Journal of
Threatened Taxa | www.threatenedtaxa.org | 26 July 2018 | 10(8): 12064–12072
Vegetative and reproductive phenology of Aquilaria malaccensis Lam. (Agarwood) in Cachar District, Assam, India
Birkhungur Borogayary1, Ashesh Kumar Das2 & Arun Jyoti Nath3
1,2,3 Department of Ecology and Environmental
Science, Assam University, Silchar, Assam 788011,
India
1birkhungari@gmail.com, 2asheshkd@gmail.com
(corresponding author), 3arunjyotinath@gmail.com
Abstract: Aquilaria malaccensis Lam., a threatened tree commonly called
agarwood, is emerging as one of the most promising
commercially important aromatic species in the world. This paper presents the findings on the
vegetative and reproductive phenology of Aquilaria
malaccensis from the secondary tropical evergreen
forest in Cachar district, Assam. The effect of tree phenology and the
influence of seasonal drought and environmental variables, especially
temperature and precipitation, on various phenophases
such as leaf initiation, leaf-fall, flowering, and fruiting were
investigated. For this, a quantitative
assessment was made at 15-day intervals by tagging 35 trees over a period of
two years. Seasonal influence on the
phenology of different phenophases was correlated
with environmental variables and Spearman’s rank correlation coefficient was
employed. Leaf initiation was positively
correlated with temperature (rs=0.694,
p=<0.05), while leaf-fall was negatively correlated with temperature (rs=-0.542, p=<0.05) and rainfall (rs=-0.521, p=<0.05). Flowering (rs=0.713,
p=<0.01; rs=0.713, p=<0.01) and
fruiting (rs=0.721, p=<0.01; rs=0.775, p=<0.01) were positively and
significantly influenced by temperature and rainfall. The study suggests that temperature and
rainfall were major determinants of the vegetative and reproductive phenology
of A. malaccensis, and any changes in these
variables under expected climate change phenomenon may have a profound effect
on phenophases of this threatened tree species.
Keywords: Agarwood, evergreen, phenology, tropical
secondary forest.
doi: http://doi.org/10.11609/jott.3825.10.8.12064-12072
Editor: A.J. Solomon Raju,
Andhra University, Visakhapatnam, India. Date
of publication: 26 July 2018 (online & print)
Manuscript details: Ms
# 3825 | Received 26 October 2017 | Final received 14 May 2018 | Finally
accepted 02 July 2018
Citation: Borogayary, B., A.K. Das &
A.J. Nath (2018).
Vegetative
and reproductive phenology of Aquilaria malaccensis Lam. (Agarwood)
in Cachar District, Assam, India. Journal
of Threatened Taxa 10(8): 12064–12072; http://doi.org/10.11609/jott.3825.10.8.12064-12072
Copyright: © Borogayary et al. 2018.
Creative Commons Attribution 4.0 International License.
JoTT allows unrestricted use of this article in any
medium, reproduction and distribution by providing adequate credit to the
authors and the source of publication.
Funding: Mr. Birkhungur
Borogayari received
fellowship grant from the
University Grants Commission (UGC) under Basic Science Research
(BSR) programme (F.7-238/2009 (BSR).
Competing interests: The authors declare no competing interests.
Author
Details: Mr.
Birkhungur Borogayari is a senior research fellow (UGC-BSR) and
pursuing his PhD programme in the Department of
Ecology and Environmental Science, Assam University. Prof. Ashesh Kumar Das and Dr. Arun Jyoti Nath are involved in
teaching and research in the Department of Ecology and Environmental Science at
Assam University, Silchar,Assam.
Author
Contribution: Research
design (AKD, AJN and BB); field study, data analysis and photography and
manuscript writing (BB); manuscript correction and revision (BB, AKD and AJN). All
authors approved the final version of the manuscript.
Acknowledgements: The authors gratefully acknowledge the infrastructural facilities
provided by the UGC-SAP and DST-FIST assisted Department of Ecology and
Environmental Science, Assam University, Silchar. We are thankful to Mr.
Babulal Goala for assisting
in the field during data collection.
Authors are grateful to Tocklai Tea Research
Association, Silcoorie, Assam for providing
meteorological data. The fellowship
provided by the University Grants Commission, Basic Scientific Research
(UGC-BSR), New Delhi, Govt. of India to the senior
author is gratefully acknowledged. The
authors thank the anonymous reviewers for critically evaluating the manuscript
and providing suggestions for improvement.
INTRODUCTION
Phenology
of tropical trees has attracted much attention nowadays from the point of view
of conservation of tree genetic resources as well as forestry management, and
for a better understanding of the ecological adaptations of plant species and
community-level interactions. The study
of tree phenology provides knowledge about the pattern of tree growth and
development as well as the effects of environment and selective pressures on
flowering and fruiting behaviour (Zhang et al. 2006). Phenology of vegetative phases is important,
as cycles of leaf flush and leaf-fall are intimately related to processes such
as growth, plant water status, and gas exchanges (Reich 1995). Studies of phenology are of great importance
in determining the temporal changes that constrain the physiological and
morphological adaptations in plant communities for utilization of resources by
fauna (van Schaik et al. 1993). The sunshine hours, temperature, and annual
precipitation have been recognized as the main environmental indications for
leafing and flowering in the tropics. In
many evergreen species, leaf flush and flowering occur close in time on the
same new shoot. Variation in flowering
time relative to vegetative phenology, induced by a variety of factors
(significant rain in winter/summer, decreasing or increasing photoperiod, or
drought-induced leaf-fall), results in a number of flowering patterns in
tropical trees (Borchert et al. 2004). Phenological
processes are significant constituents of plant fitness, since the time and
duration of vegetative and reproductive cycles affect the capability of a plant
species to establish itself in a given site (Pau et al. 2011). Singh & Kushwaha
(2005) suggested that climate change forced deviations in the length of the
growing period, and competition among species may change the resource use
patterns in different species. Global
climate change may force variations in timing, duration, and synchronization of
phenological events in tropical forests (Reich 1995).
Although
a few research works have addressed the population dynamics of the species in homegardens, northeastern India (Saikia & Khan 2013), an attempt has been made to study
the phenology of A. malaccensis, which could
contribute towards the conservation and management of the species, considering
its almost extinct status in the wild (Anonymous 2003). Therefore, the present study is aimed to
assess the phenological behaviour of Aquilaria malaccensis in
a secondary tropical evergreen forest to understand the response of climatic
variables and the periodicity of seasons.
MATERIALS AND
METHODS
Study area
The phenological study was conducted in a secondary tropical
evergreen forest located at Sonachera in Cachar District of Assam, northeastern
India (Fig. 1). Secondary forests are
those forests that regrow largely through natural processes after significant
anthropogenic disturbance of the primary forest vegetation at a single point in
time or over an extended period of time, and place prominently a major change
in tree diversity and/or species composition with respect to nearby original
forests on similar sites (Chokkalingam & de Jong
2001). The studied secondary tropical
evergreen forest covers an area of 5 hectares.
The geographical location of the study site is 24.36˚N latitude &
92.44˚E longitude and altitude range from 73 to 102 m.
Topographically,
the area is characterized by typical terrain and hillocks that harbour diverse
biological diversity. The climatic
condition of the study area is subtropical, warm, and humid. Maximum precipitation occurs during the
months of May to September, which is mainly controlled by the south-west monsoon season.
The mean annual rainfall of the study area during the study period
(2013–15) was about 2055.8mm, most of which (94%) occurred during
April–September. The mean annual minimum
and maximum temperatures were 19.90C and 31.60C,
respectively (Fig. 2). The mean annual
relative humidity was recorded at 75.9%.
The
forest is categorized as “Cachar Tropical Evergreen
Forest (Champion & Seth) (reprinted) (2005) (1B/C3)” type dominated by Chrysophyllum roxburghii,
Maniltoa polyandra,
Memecylon celastrinum,
Mesua floribunda, Palaquium
polyanthum, and Pterospermum
lanceifolium.
The selected secondary forest site is more than 35 years old. The secondary forest of this region is
relatively unexplored and harbours a rich plant
diversity.
Study species
Aquilaria malaccensis Lam. (Thymelaeaceae)
is one of the most important species of commercial products in the world and is
valued for its fragrant resinous dark-coloured wood known in trade as agar.
Agarwood is formed by a complex
plant-microbial interaction of a parasitic ascomycetous
fungus known as Phaeoacremonium parasiticum (Ng et al. 1997). Phytogeographically,
the distribution of A. malaccensis comprises
the region of India, Myanmar, Sumatra, Peninsular Malaysia, Singapore, Borneo,
and the Philippines (Chua 2008). In northeastern India, it occurs mostly in the foothills of
Arunachal Pradesh, Assam, Manipur, Meghalaya, Mizoram, Nagaland, Sikkim, and
Tripura (Saikia & Khan 2012a). In Upper Assam, the species is commonly
cultivated in home gardens in association with other valuable plants for its
high commercial demand (Saikia & Khan
2012c). The bark of the plant is also
used as raw material for preparing a writing paper called ‘Sanchi
pat’ for writing religious scripts (Nath & Saikia 2002). The agarwood is imported locally and exported internationally
due to its wide use in the incense and perfume industry (Manohara
2013). Agarwood
oil is a valuable component and is used as a digestive, sedative, analgestic, antiemetic and antimicrobial agents in
tradition medicine (Cui et al. 2013). In the past few years, large-scale harvesting
has caused rapid depletion of the stock in the natural forests. According to the IUCN Red List, the species
is globally Vulnerable A1cd (Ver 2.3; IUCN 2017) and
has been included in The World List of Threatened Trees (Oldfield et al. 1998). The species is also listed in Appendix II of
the Convention on International Trade in Endangered Species of Wild Fauna and
Flora (CITES 1994).
Methods
A total
of 35 individuals with girth size ranging from 12.7 to 81.7 cm were selected
for phenological observations. The selected trees were marked with a metal
tag for phenological observations. Using binoculars, phenological
observations were made on leaf initiation, leaf-fall, flowering, and fruiting
of the marked individuals. Phenological observations were based on phenological
score: zero for no phenophase, one for less, two for
moderate, and three for high (Broadhead et al.
2003). Detailed observations were
carried out at 15-day intervals over a period of two years from February 2013
to January 2015.
Data analyses
Data
analysis was performed using statistical software (MS Excel 2010) and (SPSS 21)
version. Spearman rank correlations were
performed to investigate correlations between monthly phenophase
activity and environmental variables such as temperature and rainfall following
(Zar 1984).
The duration was classified as short (<2 months), intermediate (2-5
months), or extended (>5 months) based on the mean number of months in which
the phenophase occurred (Luna-Nieves et al.
2017). Circular statistical analyses
were performed to determine whether the vegetative and reproductive phenophases were homogenously distributed throughout the
year. For this purpose, months were
converted into angles with intervals of 30°, and then the mean angle or mean
date (α), the circular concentration (r), and the circular standard
deviation (SD) were calculated. (α) indicates the time (month) of the year in which the largest
number of individuals of a given species presented a phenophase,
while (r) indicates the degree of dispersion or concentration of the
observations (Zar 1984). To determine the significance of the angle, a
Rayleigh test (z) was used. There is a seasonality in the phenophases
if the average angle is significant. The
intensity of circular concentration (r) values varies from 0 (phenological activity uniformly distributed throughout the
year) to 1 (phenological activity concentrated in a
particular period of the year) (Morellato et al.
2010). We used the program ORIANA 3
(Kovach 2007) for these analyses. The
meteorological data of the study area are presented in (Fig. 2).
RESULTS
Leafing activity
A. malaccensis initiated leafing during the pre-monsoon
period (March–April) and continued up to a warm monsoon period throughout the
favourable season (July–August) (Fig. 3A).
The degree of circular dispersion or concentration (r=0.99) indicates
that the phenophase leaf initiation was concentrated
in a particular period of the year (Fig. 5).
The phenophase leaf initiation was seasonal
(Rayleigh Z, p < 0.01), and it occurred once a year. Peak leaf initiation was observed during
March–April (Fig. 4). During the years
2013–14 and 2014–15, temperature registered its influence on leaf initiation
significantly whereas rainfall displayed its impact in 2014–2015 (Table
1). The combined effect of temperature
and precipitation, rather than their individual effects, more strongly
influenced leaf initiation. Leaf-fall
occurred during November–March with peak fall during January–February (Fig.
4). Rainfall and temperature presented a
negative slope in correlation with leaf-fall due to decreasing day length and
rainfall (Table 1).
Flowering
Flowering occurred during April–June (Fig. 3C
& 4). The degree of circular
dispersion or concentration (r=0.97) indicates that the phenophase
flowering was concentrated in a particular period of the year (Fig. 5). The flowering phenophase
was intermediate (Rayleigh Z, p < 0.01), and the open flower lasted
one month. The duration of flowering phenophase ranged from 30 to 85 days with an average
duration of 58.05 ± 6.35 days during 2013–14 and 32–90 days with an average
duration of 61 ± 6.37 days during 2014–15, and it varied greatly among the
individuals with a coefficient of variation (C.V. % =20.62). Flowering was significantly influenced by
temperature and rainfall while in one-month lag period only rainfall was
significantly correlated with flowering in 2013–2015 (Table 1). The flowers are yellowish-green and produced
in umbels (Image 1a & b); the fruit is a woody capsule (Image 1e & f).
Fruiting
The
fruiting phase extended over the monsoon period (April–September) with a peak
during May (Fig. 3D & 4). The degree
of circular dispersion or concentration (r=0.98) indicates that the phenophase fruiting was concentrated in a particular period
of the year (Fig. 5). The fruiting phenophase duration was intermediate (Rayleigh Z, p <
0.01), and the unripe fruits lasted for two months. The duration of fruiting phenophases
ranged from 28 to 65 days with an average duration of 46.57 ± 5.24 days during
2013–14 and 30–72 days with an average duration of 51 ± 5.26 days during
2014–15, and fruiting duration varied greatly among the individuals with a
coefficient of variation (C.V. % =23.37).
Fruiting presented the correlation distinctly with temperature and
rainfall while in one-month lag only rainfall was significantly related with
fruiting (Table 1). Availability of
seasonal water had a strong impact on fruiting indicating that there was a
significant relationship between one-month lag rainfall and fruiting. Fruits mature by the end of July. The fruit is a single seed
which remains hanging through a small thread-like structure (Image 1f)
for a few days before dehiscence. Each
seed bears a conspicuous crimson red, fleshy caruncle
at the tip.
Table 1.
Phenological patterns of A. malaccensis in relation to corresponding month and one
month lag period of temperature and rainfall in Cachar
District, Assam
|
Environmental factors |
|||
|
Spearman's rank correlation coefficients
(rs) |
|
||
Phenophases |
Temperature (˚C) |
Rainfall (mm) |
||
|
2013-14 |
2014-15 |
2013-14 |
2014-15 |
Leaf initiation |
0.694* |
0.861** |
(0.251 NS) |
0.528* |
|
(0.125 NS) |
(0.340 NS) |
(0.427 NS) |
(0.199 NS) |
Leaf-fall |
-0.542* |
-0.661* |
-0.521* |
(-0.444 NS) |
|
(-0.293 NS) |
(-0.358 NS) |
(-0.174 NS) |
(-0.358 NS) |
Flowering |
0.713** |
0.684* |
0.713* |
0.595* |
|
(0.509 NS) |
(0.382 NS) |
0.833** |
0.683* |
Fruiting |
0.721** |
0.824** |
0.775 ** |
0.662* |
|
(0.518 NS) |
0.679* |
0.601* |
0.833** |
DISCUSSION
The phenological observations on the species and climatic
characteristics of the study site suggest that the A. malaccensis
is a seasonal flowering and fruiting tree species. Correlation of phenological
characteristics with naturally occurring climatic events may be best documented
by the pattern of leaf-fall. The
greatest tendency of leaf-fall practice coincides with the relatively dry season
during January–February. The timing of leaf-shedding is strongly correlated with a gradual increase
in day-length, temperature, and solar insolation. This finding is in conformity with Mishra et
al. (2006) who stated that maximum leaf-fall occurs during the dry period in
tropical forest trees. Further,
leaf-fall during this period appears to be an inherent strategy to minimize
water loss and maximize photosynthetic activity during monsoon season (Rivera
et al. 2002; Hamann 2004).
Leaf
production and flushing of A. malaccensis start
towards the end of the dry season. Short
dry period, maximum temperature, and increased day length triggered the
emergence of new leaves during the pre-monsoon period. The advantages of peak leaf initiation during
pre-monsoon period could possibly be explained by the fact that it was to take
advantage of the long rainfall period by the fully expanded foliage on trees
(Singh & Kushwaha 2005). Maximum temperature and photoperiod as
driving factors for leaf initiation have been reported for other tropical trees
(Rivera et al. 2002; Singh & Kushwaha 2005). Saikia & Khan
(2012b) observed that leaf flushing in A. malaccensis
in home gardens starts in March and continues up to October. Species that produce leaf during the rainy
season tend to have shorter periods of leaf production because this period of
abundant water will normally last only for a few months. The species that greatly depend on rainfall
for initiation of the leaf would also be expected to show rapid leaf growth in
order to maximize photosynthetic activity during the rainy season (Reich 1995),
and this type of behavior is quite common in plants
growing in seasonally dry environments (Wright et al. 2002). Leaf initiation in the early rainy season is
attributed to the end of the long dry season and also due to the joint action
of increasing day length and temperature (Kushwaha et
al. 2010). Rivera et al. (2002) have
implicated that increasing day length acts as the inducer of flushing which is
relevant to the leaf phenology in A. malaccensis.
Flowering
during the pre-monsoon season can be viewed as a strategy to make flowers more
visible to pollinators and supply food sources during the poor periods of
floral resources (Murali & Sukumar
1993). Species flowering during the
pre-monsoon period can be capable of storing water in sufficient quantities to
permit flowering even in the absence of rainfall (Borchert
1994). A. malaccensis as a dry season bloomer showed a
significant positive correlation with photoperiod as observed for trees in
tropical dry forests by Borchert et al. (2004). Soehartono &
Newton (2001) reported flowering and fruiting in A. malaccensis
growing in botanical gardens of Indonesia from April–September. Beniwal (1989)
found flowering in March and fruiting in the middle of June in plantations of
Arunachal Pradesh, northeastern India. Saikia & Khan
(2012b) observed initiation of flowering from mid-February to May following
fruiting from May and ending in August.
A. malaccensis concentrated peak fruiting during the wet
season, producing dry fruits with small seeds.
In tropical forests, fruiting during the rainy season may have evolved
to ensure dispersal of seeds when soil water status is favourable for seed germination,
seedling growth, and survival (Kushwaha et al.
2011). The requirement of moisture level
for the proper development of fruits indicates that the decrease of soil water
status reduced the rate of enlargement and final size of these fruits. During the wet season, availability of high
moisture level also favours germination and establishment of seeds. The flowering phenology observed in A. malaccensis is reported in Psidium
guajava and Vatica
lanceaefolia growing in the home gardens of Barak
Valley, northeastern India (Das & Das 2013). Synchronization of flowering during a
particular season appears to be under the control of the prevailing climatic
condition of that season (Singh & Kushwaha
2005). Maximum flowering activity during
the pre-monsoon period may be related to the high insect population as pollen
vectors in tropical forests. Further,
seasonal flowering strategy observed in A. malaccensis
may be a strategy to escape from seed predation on a timely basis.
In A.
malaccensis, fruiting initiation during the rainy
season is indicative of a close relationship between rainfall and fruiting, as
the rainfall factor acts as a cue for reproductive phenology, especially in dry
tropical forests as stated by Griz & Machado
(2001). Further, autochorous
seed dispersal in this species is also probably related to the humidity factor
as it has an influence on fruit dehiscence.
Fruit dehiscence during the monsoon season may enable the plant to
escape from seed predators and produce seedlings for continued survival (Hamann 2004).
Fruiting during the rainy season in tropical forests evolved to ensure
dispersal of seeds and this could be attributed to utilization of available
soil water for seed germination and seedling establishment (Singh & Kushwaha 2006).
Tropical trees have adopted a systematic strategy so that there is
adequate development time from flowering to seed dispersal so that seeds are
released during the rainy period (Stevenson et al. 2008) when germination is
most likely to be induced and seedlings start growing with a low probability of
drought.
In the
present study, the duration of flowering was longer (59.52 ± 6.36 days) and
fruiting was shorter (48.78 ± 5.25 days) in A. malaccensis
during the two years of study. This
longer duration of flowering can be viewed as a difference in time taken for
the formation to the maturation of buds.
The short duration of fruiting is advantageous for the plant to mature
fruits during the rainy season due to the availability of highest
precipitation. This flowering and
fruiting duration does not agree with the reports on the same in the tropical montane evergreen forest of southern India (Mohandass et al. 2016).
Further, the duration of these two phenophases
appears to be influenced by the changes in day length, temperature, sunshine
hours, and precipitation associated with the season (Bawa
et al. 2003).
The
present study indicates that the vegetative and reproductive phenological events in A. malaccensis
display a general annual flowering and fruiting pattern with a peak in these
events during the pre-monsoon and monsoon seasons. Temperature and precipitation (by themselves)
do not show any influence on leaf initiation but cumulatively show influence on
leaf initiation. Availability of
seasonal water had a strong impact on fruiting indicating that there is a
significant relationship between one-month lag rainfall and fruiting. It seems that changes in temperature and
rainfall pattern have a pronounced effect on the phenology of A. malaccensis.
This information may be used as a baseline for further evaluation of phenological variations for this vulnerable tree with
reference to climate change. The study
suggests that there is a need to develop a long-term monitoring strategy on phenological aspects of A. malaccensis
in order to understand the impact of climate change on phenology.
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