGS 0 and took place

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during the early spring (Jan-Feb) in the primary flush and during the early monsoon (June-

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July) in the secondary flush (Fig. 2). It took 33 days for the tree to complete bud development during the primary flush and 26 days during the secondary flush (Table 1). The average temperature and average photoperiod for PGS 0 during primary flush (January-February) were 15.3°C and 10.6 h, respectively; whereas, the average temperature was remarkably high for the secondary flush (June-July), at 31.3°C with an average photoperiod of 13.9 h (Fig. 2).

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Bud development is succeeded by the unfolding of leaves, as represented by PGS 1. Each bud enclosed 3-6 leaves that were broadly ovate with pointed tips and coarsely serrated edges, and pubescent on their petioles and abaxial surfaces (11-19) (Table 1; Fig. 1a). The leaves were mostly unlobed, but some bore 3 to 5 lobes. Leaf development continued for two weeks during both flushes (Table 1). The average temperature was recorded to be 17.5°C during the primary flush (February) and 30.3°C during the secondary flush (July), whereas the average photoperiod was 11.0 h and 13.7 h, respectively (Fig. 2).

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However, as more and more of the leaves unfolded, the subsequent PGSs, such as shoot elongation (PGS 3), inflorescence emergence (PGS 5) and flowering (PGS 6), accompanied the process and proceeded concurrently (Table 1). Female and male plants were nearly

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indistinguishable until the unfolding of the first few leaves revealed the primary reproductive buds (51). Notably, the female bud was purple, whereas the male bud was slightly brown in

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color. For the females, the thread-like, sessile, light purple flowers began to open as soon as

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the inflorescence appeared, and their development coincided with an increase in the size of the sphere-headed female inflorescence (51F-59F; 61F-67F) (Table 1; Fig. 1b). The size of the globose inflorescence reached 3.0±0.13 cm in diameter, and the pistillate flowers grew to

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1.1±0.09 cm in length. The male inflorescence formed drooping catkins, but their flowers remained closed until the inflorescences reached their maximum length, a mean of 11.5±0.42

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cm (51M-59M) (Table 1; Fig. 1b). Length of the dried catkin as measured from the

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vouchered specimen (PAN21500) was 9.8 cm. The duration of PGS 5 varied remarkably between the two flushes, with the primary one taking nearly 19 days for full inflorescence development, while the secondary one completed the process within 8 days (Table 1). Apart from that, the average temperature and photoperiod increased by 10.9°C and 2.3 h, respectively, from the primary (February-March) to the secondary (July) flush during PGS 5 (Fig. 2).

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Along with the leaf and inflorescence emergence, the process of shoot elongation was also initiated. As the developmental cycle proceeded, the size of the leaves increased; and these were arranged alternately on the newly formed shoot with the first leaf being at the basal position (3139) (Table 1; Fig. 1a). Each leaf gave rise to a reproductive bud in its axil in acropetal succession, the youngest bud being in the terminal position. Although the BBCH scale described only the development of primary reproductive bud, the development of subsequent buds proceeded in a similar manner. In the meantime, light yellow, 4-lobed male

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flowers in the catkins began to open and shed pollen (61M-67M).

After fertilization, the male and female flowers withered, marking the beginning of fruit development as well as senescence (69) (Table 1; Fig. 1b). Shoot elongation also continued

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until the beginning of senescence, reaching an average maximum shoot length of 23.1±1.89

cm. At the same time, the leaves attained their maximum size, which varied between 5-25 cm

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and 7-20 cm in length and width, respectively.

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PGS 3 and PGS 6 were thus, entirely parallel and continued for 29 days during the primary flush and 17 days during the secondary flush (Table 1). Since these were prolonged

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events, the average temperature for PGS 3 and PGS 6 was recorded to be 19.4°C during the primary flush (February-March) and 30°C during the secondary flush (July-August; Fig. 2). On the other hand, the average photoperiod was recorded to be 11.4 hours and 13.4 hours

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during primary and secondary flush, respectively (Fig. 2).

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A long pause was observed between the withering of male/female flowers and the development of fruit structures, extending up to 15-20 days during both flushes (PGS 7; PGS 8). When the average daily temperature reached ~ 28°C, fruits (in the form of achenes/syncarps) began to emerge from the female inflorescences (71). This was the only growth stage where temperature conditions were similar during both flushes (Table 1). In contrast, the average day length varied by nearly one hour between the primary (13.1 h;

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April-May) and the secondary flushes (11.7 h; September-October; Fig. 2). The fruiting period during the secondary flush was noticeably shorter, at 1 month and 15 days, than it was during the primary flush, when it took nearly 2 months for full development/maturation of achenes (71-79; 81-89) (Table 1; Fig. 1b). The fully developed fruits were 2.5-3.5 cm in diameter, bright orange in colour, globose in shape and arranged in the form of aggregates. The fruit is not only visually attractive, but also edible, due to its pulp and juice content. This is a strategy to attract dispersers for spread of its seed, which plays a crucial role in invasion.

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Each dried fruit aggregate produced approximately 228.3±18.4 seeds that were light brown to black and weighed 133.4±5.85 mg/1000 seeds. Year-round reproduction and production of seeds assist the invasion process in B. papyrifera.

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Each phenological cycle closed with a single period of senescence (PGS 9). Although, the early signs of senescence, such as leaf yellowing and initial leaf fall, started even before fruit

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development, it took three to four months for the tree to turn entirely leafless (91-97).

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Senescence observed after the primary flush continued for 106 days (March-June), when it was succeeded by the initiation of the secondary flush (Table 1; Fig. 1c; Fig. 2). In contrast, after going entirely leafless within 118 days (August-November) during the secondary flush,

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trees remained leafless in the month of December when low temperatures were unfavourable for another developmental cycle (Table 1; Fig. 2). The average temperature and average

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photoperiod for PGS 9 during the primary flush (March-June) were 28.2°C and 13.0 hours,

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respectively; whereas, the average temperature was remarkably high for the secondary flush (August-November), at 26°C with an average photoperiod of 11.7 hours (Fig. 2). Comparing the total precipitation (P) in both the flushes, it was observed that the

secondary flush experienced nearly 3 times higher rainfall (897.4 mm) than did the primary flush (284.5 mm). Similarly, potential evapotranspiration (PE) and actual evapotranspiration (AE) also varied between both the flushes, with the primary flush witnessing PE of 784.6 mm

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and AE of 533.2 mm, whereas PE of 974.6 mm and AE of 855.5 mm were recorded during the secondary flush. It has also been concluded that the soil was water deficient (WD= 251.3 mm; WS= 31.1 mm) during the primary flush, but, in contrast, water surplus conditions (WD= 119.1 mm; WS= 195.7 mm) prevailed during the secondary flush (Table 2).

4. Discussion 4.1. Phenophases of B. papyrifera in relation to invasion

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Recent surveys have documented how phenology can be strongly linked to the superior competitive ability of invasive plants (Marushia et al., 2010; Fridley, 2012; Polgar et al.,

2014). In contrast to natives, invasive species generally leaf out, bloom or fruit earlier and for

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longer periods, sustain a broader niche, and demonstrate better phenological

plasticity/adaptability (Morellato et al., 2016). The phenological descriptions of invasive

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species may disclose remarkable attributes driving their invasion potential, while also

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highlighting suitable management tricks for their control (Jaryan et al., 2014; Kaur et al., 2017). The BBCH scale, used herein to illustrate phenological adaptations of B. papyrifera, has been successfully applied in other studies of horticultural trees and urban forestry

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(Alcaraz et al., 2013; Ramírez and Davenport, 2016). In the present study, we explain eight phenological growth stages of B. papyrifera by

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using an extended BBCH scale, derived from data collected in Chandigarh, India. Most of

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our observations are consistent with published morphological and phenological descriptions of this tree (Krishnaswamy, 1957; Whistler and Elevitch, 2006; CABI, 2019); however, some of our observations differ from previous findings. For instance, considerable variability has been reported in the shape of leaves of B. papyrifera, with some studies ascertaining the leaves to be entirely unlobed and others reporting them to be highly lobed (Whistler and Elevitch, 2006; CABI, 2019). In our study, both types of leaves were encountered, with the

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younger ones being more lobed than ones that developed earlier. For another example, we recorded male catkins up to 11.5±0.4 cm long, exceeding previous reports indicating that catkins attain lengths of up to 8 cm (Krishnaswamy, 1957; Whistler and Elevitch, 2006; Yatskievych, 2013; CABI, 2019). Even considering the possibility that catkin length (8 cm) given in earlier reports was measured from dried herbarium specimens, our vouchers displayed lengths up to 9.8 cm. Considering the phenology of B. papyrifera, the first and foremost aspect is the

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occurrence of two developmental cycles within a single year, involving a primary flush (January-June) and a secondary flush (June-November). A similar surveillance in Ghana also noted this phenomenon (Kyereh et al., 2014). The reproductive phase of B. papyrifera

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continued for 7 months, constituting a major part of its life cycle, which not only enhances its reproductive output but also provides a longer window for seed dispersal. In a similar report

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from Ghana, the tree fruited twice a year, with one season producing fruits for a longer

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duration than the other (Kyereh et al., 2014). Reports indicate that invaders with gap‐filling phenology (i.e., production of fruits during seasonal lows and for longer periods) not only face reduced competition for dispersers from equally attractive native fruits but may also

Voigt et al., 2011).

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allow year‐round persistence of local dispersal agents (Gosper, 2004; Buckley et al., 2006;

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Furthermore, the fruits of B. papyrifera are brightly colored, attractive in appearance and

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highly pulpy and juicy, and meant to attract dispersal agents (Kyereh et al., 2014; Agyeman, 2016). In Ghana, its seeds are known to be dispersed over large areas by frugivorous birds and bats (Agyeman, 2016). Diverse dispersal agents, such as insects, birds, and mammals, ensure its long-distance spread (Kyereh et al., 2014).

4.2. Relationship between phenology of B. papyrifera and climatic variables

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Upon relating meteorological data to the plant’s developmental stages, certain important observations were made. We observed that fruit development (PGS 7) was the only growth stage where temperature conditions were similar during the primary and secondary flushes (Table 1). We therefore hypothesize that an average daily temperature of about 28°C is required for fruit development in B. papyrifera. Previous findings also suggested that the climatic factors play an effective role in plant vegetative and reproductive performance. Growth rates, biomass allocation patterns, and flowering phenology in different populations

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of the invasive ragweed, Ambrosia artemisiifolia, in Frankfurt am Main, Germany were found to be strongly related to environmental attributes, such as the latitudinal gradient

(directly connected to photoperiod regimen), temperature and precipitation (Leiblein-Wild

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and Tackenberg, 2014). Latitudinal trends also significantly affected growth and reproductive characteristics in the invasive species, Phytolacca americana, in central and southern China

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(Xiao et al., 2019).

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Furthermore, a wide range of daily temperatures was observed (2.1°C-43.4°C) during different growth phases of the tree. Similar observations in Florida pointed out that B.

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papyrifera can thrive under a wide range of climatic conditions (Morgan et al., 2019). Low temperature conditions can cause winter injury in woody species, limiting their growth and development (Widrlechner et al., 2012). However, B. papyrifera is known to be a chilling

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tolerant woody species that can endure frost conditions and survive temperatures as low as

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‒25°C (Peng et al., 2015; Pi et al., 2017). In fact, the tree has been found to spread well within USDA Hardiness Zone 6, which experiences an average annual minimum temperature of ‒17.8 to ‒23.3°C (Kartesz, 2015). Further in our case, the study area lies in subtropical region (Plant Hardiness Zone: 10b; Widrlechner et al., 2012) and, therefore, never experiences such extreme low temperatures. At the lowest (2.1°C) and highest temperatures (43.4°C) recorded during the entire study period, B. papyrifera continued its developmental

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cycle. Therefore, we cannot say that extreme temperatures observed during the present study influenced life history events in B. papyrifera, except in December when the tree faced vegetative dormancy. The dormancy in deciduous trees is mainly driven by temperature and photoperiod. However, these environmental cues alone cannot fully explain the process. Endodormancy also plays an equally important role and during this phase the growth is arrested by internal physiological factors (Bilavik et al., 2015). We have also established that developmental stages in this tree are relatively insensitive

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to photoperiodic conditions at about 30° N latitude, as is evident from the photoperiod variation of comparable PGSs between primary and secondary developmental cycles. Studies assessing the effect of photoperiod on phenological aspects of B. papyrifera are not available,

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but a report suggests that most members of the Moraceae are day-neutral (Milton, 1991) with regard to leafing, flowering and fruiting.

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Upon exploring the relationship between two developmental cycles and climatic water

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balance, we observed that the primary flush experienced water deficit conditions while the secondary flush flourished during water surplus conditions. Ample moisture may contribute to the shorter duration of different vegetative and reproductive phenophases during the

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secondary flush. Water availability and the timing of rainfall are known to influence phenological patterns in deciduous species (Monasterio and Sarmiento, 1976; Valdez-

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Hernández et al., 2010; Fitchett et al., 2015). In contrast, senescence was faster by nearly 15

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days during the primary flush, which could also be attributed to the low precipitation and water deficit conditions during that period. Vál'ková and Jančo (2017) reported similar results where most of the broadleaved trees in their study experienced early leaf yellowing and leaf fall under low precipitation conditions or extended drought. Such relationships between life history traits and soil/climatic factors can help define this species’ niche requirements, which might be used to predict its future spread to new environments.

19

4.3. Control measures based on phenology of B. papyrifera Successful implementation of control measures requires prior knowledge of the characteristic “behaviours” and adaptive strategies of a species that contribute to its invasion success (Williams et al., 2019). This allows land managers to apply control strategies at an invasive species’ most vulnerable developmental stages (Morellato et al., 2016). Here we suggest some management approaches, keeping in mind the context of urban landscapes and

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urban-forest interfaces. In B. papyrifera, mechanical control is generally the most suitable management option, and we advise targeting these trees at early reproductive stages, i.e.,

before the formation of fruit (PGS 7). Clearance of areas infested by B. papyrifera should be

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carried out before the months of April and September (between the period of dormancy [00] and initiation of fruit development [69]). However, it should be noted that this tree is capable

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of producing new shoots through stump and root suckers and, therefore, can spread even after

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mechanical removal of the aboveground parts. There are a few studies that suggest the use of mechanical methods in combination with herbicides to ensure successful management of B. papyrifera, for instance, squirting the stumps of mature trees with appropriate chemicals

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(e.g., Garlon 4®) after cutting (Apetorgbor and Bosu, 2011); manual removal followed by application of a suitable non-selective herbicides, like triclopyr or imazapyr as a spray for

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saplings and through injectors for mature trees (Marwat et al., 2010; Cowie et al., 2018). The

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leaves of B. papyrifera are rich in protein, nitrogen, and lignocellulose, and can be used as a source of high-quality feed (Xu et al., 2018; Geng et al., 2019; He et al., 2019). Therefore, saplings can also be controlled by allowing livestock to graze areas invaded by the tree, particularly during February/March, and July/August when leaves are young and nutrientrich.

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Another strategy that could be adopted for fruit-bearing B. papyrifera trees (i.e., after the tree has achieved PGS 7 and 8) is to use fruit‐spoiling insects to decrease the attractiveness of its pulpy fruits. Such biological control agents may help in repelling dispersers, especially the frugivores (Buckley et al., 2006). A study involving the fruit‐damaging fly, Ophiomyia lantana, on the invasive shrub, Lantana camara, showed that the fly affected the feeding patterns of frugivores as they avoided selecting larvae‐infested fruits (Vivian‐Smith et al., 2006). So far, no bio-control option is available for this tree, and there is a strong need to

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explore this aspect. Several natural pests of Broussonetia (12 species of fungi and 13 species of insects and mites) have been reported (Zheng et al., 2005). Of these, three fungal species, Aecidium mori var. broussonetia, Dendryphiella broussonetiae, and Phomopsis

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broussonetiae (Sacc.) Diet., are host specific to B. papyrifera (Zheng et al., 2005). Various arthropods, such as Eotetranychus spp., Tetranychus spp., are known to attack leaves and

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fruits of B. papyrifera (Bolland et al., 1998; Zheng et al., 2005). These species might be

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exploited for management of the tree. Fruit-spoiling insects can be used during April-May and September-October, whereas insects that attack leaves of B. papyrifera should be employed during February-March and July-August. Furthermore, considering the risk of

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using bio-control agent due to lack of specificity in their feeding habits, we recommend exhaustive studies under controlled laboratory and greenhouse conditions prior to testing

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these species in the field as bio-control agents.

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In addition, alternative food sources could be provided to dispersal agents by planting equally attractive, fruit-bearing native trees nearby (Gosper et al., 2005), targeting those species that have the same fruiting period as that of B. papyrifera. For instance, in India, noninvasive species with a similar fruiting period, such as Bischofia javanica (May-June), Ehretia pubescens (August-November), Ficus spp. (throughout the year), Manilkara hexandra (March-May), Ochna obtusata (May-July), Salvadora persica (March-June), and

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Walsura trifoliata (May-August) can be planted in areas invaded by B. papyrifera (Kohli et al., 2000; David et al., 2015). Utilization of leaves, roots, bark, and fruits of B. papyrifera for medicinal purposes, papermaking, feed, and fodder is another option that can be used in conjunction with its management (Xu et al., 2018; Geng et al., 2019). The phenological description provided in this study can be helpful in deciding the timing of utilization for local or industrial purposes. In addition, mapping of invasive species via hyperspectral remote sensing can also exploit

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the unique phenology of invasive species (He et al., 2011; Bradley, 2014). The exhaustive phenological description of B. papyrifera provided in our study can assist the identification of

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spectral differences between it and co‐occurring native vegetation for such mapping.

5. Conclusions

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There are relatively very few attempts to trace the phenology of invasive species with a

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standardised, descriptive system, despite the possibility that such studies can reveal valuable patterns. The data collected in the present study are informative, based on two years of observations on B. papyrifera, coded following BBCH scale, an internationally recognised

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phenological system. They can be used by landscape managers to help check the spread of this tree in urban or suburban areas and at urban-forest interfaces. Better control should be

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obtained if management of B. papyrifera can be timed to take advantage of vulnerable points

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in its annual life cycle. Further, these findings can be utilized by researchers and environmentalists for predicting its invasive potential and climatic suitability, and potential niches available for its spread. The scale may also facilitate further research based on phenology and its interactions with other local biotic and abiotic factors.

Author Contributions

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IM, HPS, and DRB designed the work. IM collected the data. IM, AK and DRB analysed and interpreted the data. IM, AK and HPS drafted the manuscript. HPS, AK, DRB, and RKK edited and contributed to the manuscript.

6. Acknowledgements This work was supported by DST-INSPIRE, India [grant number IF140697/2014/286], and

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University Grants Commission, India [grant number F. 25-1/ 2013-14 (BSR)/ 7-151/ 2007 (BSR) Dated 30/05/2014]. The scientists and technicians of the India Meteorological

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acknowledged for their contribution in this research.

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Department, Chandigarh, India, and ICAR-ICSSR, Karnal, Haryana, India are also

7. Conflict of Interest

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The authors declare that the research was conducted in the absence of any commercial or

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bark. Indian J. Pharmacol. 44, 26-30. https://doi.org/10.4103/0253-7613.91862 Xiao, L., Hervé, M.R., Carrillo, J., Ding, J., Huang, W., 2019. Latitudinal trends in growth, reproduction and defense of an invasive plant. Biol. Invasions 21, 189-201.

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https://doi.org/10.1007/s10530-018-1816-y

Xu, Z., Yang, G., Dong, M., Wu, L., Zhang, W., Zhao, Y., 2018. The complete chloroplast

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genome of an economic and ecological plant, paper mulberry (Broussonetia kazinoki×

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Broussonetia papyifera). Mitochondrial DNA B 3, 28-29. https://doi.org/10.1080/23802359.2017.1419088

Yatskievych, G., 2013. Steyermark’s Flora of Missouri, vol.3, rev. ed. Missouri Botanical Garden Press, St. Louis, and Missouri Dept. of Conservation, Jefferson City. Zheng, H., Wu, Y., Ding, J., Binion D., Fu W., Reardon, R., 2005. Invasive Plants of Asian Origin Established in the United States and Their Natural Enemies, vol.2. Chinese

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Academy of Agricultural Sciences, Beijing, and USDA Forest Service, Morgantown.

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Table 1. Description of the phenological growth stages of Broussonetia papyrifera according to the two-digit extended BBCH scale. The first digit of the two-digit code represents the principal growth stage (PGS) and the second digit represents the secondary growth stage (SGS). The overlapping SGSs are presented as concomitant stages. M and F represent reproductive development of male and female trees, respectively. Two-

Concomitant

digit

stages

Description

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code PGS 0: Bud development

(Primary flush: 33 days; Secondary flush: 26 days) -

Dormancy: Vegetative bud closed; covered with a brown scale

01

-

Beginning of bud swelling: Bud begins to swell; difference in the

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00

-

End of bud swelling: Dark purplish scale begins to separate; green

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03

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color of scale starts appearing

color of the bud visible -

Beginning of bud breaking: Green leaf tips visible

09

-

End of bud breaking: Leaf tips visible 10 mm above the scale

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07

PGS 1: Leaf development

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(Primary flush: 15 days; Secondary flush: 16 days)

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-

First leaf unfolded: First leaf completely unfolded; others unfolding; leaves light green in color

13

31/51/60

More leaves unfolded

15

33/53/61

Most leaves unfolded: Majority of the leaves unfolded; inflorescence visible

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19

35/55/65

Leaf unfolding completed: All leaves unfolded

PGS 3: Shoot elongation (Primary flush: 29 days; Secondary flush: 17 days) 13/51/60

Beginning of the shoot elongation: Shoot 10% of its final length

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15/53/61

Shoot development continued: Shoot 30% of its final length

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19/55/65

Shoot development continued: Shoot 50% of its final length

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69/90

Shoot development completed: Shoot 90% of its final length;

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leaves attained final size; color changed to dark green

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PGS 5: Inflorescence emergence (Primary reproductive bud)

13/31/60F

Inflorescence visible: Reproductive male/female bud visible

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51M/F

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(Primary flush: 19 days; Secondary flush: 8 days)

within leaves; female bud purple in color and male bud brown in color 15/33/61F

Inflorescence separated: Reproductive bud emerged out of the

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53M/F

leaves; color changes to light green

19/35/65F

Inflorescence development continued: Reproductive bud attained

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55M/F

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50% of the final size; female inflorescence formed a globose

59M/F

67F

structure and male inflorescence appeared as a pendulous catkin Inflorescence development completed: Reproductive bud attained 90% of the final size; male flowers still closed

PGS 6: Flowering

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(Primary reproductive bud) (Primary flush: 29 days; Secondary flush: 17 days) 60M/F

13/31/51F

Beginning of flower development: Sessile female flowers emerged from the bud; light purple in color and 4-lobed male flowers in the catkin begin to open; light yellow in color

61M/F

15/33/53F

Flower development continued: Female flowers attained 10% of the maximum length and 10% of the male flowers opened

19/35/55F

Flower development continued: Female flowers attained 50% of

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65M/F

the maximum length and 50% of the male flowers opened 67M/F

59F

Flower development completed: Male/female flowers fully

39/90

End of flowering: Male/female flowers withered

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69M/F

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developed; begin to dry

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PGS 7: Fruiting

(Primary reproductive bud)

(Primary flush: 55 days; Secondary flush: 44 days)

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83

75

85/93 89

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Beginning of fruit development: 10% of the achenes developed

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81/92

Fruit development continued: 30% of the achenes developed Fruit development continued: 50% of the achenes developed

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Fruit development completed: 90% of the achenes developed

PGS 8: Ripening of fruit (Primary reproductive bud) (Primary flush: 55 days; Secondary flush: 44 days)

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71/92

Beginning of fruit ripening: 10% of the achenes ripened; globose,

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fleshy and pulpy in appearance; bright orange in color 83

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Fruit ripening continued: 30% of the achenes ripened

85

75/93

Fruit ripening continued: 50% of the achenes ripened

89

79

Fruit ripened: 90% of the achenes ripened; beginning of abscission of fruits

PGS 9: Senescence

91

39/69

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(Primary flush: 106 days; Secondary flush: 118 days) Beginning of senescence: shoot growth completed; terminal bud developed; foliage still green 71/81

Senescence continued: Beginning of leaf discoloration

93

75/85

Senescence continued: Beginning of leaf fall

95

-

Senescence continued: 50% of the leaves fallen

97

-

Senescence completed: End of leaf fall

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92

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Table 2. Climatic water balance for the study area during primary and secondary flushes of developmental cycle of Broussonetia papyrifera.

February 38.9 25.1 25.1 0 13.8

P PE AE WD WS

June 145.2 277.8 182.5 95.3 0

July 280.4 210.8 210.8 0 69.6

May 28.4 246.9 128.8 118.1 0

June 145.2 277.8 182.5 95.3 0

284.5 784.6 533.2 251.3 31.1

October 21.9 104.5 91.4 13.1 0

November 9.4 44.4 34.4 10 0

897.4 974.6 855.5 119.1 195.7

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P PE AE WD WS

January 33.1 15.8 15.8 0 17.3

Primary flush March April 30.4 8.5 69.8 149.2 67.7 113.3 2 35.9 0 0 Secondary flush August September 307.5 133 181.5 155.6 181.5 154.9 0 0.7 126.1 0

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P: Average monthly precipitation in mm PE: Adjusted potential evapotranspiration in mm, as per the meteorological data for study area AE: Actual evapotranspiration in mm WD: Water deficit in mm WS: Water surplus in mm

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Legend to Figures

Fig. 1. Pictorial representation of phenological growth stages of Broussonetia papyrifera according to the two-digit extended BBCH scale. a) Vegetative growth stages, b) Reproductive growth stages, and c) Senescence. The first digit of the two-digit code represents the principal growth stage and the second digit represents the secondary growth stage. M and F represent reproductive development of male and female trees, respectively.

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For description of the two-digit coding system please see Table 1.

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Fig. 2. Schematic representation of the principal growth stages of Broussonetia papyrifera according to the extended BBCH scale, along with duration, average air temperature (T [°C])

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and day length (h) during each principal growth stage.

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