Regular Article pISSN: 2288-9744, eISSN: 2288-9752 J F E S Journal of Forest and Environmental Science Journal of Forest and Vol. 34, No. 6, pp. 435-450, December, 2018 Environmental Science https://doi.org/10.7747/JFES.2018.34.6.435 Phenological Characteristics of Species in Temperate Mixed Broad-leaved Forests of Arunachal Himalaya,

Ashish Paul1,*, Mohamed Latif Khan2 and Ashesh Kumar Das3 1Department of Forestry, North Eastern Regional Institute of Science and Technology (Deemed to be University), Nirjuli 791109, , India 2Department of Botany, Dr. Hari Singh Gour Central University, Sagar 470003, Madhya Pradesh, India 3Department of Ecology and Environmental Science, University, Silchar 788011, Assam, India

Abstract Phenological events of four Rhododendron tree species (viz. R. arboreum, R. arboreum ssp. delavayi var. delavayi, R. barbatum and R. kesangiae) was monitored in temperate mixed broad-leaved forests of Arunachal Pradesh, India. Phenological events like flower bud formation, flowering, fruit setting, fruit maturing, seed dispersal, leaf bud formation, leaf flushing, and leaf shedding were recorded. Indices i.e., phenophase sequence index (PSI), active phenophasic period of the species (APS) and index of reproductive/vegetative activity (RVA) were also calculated. Present study revealed that bark consistency, growth form and leaf pattern of the studied species have showed variations among the species. Rhododendron species exhibited the phenological events overlapping with other phenophases. The peak flower bud formation was observed during the winter; R. arboreum ssp. delavayi var. delavayi start flowering from December, while the flowering in rest three species exhibited during February to April. Fruit setting occurred during summer to autumn while fruit maturation revealed peak during November. Leaf bud formation illustrated two peaks in April and May, leaf flushing exhibited peak in June, while leaf shedding peaked during October to November. Active phenophasic period of the species were found 12 months, which revealed that species engage in various phenophase activities throughout the year. Phenophase sequence index ranged between 0.8 to 0.9 (PSI ≥0.6), signifies that species have a sequential arrangement of phenophases. Index of reproductive/vegetative activity of the species exemplified ＞1, indicate that the reproductive phenophases were dominance over vegetative phenophases. The study have provided substantial insight on the life cycle events of Rhododendron species and ecological approaches for further scientific study with recent climate change and effective management and conservation.

Key Words: phenology, phenophase, reproductive, , vegetative

Introduction (Fenner 1998). The life cycle events timing throughout the year is the key for to adapt the seasonal ecological The life cycle events are the most vital phenomena re- changes (Orshan 1989; Schwartz 2003). Systematic ob- lated to time and seasons. In temperate and Polar regions, servation of life cycle events of species is most im- changes of annual temperature play a great role in the cyclic portant for better understanding of vegetation dynamics events of development and reproduction of the flora within the intricate ecological context (Liang and Schwartz

Received: April 25, 2018. Revised: November 11, 2018. Accepted: November 21, 2018.

Corresponding author: Ashish Paul

Department of Forestry, North Eastern Regional Institute of Science and Technology (Deemed to be University), Nirjuli 791109, Arunachal Pradesh, India Tel: 91-9862035885, Fax: 91-360-2257872, E-mail: [email protected]

J For Environ Sci 34(6), 435-450 435 Phenological Characteristics of Rhododendron Species

2009). Changes in phenological events influence the re- Parmesan and Yohe 2003; Root et al. 2003). In the higher production, population existence, limitations of organisms elevational environments, the impact of climate change con- and ecosystem services (Kameyama and Kudo 2009; sidered the most pronounced (IPCC 2007) and these are Chuine 2010; Miller-Rushing et al. 2010). Phenology is severe risk to the biological diversity. Limited photo- one among the most initial and perceptible characters by synthetic activity and a very short growing season are the means of which organisms response to change of climate characteristics of high altitude regions, which interlinked (Parmesan and Yohe 2003; Parmesan 2006; Bertin 2008; with the snow or ice (Inouye and Wielgolaski 2003). Wolkovich et al. 2014). Studies on phenology are also sig- Naturally, the annual life cycle events of plant species in the nificant to understand the interactions among the species high altitude regions including alpine and montane zones and the function of community in the altitudinal gradient having temperate weathers is determined by the climatic (Fenner 1998). Generally, in high seasonal climate, like condition like, snowmelt, soil defrosting and the fulfillment temperate and dry tropics the life cycle evens of the com- of scary necessities (Inouye and Wielgolaski 2003; Körner munity largely follow the related pattern year after year with 2003; Luedeling et al. 2011). Thus, the phenology of the the alterations due to climatic changes between the years plant species of the high altitudinal regions affected by the (Fenner 1998). Most significant aspects of phenological changing global climate (Inouye and Wielgolaski 2003). studies are to explore the factors that elucidate the pheno- Phenophase represent the periodic phenomenon and logical behaviour of the species. Several studies have re- their distribution throughout the year, which constitutes the vealed the biological changes due to the present change of plants’ phenological pattern. Plants dispense phenological climate (Parmesan and Yohe 2003; Root et al. 2003; Bertin events like shoot growth, flowering, fruit setting, seed dis- 2008), particularly spring phenology in temperate regions persal, leaf shedding, etc. across the seasons of the year. (Menzel et al. 2006; Ibáñez et al. 2010). Factors like pre- These are an imperative element of the plant’s technique to cipitation, temperature, soil and photoperiod trigger the perform with the seasonal changes (Beatley 1974; Mooney phenology of plant species (Blake and Harris 1960; Lucier 1983; Diaz and Cabido 1997) and these facts are con- and Hinckley 1982; Jackson and Bliss 1984; Johansen et al. tributing to the familiarity of ecosystem function (Körner 1985; van Schaik et al. 1993; Newstrom et al. 1994a; Min 1993; Paruelo et al. 2001; Liang et al. 2011). Phenological 2000; Morellato et al. 2000; Sparks et al. 2000; Fitter and study pay for the facts on growing form and progress of Fitter 2002; Borchert et al. 2004; Menzel et al. 2005; plant species along with the environmental consequences Miller-Rushing and Primack 2008; Kalbarczyk 2009; like behaviour of flowering and fruiting (Marques et al. Seghieri et al. 2009; Körner and Basler 2010; Tooke and 2004; Zhang et al. 2006). These studies are too essential to Battey 2010; Primack and Miller-Rushing 2011; Robbirt comprehend the ecosystem processes like growth, biomass et al. 2011; Ranjitkar et al. 2013). While, edaphic factors and water stress to plants (Kikuzawa and Lechowicz 2011). (like, soil nitrogen and organic matter), canopy cover and Presently, more concentration are given to the studies on other ecological factors (Joiner and Gruis 1959; Blake and phenology owing to significant mechanism in environ- Harris 1960; Ma et al. 1997; Wielgolaski 2001; Dahlgren mental response to the global changes of climate (Morisette et al. 2007; Kudo et al. 2008; Nord and Lynch 2009) are al- et al. 2009; Korner and Basler 2010). Studies on life cycle so influencing the plant phenology. Likewise, type of fruits, events at the species level are very much important for elu- pollination and dispersal of seeds are also essential to under- cidating the reaction of plants to different micro-climatic stand the plant species flowering and fruiting patterns circumstances. Therefore, it is very significant to perceive (Bawa et al. 1985; Ibarra-Manriquez et al. 1991; Ibarra- the plant species phenological changes in regards to Manriquez and Oyama 1992; van Schaik et al. 1993; changes of climate. Moreover, owing to hilly, undulating Newstrom et al. 1994b; Wright and Calderon 1995; Poulin topography and remoteness, no extensive study has been et al. 1999; Spina et al. 2001; Bolmgren et al. 2003). carried out in the eastern Himalayan region. Santy of liter- Biodiversity dispersion and effective measures are influ- atures on phenology and insufficient research amenities is enced by the changes of climate (Walther et al. 2002; additional constrictions at species level long term records,

436 Journal of Forest and Environmental Science http://jofs.or.kr Paul et al.

especially in the eastern Himalayan region. gion of Indian . Only limited information are Rhododendron L. is the largest in the family available in few flora or taxonomic monographs in which having over 1000 species distributed throughout the life cycle events appear in the form of herbarium speci- Asia, Europe, North America and. Australia (Chamberlain mens but not as periodical field observations. The foremost et al. 1996; Fang et al. 2005; Gibbs et al. 2011). Habit of purpose of this study was to document phenological events rhododendrons ranged from tiny mat-like (2.5 cm) to large of selected rhododendrons (viz., R. arboreum, R. arboreum trees up to 40 m height consisting of evergreen, semi decid- ssp. delavayi var. delavayi, R. barbatum and R. kesangiae). uous or deciduous (Hora 1981; Mao et al. 2017) and Sympathetic life cycle events of Rhododendron species in the growing healthy in open, loose, well aerated acidic soil temperate forest of western Arunachal Himalaya will give (Ross 1998; de Milleville 2002). Besides their aesthetic and important baseline information for further scientific study sacred values, many species have ethnobotanical im- on rhododendrons with recent climate change. Keeping in portance and a preferred fuel wood in the mountainous re- view, the present study has been conducted in temperate mixed gion of Eastern Himalaya (Paul et al. 2010b) and having broad-leaved forests of Tawang and West Kameng districts of ecological and economic importance. It has good horti- Arunachal Pradesh with the objectives: (i) to examine the culture/floriculture values and under hybridization to pro- eco-morphological characteristics of selected Rhododendron duce more attractive flowers. In temperate, subalpine and species, (ii) to document the various phenological events or alpine region of Eastern Himalaya, the genus Rhododendron is phenophases of selected rhododendrons, (iii) to determine the the dominating group of plants and maintains biological degree of arrangement of vegetative and reproductive pheno- communities and services (Paul et al. 2005). Rhododendrons phases, (iv) to examine the span of phenological cycle of the se- play a significant role in ecosystem services in the high alti- lected species and (v) to determine the rapport between re- tude region as most of the rhododendrons having long last- productive and vegetative phenological events. ing evergreen leaves which help as an important nutrients storage (Monk et al. 1985). Rhododendron considered a key- stone species in the high altitude region of Eastern Himalaya (Paul et al. 2010a). It associate and support sev- eral flora (Acer pectinatum, Aconitum ferox, Aconogonon molle, latifolia, Betula alnoides, Castanopsis tribuloides, acuminatus, Daphne papyracea, Eurya acuminata, Gaultheria fragrantissima, Ilex dipyrena, Lyonia ovalifolia, Paris polyphylla, Quercus griffithii, Swertia chirata, Valeriana jatamansii, etc.) (Paul 2008). Rhododendrons are also sup- porting and providing shelter and food to varieties of wildlife (Garrulax leucolophus, Ithaginis cruentus, Lophophorus im- pejanus, Phylloscopus chloronotus, Pyrrhoplectes epauletta, bum- ble bee, musk deer, sunbirds, warblers, etc. (Basnett 2013; Basnett and Devy 2015) those are playing important role in environmental stability along the high altitude ecosystems. Rhododendrons are one among the key dominant species in temperate, subalpine and alpine regions of western Arunachal landscape with significant ecological and economic importance. Despite several studies across the world, very less scientific information presented on the phenological studies of Rhododendron species in temperate Fig. 1. Map of selected study sites in Tawang and West Kameng districts of regions of Arunachal Himalaya, the rich biodiversity re- Arunachal Pradesh.

J For Environ Sci 34(6), 435-450 437 Phenological Characteristics of Rhododendron Species

Fig. 2. Climatogram of study area (a) Paipraw and Falockchar of Tawang, (b) Sangpasa and Wangu of West Kameng districts of Arunachal Pradesh.

Ta ble 1 . Physico-chemical properties of soil, geology and land use in different study sites of Rhododendron forests Altitude Land use Parameters/Depth 0-10 (cm) 10-20 (cm) 20-30 (cm) Geology (m asl) history Paipraw 2949 Bulk density (g cm-3) 0.55±0.02 0.51±0.01 0.57±0.01 Moisture content (%) 50.81±0.73 49.59±0.69 48.72±0.77 WHC (%) 50.87±0.54 50.13±0.82 48.90±0.57 pH 3.45±0.02 3.66±0.01 3.84±0.13 Sillimanite bearing Soil Organic Carbon (%) 5.91±0.67 5.09±0.70 3.79±0.19 schists, gneisses and Total Kjeldahl Nitrogen (%) 0.51±0.03 0.31±0.01 0.25±0.02 migmatites belonging Forest Falockchar 3300 to Sela Group of rocks Bulk density (g cm-3) 0.36±0.01 0.38±0.02 0.56±0.02 of Paleoproterozoic Moisture content (%) 48.41±0.97 46.78±0.86 45.77±0.78 age (SRSAC 2007a) WHC (%) 49.56±0.20 45.92±0.60 42.40±0.51 pH 3.70±0.07 3.92±0.09 4.17±0.08 Soil Organic Carbon (%) 9.05±0.19 6.03±0.47 4.99±0.05 Total Kjeldahl Nitrogen (%) 0.44±0.01 0.34±0.01 0.26±0.03 Sangpasa 1986 Bulk density (g cm-3) 0.55±0.03 0.68±0.02 0.75±0.05 Moisture content (%) 23.46±0.35 21.98±0.63 19.17±0.26 WHC (%) 45.98±0.51 42.10±0.74 37.91±0.28 pH 4.30±0.07 4.51±0.04 4.64±0.00 Sillimanite bearing Soil Organic Carbon (%) 5.00±0.57 3.43±0.21 3.25±0.26 schists, gneisses and Total Kjeldahl Nitrogen (%) 0.42±0.06 0.26±0.01 0.17±0.01 migmatites belonging Forest Wangu 2315 to Sela Group of rocks -3 Bulk density (g cm ) 0.56±0.00 0.57±0.03 0.63±0.05 of Paleoproterozoic Moisture content (%) 25.91±0.62 23.60±0.54 22.26±0.64 age (SRSAC 2007b) WHC (%) 51.88±0.37 46.01±0.36 42.73±0.70 pH 4.44±0.03 4.50±0.02 4.56±0.00 Soil Organic Carbon (%) 5.29±0.05 2.82±0.09 4.3±0.19 Total Kjeldahl Nitrogen (%) 0.37±0.02 0.28±0.00 0.17±0.01 ±Standard error.

438 Journal of Forest and Environmental Science http://jofs.or.kr Paul et al.

Ta ble 2 . Characteristics of selected Rhododendron species

Local Altitudinal *Cold Distribution Conservation Scientific name name Habit Habitat range hardiness/ Other status India (Monpa Tribe) (masl) temperature countries (IUCN) Rhododendron Udongsheng/ Evergreen Open or mixed 1500-3500 10°F AP, HP, JK, , , LC arboreum Sm Udongminto large tree forest and pure (-12°C) Ma, Meg, Myanmar, stands Mi, Nag, , Sri Si, Utt and Lanka, WB Thailand and Vietnam Rhododendron Gidangsheng/ Evergreen Open forest, 1500-3000 10°F AP, Ma, Bhutan, China, LC arboreum Sm. ssp. Gidangminto large tree conifer and (-12°C) Meg, Mi Myanmar, delavayi var. mixed forest, and Nag Thailand delavayi (Franch.) hill slopes, forest and Vietnam D. F. Chamb. margins, valleys and rocky slopes Rhododendron Galongsheng/ Evergreen Mixed forest 2000-4000 5°F AP, Si, Utt Bhutan, China, GT barbatum Wallich Ta ma s h e n g large with other (-15°C) and WB Nepal and ex G. Don shrub or rhododendrons Tibet small tree in hill sides and thickets Rhododendron Latasheng/ Evergreen Mixed and 3000-4000 0°F AP Bhutan LC kesangiae Lasheng large tree conifer forests, (-18°C) D. G. Long & with other Rushforth rhododendrons, pure stands and in open areas with bamboos AP, Arunachal Pradesh; HP, Himachal Pradesh; JK, Jammu and Kashmir; Ma, Manipur; Meg, Meghalaya; Mi, Mizoram; Nag, Nagaland; Si, ; Utt, Uttrakhand; WB, West Bengal. *Source: https://www.rhododendron.org/descriptions. LC, least concern; GT, globally threatened (Gibbs et al. 2011).

Materials and Methods Wangu under Bomdila circle of West Kameng district of Arunachal Pradesh. The Paipraw is a primary forest domi- Study sites nated by Rhododendron arboreum whereas, Falockchar is a The study sites are located in Tawang and West Kameng mixed primary forest dominated by Rhododendron arboreum, districts of western Arunachal Pradesh. Based on the acces- Rhododendron barbatum and Rhododendron kesangiae. The sibility and availability four sites viz., Paipraw, Falockchar, Sangpasa and Wangu are the primary forests, mainly com- Sangpasa and Wangu were selected to monitor the pheno- posed of Rhododendron arboreum ssp. delavayi var. delavayi. logical events or phenophases of selected Rhododendron spe- The average monthly rainfall was recorded between 7 mm cies (Fig. 1). The selected study sites are categorized as to 500 mm while the mean monthly minimum and max- temperate mixed broad-leaved forest and Rhododendron spe- imum temperature ranged between - 2.4°C to 25.5°C. cies growing in communities or patches are the main domi- Relative humidity varied from a minimum of 47% to a max- nant evergreen tree species. Paipraw is located under Jang imum of 80% in the study area of Tawang district (Fig. 2a). circle while, Falockchar under Mukto circle of Tawang Whereas, the average monthly rainfall ranged between 1.90 district. Sangpasa is located under Dirang circle whereas, mm to 484 mm and the mean monthly minimum and max-

J For Environ Sci 34(6), 435-450 439 Phenological Characteristics of Rhododendron Species

imum temperature ranged between 1.2°C to 23.9°C. Eco-morphological characteristics of study species Relative humidity varied from a minimum of 78% to a max- imum of 89% in the study area of West Kameng district The eco-morphological characteristics, i.e., the growth (Fig. 2b) [2004-2005 meteorological data from the Rural form of the selected Rhododendron species such as season- Works Department, Government of Arunachal Pradesh]. ality, shade tolerance, bark consistency, leaf shape, fruit type The soil physico-chemical characteristics, geology and land and dispersal agents were recorded in the field based on use history of the selected study sites are represented in ground truth observation. Table 1 . Phenological events Study species Ground truth sampling was carried out during January The study species are evergreen broad-leaved trees, 2004 to December 2005 and field data were recorded fol- growing in communities or patches in the mixed temperate lowing Misra (1968). To document the phenological broad-leaved forest of Tawang and West Kameng districts events, ten healthy (without any insect affected, malforma- of western Arunachal Pradesh. R. arboreum Sm. is widely tion, etc.) individuals (≥20 cm girth) from each of the spe- distributed, occurring from western to the eastern cies were selected arbitrarily. The individuals were tagged Himalayan region of India and other neighbouring with aluminum tags from each of the two populations. The countries. R. arboreum Sm. ssp. delavayi (Franch.) D. F. individuals were selected from the girth classes (i.e. 20-150 Chamb. var. delavayi is distributed in Bhutan, China, cm gbh), height, dense crown, slope and aspect from each India, Myanmar, Thailand and Vietnam. R. barbatum of the population. The phenological study of the selected Wallich ex G. Don occurring in Bhutan, China, India, species were monitored following the standard method- Nepal and Tibet while, R. kesangiae D.G. Long and ologies (Wan and Liu 1979; Orshan 1989; Lu et al. 2006). Rushforth found in Bhutan and India (Table 2). Phenological events (vegetative and reproductive phenp- Relevant information like habit, habitat and geographic phases) were monitored monthly during January 2004 to locations (with the help of GPS: Garmin) were docu- December 2005 and data were recorded. The phenological mented for each of the species (Table 2). Herbarium speci- events or phenophases were monitored on all specific trees mens were prepared following the methods outlined by Jain monthly counts: reproductive phenophase [Flower bud and Rao (1977). The species were identified with the help formation (FBF), Flowering (F), Fruit setting (FS), Fruit of flora references (Hooker 1849; Kanjilal et al. 1939; maturing (FM), Seed dispersal (SD)] and vegetative phe- Pradhan and Lachungpa 1990; Cox and Cox 1997; de nophase [Leaf bud formation (LBF), Leaf flushing (LF), Milleville 2002; Fang et al. 2005; Polunin and Staninton Leaf shedding (LSD)]. The phenological schedules were 2006; Chowdhery et al. 2008). Several herbaria like, State averaged for each of the species and represented Forest Research Institute (SFRI) , Botanical accordingly. The vegetative growth of dolichoblasts (DVG) Survey of India (BSI) Itanagar and Shillong and Central and vegetative growth of brachyblasts (DVB) were meas- National Herbarium (CNH) Kolkata were also consulted ured based on length of branches (Orshan 1989). Three for validation of identifications. Further validation was done phenological indices viz., phenophase sequence index by consultation with Rhododendron taxonomists Mr. (PSI), active phenophasic period of the species (APS) and Kenneth Cox and Dr. Ashiho Asosii Mao. Other in- index of reproductive/vegetative activity (RVA) were also formation like altitudinal range, cold hardiness, distribution calculated and as described below. and conservation status of the examining Rhododendron spe- Phenophase sequence index (PSI) cies are also given in Table 2. Conservation status of the se- lected Rhododendron species were consigned according to To assess the degree of sequence of vegetative and re- Gibbs et al. (2011). productive phenophases, the phenophase sequence index (PSI) was calculated following Pilar and Gabriel (1998) as PSI=t (DVG+FBF+F)/[t (DVG)+t (FBF)+t (F)],

440 Journal of Forest and Environmental Science http://jofs.or.kr Paul et al.

where t is the number of months require completing the (DVG+DVB+FBF+F+FS) i.e., APS=Number of phenophases, DVG: dolicholoblasts vegetative growth, FBF: months per year in which the species shows activity with re- flower bud formation and F: flowering. The PSI values spect to the phenological events that indicate favourable varies from 0.33 to 1. The PSI value (PSI＜0.6) or close to conditions for flower bud formation, flowering, fruit setting zero indicate high degree overlap of phenophases, whereas and vegetative growth of dolicholoblasts (DVG) and bra- the index value (PSI≥0.6) or close to one signify a high chyblasts (BVG). Whereas, discarding mechanical factors degree of sequential arrangement of phenophases. like seed dispersal of dry fruits, external vectors (seed dis- persal of fleshy fruits) or those cause the reduction in the Active phenophasic period of the species (APS) body of the plant (leaf shedding). A qualitative scale of the To measure the span of phenological cycle, the active APS has been made into 1: activity throughout the year; 2: phenophasic period of the species (APS) was calculated fol- long active phenophasic period of the species (10-11 lowing Pérez Latorre and Cabezudo (2002). APS=t months); 3: medium active phenophasic period of the spe-

Ta ble 3 . Eco-morphological characteristics of selected Rhododendron species Scientific name RW GF SO ST BC S LS LI FT OS DA R. arboreum mePh T E no Rough no L to OL yes d L Wind R. arboreum ssp. delavayi var. delavayi mePh T E no Rough, Crack no L to NE yes d L Wind R. barbatum mePh S/T E no Smooth, Flaky no E to EL yes d L Wind R. keasngiae mePh T E no Rough, Crack no BE to O yes d L Wind RW, renewal buds position (mePh: Mesophanerophytes); GF, growth form (T: Tree, S/T: Small tree); SO, seasonality of assimilating organs (E: Evergreen); ST, shade tolerance; BC, bark consistency; S, spinescence; LP, leaf shape (L, lanceolate; OL, oblong-lanceolate; E, elliptic; EL, elliptic-lanceolate; NE, narrowly elliptic; BE, broadly elliptic; O, obovate); LI, leaf indumentum; FT, fruit type (d, dry); OS, organs shed rhythmically (L, leaves) and DA: dispersal agents.

Fig. 3. Phenological observations of the studied species. FBF, flower bud formation; F, flowering; FS, fruit setting; FM, fruit maturing; SD, seed dispersal; LBF, leaf bud formation; LF, leaf flushing, LSD, leaf shedding and APS, active phenophasic period of the species.

J For Environ Sci 34(6), 435-450 441 Phenological Characteristics of Rhododendron Species

and leaf pattern showed variations among the species. The selected species are mesophanerophytes, evergreen and light demander in nature (Table 3). Rhododendron species viz. R. arboreum, R. arboreum ssp. delavayi var. delavayi and R. keasngiae is multi-trunked large trees except R. barbatum, which is a large shrub or small tree in habit. R. arboreum has rough bark while R. arboreum ssp. delavayi var. delavayi and R. keasngiae has rough and cracking bark. However, R. bar- batum has smooth and flaky bark. Leaf shape varies from species to species. R. arboreum (Lanceolate to ob- Fig. 4. Time course of the reproductive phenological phases expressed as long-lanceolate), R. arboreum ssp. delavayi var. delavayi the percentage of the species that show each phenophase. Flower bud for- mation (FBF), flowering (F), fruit setting (FS), fruit maturing (FM) and (Lanceolate to narrowly elliptic), R. barbatum (Elliptic to seed dispersal (SD). elliptic lanceolate) while, R. keasngiae (Broadly elliptic to obovate) (Table 3). cies (7-9 months) and 4: short active phenophasic period of Phenological events the species (＜7 months). The APS may vary from a max- imum of 12, the species which do their activity though out Different phenological events like leaf bud formation, the year and to a minimum of 1 for the short-lived ther- leaf flushing, leaf shedding, flower bud formation, flower- ophytes in arid zones. ing, fruit setting, fruit maturing and seed dispersal of each of the selected Rhododendron species have been presented in Index of reproductive/vegetative activity (RVA) Fig. 3. All the species followed a sequential order of pheno- To assess the relationship between reproductive and veg- logical events with overlap between any three events. In R. etative phenophases, the index of reproductive/vegetative arboreum and R. arboreum ssp. delavayi var. delavayi fruit activity (RVA) of the species was calculated following Pérez maturing overlapped with seed dispersal and leaf bud for- Latorre and Cabezudo (2002) as RVA=t (FBF+F+ mation with leaf flushing. In R. barbatum and R. kesangiae FS)/t (DVG+DVB). RVA=Ratio between the sum of fruit setting overlapped with fruit maturing while fruit ma- months with reproductive phenological phases (flower bud turing overlapped with seed dispersal and leaf bud for- formation, flowering, fruit setting) and number of months mation overlapped with leaf flushing (Fig. 3). with vegetative phenological phases (vegetative growth). Rhododendron species exhibited annual flowering, however, The RVA provides the idea of various approaches of plant asynchronous flowering was observed among the species. species pertaining to time and resources used in the two While, synchronous flowering was recorded within and be- types of phenophases. The low value (RVA＜1) is the pre- tween the population. In the present study, no variations on dominance of vegetative phenophases and devote more phenological events amongst the individuals and pop- time and resources on vegetative functions to the detriment ulations were observed. of reproductive functions. On the contrary, dominant (RVA All the study species exhibited flower bud formation dur- ＞1) specifies a predominance of the reproductive func- ing autumn (September to November) to winter (December tions to the detriment of the vegetative. Whereas, the value to February) and was peaking in winter (December to (RVA=1) indicate no predominance of phenophase. February). R. arboreum ssp. delavayi var. delavayi starts flower bud formation in October while R. kesangiae in Results December. It has been observed that R. arboreum ssp. de- lavayi var. delavayi which flowered in during December to Eco-morphological characteristics of study species January while the other species flowered during January to Most of the eco-morphological characters of the studied May (Fig. 4). Fruit setting was recorded maximum during species were similar while bark consistency, growth form summer (June to August) to autumn (September to

442 Journal of Forest and Environmental Science http://jofs.or.kr Paul et al.

Ta ble 4 . Phenophase sequence index (PSI) and index of re- productive/vegetative activity (RVA) of the studied species Scientific name PSI RVA R. arboreum 0.9 2.3 R. arboreum ssp. delavayi var. delavayi 0.8 1.6 R. barbatum 0.9 2.3 R. keasngiae 0.9 2.3

Phenophase sequence index (PSI), Active pheno- Fig. 5. Time course of the vegetative phenological phases expressed as the phasic period of the species (APS) and Index of re- percentage of the species that show each phenophase. Leaf bud formation (LBF), leaf flushing (LF) and leaf shedding (LSD). productive/vegetative activity (RVA) Value of phenophase sequence index (PSI) for all se- November) for all the species while fruit maturation lected Rhododendron species ranged from 0.8 to 0.9 (PSI ≥ showed a peak in November. R. arboreum fruit matured 0.6), which is nearly one, indicates that the species have a during October to December, R. arboreum ssp. delavayi var. sequential arrangement of the phenophases (Table 4). delavayi during September to November, R. barbatum Except R. arboreum ssp. delavayi var. delavayi (0.8), the PSI showed peak fruit maturation during October to value of other three species showed similar value (0.9). The November while R. kesangiae fruit matured during active phenophasic period of the species were found 12 November to January. It was recorded that seed dispersal months for the selected species (APS qualitative scale is 1 was concentrated in November to January for all the i.e. activity throughout the year) which exhibited that the species. R. arboreum ssp. delavayi var. delavayi and R. barba- selected species are involved in different activities through- tum dispersed the seeds during September to November out the year (Fig. 3). The reproductive/vegetative activity while in R. arboreum and R. kesangiae seeds are dispersed value of the selected species ranged between 1.6 to 2.3. All during November to January (Fig. 4). the selected rhododendrons exhibited similar RVA value All the species exhibited highest periods in leaf bud for- (2.3) except R. arboreum ssp. delavayi var. delavayi (1.6). mation during April to May. The leaf bud formation of R. Index of reproductive/vegetative activity of the species arboreum and R. barbatum occurred during April to May (RVA) illustrated that RVA ＞1 for all the species, repre- while that of R. arboreum ssp. delavayi var. delavayi start senting dominance of reproductive phenophases over the from February. However, leaf bud formation of R. kesangiae vegetative phenophases (Table 4). occurred during May to June. Leaf flushing occurred in summer i.e., in the month of June for all the species (Fig. 5). The leaf flushing of R. arboreum, R. arboreum ssp. dela- Discussion vayi var. delavayi and R. barbatum occurred during May to June while that of R. kesangiae during June to August. On The study revealed that, except few morphological char- the other hand, leaf shedding revealed peak period during acters like bark consistency, growth form and leaf pattern, October and November. R. arboreum and R. kesangiae ex- the studied species have not shown great variations with hibited leaf shedding during October to December, where- time and space. The growth habit of the selected species is as, R. arboreum ssp. delavayi var. delavayi and R. barbatum large shrub or small tree and multi-trunked large tree. The exhibited leaf shedding during September to November species are light demander and evergreen in nature. (Fig. 5). Variation in bark consistency among the species was ob- served which may be considered as a useful character for identification of species. Phenological events exhibited var-

J For Environ Sci 34(6), 435-450 443 Phenological Characteristics of Rhododendron Species

iation among different Rhododendron species with respect to of flowering and fruiting during rainy season and at the ear- vegetative (leaf bud formation, leaf flushing, leaf shedding) ly dry season exhibited low seasonal variation and reproductive (flower bud formation, flowering, fruit (Cornejo-Tenorio and Ibarra-Manriquez 2007). Fruit set- setting, fruit maturing, seed dispersal) phenophasic pat- ting continued through the summer having a secondary terns, which have been revealed from life cycle events of the peak in autumn may be due to the favourable condition to study species. Although, flower bud formation in studying develop this phenological event which illustrates the various Rhododendron species displayed a long span from autumn to functional tactics of the species. Pérez Latorre and winter, but peak flowering occurred during January to May Cabezudo (2002) reported a similar incident in Quercus sub- except R. arboreum ssp. delavayi var. delavayi that starts er from Spain. Fruit maturation showed peak in November flowering during December to January. This demonstrates for all the Rhododendron species that may be due to physio- that January to May is the most favourable for logical and climatic condition that favours the species. Rhododendron flowering which may be due to the resources Rhododendron species are dispersed by wind. In con- owed to the mother plants for growth, germination and sequence, suitable dispersal season linked with the fruit ma- production. Winter temperature is the utmost significant turing/ripening and the species dispersed by wind are ripen variable for early and peak flowering of Rhododendron along in the course of the dry season (Lieberman 1982; Morellato the altitudinal gradient in the Eastern Himalayas et al. 1990; Ibarra-Manriquez et al. 1991; Batalha and (Ranjitkar et al. 2013). Sharp peak flowering in April in the Martins 2004). Cornejo-Tenorio and Ibarra-Manriquez temperate forest tree species of Kumaun Himalaya was re- (2007) reported that all the tree species showed flowering ported by Ralhan et al. (1985) from Kumaun Himalaya, and fruiting for the period of dry season in the temperate while Sundriyal (1990) reported blooming during April to forest of the Monarch Butterfly Biosphere Reserve, May in the temperate zone of Garhwal Himalaya, India. Mexico. It has been observed that seed dispersion showed However, Kudo (1993) reported that the flowering time of two peaks in autumn and in winter. This may be due to mi- Rhododendron aureum varied from mid June to late July. croclimatic and edaphic condition of the study sites that as- Kudo and Suzuki (2002) further described that flowering sist the species in this event. Pérez Latorre and Cabezudo season varied in relation to changes in seasonal temperature (2002) observed a similar results in Quercus suber of Spain. for the period of late May to early August in alpine fellfields Sundriyal (1990) however, found that seed maturation and in the Taisetsu Mountains, northern Japan. On the other dispersal coincides with rainy season (June to September) hand, Kudo and Suzuki (2004) observed that the flowering for angiosperms and in October to November for gymno- patterns varied among alpine dwarf-tree species such as sperms in temperate forest of Garhwal Himalaya. While, Rhododendron buxifolium flowered widely during March to maximum number plant species reported to bear ripen fruit May, whereas Rhododendron ericoides bloomed continuously for the period of January to February in temperate forest of through the year showed continuous flowering throughout southern South America (Amico and Aizen 2005). the year. Two species Rhododendron buxifolium and Moreover, all the selected species having profound rooting Rhododendron ericoides grow tropical high mountain and be- could help them to store accessible water for the pheno- long to subgenus Rhododendron section Vireya. However, logical events rather than seasonal impact (Sarmiento and Sharp et al. (2009) observed that rhododendrons were Monasterio 1993). On the other hand, Lieberman (1982) flowered earlier under water deficit conditions. Age of the reported flowering, fruiting, leaf flushing, leaf shedding tree influence the flowering and fruiting while, flowering demonstrated strong seasonal pattern in a tropical forest and fruiting take place earlier in older than the younger and grassland/thicket mosaic in Ghana. The present study trees (Yelemou et al. 2009). Furthermore, Batalha and revealed no variations amongst the individuals, thus ob- Martins (2004) observed that the flowering of woody spe- servations were based on per species. Similarly, there were no cies for the period of late dry and early wet season while variations amongst the populations, which might be due to flowering of herbs concurred in the late wet season in Emas common geographical area and microclimatic conditions. National Park, central Brazil. On the contrary, occurrence Vegetative growth, i.e., leaf bud formation of the selected

444 Journal of Forest and Environmental Science http://jofs.or.kr Paul et al.

species was observed during the spring, whereas leaf flush- September in Kumaun Himalaya (Pangtey et al. 1990; ing was during summer (April to August) which may be at- Negi and Singh 1992). Conversely, Pérez Latorre and tributed to warmer climatic condition and rise in temper- Cabezudo (2006) reported that growth form and phenol- ature unlike in tree species from Spain observed by Pérez ogy of Rhododendron ponticum allied with the subtropical Latorre and Cabezudo (2002; 2006). On the contrary, con- lauroid vegetation, which have associations with Quercus tinuous leaf flushing of R. kesangiae in the course of mid wet species due to its adaptation to the climatic condition. season might be attributed to inherent factors. Results cor- The selected Rhododendron species showed the sequen- respond to the outcomes of Kramer et al. (2000) who stated tial organization of phenophases. The sequential arrange- that the phenological activities of the boreal and temperate ment of phenophases of the selected species play a sub- forest tree species largely determined by temperature. stantial role in growth and survival because which helps the Present result is also in conformity with the findings of species gathering resources in the course of phenophase Nilsen (1986) who observed increased reproductive events growth (Ratcke and Lacey 1985). Similar pattern of se- of Rhododendron maximum L. with increasing radiance in quential arrangement of phenophases of plant species were Southern Appalachian Mountains. Our results confirm also reported by Rodríguez-Gallego and Navarro (2015). with the findings of Sundriyal (1990) who also observed Species have long phenological activity mainly due to more leaf flushing and production throughout the completion of duration of reproductive phenophase than the vegetative the dry period and before the raining period. Furthermore, phenophase. Thus, the species reduces the intra plant com- Lieberman (1982) reported that leaf flushing is exclusively petition and resource shortage by developing the sequential scarce to wet seasons in dry tropical forest of Ghana. All the phenophases (Pilar and Gabriel 1998). The selected species species shed their leaves during early or mid winter which exhibited similar value of active phenophasic period (12 may be due to cool and dry weather. Present results confirm months) of the species due to the same phenological events with the findings of Lieberman (1982) who also observed in spite of different eco-morphological, ecological, edaphic leaf shedding in the dry season. Leaf shedding was observed and plant species composition (Paul 2008; Pérez-Latorre et maximum during October and November, coinciding with al. 2010). The selected rhododendrons demonstrated dif- the dry period. Present observation is in accordance with ferent phenophase activities, i.e., reproductive and vegeta- the findings of Pérez Latorre and Cabezudo (2002) who tive throughout the year. This may be due to microclimatic recopded leaf shedding in Quercus broteroi and Quercus suber and edaphic conditions which are favourable for the various occurred mostly during October and November. Several activities. The result obtained on the reproductive/vegeta- researchers have also reported similar results from their re- tive activity index (RVA＞1) point towards the dominance spective studies (Boojh and Ramakrishnan 1981; Shukla and of reproductive phenophases than the vegetative phenophases. Ramakrishnan 1982; Ralhan et al. 1985; Kikim and Yadava Thus, species spent more time for different reproductive 2001). Furthermore, Sundriyal (1990) observed peak leaf phenophase development than the vegetative phenophases. shedding during winter (December to February). Leaf Moreover, the period of vegetative and reproductive shedding of R. arboreum ssp. delavayi var. delavayi and R. growth are significant in integration and use of carbon barbatum occurred during September to November, where- (Mooney et al. 1977). Similar pattern of results were also as R. arboreum and R. kesangiae showed this activity from reported in Quercus suber where apart from few shrubs (viz., October to December. Micro-environment, growth form Cytisus L., Genista L. and Erica arborea L.) all trees and and specific-specific conditions may be influencing the leaf shrubs scored in excess of 1 (Pérez Latorre and Cabezudo shedding differences among the examining species. Boojh 2002; 2006). However, predominate vegetative pheno- and Ramakrishnan (1981) and Sundriyal (1990) have re- phases over the reproductive phenophases was reported by ported similar results from their respective studies. Rodríguez-Gallego and Navarro (2015). However, it has also been reported that high altitude plants Therefore, from eco-morphological characteristics of succeeded various life cycle events sequentially for a period studied Rhododendron species, it can be concluded that, of four months from early June to October and May to except few characters like bark consistency, growth form

J For Environ Sci 34(6), 435-450 445 Phenological Characteristics of Rhododendron Species

and leaf pattern, the studied species have not shown any and Mr. Pankaj Das, Rural Works Department, prominent variations. All the Rhododendron species ex- Government of Arunachal Pradesh for providing the mete- hibited variation in phenological events with the environ- orological data. Thanks also go to Mr. Biswajit Das for mental conditions; however, there were no variations helping in preparation of the study site map. amongst individuals of different populations. Rhododendron species have a sequential arrangement of phenophases and References the predominance of the reproductive phenophases over the vegetative phenophases. Species however performed differ- Amico GC, Aizen MA. 2005. [Seed dispersal by birds in a temper- ent phenological events throughout the year, along with the ate forest of southern South America: who disperses to whom]? change in environmental conditions that do have the po- Ecol Austral 15: 89-100. Spanish. tentiality of natural regeneration. Understanding the phe- Basnett S, Devy S. 2013. Rhododendrons. Beyond just beautiful flowers. Sanctuary Asia, Mumbai, 61-63. nological patterns at the species level as well as ecosystems Basnett S, Devy SM. 2015. Fragrance of life. Down to Earth, New is most important for better managing and enduring eco- Delhi, 46-48. systems management. Rhododendrons are considered as Batalha MA, Martins FR. 2004. Reproductive phenology of the sensitive to climatic variations which may be used as an im- cerrado plant community in Emas National Park (central portant means to monitor global warming through pheno- Brazil). Aust J Bot 52: 149-161. Bawa KS, Bullock SH, Perry DR, Coville RE, Grayum MH. logical observations. An improved habitat management of 1985. Reproductive biology of tropical lowland rain forest trees. present area is most vital part in the conservation of II. pollination systems. Am J Bot 72: 346-356. Rhododendron taxa in Arunachal Himalaya, especially in Beatley JC. 1974. Phenological events and their environmental western Arunachal Pradesh. The results have provided triggers in Mojave desert ecosystems. Ecology 55: 856-863. substantial information and the ecological approaches reck- Bertin RI. 2008. Plant phenology and distribution in relation to re- cent climate change. J Torrey Bot Soc 135: 126-146. oned through this pilot study if are dealt in a more prag- Blake J, Harris GP. 1960. Effects of nitrogen nutrition on flower- matic manner can substantially contribute towards a better ing in carnation. Ann Bot 24: 247-256. management and conservation of the plant taxa in their nat- Bolmgren K, Eriksson O, Linder HP. 2003. Contrasting flowering ural habitat. phenology and species richness in abiotically and biotically polli- nated angiosperms. Evolution 57: 2001-2011. Boojh R, Ramakrishnan PS. 1981. Phenology of trees in a Acknowledgements sub-tropical evergreen montane forest in north-east India. Geo Eco Trap 5: 189-209. The financial assistance provided by the Council of Borchert R, Meyer SA, Felger RS, Porter-Bolland L. 2004. Scientific and Industrial Research (CSIR), New Delhi Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Glob Ecol Biogeogr 13: [38(1052)/02/EMR-II] is thankfully acknowledged. The 409-425. authors are express heartfelt thanks to local field guides, vil- Chamberlain DF. 1996. The Genus Rhododendron: it's classi- lage headmen and villagers for their help and support dur- fication and synonymy. Royal Botanic Garden Edinburgh, ing the course of study. We are grateful to Principal Chief Edinburgh, 181 pp. Conservator of Forest, Department of Environment and Chowdhery HJ, Giri GS, Pal GD, Pramanik A, Das SK. 2008. Materials for the Flora of Arunachal Pradesh. Vol. 2. - Forests, Government of Arunachal Pradesh for allowing us Ceratophyllaceae. Botanical Survey of India, Calcutta, pp 73-98. to work in forest areas of the state. Thanks also due to Dr. Chuine I. 2010. Why does phenology drive species distribution? Pijush Kumar Dutta, Mr. Bijit Basumatary and the army Philos Trans R Soc Lond B Biol Sci 365: 3149-3160. personnel for their help and support during the field study. Cornejo-Tenorio G, Ibarra-Manríquez G. 2007. Plant re- We are obligated to Mr. Kenneth Cox, Dr. Ashiho Asosii productive phenology in a temperate forest of the Monarch Butterfly Biosphere Reserve, Mexico. Interciencia 32: 445-452. Mao, Dr. K. Haridasan and Dr. Debjyoti Bhattacharyya Cox PA, Cox KNE. 1997. The Encyclopedia of Rhododendron for helping in identification of rhododendrons. We are Species. Glendoick Publishing, Glencarse, Perth, 416 pp. thankful to all, those who protracted their help during the Dahlgren JP, Zeipel Hv, Ehrlén J. 2007. Variation in vegetative and field study. The authors are also thankful to the Director flowering phenology in a forest herb caused by environmental

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