Pollination biology of the
crypto-viviparous Avicennia species (Avicenniaceae)
A.J. Solomon Raju 1, P.V. Subba Rao 2, Rajendra
Kumar 3 & S. Rama Mohan 4
1,4 Department of Environmental Sciences, Andhra
University, Visakhapatnam, Andhra Pradesh 530003, India
2,3 Ministry of Environment and Forests,
Paryavaran Bhavan, CGO Complex, Lodhi Road, New Delhi 110003, India
Email: 1 solomonraju@gmail.com (corresponding author), 2pvsrao8@gmail.com, 3 rajekr.72@gmail.com
Date of publication (online): 26
December 2012
Date of publication (print): 26 December 2012
ISSN 0974-7907 (online) | 0974-7893 (print)
Editor: Cleofas Cervancia
Manuscript details:
Ms # o2919
Received 20 August 2011
Final received 06 December 2012
Finally accepted 06 December 2012
Citation: Raju, A.J.S., P.V.S. Rao, R. Kumar & S.R. Mohan (2012). Pollination biology of the crypto-viviparous Avicenniaspecies (Avicenniaceae). Journal of Threatened Taxa4(15): 3377–3389.
Copyright: © A.J. Solomon Raju, P.V. Subba Rao, RajendraKumar & S. Rama Mohan 2012. Creative Commons Attribution
3.0 Unported License. JoTT allows unrestricted use of this article in
any medium for non-profit purposes, reproduction and distribution by providing
adequate credit to the authors and the source of publication.
Author Details:
Prof. A.J. Solomon Raju is Head in 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 UGC and MoEF, and on mangroves of Andhra Pradesh with financial
support from MoEF.
Dr. P.V. Subba Rao is Assistant Director working in the Ministry of Environment
& Forests, Government of India, New Delhi.
Mr. Rajendra Kumar is Research Officer working in the Ministry of Environment
& Forests, Government of India, New Delhi, and also pursuing PhD
(part-time) under Prof. A.J. Solomon Raju.
Dr. S. Rama Mohan is Assistant Director, Department of Horticulture, Government of Andhra Pradesh. He has worked under Prof. A.J.
Solomon Raju for PhD during which he did part of the work reported in this
paper.
Author Contribution: The field work was done by all but it
is mainly carried out by AJSR and SRM. All four authors have contributed in the preparation of manuscript but
Prof. Raju is the main person among all.
Abstract: Floral biology, sexual system, breeding system, pollinators, fruiting
and propagule dispersal ecology of crypto-viviparous Avicenniaalba Bl., A.
marina (Forsk.) Vierh. and A. officinalis L. (Avicenniaceae)
were studied in Godavari mangrove forests of Andhra Pradesh State, India. All the three plant species initiate
flowering following the first monsoon showers in June and cease flowering in
late August. The flowers are
hermaphroditic, nectariferous, protandrous, self-compatible and exhibit mixed
breeding system. Self-pollination
occurs even without pollen vector but fruit set in this mode is
negligible. In all, the flowers are
strictly entomophilous and the seedlings disperse through self-planting and
stranding strategies.
Keywords: Avicennia species,
entomophily, mixed breeding system protandry, self-compatibility.
For figures, images, tables -- click here
Introduction
The family Avicenniaceae comprises of only one genus Avicennia. The genus consists of at least eight
tree species which grow in the inter-tidal zone of coastal
mangrove forests and ranges widely throughout tropical and warm
temperate regions of the world (Tomlinson 1986; Duke 1991). These species occupy diverse mangrove
habitats, either within the normal tidal range or in back mangal and a high
tolerance of hyper-saline conditions. Of these, three species occur in Atlantic-East Pacific and five species
in the Indo-West Pacific (Duke 1992). The East Africa and the Indo-Pacific species include A. officinalis, A. marina, A. alba, A. lanata, A.
eucalyptifolia, A. balanophora and only the first three species reached the
Indian subcontinent (Duke et al. 1998). A. officinalis has a wide range from
southern India through Indo-Malaya to New Guinea and eastern Australia. A. marinahas the broadest distribution, both latitudinally and longitudinally with a
range from East Africa and the Red Sea along tropical and subtropical coasts of
the Indian Ocean to the South China Sea, throughout much of Australia into
Polynesia as far as Fiji, and south to the North Island of New Zealand
(Tomlinson 1986). A. marina has the distinction of being the most widely
distributed of all mangrove tree species. The ubiquitous presence in mangrove habitats around the world is due to
the ability to grow and reproduce across a broad range of climatic, saline, and
tidal conditions and to produce large numbers of buoyant propagules annually
(Duke et al. 1998). A. alba has a wide distribution from India to Indochina,
through the Malay Archipelago to the Philippines, New Guinea, New Britain, and
northern Australia.
Tomlinson (1986) gave a brief account of the floral biology of Avicenniaspecies. A. officinalisis self-compatible and occasionally self-pollinating. Self-pollination of individuals is
unlikely due to protandry, but the sequence and synchrony of flowering,
together with pollinator behaviour favours geitonogamy. Clarke & Meyerscough (1991) reported
that it is pollinated by a variety of insects in Australia. These authors also reported that A.
marina is visited by ants, wasps, bugs, flies, bee-flies,
cantherid beetles, and moths but the most common visitor is Apis mellifera. Tomlinson (1986) described that A.
alba, A. marina and A. officinalis have very similar flowers and
hence may well be served by the same class, if not the same species of
pollinators; when these species grow together, there is evidence of
non-synchrony in flowering times, which might minimize the competition for
pollinators (probably bees) and at the same time spread the availability of
nectar over a more extended period. This state of information in a preliminary mode provided the basis for
taking up the present study on the pollination biology of crypto-viviparous Avicenniaalba Bl., A. marina (Forsk.) Vierh. and A. officinalis L. in Coringa mangrove forest of
Andhra Pradesh. This paper
describes the details of floral biology, sexual system, breeding system,
pollinators and seedling ecology of these three Avicennia species. Further, these aspects have been
discussed in the light of the existing relevant literature.
Materials and Methods
Floral biology
The crypto-viviparous Avicennia alba, A.
marina and A. officinalis (Avicenniaceae) occurring in Godavari
mangrove forest (16030’–17000’N & 82010’–80023’E)
in the state of Andhra Pradesh, India, were used for the present study. The study was conducted during February
2008–April 2010. Regular
field trips were conducted to track the flowering season in order to take up
intensive field studies at weekly intervals during their flowering and fruiting
season. The flower’s morphological
characteristics were described based on 25 flowers collected at random for each
species. Quantification of the
number of flowers produced per inflorescence and the duration of inflorescence
were determined by tagging 10 inflorescences, which have not initiated
flowering, selected at random and following them daily until they ceased
flowering permanently. Anthesis was
initially recorded by observing marked mature buds in the field. Later, the observations were repeated
3–4 times on different days during 0600–1400 hr in order to provide
accurate anthesis schedule for each plant species. Similarly, the mature buds were followed
for recording the time of anther dehiscence. The presentation pattern of pollen was
also investigated by recording how anthers dehisced and confirmed by observing
the anthers under a 10x hand lens. Twenty five mature but undehisced anthers was collected from
different plants 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 mean pollen output per anther was
multiplied by the number of anthers in the flower for obtaining the mean number
of pollen grains per flower. The
characteristics of pollen grains were also recorded. The pollen-ovule ratio was determined by
dividing the average number of pollen grains per flower by the number of ovules
per flower. The value thus obtained
was taken as pollen-ovule ratio (Cruden 1977). The presence of nectar was determined by
observing the mature buds and open flowers. The volume of nectar from 20 flowers
collected at random from each plant species was determined. Then, the average volume of nectar per
flower was determined and expressed in µl. The flowers used for this purpose were bagged at mature bud stage,
opened after anthesis and squeezed nectar into micropipette for measuring the
volume of nectar. Nectar sugar
concentration was determined using a Hand Sugar Refractometer (Erma,
Japan). For the analysis of sugar
types, paper chromatography method described by Harborne (1973) was followed.
Nectar was placed on Whatman No. 1 of filter paper along with standard samples
of glucose, fructose and sucrose. The paper was run ascendingly for 24 hours with a solvent system of
n-butanol-acetone-water (4:5:1), sprayed with aniline oxalate spray reagent and
dried at 1200C in an electric oven for 20 minutes for the
development of spots from the nectar and the standard sugars. Then, the sugar types present and also
the most dominant sugar type were recorded based on the area and colour
intensity of the spot. Nectar amino
acid types present in A. officinalis were also recorded as per the paper
chromatography method of Baker & Baker (1973). Nectar was spotted on Whatman No. 1
filter paper along with the standard samples of 19 amino acids, namely,
alanine, arginine, aspartic acid, cysteine, cystine, glutamic acid, glycine,
histidine, isolecuine, leucine, lysine, methionine, phenylalanine, proline,
serine, threonine, tryptophan, tyrosine and valine. The paper was run ascendingly in chromatography
chamber for 24 hours with a solvent system of n-butanol-glacial acetic
acid-water (4:1:5). The
chromatogram was detected with 0.2% ninhydrin reagent and dried at 850C
in an electric oven for 15 minutes for the development of spots from the nectar
and the standard amino acids. The
developed nectar spots were compared with the spots of the standard amino
acids. Then, the amino acid types
were recorded. The stigma
receptivity was observed visually and by H2O2 test. In
visual method, the stigma physical state (wet or dry) and the unfolding of its
lobes were considered to record the commencement of receptivity; withering of
the lobes was taken as loss of receptivity. H2O2 test as given
in Dafni et al. (2005) was followed for noting stigma receptivity period.
Pollinators
The insect species visiting the flowers were observed visually and by
using Olympus Binoculars (PX35 DPSR Model). There was no night
time foraging activity at the flowers. Their foraging activity was confined to
daytime only and were observed on a number of occasions on each plant species
for their foraging behaviour such as mode of approach, landing, probing
behaviour, the type of forage they collect, contact with essential organs to
result in pollination and inter-plant foraging activity in terms of
cross-pollination. The foraging
insects were captured during 1000–1200 hr on each plant species and
brought them to the laboratory. For
each insect species, 10 specimens were captured and each specimen was washed
first in ethyl alcohol, the contents stained with aniline-blue on a glass slide
and observed under microscope to count the number of pollen grains
present. In case of pollen
collecting insects, pollen loads on their corbiculae were separated prior to
washing them. From this, the
average number of pollen grains carried by each insect species was calculated
to know the pollen carryover efficiency of different insect species.
Breeding system
Mature flower buds of some inflorescences on different individuals were
tagged and enclosed in butter paper bags for breeding experiments. The number of flower buds used for each
mode of pollination for each species was given in Table 1. The stigmas of flowers were pollinated
with the pollen of the same flower manually by using a brush; they were bagged
and followed to observe fruit set in manipulated autogamy. The flowers were fine-mesh bagged
without hand pollination to observe fruit set in spontaneous autogamy. The emasculated flowers were
hand-pollinated with the pollen of a different flower on the same plant; they
were bagged and followed for fruit set in geitonogamy. The emasculated flowers were pollinated
with the pollen of a different individual plant; they were bagged and followed
for fruit set in xenogamy. If fruit
set is there, the percentage of fruit set was calculated for each mode. The flowers/inflorescences were tagged
on different plant species prior to anthesis and followed for fruit and seed
set rate in open-pollinations.
Seedling ecology
Fruit maturation period and hypocotyl or seedling growth period prior to
detachment from the parent tree were also recorded. Rose-ringed Parakeet feeding on fruit
and/or hypocotyls of A. alba and A.
marina was observed. A sample
of fruits/hypocotyls was collected at random from these plant species to
calculate the percentage of damage. Casual observations on seedling dispersal during low and high tide
periods were made to record the dispersal mode.
Photography
Plant, flower and fruit details together with insect foraging activity
on flowers were photographed with Nikon D40X Digital SLR (10.1 pixel) and TZ240
Stereo Zoom Microscope with SP-350 Olympus Digital Camera (8.1 pixel).
Results
The three Avicennia species are evergreen trees with irregular
spreading branches (Image 1a; 2a). Following monsoon showers in June, they initiate flowering and continue
flowering until the end of August. Individual trees flower for 35±4 (Range
32–48) days in A. alba, 33±2 (Range
32–35) days in A. marina and 38±4 (Range 36–41) days in A.
officinalis. In all the three
species, the flowers are borne in terminal or axillary racemes/panicles (Image
1b; 2b; 2a). An inflorescence
produces 52.34±26.96 flowers (Range 15–123) over a period of 25 days
(Range 24–28) in A. alba, 47±13.97
flowers (Range 26–76) over a period of 22 days (Range 15–22) in A.
marina and 32±11 flowers (Range 9–35) over a period of 16–25
days in A. officinalis.
The flowers are sessile, small (4mm long; 3mm diameter), orange yellow,
fragrant, actinomorphic and bisexual in all the three species. They are slightly scented in A. alba and A. marina while foetid in A.
officinalis. The flowers are
4mm long and 3mm diameter in A. alba, 6mm long
and 5mm diameter in A. marina, and 10mm long and 10mm diameter in A.
officinalis. Calyx is short,
elliptic and has four ovate, green, pubescent sepals with hairs on the outer
surface. Corolla has four thick,
orange yellow ovate petals forming a short tube at the base. The petals are glabrous inside and hairy
outside in A. marina while the adaxial petal is the broadest and
shallowly bi-lobed in A. officinalis. Stamens are four, epipetalous, occur at
the throat of the corolla. The
anthers are basifixed, exserted, introrse and arranged alternate to
petals. The ovary is 2mm long in A.alba and A. marina while it is 7mm long in A.
officinalis. In all, it is
conspicuously hairy and bicarpellary syncarpous with four imperfect locules and
each locule contains one pendulous ovule. It is terminated with a 1–2 mm long
glabrous style tapered to the bifid hairy stigma. The light yellow style and stigma arise
from the center of the flower and stand erect throughout the flower life. In A. officinalis, the entire
female structure is over-arched by stamens above. The style is bent, situated below the
adaxial corolla lobe but not in the center of the flower.
The mature buds open throughout the day but most buds opening during
0900–1200 hr in A. alba (Image 1c,d), during 1000–1300 hr inA. marina (Image 2c,d) and during 0800–1100 hr in A.
officinalis (Image 3b–d). The petals slowly open and take 3–4 hours for complete opening to
expose the stamens and stigma. The
stamens bend inward overarching the stigma at anthesis and the all the anthers
dehisce ½ hour after anthesis by longitudinal slits. The stigma is well seated in the center
of the flower. In A. officinalis,
the stamens gradually stand erect and bend backwards over a period of three
days. After anthesis, the stigma
grows gradually and becomes bifid on the morning of the 2nd day in A. alba (Image 1e,f) and A. marina (Image
2e,f) and on the 3rd day in A. officinalis (Image
3e–h). The bifid condition of
stigma is an indication of beginning of stigma receptivity and it remains
receptive for two days in A. alba and A.
marina, and for five days in A. officinalis. The stigmatic lobes recurve
completely. The flower life is six
days in A. alba, five days in A. marinaand seven days in A. officinalis. The petals, stamens and stigma drop off while the calyx is persistent in
all the three species.
The pollen production per anther is 1,967±31.824.3 (Range
1,929–2,010) in A. alba, 1,643.2±31.8
(Range 1,600–1,690) in A. marina and 2,444±202.4 (Range
2,078–2,604) in A. officinalis. In all, the pollen grains are light
yellow, granular, tricolporate, reticulate, muri broad, flat, thick; lumina
small irregularly shaped and colpi deeply intruding (Image 6a–c). Their size is 24.9μm in A. alba and 33.2μm in both A. marina and A.
officinalis. The pollen-ovule
ratio is 1,967:1 in A. alba, 1,643.2:1 in A.
marina and 2,209.3:1 in A. officinalis. In all, the flowers begin nectar
secretion along with anther dehiscence. The nectar secretion occurs in minute amount whichis accumulated at the ovary base and on the yellow part of petals; the nectar
glitters against sunlight. A flower
produces 0.5±0.1 (Range 0.4–0.7) μl of nectar with 40% sugar
concentration in A. alba, 0.4±0.08 (Range 0.3–0.5) μl of
nectar with 38% sugar concentration in A. marina and 0.65±0.09 (Range
0.5–0.8) μl of nectar with 39% sugar concentration in A.
officinalis. The sugar types
included glucose and fructose and sucrose with the first as dominant in A.
alba and A. marina and the last as dominant in A. officinalisin which the nectar amino acids included aspartic acid, cysteine, alanine,
arginine, serine, cystine, proline, lysine, glycine, glutamic acid, threonine
and histidine.
In all three Avicennia species, the results of breeding systems
indicate that the flowers are self-compatible and self-pollinating. In A. alba, the fruit set is
17.5% in spontaneous autogamy, 40% in hand-pollinated autogamy, 62.5% in
geitonogamy, 64.28% in xenogamy and 42% in open pollination (Image 1i) (Table
1). In A. marina, the fruit
set is 12% in spontaneous autogamy, 33.33% in hand-pollinated autogamy, 40% in
geitonogamy, 68% in xenogamy and 55% in open pollination (Image 2j) (Table
1). In A. officinalis, the
fruit set is 21.42% in spontaneous autogamy, 42.85% in hand-pollinated
autogamy, 63.33% in geitonogamy, 67.85% in xenogamy and 58.13% in open
pollination (Image 5a) (Table 1).
The insects foraged the flowers of Avicennia species during day time from 0700–1700 hr. They were Apis dorsata, A. florea,Nomia sp., Chrysomya megacephala, an unidentified fly (Image 1g),Danaus chrysippus and Everes lacturnus (Image 1h) in A. alba;Halictus sp., Chrysomya megacephala, Eristalinus arvorum (Image
2h), Rhyncomya sp. (Image 2i), an unidentified fly (Image 2g), Polistis
humilis and Catopsilia pyranthe in A. marina; and Apis
dorsata (Image 4a), Xylocopa pubescens, Xylocopa sp. (Image
4b,c), Eristalinus
arvorum, Chrysomya megacephala(Image 4d), Sarcophaga sp. (Image 4e), Euploea core (Image 4j),
Danaus chrysippus, D. genutia (Image 4h), Junonia lemonias, J. hierta(Image 4i), a fly (Image 4f) and a wasp (Image 4g) (unidentified) in A.
officinalis. The flies
visited the flowers in groups while all other insects visited
individually. The bees were both
pollen and nectar feeders while all other insects only nectar feeders. All the insects probed the flowers in
upright position to collect the forage. In case of Xylocopa bees, they made audible buzzes while
collecting nectar aliquots from the petals. Butterflies landed on the petals,
stretched their proboscis to collect nectar aliquots on the petals and at the
flower base. In this process, all
the insects invariably touched the anthers and the stigma; the ventral side of
all insects was found powdered with pollen. Further, the body washings of the all
insect species revealed the presence of pollen; the average number of pollen
grains per insect for each species varied from 67.6 to 336.2; in A. albafrom 63.1 to 227.4, in A. marina, and from 73 to 550.2 in A.
officinalis (Table 2). As the
nectar is secreted in minute amounts, the insects made multiple visits to most
of the flowers on a tree and moved frequently between trees to collect
nectar. Such foraging behaviour was
considered to be effecting self- and
cross-pollination.
In all Avicennia species, pollinated and fertilized flowers
initiate fruit development immediately and take about 4–6 weeks to
produce mature fruits. In
fertilized flowers, only one ovule produces seed. Fruit is a 1-seeded leathery pale green
capsule with persistent reddish brown calyx. It is 40mm long, 15mm wide in A. alba, 30–35 mm long, 25mm wide in A. marinaand 30mm long, 25mm wide in A. officinalis. It is abruptly narrowed to a short beak
and hairy throughout. Seed produces
light green, hypocotyl which completely occupies the
fruit cavity (Image 5b). Fruit set
to the extent of 6% in A. alba and to the
extent of 4% in A. marina was damaged by the Rose-ringed Parakeet Psittacula
krameri which fed on the concealed hypocotyl in fruits and such fruits were
found to be empty. In all three Avicenniaspecies, the fruit together with hypocotyl falls off the mother plant; settles
in the substratum immediately at low tide period when the forest floor is
exposed; it floats in water and disperses by tidal currents at high tide period
until settled somewhere in the soil. The radicle side of hypocotyl penetrates the soil and produces root
system while plumule side produces new leaves and subsequent aerial
system. The fruit pericarp detaches
and disintegrates when plumular leaves are produced.
Discussion
All the three Avicennia species studied are principally
polyhaline evergreen tree species. These tree species show flowering response to monsoon showers in June; the first monsoon showers seem to provide the necessary
stimulus for flowering. Opler et
al. (1976) and Ewusie (1980) have reported such a flowering response to light
rains in summer season in a number of plants occurring in coastal
environments. The flowering
period extends until August in all the three species of Avicennia at the
study sites, indicating that the flowering season is only for three months in a
year. On the contrary,
Wium-Andersen & Christensen (1978) reported that in A. marina,
flowering occurs during April–May. Further, Mulik & Bhosale (1989) noted that the flowering in this
species is from April–September. These authors also mentioned that the flowering occurs during March-July
in A. officinalis. The
variation in the schedule and length of flowering season in these species may
be a response to local environmental conditions and to avoid competition for
the available pollinators depending on the flowering seasons and population
size of the constituent plant species which vary with
each mangrove forest. In all the
three species, the flowers are borne either in terminal or axillary
inflorescences. But, the average
number of flowers per inflorescence varies with each species; it is the highest
in A. alba, moderate in A. marina and
the least in A. officinalis. This flower production rate at inflorescence level may serve as an
important taxonomic characteristic for the identification of these three
species.
In all, the flowers are strongly protandrous and the stamens with
dehisced anthers over-arch the stigma. The stigma shows post-anthesis growth. It is erect and seated in the
center of the flower in A. alba and A.
marina while it is bent and situated below the adaxial corolla lobe in A.
officinalis. The erect stigma
does not change its orientation throughout the flower life in A. alba and A. marina while the bent stigma becomes
erect on day 3. The stigma is bifid
and appressed on the day of anthesis in all the three species; it remains in
the same state also on day 2 in A. officinalis. The stigma commences receptivity by
diverging in dorsi-ventral plane; it is receptive on day 2 and 3 in A. alba and A. marina, and on day 3, 4 and 5 in A.
officinalis. The timing of
commencement of stigma receptivity in A. officinalis strongly
contradicts with an earlier report by Reddi et al. (1995) that the stigma
attains receptivity three hours after anthesis with the bent stigma becoming
erect. In A. officinalis,
stigma behaviour is more advanced towards achieving cross-pollination. In all
the three species, self-pollination of individual flowers is unlikely on the
day of anthesis due to protandry but the stamens with dehisced anthers
over-arching the stigma may facilitate the fall of pollen on the receptive
stigma when the latter attains receptivity. In effect, self-pollination may occur
and the same is evidenced through fruit set in bagged flowers without manual
self-pollination. Further, the
sequence and synchrony of flowering, and pollinator behaviour at tree level
contribute to geitonogamy (Clarke & Meyerscough 1991). Hand-pollination results indicate that
it is self-compatible and fruit set occurs through autogamy, geitonogamy and
allogamy. The hermaphroditic
flowers with strong protandry and long period of flower life in these species
suggest that they are primarily adapted for cross-pollination. Clarke & Meyerscough (1991) also
reported that A. marina is protandrous, self-compatible and
self-pollinating but the fruits resulting from spontaneous self-pollination
showed a higher rate of maternal abortion reflecting an inbreeding
depression. Coupland et al. (2006)
reported that in A. marina, autogamy is most unlikely and emphasized the
importance of pollen vectors to the reproductive success. This report is not in agreement with the
results obtained in hand-pollination experiments on A. marina. Primack et al. (1981) suggested that
protandry promotes out-crossing in mangroves, and that insect pollination facilitates
it. They also suggested that
geitonogamy in coastal colonizing plants would allow some fruit set in isolated
colonizing plants, and thereafter the proportion of such pollinations would
decline as pollen is transferred between plants. Pollen transfer between plants in such
situations would still result in sibling mating. However, this is counteracted by
dispersal of propagules, canopy suppression of seedlings and irregular yearly
flowering among trees in close proximity. Clarke & Meyerscough (1991) reported that in A. marina, some
trees flower and fruit every year while some others do not flower every
year. Those with complete canopy
crops did not produce another large crop the following year. A similar pattern observed within a tree
where fruit is produced on one branch and in the following year heavy flowering
shifts to another branch. In the
present study, all the three species of Avicennia flowered annually and
the flowering is uniform on all branches within a tree. The study suggests that annual mass
flowering, protandry, self-compatibility and self-pollination ability are
important adaptations for Avicennia species to successfully colonize new
areas and expand their distribution range as pioneer mangroves.
All the three species of Avicennia are hermaphroditic and have
similar floral architecture. In
all, the flowers are of open type and shallow with small aliquots of nectar which is exposed to rapid evaporation resulting in
increased nectar sugar concentration. Corbet (1978) considered these characteristics as adaptations for fly
pollination. Hexose-rich nectar is
present in A. alba and A. marina while
sucrose-rich nectar in A. officinalis. Hexose-rich nectar is the
characteristic of fly- and short-tongued bee-flowers while sucrose-rich nectar
is the characteristic of wasps and butterflies (Baker & Baker 1982;
1983). The nectar sugar
concentration is high and ranged from 38–40 % in all the three Avicenniaspecies. Cruden et al. (1983) reported that high nectar sugar concentration
is the characteristic of bee-flowers while low nectar sugar concentration is
the characteristic of butterfly-flowers. Baker & Baker (1982) reported that the floral nectar is an important
source of amino acids for insects. Dadd (1973) stated that insects require ten essential amino acids of
which arginine, lysine, threonine and histidine are present in the nectar of A.
officinalis. He also reported
that proline and glycine are essential amino acids for some insects; these two
amino acids are also present in the nectar of A. officinalis. He further stated that other amino acids
such as alanine, aspartic acid, glutamic acid, glycine and serine while not
essential do increase insect growth. All these amino acids are also present in the nectar of A.
officinalis. Shiraishi & Kuwabara (1970) reported that proline
stimulates salt receptor cells in flies. Goldrich (1973) reported that histidine elicits a feeding response while
glycine and serine invoke an extension of the proboscis. The nectars of A. alba and A. marina have not been analyzed for
amino acids and hence this aspect has not been discussed.
The flowers of all the three species of Avicennia with
differences in their structural and functional characteristics as stated above
have been able to attract different classes of insects—bees, wasps, flies
and butterflies. Of these, bees
while collecting pollen and nectar, and all other insects while collecting
nectar effected pollination and their ability to carry pollen has been
evidenced in their body washings. Flies
are known as short distance fliers and such behaviour largely results in
autogamy or geitonogamy. Since
these flies visit the flowers as large groups, there is automatically a
competition for the available nectar which is secretedin small aliquots on the petals of all the three Avicennia species. In consequence, they shift from tree to
tree in search of nectar forage and in the process they contribute to both
self- and cross-pollination. All
other insects are habitual long-distance fliers and effectboth self- and cross-pollination. An earlier report by Subba Reddi et al.
(1995) showed that only bees and flies are the pollinators of A. officinalisat the study sites. Tomlinson
(1986) mentioned that Avicennia flowers are bee-pollinated. In Australia,A. marina is pollinated by ants, wasps, bugs, flies, bee-flies,
cantharid beetles and moths (Clarke & Meyerscough 1991).
Tomlinson (1986) documented that A. alba, A. marina and A.
officinalis have very similar flowers and hence may well be served by the
same class, if not by the same species of pollinators; when these species grow
together, there is evidence of non-synchrony in flowering times, which might
minimize the competition for pollinators (probably bees) and at the same time
spread the availability of nectar over a more extended period. In the present study, these plant
species grow together, flower synchronously but served by the same classes of
insects. There is no competition
for pollen among different classes of insects since only bees collect pollen
while all other classes of insects collect only nectar. Fly pollinators with their swarming
behaviour at the flowers may enable the plant species to set fruit to the
extent possible. Flies and bees are
usually consistent and reliable when compared to wasps and butterflies. Therefore, the study shows flies and
bees play an important role in the success of sexual reproduction in all the
three species of Avicennia. Despite being pollinated by different
classes of insect pollinators and having the ability to self-pollinate even in
the absence of insect activity as evidenced in bagged flowers, the natural
fruit set stands at 42–58 % in these plant species. This low fruit set
could be due to maternal abortion of self-pollinated fruits as reported by Clarke
& Meyerscough (1991), non-availability of sufficient pollen to receptive
stigmas due to pollen feeding activity of bees and the nutritional resource
constraint to the maternal parent. Coupland et al. (2006) while reporting on fruit set aspects of A.
marina in Australia mentioned that fruit set is not pollinator limited but
resource limited.
In Avicenniaceae, the flowers have been reported to contain four ovules
(Tomlinson 1986). In the present
study, all the three species of Avicennia are 4-ovuled but only one
ovule develops into mature seed in fertilized and fruited flowers as in
Rhizophoraceae. The production of
one-seeded fruits may be due to maternal resource constraint or maternal
regulation of seed set. Fruits grow
and mature within 5–6 weeks in A. alba and
within 4 weeks in the other two Avicennia species. The duration of fruit maturation is not
in agreement with the report of Wium-Andersen & Christensen (1978) who
stated that the development from flower bud to mature fruit takes a few months. The calyx is persistent in all the three
species but it does not expand to enclose the growing fruit. Therefore, the calyx has no role in
sheltering or protecting the fruit. As the fruit is a leathery capsule, it does not require any protection
from the calyx.
The single seed formed in the fruit is not dormant and germinates
immediately to produce chlorophyllous seedling whichremains within the fruit, while still on the maternal parent. This is a characteristic of
“crypto-viviparous” species; similar situation exists in the genera such as Aegiceras,
Aegialitis, Nypa and Pelliciera (Tomlinson 1986). In all these species, fruit is the
propagule; the seedling occupies the fruit cavity. The chlorophyllous seedling actively
photosynthesizes while the maternal parent supplies the water and necessary
nutrients (Selvam & Karunagaran 2004). In Avicennia species, the
propagules are small, light and the entire embryo is buoyant after detachment
from the maternal parent. Gradually, the fruit pericarp is lost exposing the leathery succulent
cotyledons to tidal water. Rabinowitz (1978) reported that A. marina has an absolute
requirement for a stranding period in order to establish since its propagules
always float in tidal water. He
also felt that the propagules must have freedom from tidal disturbance in order
to take hold in the soil. In
consequence, this species is restricted to the higher ground portions of the
swamp where the tidal inundation is less frequent. In the present study, Avicenniaspecies exhibit self-planting strategy at low tide and stranding strategy at
high tide. However, their seedlings
disperse widely in tidal water but establishment is mainly stationed in the
polyhaline zone. Duke et al. (1998)
reported that Avicennia seedlings disperse widely and are genetically
uniform throughout their range. In
the study areas, genetic studies are required to know whether all the three
species studied are genetically uniform. When the seedlings settle, radicle penetrates the sediment before the
cotyledons unfold. The first formal
leaves appear one month after germination and the second pair one to two months
(Wium-Andersen & Christensen 1978).
Coupland et al. (2006) reported that Avicennia propagules are a
rich source of nutrients and attract a diverse range of insect predators which in turn influence the rate of seedling
maturation. Resource constraints
and insect predation on developing fruit and seedling may both act to reduce
fruit set. In A. marina and A.
germinans, the seedlings tend to be high in nutritive value and have
relatively few chemical defenses (Smith 1987; McKee 1995). These species tend to exhibit a pattern
of very rapid initial predation (Allen et al. 2003). In the present study, seedling predation
has been evidenced in A. alba and A. marinaonly; in both the species, the Rose-ringed Parakeet Psittacula krameriattacks propagules prior to their detachment from the maternal parent. Seedling predation by crabs after
detachment from the maternal parent may be expected since different species of
crabs have been found in the study areas. Therefore, seedling predation may reduce the success of seedling
establishment in all the three species of Avicennia.
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