Reproductive
ecology of Syzygium alternifolium (Myrtaceae), an endemic and endangered tropical tree species
in the southern Eastern Ghats of India
A.J. Solomon Raju 1, J. RadhaKrishna 2 & P. Hareesh Chandra 3
1,2,3 Department of
Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh
530003, India
1ajsraju@yahoo.com
(corresponding author), 2jrkrishna30@gmail.com, 3hareeshchandu@gmail.com
Abstract: Syzygium alternifolium is a
semi-evergreen mass-flowering tree species of dry deciduous forest in the
southern Eastern Ghats of India. It
is a mass bloomer with flowering during dry season. The floral traits suggest a mixed
pollination syndrome involving entomophily and anemophily together called as ambophily. Further, the floral traits suggest generalist pollination system adapted
for a guild of pollinating insects. The plant is self-incompatible and obligate
out-crosser. The flowers are many-ovuled but only a single ovule forms seed and hence, fruit
and seed set rates are the same. Natural fruit set stands at 11%. Bud infestation by a moth, flower predation by the beetle, Popillia impressipygaand bud and flower mounds significantly limit fruit set rate. The ability of the plant to repopulate
itself is limited by the collection of fruits by locals due to their edible
nature, short viability of seeds, high seedling mortality due to water stress,
nutrient deficiency and erratic rainfall or interval of drought within the
rainy season. Therefore, S. alternifolium is struggling to populate itself under
various intrinsic and extrinsic factors. Further studies should focus on how to assist the plant to increase its
population size in its natural area taking into account the information
provided in this paper.
Keywords: Ambophily, bud
infestation, flower predation, generalist pollination system,
self-incompatibility, seedling mortality, Syzygium alternifolium.
doi: http://dx.doi.org/10.11609/JoTT.o3768.6153-71
Editor: Raju Sekar, Xi’an Jiaotong-Liverpool
University, Suzhou, China. Date of publication: 26 August 2014 (online &
print)
Manuscript details: Ms # o3768 |
Received 15 September 2013 | Final received 28 July 2014 | Finally accepted 04
August 2014
Citation: Raju, A.J.S., J.R. Krishna & P.H. Chandra (2014).
Reproductive ecology of Syzygium alternifolium (Myrtaceae), an
endemic and endangered tropical tree species in the southern Eastern Ghats of
India. Journal of Threatened Taxa 6(9): 6153–6171; http://dx.doi.org/10.11609/JoTT.o3768.6153-71
Copyright: © Raju et al. 2014. Creative
Commons Attribution 4.0 International License. JoTTallows unrestricted use of this article in any medium, reproduction and
distribution by providing adequate credit to the authors and the source of
publication.
Funding: Ministry of
Environment & Forests, Government of India, New Delhi.
Competing Interest: The authors
declare no competing interests.
Author Contribution: AJSR has conceived the concept, ideas, plan of work and did part of field work and prepared the paper. JRK and PHC did field
work and tabulated the observational and experimental work of the paper.
Author Details: Prof. A.J. Solomon Raju is Head of the Department of Environmental Sciences, Andhra University,Visakhapatnam. He is presently working on endemic and
endangered plant species in southern Eastern Ghats forests with financial
support from MoEF and CSIR. J. Radha Krishna is working as a
Junior Research Fellow in the MoEF&CC research
project registered for a PhD degree under Prof. A.J.
Solomon Raju. P.Hareesh Chandra is working as a senior
research fellow in the MoEF&CC research project
registered for a PhD degree under Prof. A.J. Solomon Raju.
Acknowledgements: This study is a part of the research work carried out under an All
India Coordinated Research Project on Reproductive Biology of RET Tree species
(MoEF No. 22/6/2010-RE) funded by the Ministry of
Environment, Forests & Climate Change, New Delhi
sanctioned to AJSR. The second
author is JRF and third author is SRF working in this project. We thank Mr. K. Venkanna,
Technical Officer, Central Research Institute for Dry land Agriculture,
Hyderabad, for doing soil NPK analysis.
For figures, images, tables -- click here
INTRODUCTION
Syzygium (Myrtaceae) is native
to the tropics, particularly to tropical America and Australia. It has a worldwide, although highly
uneven, distribution in tropical and subtropical regions. It is known from many countries
including South Africa, South America, South East Asia and Australia. The genus comprises about 1,100 species,
and has a native range that extends from Africa and Madagascar through southern
Asia east through the Pacific. Its
highest levels of diversity occur from Malaysia to northeastern Australia,
where many species are very poorly known and many more have not been described
taxonomically (Wrigley & Fagg, 2003). In India, Syzygiumhas 75 species. This genus is of
commercial importance with timber yielding plants such as S. aqueum and S. bracteatumand with fruit trees such as S. cuminii and S.aromaticum which are highly adapted to adverse conditions. The fruits of many plants are edible and
found to be used in local medicine (Anonymous 1956). A list of 18 Syzygium species is included in the International Union for the Conservation of
Nature (IUCN) Red List Plants of India (Reddy & Reddy 2008). They are S. andamanicum,
S. courtallense, S. manii,
S. palghatense, S. travancoricum(Critically Endangered), S. beddomei, S. bourdillonii, S. chavaran, S. microphyllum, S. myhendrae, S. parameswaranii, S. stocksii(Endangered), S. benthamianum, S. densiflorum, S. occidentale, S. ramavarma (Vulnerable), S. utilis(Data Deficient) and S. gambleanum(Extinct). Reddy & Reddy (2008)
documented that S. alternifolium is an endemic
and globally endangered species as per the criteria of IUCN but not yet
included in the IUCN Red List.
Sanewski (2010) stated
that the studied species of Syzygium for
their reproductive ecology indicate that both self-compatible and
self-incompatible species exist in this genus but the self-compatible species
are most common. The author
documented some self-compatible species which include S. tierneyanumand S. nervosum from north Australia (Hopper
1980; Shapcott 1998), S. cuminiifrom India (Reddi & Rangaiah(1999–2000), S. rubicundum from Sri
Lanka (Stacey 2001), S. lineatum from
Indonesia (Lack & Kevan 1984), and S. samarangense, S. jambos, S. megacarpum, and S. formosumfrom Thailand (Chantaranothai & Parnell
1994). In Australia, a variety of
nectar feeding animals visit and pollinate S. tierneyanumwhile blossom bats and honeyeaters are primary pollinators of S. sayeri, although butterflies, flies, thrips and wasps also playing a role in pollination
(Williams & Adam 2010). S. cormiflorum is mainly
pollinated by bats and followed by birds and insects (Crome& Irvine 1986) while S. paniculatum is
pollinated by honeybees, hawk moths, honeyeaters and butterflies (Payne 1991,
1997). S. floribundum is pollinated by a guild of
short-tongued unspecialized insects (Williams & Adam 2010). In American Samoa, S. inophylloides and S. samarangenseare regularly foraged by birds (Cox et al. 1992). S. dealatum is both entomophilousand anemophilous (Webb & Solek1996). Empirical studies on the
pollination of other Syzygium species in Samao are absent but observers have suggested that bats are
important pollinators of these species (Wiles & Fujita 1992; Trail 1994; Banack 1996). In Sulawesi, S. syzygiodes is
pollinated by a variety of short-tongued unspecialized insects (Williams &
Adam 2010). In East Java, S. pycnanthum attracts a variety of insects but their
pollination role has not been studied (Mudiana & Ariyanti 2010). In Africa, S. guineense is reported to
be a honeybee plant but details of pollination are lacking (Verdcourt2001). In Mauritius, S. mamillatum is a rare and endemic cauliflorus species and it is pollinated by a variety of
birds (Kaiser et al. 2008). In
India, only S. mundagum and S. cuminii have been studied for their pollination
biology. S. mundagum in the Western Ghats is pollinated
exclusively by bats while seed dispersal takes place largely by bats (Ganesh
1996). S. cuminii is pollinated by wind, insects and
gravity (Misra & Bajpai1984; Bajpai et al. 2012). Despite the richness of Syzygium species in India, the pollination biology
of all other species has not been studied so far.
S. alternifolium occurs in the
tropical dry deciduous forests of Kurnool, Cuddapahand Chittoor districts of Andhra Pradesh, Chengalpattu
and North Arcot districts of Tamil Nadu and Bangalore
District in Karnataka in India (Gamble 1957; Chitra1983; Saldanha 1996; Reddy et al. 2006). Mohan & Lakshmi (2000) reported thatS. alternifolium occurs in the upper plateau,
slopes and valley tops with dry, slaty and rocky
conditions at an elevation ranging from 600–1000 m in Sri Venkateswara Wildlife Sanctuary of Chittoorand Cuddapah districts. They stated that the distribution of
this species appears to be related to the geology and rock structure along with
elevation and aspect.
S. alternifolium is a fruit tree
of great timber, medicinal and economic importance. Timber is used for making furniture and
agricultural implements. The plant
tops are used to cure skin diseases as it has excellent anti-fungal properties
(Reddy et al. 1989). The leaves are
used in the treatment of liver cirrhosis, hepatitis, infective hepatitis, liver
enlargement, jaundice and other ailments of liver and gall bladder. Leaves fried in cow ghee are used as a
curry to treat dry cough. A mixture
of leaves and mineral oil is used to maintain dark hair and also to promote
hair growth by external application to the scalp. Tender shoots, fruits and leaf juice are
used to treat dysentery, seeds for diabetes and stem bark for gastric
ulcers. Flowers yield honey and
possess antibiotic properties. The
ripe fruits are used in making squashes and jellies. Fruit juice is used to cure stomach-ache and ulcers while the external application of
fruit pulp reduces rheumatic pains (Reddy et al. 1989; Nagaraju& Rao 1990; Rao & Rao 2001; Bakshu 2002; Mohan et
al. 2010). Despite its multiple
medicinal and economic uses, the plant has not been studied for any aspect of
pollination ecology. In recent
years, its population size is declining due to cut down of trees and collection
of fruits leaving less possibility for the plant to repopulate itself in its
natural area. Keeping this in view,
the present study is contemplated to describe the chronological events of
pollination biology of S. alternifolium(Wight) Walp. (Myrtaceae). The observational and experimental data
collected on the studied aspects are discussed in the light of relevant
existing information on other Syzygiumspecies.
MATERIALS AND
METHODS
Study area
A population of
about 80 individuals of S. alternifoliumlocated in the hill and slopes of Tirumala (13042”N
& 79020”E, 858m) was used for the study during
2011–2013. This area is a
part of Seshachalam Hills and this
region is declared in 2011 as Seshachalam Biosphere
Reserve by the Ministry of Environment and Forests, Government of India. The reserve lies between 13038”–13055”N
& 79007”–79024”E. It is spread over 4756km2 in
both Kadapa and Chittoordistricts of southern Andhra Pradesh. The vegetation is a unique mix of the dry deciduous and moist deciduous
types. The elevation ranges from
150–1,130 m and the terrain undulating with deep forest-covered valleys
and characterized by steep slopes, rocky terrain, dry and poor stony
soils. The area receives most of
the rainfall from northeast monsoon and little from southwest monsoon (Guptha et al. 2012).
Floral biology
Field observations
on flowering intensity were made during 2011–2013. Twenty-five trees (Diameter, Breast and
Height 15±4) were tagged for recording the phenologicalevents for two consecutive years 2011 and 2012. Fifty tagged mature buds from 10 trees
were followed for recording the time of anthesis and
anther dehiscence; the mode of anther dehiscence was also noted by using a 10x
hand lens. Five flowers each from
ten trees selected at random were used to describe the flower details. Twenty mature but undehiscedanthers from the flowers of 10 different plants were collected and placed in a
petri dish. Later, each time a single anther was taken out and placed on a
clean microscope slide (75x25 mm) and dabbed with a needle in a drop of lactophenol-aniline-blue. The anther tissue was then observed
under the microscope for pollen, if any, and if pollen grains were not there,
the tissue was removed from the slide. The pollen mass was drawn into a band, and the total number of pollen
grains was counted under a compound microscope (40x objective, 10x eye
piece). This procedure was followed
for counting the number of pollen grains in each anther collected. Based on
these counts, the mean number of pollen produced per anther was
determined. The pollen grain
characteristics were recorded by consulting the book of Bhattacharya et al.
(2006). Pollen
dispersal rate as single grains or in aggregates was ascertained by gently
touching the dehisced anthers and collecting the liberated pollen on microscope
slides placed close to the anthers. The hourly pollen concentrations in
the plant canopy were determined by operating rot rod samplers. Pollen spread downwind of the source, during the period of anther dehiscence was measured
at a distance of 0, 5, 10, 15, 20 and 25 meters using rotor samplers (Perkins
1957). Five flowers each from ten
trees were used for testing stigma receptivity, nectar volume, sugar
concentration, sugar types, protein content and amino acids. These aspects were examined following
the protocols given in Dafni et al. (2005). Nectar was also analyzed for amino acid
types by following the Paper Chromatography method of Baker & Baker (1973).
Foraging activity
The foraging
activity of insects was observed during day and night for 15 days in each
year. In the 3-year period, the
same insects were recorded. The
census of foraging visits of each insect species was recorded on three different
occasions in each year and the data thus collected was compiled to arrive at
the average foraging visits made by each species at each hour and for the
day. They were observed with
reference to the type of forage they collected, contact with essential organs
to result in pollination and inter-plant foraging activity in terms of
cross-pollination.
Predation and
breeding systems
Bud and flower
infestations were also observed in each study year and recorded their intensity
to the extent possible. Fifty
mature buds, five each from 10 inflorescences on five trees were bagged prior
to anthesis around noon time without manual
self-pollination to know whether the fruit set occurs through autogamy. Another set of 50 mature un-dehisced
buds was selected in the same way and bagged. On the next day, the bags were removed,
manually self-pollinated and bagged again to know whether fruit set occurs
through manual self-pollination. Another set of 50 mature buds was selected again, then emasculated and
bagged. The next day, the bags were
removed and the stigmas were brushed with the freshly dehisced anthers from the
flowers of the same tree and re-bagged to know whether fruit set occurs throughgeitonogamy. Another set of 50 mature buds was selected in the same way, then
emasculated and bagged. The next
day, the bags were removed and the stigmas were brushed with freshly dehisced
anthers from the flowers of other trees and re-bagged to know whether fruit set
occurs through xenogamy. Ten inflorescences on each tree were
tagged for fruit set in open-pollination. The bagged flowers and tagged inflorescences were followed for eight
weeks to record the results.
Fruiting and
seedling ecology
Fruits and seed
characteristics were also recorded. Field observations on the fruit maturation duration and dispersal mode
were recorded. In vitro experiments
for seed germination rate were conducted in the local forest nursery. A total of 195 seeds were sown in
experimental bags and followed for result for two months. A total of 144 seeds germinated within
two weeks. Further, observations
were made on seed germination and seedling establishment rates in natural
habitat.
Soil analysis
The soil analysis for NPK was done by the Central Research Institutefor Dry land Agriculture, Hyderabad. Field observations on soil status in natural habitat were also noted.
Photography
The plant habit,
flowers, fruits, seeds, seedlings, flower foragers and
bud and flower infestations were photographed with a Nikon D40X Digital SLR
camera (10.1 pixel).
GPS coordinates
Magellan Explorist 210 Model Digital Global Positioning System was
used to record the coordinates - latitude, longitude and altitude.
RESULTS
Phenology
S. alternifolium is a
semi-evergreen mass-flowering tree species of dry deciduous forest (Image
1a). Leaf shedding is partial
during January–March. Flower
bud initiation occurs in late March while flowering occurs during mid-April to
mid-May at population level (Image 1c,d). All the trees flowered massively in 2011; moderate flowering or
flowering in a few branches occurred in only four trees in 2012 and 2013 and in
five others only in 2012. Five
others showed scattered flowering on a few branches only in 2013. Flowering was totally absent in 11 trees
in 2012 and 2013. The flowering
lasts 21 days (Range 16–26) in individual trees (Table 1). The flowering is almost synchronous
within the population. The number
of flowers opening each day is initially small, but increases rapidly, with a
peak mass flowering for a fortnight and then declining rapidly. Leaf flushing begins at the end of
flowering and continues into rainy season from June–August (Image
1b). The shedding of still intact
old leaves takes place simultaneously.
Flower morphology
The flowers are
borne in 8.62±1.26 cm long, terminal and axillary cymes with divaricating
branches. Each inflorescence consists of 22–53 flowers. They are pedicellate,
creamy-white, 16mm long and 2mm wide, cup-shaped (4mm), actinomorphic, bisexual
and sweet scented. The calyx and
corolla are joined to form a cap over the bud, which falls off as a calyptra
due to the pressure of the growing stamens. The stamens are epigynous,
white, free, polystemonous (127±3), shaving-brush
type and arranged on the rim of the receptacle in two whorls; the outer whorl
stamens are 9mm long while inner whorl stamens 6mm long. The filaments are bent inwards in the
bud condition but straighten at the time of anthesis. The anthers are 1mm long, versatile, dithecous and introrse. The ovary is bicarpellaryand bilocular syncarpous;
it is 4mm long and contains 21–38 ovules on axileplacentation (Image 1n). The style
tipped with semi-wet simple stigma is 8mm long when fully grown,arises from the center of the cup and stretches out of the stamen ring by
2–3 mm (Image 1lm).
Floral biology
The flowers open
during 16:00–18:00 hr with maximum flower
production at 17:00hr (Image 1 e–k). Anther dehiscence occurs following anthesis by
longitudinal slits. Each anther
produces 4136±192 pollen grains and the total pollen output per flower is
5,25,272±12,408. The pollen-ovule ratio varies from 13,833 to 25,013. The pollen grains are creamy-white,
triangular, tricolporate, triangular, 16.6µm in size,
powdery and fertile (Image 1o). The
apertures appear as short furrows in a thickened portion of the wall. The distinctive
pattern seen in polar view is formed by thinning of the exine. Most of the pollen is dislodged as
single grains and it enters the ambient environment by wind. Two peak pollen concentrations were
recorded, one with 17,832 pollen grains per m3 of air sampled in the
evening hours between 17:00 and 20:00 hr and another
with 5,721 pollen grains per m3 of air sampled in the morning hours
between 07:00 and 10:00 hr. In the circadian cycle, the pollen grain
concentrations varied between 17,832 and 843 for cubic meter of air
sampled. The pollen concentration
at peak pollen release hour (19:00hr) at a distance of 0m was 17,832, at 5m
15,821, at 10m 12,981, at 15m 7,432, at 20m 1500, and at 25m 659. The pollen concentration at second peak
hour (09:00hr) was 5,721 at 0m, 4057 at 5m, 3947 at 10m, 3254 at 15m, 2874 at
20m and 1647 at 25m. The stigma
receptivity begins at 20:00hr and remains until the end of 2ndday. The stamens fall at the 2ndday of flower life while the remaining parts of the flower remain intact for
five days if not pollinated. In
pollinated flowers, the calyx cup is persistent and the fruit emerges out when
fully grown. The nectar is secreted
in the orange coloured part of the cup continuously
for a period of four days from the time of anthesis. A total of 12.7±4.32 µl of nectar is
produced in the total life span of the flower. The nectar sugar concentration is
16.44±3.1 %; the sugars include sucrose (2.55µg), fructose (2.37µg) and glucose
(0.13µg). The nectar includes six
essential and nine non-essential amino acids. The essential amino acids are arginine, histidine, lysine, threonine, tryptophan and valine. The
non-essential amino acids are alanine, aspartic acid, cysteine, cystine, glutamic acid, glysine, hydroxyproline, serine and tyrosine. The total protein content in the nectar
is 2.55µg.
Flower visitors
and pollination
The flowers
completely expose the anthers as well as the stigma. The flower visitors accessed the floral
rewards with great ease. A total of
33 species consisting of bees, wasps, flies, beetles, butterflies (diurnal
foragers), the hawk moth (crepuscular forager), and the reptilian (nocturnal
forager) was recorded (Table 2). The bees included Apis dorsata (Image 2c), A. cerana(Image 2d), A. florea, Trigona iridipennis (Image 2e), Amegilla sp. (Image 2f) and Stizus sp. (Image
2g). Of these, Trigonabees foraged for nectar and also pollen, while all others for nectar only. The
wasps were nectar foragers and they were Eumenes sp. (Image 2h), Vespa cincta (Image 2i)
and V. orientalis (Image 2j). Both the bees and wasps were regular
foragers. Flies were occasional nectar foragers and they were Chrysomya megacephala(Image 2k) and Helophilus sp. (Image 2l). Beetles were Popillia impressipyga (Image 2m) and one unidentified
species (Image 2n); the former was a resident forager feeding on flower parts
and contributed to 26% of flower damage in 2011, 20% in 2012 and 6% depending
on flowering intensity while the latter was an occasional nectar forager. The
butterflies were regular foragers and they were Papilio polytes (Image 3a), Graphium nomius, Catopsilia pyranthe (Image 3b), C. pomona(Image c,d), Euploea core (Image 3e), Tirumala limniace (Image 3f), Precis iphita (Image 3g), Junonia lemonias (Image 3h), Melanitis leda (Image 3i), Danaus genutia (Image 3j), Neptis hylas (Image 3k), Mycalesis perseus (Image 3l), Moduza procris, Arhopala amantes (Image 3m), Pseudocoladenia indrani (Image 4a), Borbo cinnara (Image 4b), Hasora chromus (Image 4c) and Celaenorrhinus ambareesa (Image 4d). The sphingid, Cephonodes hylas(Image 4e) was the only diurnal moth visiting the flowers regularly. The African fat-tailed gecko, Hemitheconyx caudicinctuswas a resident nectar forager during night time from
0600–1000 hr (Image 2o).
The first visitor
to just open flowers in the evening was the diurnal hawk moth, Cephonodes hylas;
it continued its foraging from 16:00–19:00 hr. The same moth was the first visitor to
the flowers in the morning and it foraged from 06:00–09:00 hr (Fig. 7). All other insects visited the flowers from 07:00–12:00/13:00 hr (Fig. 1–6); the flies
made a few visits during 15:00–16:00 hr (Fig.
3). The intense foraging activity
was recorded during 09:00–11:00 for most of the insects. Of the total foraging visits made by
insects except beetles during the 3-year period, bees constituted 25%, wasps
15%, flies 3%, butterflies 50% and hawk moth 7% (Fig. 8). The honey bee, A. dorsata,
wasps, butterflies and the hawk moth foraged for nectar very frequently between
closely and distantly spaced conspecific trees while other bees, the
unidentified beetle and the gecko tended to stay mostly on the same tree for
forage collection.
Flower bud as oviposition site for an unidentified moth
A moth species (unidentified)
used the flower buds as oviposition site. It deposited its eggs in young flower
buds and the emerged larvae consumed the entire bud over a period of
approximately 3–4 days (Image 2a,b). The percentage of infested flower buds is 21% in 2011, 17% in 2012 and
4% in 2013. Consolidated mounds
formed by buds and flowers were also found and such flowers subsequently fell
off (Image 4f). These infested
flowers were found on all flowering branches in 2011, randomly in 2012 and
rarely in 2013. These bud and
flower infestations were found be to be related to the intensity of flowering
in each study year.
Breeding and
fruiting behavior
Hand-pollination
experiments indicated that autogamy and geitonogamyare non-functional while xenogamy is the only mode of
pollination for fruit set. In this mode, fruit set stands at 56% while in
open-pollination mode, it is 11% only (Table 3). The fertilized flowers grow, mature and
ripen within two months (Image 4g-k). Fruit exhibits different colours - green, light purple, dark purple and violet
during growing and maturing phase (Image 4l). It is a globoseberry, luscious, fleshy, 25–30 mm in diameter and edible. It has a combination of sweet, mildly
sour and astringent flavor and colours the tongue
purple when eaten. The green and
light purple fruits are very tasty and sweet while the dark purple and violet
ones are sweet and bitter. Each
fruit produces a single large seed only. The fruits fall off during late July–August. The locals were found to collect ripe
fruits from trees and fallen fruits from the ground since they are edible and
have commercial value.
Seedling ecology
The habitat of the
plant is rocky with steep slope covered with little litter and moisture. The seedlings recorded in the area were
58 in 2011, 32 in 2012 and 17 in 2013. These were subjected to drought stress due to erratic rainfall. Further, extensive and robust grass
cover during that period was found to be having impact on the surviving
seedlings of the plant. Finally, 27
seedlings in 2011, 16 in 2012 and seven in 2013 have established and are
growing continually at slow pace. The soil analysis for available nitrogen (N), phosphorous (P) and
potassium (K) indicated that N is 270 kg/ha, P 13.57 kg/ha and K 282
kg/ha. These values show that these
nutrients are not present in optimal levels and hence there is a deficiency in
essential nutrients in the soil. The seeds sown in experimental bags showed that seeds germinate within
two weeks and form seedlings subsequently (Image 4m-p). The seed germination
rate is 74%.
DISCUSSION
S. alternifolium is a
semi-evergreen mass-flowering tree species in the study area. It is not only
endemic but also endangered due to its declining population. The plant is not found in some sites
where it was reported by previous workers as cited above. It is exploited for various local uses
and hence it has now attained “Endangered” status. It qualifies for inclusion in the IUCN
Red List.
In Syzygium genus, the flowering pattern is of two
types, mass flowering and short-period steady state flowering but most species
exhibit mass flowering such as S. tierneyanum(Lack & Kevan 1984), S. cuminii(Reddi & Rangaiah1999–2000), S. luehmannii (Sanewski 2010), S. sayeri(Williams & Adam 2010) and S. aqeum (Tarai & Kundu 2008). S. alternifolium is also a mass bloomer and it
flowers during dry season. The
flowering occurs after partial leaf shedding and leaf flushing occurs after the
completion of flowering. This
finding does not agree with the observation made by Mohan & Lakshmi (2000)
that the flowering and fruiting events occur after new leaf formation in this
species. The 3-year study on the
flowering phenology of S. alternifoliumindicated that mass flowering is not a regular event since the observations
showed that flowering intensity varied, it is massive in the first year and
moderate in the second and third year, and also little flowering on a few
branches of some trees in the third year. Such a flowering pattern appears to be a function of abrupt changes in
water availability and temperature due to erratic and low rainfall, and below
optimal NPK nutrient levels in soil due to rocky terrain, dry and poor stony
soils with little in situ litter accumulation. Sanewski(2010) stated that such a flowering pattern occurs in Syzygiumspecies and the author related it to abrupt changes in water availability and
temperature in monsoon sites. Troncoso et al. (2006) reported that flowering in Olea europaea is
not an annual event and observed a considerable depletion of the N and K
contents in the leaves at the end of the fruiting year and an increase in these
values at the end of the non-flowering season. They stated that a recovery of the
mineral content is required for flower bud differentiation to reoccur and water
and thermal stress may induce an imbalance between vegetative development and
fruiting. Lavee(2007) suggested that flowering and subsequent fruit bearing could be a
built-in character and over all controlled by an interaction between vegetative
growth and fruit load. Such an
expression involves a wide range of changes in activation and repression of
endogenous metabolic pathways. A
continuous and complex interaction between the ambient temperature, humidity
and other environmental factors is involved in both the vegetative and
reproductive development. Sanewski (2010) stated that in most tree species, adequate
starch levels are required for the production of flowers, particularly
mass-flowering species, like most of the Syzygium. Trees with insufficient starch levels
may not flower heavily in that year and hence, gradually move into an alternate
bearing pattern. Adequate starch
reserves are a pre-requisite for flowering while environmental factors are
usually the trigger. The variation
in flowering intensity in the mass blooming S. alternifoliumcould be attributable to starch levels available at the time of flowering
season. Several studies have
documented the influence of rainfall or water levels on the flowering intensity
in mass blooming Syzygium species. In southern Taiwan, Liao & Lin
(2001) reported that S. samarangense exhibited
early mass flowering in summer after flooding for about 40 days at the
site. Falcaoet al. (2002) reported that S. malaccensisflowers twice in a single year, the first spell in wet season and the second
spell in dry season in Brazil (Falcao et al.
2002). Tarai& Kundu (2008) noted that S. aquem flowers twice in a single year in India. Sanewski(2010) observed that S. luehmannii flowered
massively in the first spell and showed minor flowering in the second spell
after unseasonal heavy rainfall in spring in southeast Queensland, Australia
and attributed such a flowering response to the prevailing temperature and
water availability (Sanewski 2010). Law et al. (2000) reported that high
rainfall in summer-autumn period resulted in heavy flowering in spring for most
of the Myrtaceae members. Keatley et al.
(2002) reported a significant relationship between temperature and rainfall and
flowering in eucalypts over 23 years. Therefore, water, temperature and soil nutrient status appear to
influence and regulate the flowering event collectively in S. alternifolium.
The studied
species of Syzygium for their breeding
systems indicate that both self-compatible and self-incompatible species exist
in this genus but self-compatible species are most common (Sanewski2010). S. tierneyanum and S. nervosumin northern Australia (Hopper 1980; Shapcott 1998), S.cuminii in India (Reddi& Rangaiah 1999–2000), S. rubicundum in Sri Lanka (Stacey 2001), S. lineatum in Indonesia (Lack & Kevan1984), and S. samarangense, S. jambos,
S. megacarpum, and S. formosumin Thailand (Chantaranothai & Parnell 1994) are
self-compatible. S. syzygiodesis strongly self-incompatible in Sulawesi (Williams & Adam 2010) and S. cormiflorum in Australia is basically a xenogamous species (Crome &
Irvine 1986). The present study
shows that S. alternifolium is
self-incompatible and an obligate out-crosser. Khan et al. (1999) also mentioned that
it is an out-breeder and routinely propagated by seed. Floral overproduction through mass
flowering pattern and production of floral rewards in all flowers through
hermaphroditic sexual system appear to be evolved characters for the attraction
of more pollinators and for the function of obligate out-crossing breeding
system. However, the success of
this breeding system depends on the cross-pollination rate
which in turn is linked to the foraging efficiency and the frequency of
inter-plant foraging visits by effective pollinators. Although the plant is characteristically
a mass bloomer, all the individuals do not flower consecutively and even those
flowering in consecutive years do not show mass blooming. Such a flowering pattern affects the
out-crossing rate as well as fruiting rate and hence, is a limitation for the
success of sexual reproduction in S. alternifolium. Nevertheless, the mass blooming years
facilitate higher fruit set and provide a ‘reproductive assurance’ against
moderate to sparse flowering years and losses due to bud and flower
infestations which are evidenced in the present study. The bud infestation in S. alternifolium is because of breeding by a moth
species. The adult moth deposits
its eggs in young flower buds and the developing larvae consume the entire bud
over a period of approximately one week. Such a bud infestation by a moth, Polyhymnosp. has been reported in S. mamillatum (Kaiser
et al. 2008).
Myrtaceae members, in
general, do not have specialized pollination systems and attract a wide range
of vertebrate and invertebrate floral visitors (Eldridge 1970; Carpenter 1976;
Hopper 1980; Hopper & Moran 1981). Williams & Adam (2010) documented the pollination biology aspects ofSyzygium tierneyanum,
S. sayeri, S. floribundumand S. cormiflorum. S. tierneyanum is visited by 45 species of nectar
feeding animals; honeyeaters and hawk moths are considered as most important
pollinators due to their abundance and foraging behavior despite the honeybees
being the prolific visitors. Blossum bats and honeyeaters contribute about half of the
pollination rate and the rest is contributed mainly by
butterflies, flies, thrips and wasps in S. sayeri. The mass-flowering S. floribundum is
pollinated by a guild of insects but bats do not visit its flowers although
they occur in the area. In S. cormiflorum,
birds, insects and particularly blossom bats are effective pollinators; the
last together with hawk moths constitute a greatest percentage of successful
pollination (Crome & Irvine 1986; Williams &
Adam 2010). S. paniculatum with generalized
pollination strategy is visited by a variety of insects (Payne 1991,
1997). In Sulawesi, S. syzygiodes and occurring in the lowland rain forest is entomophilous and pollinated by a guild of short-tongued
unspecialized insects. In Samoa, S.inophylloides and S. samarangenseare regularly foraged by birds (Cox et al. 1992). Empirical studies on the pollination of Syzygium species here are absent but observers have
suggested that bats are important pollinators of these species (Wiles &
Fujita 1992; Trail 1994; Banack 1996). In American Samoa, S.dealatum is primarily pollinated by the
invertebrates and one small vertebrate. Birds and bats do not visit its flowers
although they are present at the study site. Further, it is also considered to be anemophilous due to its location on a highly exposed rocky
point characterized by high wind speeds. Insects are relatively more important
pollinators of S. effusum and birds and
bats are likely most important pollinators of S. neurocalyx(Webb & Solek 1996). In East Java, S. pycnanthum is reported to be visitedby a guild of insects by Mudiana & Ariyanti (2010). S. mamillatumis pollinated by generalist bird species in Mauritius (Kaiser et al. 2008). S.mundagam in the wet
evergreen forest of Western Ghats of India is pollinated exclusively by bats
(Ganesh 1996). In southern India, S.cuminii with chiropterophilouspollination syndrome is in reality entomophilous and
effected by twenty-four species of insects consisting of nocturnal, crepuscular
and diurnal ones (Reddi & Rangaiah1999–2000). But, these
authors stated that entomophily is ineffective and as a result it has evolved
certain floral traits that facilitate effective anemophily.
In S. alternifolium, the floral characters such as the flower-opening during dusk hours, commencement of stigma
receptivity during late evening and weak nectar by sugar concentration are
adaptations for chiropterophily (Faegri& van der Pijl 1979; Wyatt 1983; Crome & Irvine 1986). But, bats never visited the flowers
though they are common in the region. The diurnal Hawk Moth Cephonodes hylas is the only species that visits the flowers
during dusk hours. It is a swift
flier, gathers nectar quickly from each flower and moves fast between
inflorescences and conspecific plants. It strikes the dehisced stamens and stigma while collecting nectar and
contributes primarily to cross-pollination since the stigma is not receptive then
in fresh flowers but receptive in two-day old flowers. The same moth is the first visitor to
the flowers during early morning hours and contributes to cross-pollination in
both one-day and two-day old flowers. African Fat-tailed Gecko Hemitheconyx caudicinctus is a nectar-feeder after sunset and
until late evening. It does not
contribute to cross-pollination since it remains on the same plant collecting
nectar from fresh or old flowers. The floral characters such as intense
flowering, sweet-scented and actinomorphic flowers, shaving-brush type stamens
and copious nectar are adaptive for generalist flower visitors. In line with this, bees, wasps and
butterflies are found to be prolific foragers during daytime up to noon-time. The
observed foraging behaviours of these insects
indicate that Apis dorsataand Amegilla sp. among bees and all visiting
wasps are important in effecting cross-pollination due to their frequent
foraging flights between conspecific flowering individuals while all others
play little role in promoting cross-pollination. All these insects exhibit flower
constancy during the entire length of flowering period of S. alternifolium since the flowers are important pollen
and nectar sources. The nectar is
rich in protein content, sucrose sugar and also a source of six essential and nine
non-essential amino acids for insects. Both invertebrate (insects) and vertebrate (gecko) foragers are highly
benefitted during the flowering season of S. alternifolium,
when food resources are scarce due to the absence of flowering in most of the
co-occurring plants in the study region. However, S. alternifolium is not an
assured food source for them every year due to great variation in the intensity
of flowering annually. During the
years of low intensity of flowering, they shift to Shorea roxburghii and S. tumbuggaia which flower
almost at the same time. But, the
flowers of these two species are not preferred when mass flowering occurs in S.alternifolium.
In S. alternifolium, the pollen is liberated into the ambient
environment with two peak concentrations, one at 19:00hr and the second at
09:00hr. The pollen concentration
gradually decreases with the distance from the plant. The triangular and tricolporate non-sticky pollen grains that fall in the size
range of 12–58 µm are suited for anemophily (Erdtman1952; Srivastava 1982). The pollen grains of S. alternifolium also have the same characteristics and
their size is 16.6µm. These
characteristics and the pollen release into the ambient environment conform to
the occurrence of anemophily. The
location of the plant on the exposed rocky area and the occurrence of high wind
speed are additional advantages for effective anemophily as in case of S. dealatum in American Samoa (Webb & Solek 1996). Therefore, S. alternifolium with
generalist pollination system is adapted to both entomophily and anemophily,
the occurrence of which is referred to as ambophily, sensu Yamasaki & Sakai (2013).
Webb & Solek (1996) stated that the generalist pollination system
would increase the probability of successful establishment by Syzygium species in novel environments, including
islands. Their statement appears to
be based on self-compatible species like S. cormiflorum which breeds
through geitonogamy and hence could significantly
contribute to the wide distribution of the species. In the present study, S. alternifolium with generalist pollination system cannot
establish in isolated or novel environments in the absence of other conspecific
individuals nearby or in the surroundings due to self-incompatible and obligate
out-crossing breeding system. Khan
et al. (1999) reported that vegetative propagation is also not a successful
mode in S. alternifolium. These could be
important limitations for the restricted distribution of the species only to
this part of India.
In S. alternifolium, the fruit set and seed set rates are the
same due to the production of 1-seeded fruits. With generalist pollination system and ambophily, the plant is able to set fruit at 11% despite
the presence of self-incompatibility, inefficient insect pollination, soil
water stress and nutrient deficiency. Further, highly significant bud infestation by a moth, flower predation
by the beetle, Popillia impressipygaand common occurrence of mounds formed of buds and flowers collectively show
significant negative impact on the success of sexual reproduction. Therefore,
both intrinsic and external factors regulate the production of ultimate fruit
set.
Boyer (1982)
stated that the most growing conditions enable many plant species to initiate
sufficient numbers of ovules to maximize reproduction. But most plants do not experience
optimal growth conditions and hence they inevitably abort some of these
ovules. Lee & Bazzaz (1986) reported that the nutritional demand of
reproduction frequently exceeds the carbon and nitrogen resources allocated to
the ovule under environmental stress. Consequently, the number of ovules initiated often exceeds the capacity
of the gynoecium or, by extension, the plant to provide adequate nutrition for
them all. Westgate & Boyer
(1985) reported that the rate of photosynthesis dramatically drops in maize
following water stress while Schussler & Westgate
(1995) as a follow up study reported that this dramatic drop in photosynthesis
results in reduced sugar transport into the embryo sac and in effect, it limits
resources for seed development. These authors also noted that in healthy plants, manual removal of some
developing ovules decreases the overall rate of abortion by providing more photosynthate for surviving ovules. El-Keblawy& Lovell-Doust (1999) in a subsequent study on
cucurbits reported that the total number of ovules maturing into seeds remained
steady while the rate of ovule abortion declined when a portion of the ovules
were surgically removed from the ovary. On the contrary, S. alternifolium under
water stress and nutrient-deficient environment during dry season produces the
same number of ovules per ovary but only one ovule forms the seed. It indicates that the plant does not
have any regulatory mechanism to prevent overproduction of ovules to save
energy resources for more seed output. Lughada & Proenca(1996) reported that in Myrtaceae species, the ovary
usually contains more embryos than will form seed. Arathi et al.
(1996) and Krishnamurthy et al. (1997) have studied ovule abortion in S. cuminii and related this event to an inhibition of
resource uptake by the sub-ordinate seeds. They also substantiated this observation by experimental work in which
the extracts from the dominant seeds, containing predominately indole compounds inhibited resource uptake by the
sub-ordinate seeds and hence the plant usually develops only 1 of 30 ovules to
maturity. Such a situation can be
expected in its allied species, S. alternifoliumin which also only 1 out of 21–38 ovules forms the seed.
In Syzygium genus, apomixisoccurs and it is considered to be linked to polyembryony (Chantaranothai& Parnell 1994; Lughadha & Proenca 1996). S. cuminii(Arathi et al. 1996; Krishnamurthy et al. 1997; Kader
et al. 2000), S. javanicum (Ikeda 1979), and S.jambolana (Ladhar &
Gill 1991) and S. alternifolium (Khan et al.
1995) are polyembryonic. The present study indicates that S. alternifolium is neither apomictic nor polyembryonic; the seed characteristically produces a
single seedling.
Maturation,
dispersal and germination of tree seeds in the seasonally dry tropical forest
ecosystem are synchronized to a considerable extent to seasons (Frankie et al.
1974; Garwood 1982). Dry fruits
more frequently ripen and disperse seeds during the dry season, while fleshy
and pulpy fruits ripen and disperse seeds during the rainy season (Roth 1987). A majority of fleshy and pulpy fruits
produce seeds that take a long time to germinate, possibly because of their
dependence on frugivores for dispersal. These are seeds mostly with hard,
mechanically resistant coats that protect the embryo from damage during chewing
or enzymatic action while passing through the gut. Seeds of some species of
this category take several years to germinate (Troup 1921) and length of
dormancy could be a secondary effect of a defense mechanism. Other fruits that depend on slow
decomposition or insect action for release of seeds take a long time to germinate. These requirements may have led to
selection for delayed germination. Thus, it follows that, subsequent to maturation, three conditions
determine the fate of seeds: dispersal at the appropriate season favourable for germination, germination at favourable times by those remaining dormant, until
conditions become conducive for germination, or germination after they are
carried to a habitat favourable for germination. Corlett (1996)
stated that colourful displays of ripe fruit likely
evolved in order to attract avian dispersal agents. Frugivorousbirds, thus, serve as selective agents of plants by favoring those species
whose seeds could disperse to potential safe sites. The subsequent seed dispersal pattern
not only determines the potential area of plant recruitment, but also serves as
a template for subsequent processes, such as predation, competition and mating
(Nathan & Muller-Landau 2000). The fruits of red, brown, deep brown color with pulp as a reward exhibit
animal dispersal mode (Du et al. 2009). On the contrary, S. alternifoliumexhibits colourful displays of unripe and ripe fruits
but they are never used by avians. The fallen fruits are
mostly collected by locals due to their edible nature and there was no
fruit or seed predation by animals. But, an earlier report by Mohan & Lakshmi (2000) stated that the
fruits are relished by Wild Boar, Sloth Bear and herbivores such as Sambar. Nevertheless, only the leftover fruits or seeds have the chance for
germination and subsequent formation of seedlings under optimal growth
conditions. Khan et al. (1999)
reported that seeds of S. alternifolium cannot be stored for long periods due to short viability and
insect attack. The present study
also shows that most of the seeds of S. alternifoliumare healthy, viable and germinate immediately if favourablesoil water and nutrient conditions exist; high germination rate could be
because of quality seed resulting from cross-pollination. Further, insect attack on the fruits or
seeds was not observed but the pulpy part gradually decomposed exposing the
seed during rainy season. Since the
seed viability is short, its viability span lasts only until the end of rainy
season and hence it does not have several opportunities for germination
thereafter. Even when germinated,
the seedlings experience mortality due to erratic rainfall or interval of
drought within the rainy season (Troup 1921). Therefore, rainy season is the prime
determinant of seed germination and seedling establishment in S. alternifolium. This finding is in line with the generalization made by Angevine & Chabot (1979) that in most tropical forests
of India, a 3-month monsoon period is the prime determinant of all biological
processes, including seed germination, seedling establishment and plant growth
and development. Germination
responses during monsoon period are suggestive of the occurrence of drought
avoidance syndrome in majority of tree species and most other plants in these
tropical forests.
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