Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 August 2022 | 14(8): 21642–21650
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.7930.14.8.21642-21650
#7930 | Received 23 March 2022 | Final
received 30 July 2022 | Finally accepted 10 August 2022
Zoophily and nectar-robbing
by sunbirds in Gardenia latifolia Ait. (Rubiaceae)
A.J. Solomon Raju
1, S. Sravan Kumar 2, L. Kala Grace 3, K. Punny 4, Tebesi Peter Raliengoane 5 &
K. Prathyusha 6
1,3–6 Department of
Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh
530003, India.
2 Department of Basic
Sciences & Humanities, Baba Institute of Technology & Sciences, P.M. Palem, Visakhapatnam, Andhra Pradesh 530048, India.
1 solomonraju@gmail.com
(corresponding author), 2 sravankumarsamareddy@gmail.com, 3 kalagracelankapalli@gmail.com,
4 punnykonapalli@gmail.com, 5 traliengoane@gmail.com, 6
p.kodamala@gmail.com
Editor: Cervancia R. Cleofas, University of the Philippines Los Baños, Laguna, Philippines. Date
of publication: 26 August 2022 (online & print)
Citation: Raju, A.J.S., S.S. Kumar, L.K. Grace, K. Punny, T.P. Raliengoane & K. Prathyusha (2022). Zoophily and nectar-robbing by
sunbirds in Gardenia latifolia Ait. (Rubiaceae). Journal of Threatened Taxa 14(8): 21642–21650. https://doi.org/10.11609/jott.7930.14.8.21642-21650
Copyright: © Raju et al. 2022. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by providing adequate credit to the author(s) and the source of
publication.
Funding: Self-funded.
Competing interests: The authors declare no competing interests.
Author details: Prof. A.J. Solomon Raju is the Head,
Department of Environmental Sciences, and Chairman, Board of Studies Department
of Microbiology, Andhra University, Visakhapatnam, India. Dr. S. Sravan Kumar is Assistant
Professor, Department of Basic Sciences & Humanities, Baba Institute of
Technology & Sciences, P.M. Palem, Visakhapatnam
530 048, India. L. Kala Grace, K. Punny, Tebesi Peter Raliengoane and K. Prathyusha:
All are research scholars currently working under the supervision of Prof. A.J.
Solomon Raju.
Author contributions: All authors
contributed to a similar extent overall.
Acknowledgements: We thank the Andhra University, Visakhapatnam, for providing all
physical facilities and the necessary equipment for carrying out the research
work reported in this paper.
Abstract: Gardenia latifolia is a semi-deciduous tree species which blooms
during the dry season. Its flowers are hermaphroditic, strongly fragrant, nectariferous, and specialized with a narrow corolla tube
and concealed deep seated nectar. Thrips act as
resident pollinators while bats and carpenter bees act as non-resident
pollinators. Sunbirds act as nectar
robbers and have no role in pollination.
The flowers are milky white and fragrant on days 1 and 2; they cease fragrance and change
color to golden yellow on day 3. Bats visit newly open, day 1 fragrant flowers
for pollen collection while thrips use day 1 and day
2 flowers. Carpenter bees and sunbirds visit only day 2 flowers. The flower
visiting activity of all these foragers indicates that they do not visit
non-fragrant, golden yellow colored flowers although they possess nectar. Fruit
is an indehiscent berry with seeds placed in pulp inside; the birds are the
most likely seed dispersal agents when they break the pericarp and feed on the
fruit pulp.
Keywords: Bats, carpenter
bees, Cochlospermum religiosum,
Croton scabiosus, evening anthesis,
hermaphroditism, Maerua apetala,
Mylabris phalerata,
pollination, thrips.
INTRODUCTION
In Rubiaceae, Gardenia is one of the largest genera
(Davis et al. 2009) with 142 species of evergreen shrubs and small trees
distributed in tropical and subtropical regions of Africa, Asia, Madagascar,
Australasia, and Oceania (Puttock 1988). It includes
a number of well known widely cultivated
horticultural species for their fragrant flowers (Smith 1974). This genus is
characterized by hermaphroditic flowers, often large and showy with corolla
lobes overlapping to the left, pollen in tetrads, 1-locular ovaries with two to
many parietal placentas, and fruits with numerous lenticulate seeds (Rakotonirina et al. 2012). Despite the wide distribution of this genus in tropical
belts and the value of its species in horticulture due to their floral
fragrance, there are no systematic studies on the reproductive ecology of any
species. However, there are sporadic reports on the pollinators of three Gardenia
species, G. tubifera, G. jasminoides
and G. thunbergia. Freeman et al. (1991)
reported that G. tubifera is possibly
pollinated by moths. Okomoto et al. (2008) reported
that G. jasminoides is typically a hawk-moth
pollinated species in Japan. Johnson et al. (2017) reported that the African
shrub, Gardenia thunbergia is pollinated
exclusively by the convolvulus hawk moth, Agrius
convolvuli. Reddy et al. (2021) reported that G. latifolia
commonly known as Indian Boxwood is a small deciduous tree with dense foliage.
It occurs in all deciduous forests of India. Its stem, bark and fruit are used
in the treatment of skin diseases, stomach pain & snake bite in humans, and
ephemeral fever in live stock; its fruit is used for
making perfume. Despite its common occurrence and traditional economical
values, it has not been investigated for its pollination ecology which is very
important to understand its sexual reproduction and its association with local
pollinator fauna. With this backdrop, the present study was aimed at carrying
out field studies on the pollination ecology of G. latifolia
Ait. to know whether this species is also pollinated
by hawk moths or other flower visiting insects or animals. Further, whether its
long tubular hypocrateriform flowers with deeply
seated nectar facilitates foraging visits by flower visitors to collect forage
illegitimately and if so, what would be the role of illegitimate nectar robbing
on plant fitness in dry deciduous ecosystem of Idupulapaya
Reserve Forest, Kadapa District, Andhra Pradesh, India.
MATERIALS AND METHODS
Gardenia latifolia Ait.
trees at Idupulapaya Reserve Forest representing
rocky, rugged terrain with deciduous forest ecosystem (14.33 °N 78.51 °E, 273
m) in Kadapa District, Andhra Pradesh, India, were selected for study during
February–May 2021. During this period, the tree species, Croton scabiosus Bedd. (Euphorbiaceae), Cochlospermum
religiosum (L.) Alston (Cochlospermaceae),
Maerua apetala
(Roth) M. Jacobs (Capparaceae) and Gardenia latifolia Ait. (Rubiaceae) were found blooming simultaneously. Of these,
the first two species bear new foliage during the flowering phase while the
third species is completely leafless during the flower phase. In the Indian
Boxwood, G. latifolia, the flowering phase is
initiated at the fag end of leaf fall but peak
flowering occurs when complete leaf flushing occurs (Image 1a,b). Further, C.
scabiosus and G. latifolia
trees with scattered distribution are present in considerable numbers while the
other tree species consisting of a few individuals are present here and
there. The floral aspects were carefully
observed and recorded for the characteristic traits of G. latifolia. Twenty maturing buds were tagged and followed
for recording the time of anthesis and anther dehiscence. The same buds were
followed at random for the growth and protrusion of style and stigma in
relation to the level of dehisced anthers through corolla tube to record
whether secondary pollen presentation mechanism is functional or not because
this mechanism is the rule in the Rubiaceae family.
Further, the important floral traits of the other simultaneously blooming tree species were also noted. Nectar volume
of G. latifolia was measured using a graduated pipette while its sugar
concentration was recorded using a hand sugar refractometer (Erma, Japan);
twenty flowers were used for recording these two aspects. 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 120 oC in an electric oven for 20 minutes for the
development of spots from the nectar and the standard sugars. Then, the sugar
types present were recorded.
The flower visitors were
observed on five sunny days of the flowering season for their flower
approaching, probing and forage collection behaviour.
The foraging activity was observed from sunrise to sunset to record the
flower-visiting schedules of diurnal foragers and of bats from 1700 h to 0500
h. The field methods described in Dafni et al. (2005) were followed for the
collection of data on foraging visits, foraging schedule, foraging mode and
flower handling time. The number of foraging visits made by each diurnal
foraging species was recorded for 10 minutes at each hour throughout the day
between 0600 h and 1800 h on five different days. Based on these visits, the
mean number of total foraging visits made per day was calculated. The foraging
mode employed for forage collection was also recorded while the foragers were probing
the flowers. The time spent for probing and collecting the floral reward by
each forager species was counted in seconds by using a stop watch; the number
of observations made were according to the foraging visits made to the flowers
during observation period. Based on the data, the mean time for handling
flowers to collect the forage by each forager species was calculated to
understand the flower to flower mobility rate. Among the flower visitors,
sunbirds were found to exhibit nectar robbing behaviour;
this behaviour was carefully observed with reference
to its role in effecting pollination rate negatively or positively. The flower
morphological characters were also noted to evaluate their specialized traits
that contribute to the exploitation by nectar robbing sunbirds. Further, the
observations on the foraging activity of the forager species visiting G. latifolia on other tree species simultaneously blooming
in the same area were also made to note whether they were resorting to display
illegitimate or legitimate foraging behaviour to
collect nectar. Fruit and seed characters were also described.
OBSERVATIONS
Gardenia latifolia is a medium-sized
semi-deciduous tree with grey to light brown colored exfoliating bark
displaying smooth, concave and rounded depressions. The leaves are oval to
obovate, smooth and arranged opposite to each other or in whorls with very
short stalks. Flowers are solitary, sessile, 5 cm long, extremely fragrant,
hermaphroditic and appear at the end of branches. The calyx is bell-shaped with
five valvate lobes apically. The corolla is hypocrateriform
with a narrow tube and flaring suddenly into a flat arrangement of five
obliquely obovate petals which are abot half as long
as the corolla tube. The stamens are five, epipetalous, placed at the throat of
the corolla tube; the anthers are dithecous and
dehisce by longitudinal slits. The style springs up from the center of the
flower, runs parallel to corolla tube and gradually protrudes out of the
corolla tube. The stigma is 5-lobed, green, club-shaped, thick and fleshy
(Image 1h). Fruit is a 3–5 cm long
globose indehiscent berry with crowned calyx lobes and consists of many rugose
seeds enclosed by pulp inside (Image 2h).
G. latifolia mature buds begin to
open by 1600 h and are fully open by 1830 h (Image 1c–f). The flowers either
stand erect or oriented slightly horizontally. The anthers dehisce about an
hour prior to anthesis and each anther produces copious amount of fertile
pollen (Image 1g). At anther dehiscence time, the
stigma is placed below the height of the anthers but it gradually protrudes out
of the corolla tube through the dehisced anthers at anthesis and in this
process, the stigma is partially coated with self-pollen facilitating the
occurrence of autonomous self-pollination. The stigma attains receptivity about
an hour after flower-opening and extends its receptivity until the evening of
the next day with peak receptivity from 1930 h to 1100 h on the next day. The
corolla is milky white emitting strong sweet fragrance immediately after
anthesis but it gradually fades losing fragrance simultaneously by the evening
of the next day of anthesis. Then, the corolla appears golden yellow and turns
light brown then withers and wilts on the 3rd day. The corolla
together with stamens, style and stigma fall off gradually on 4th
day while the calyx is persistent and provides protection to the apical part of
the ovary with fertilized ovules throughout fruit growth, development, and
maturation.
G. latifolia flowers initiate
nectar secretion by nectaries at the base of the
ovary during bud stage and its secretion ceases by the time of anthesis.
Individual flowers produce 3.7 ± 0.76 µl of sucrose-rich nectar with 28.7 ±
2.5% total sugar concentration. The
nectar remained in place throughout the flower life if not utilized by flower
visitors. Field observations showed that
the flower-visitors made visits to day-1 and day-2 flowers only despite the
availability of nectar in day-3 and 4 flowers.
Mature buds showed
different stages of thrips and moved out during and
after anthesis. After anthesis, the thrips that moved
out of the corolla visited the flowers of the same branch/tree. These thrips were present only in day-1 and day-2 flowers despite
the availability of full load or residual pollen and nectar in day-3 (Image 1j)
and day-4 flowers. They collected pollen and nectar and carried pollen on their
body as they were found coated all over with pollen; this foraging activity
could affect pollination within and between flowers of the same tree but their
role as resident foragers in the pollination is yet to be establied.
The fruit set rate was 21% in manipulated autogamy and 37% in geitonogamy.
G. latifolia flowers were not
foraged by hawk moths during night time but were foraged by the Indian Flying
Fox, Pteropus medius
(Image 2a,b) as soon as the flowers were fully open by 1830 h and continued
its foraging activity until 0300 h especially during peak flowering season
(Table 1). This bat foraged for pollen only as there was no possibility for it
to access the nectar which is deeply concealed and protected by a long narrow
corolla tube. Since the stigma and dehisced anthers are placed at or slightly
above the corolla throat, they easily facilitate the occurrence of pollination
while the bat was collecting pollen. The bat always collected pollen from day-1
flowers only. The flowers visited by this bat can be easily identified by the
marks of claws left on the corolla; the place of marks oxidize gradually and
become prominent as brownish scars by the next morning (Image 1i). On the
following day, the carpenter bees, Xylocopa
pubescens Spinola and X.
latipes Drury (Image 2c) foraged for pollen
collection from 0700 h to 1200 h with intense activity at 0900-1100 h (Table
1). These bees approached the flowers in upright position and probed from the
flower-opening side to collect pollen which is situated at the corolla throat;
the pollen collection activity results in the occurrence of pollination due to
the placement of both stamens and stigma at the same place at or above the
corolla throat. There is no possibility for these bees to collect deeply seated
and concealed nectar with their short proboscis/tongue. They never made any
attempts to rob nectar illegitimately bypassing the pollination apparatus and
also never visited day-3 and day-4 flowers. Further, they never made any
attempts to rob nectar illegitimately by making a slit into the corolla tube.
The Purple Sunbird, Nectarinia asiatica Latham (Image 2d,e) and the Purple-rumped Sunbird N. zeylonica
L. (Image 2f) foraged for nectar illegitimately from day-2 flowers from 0700 h
to 1600 h due to a wide mismatch between the length of their beak and the
length of the corolla tube to access nectar location (Table 1). They slit the
mid-portion of the corolla tube from outside with their curved beak to access
and collect nectar without effecting pollination. This illegitimate foraging
behavior employed by sunbirds characterizes primary nectar robbing. These birds
never made attempts to rob nectar from day-3 and day-4 flowers. Therefore, the
pollination occurs in day-1 flowers by pollen collection activity of bats and
in day-2 flowers by pollen collection activity of carpenter bees. Further, the
sunbirds rob nectar only from day-2 flowers despite the availability of nectar
in day-3 and day-4 flowers indicating that pollination occurs only in
white-colored fragrance emitting from day-1 and day-2 flowers. Flower-handling
time to collect pollen or nectar by each foraging species is given in Table 1.
G. latifolia flowers attracted a
blister beetle, Mylabris phalerata Pallas (Coleoptera,
Meloidae) (Image 2g). This beetle consumed the
corolla, stamens and partially the stigma during the entire flowering season.
Several individuals of this beetle were found on each flowering tree; 45% of
the sampled flowers on each tree were found either damaged or completely
consumed by it. This flower feeding activity by this beetle was found to be
negatively affecting the reproductive success of the plant.
In the biotope of the same forest, the tree
species, Croton scabiosus (Image 3a), Cochlospermum religiosum
(Image 3c,d), and Maerua apetala bloom (Image 3e,f) simultaneously with G. latifolia. But, these tree species are not closely
spaced and occur scattered at random. Of these, C. scabiosus
has considerable population while all other trees are represented by a few
individuals. Of these, the first species is monoecious while the other tree
species are hermaphroditic. Further, C. religiosum
is nectarless while the other tree species are nectariferous. The carpenter bees used C. religiosum flowers as pollen source effecting
pollination as in the case of G. latifolia
while M. apetala (Image 3g) was used as nectar
source effecting pollination. Since C. religiosum
is represented by about ten individuals, there was no scope for competition
between this tree species and G. latifolia for
carpenter bees which collected only pollen from these species. Further, these
bees used G. latifolia as pollen source only
and M. apetala as nectar source, hence the
question of competition between these species for pollination by carpenter bees
was ruled out. Sunbirds, N. asiatica (Image
3b) and N. zeylonica used C. scabiosus as a source of insect food in the form of
instars of larvae of an unidentified local butterfly; these birds picked up the
larval instars from the leaves throughout the day. Further, these sunbirds also
used M. apetala as nectar source by probing
the flowers legitimately and effecting pollination (Image 3h,i).
DISCUSSION
Robbrecht (1988) reported that
Rubiaceae members are entomophilous and the
pollination mechanism in this family is conspicuously specialized via stylar modifications for passive pollen presentation.
Anderson (1973) reported that in hermaphroditic isostylous
flowers, protandry is predominant; the pollen matures early and is shed at or
soon after anthesis. Before anthesis and in some cases for a period after
anthesis, the elongation of the style is arrested, the immature stigmas are
temporarily retained within the tube of the corolla, below the level of the
anthers. During and/or after the release of the pollen the style elongates,
eventually equalling or surpassing the anthers, and
the stigmas belatedly mature. In this study, G. latifolia
is a hermaphroditic isostylous species with weak
protandry which occurs shortly before anthesis. The style elongation is not
arrested but it continues to grow to surpass the dehisced anthers and matures
as soon as anthesis occurs.
Puff et al. (2005)
stated that protandry in isostylous flowers of Rubiaceae is associated with secondary pollen presentation.
In this family, four types of secondary pollen presentation have been
recognized according to the presenting area and receptive surfaces: i. pollen deposition on the style only. Here, pollen deposition is strictly on
non-receptive surfaces. The stigma and its receptive surfaces is higher up; 2.
Pollen deposition on the style and outside of the stigma lobes. Pollen is
solely deposited on non-receptive surfaces, but the abaxial surfaces of the
stigma are also involved; 3. Pollen deposition on the outer side of the stigma;
4. Pollen deposition exclusively, largely or partly on the receptive surface of
the stigma. In G. latifolia, the fourth type
of pollen presentation mechanism is functional with partial pollen deposition
on the receptive portion of the stigma. In this species, weak protandry
facilitates overlap between the functional male and female stages within and
between flowers of the same tree and hence, autonomous autogamy and geitonogamy
are unavoidable (Bremer & Eriksson 2009) but the function of these
pollination modes are not absolute. The secondary pollen presentation increases
the efficiency and accuracy of pollen transfer because of the close proximity
of pollen to the stigma (Ladd 1994). However, the proximity of pollen and
stigma could also result in self-interference (Webb & Lloyd 1986), which is
detrimental to plant fitness (Waites & Agren
2006). In G. latifolia, autonomous autogamy
and geitonogamy mediated by insects are advantageous since its flowering period
falls in summer season when pollinating insects are mostly either unavailable
or not reliable due to harsh ambient environmental conditions in the biotope of
this species.
Consolaro et al. (2005)
reported that species of Rubiaceae generally present
a wide range of floral visitors. Puff et al. (2005) reported that Rubiaceae family members present a wide range of flower
forms, sizes and colours indicating the involvement
of many different pollinators and most of them are almost exclusively
zoophilous. Most of these pollinators
include insects while birds and bats play a minor role in pollination. Among
insects also, bees are important pollinators especially for small-flowered
species; the showy large-flowered species are adapted for pollination by
butterflies and hawk moths. The butterflies are pollinators for scentless
flowers while hawk moths for long-tubed fragrant flowers. Different authors
documented that in dry lands of Africa, the Long-proboscid
Hawk Moth Agrius convolvuli is an
extremely abundant species comprising up to 50% of all hawk moths in local
assemblages. Several hundred plant species have become adapted for pollination
by this moth which is most likely a result of the abundance of its individuals
(Martins & Johnson 2013; Johnson & Raguso
2016; Johnson et al. 2017). The biotope of G. latifolia
is typically deciduous in nature with rocky terrain and a few trees in bloom
during the dry season. Despite the availability of fragrant flowers of this species
and Maerua apetala,
diurnal or nocturnal hawk moths never visited the flowers of these two species
or any other species in the forest. Surprisingly, the bat, Pteropus
medius consistently visits G. latifolia flowers for pollen collection although they
are not appropriate for its visitation; its pollen feeding activity results in
the occurrence of both self- and cross-pollination. The bat-visited flowers
present brownish scars which can be taken as an indicator of bat foraging
activity on this tree species. The G. latifolia
flowers may produce tannins and the marks left by the visiting bats on corolla
and stamens oxidize and appear conspicuous as brownish scars by the next
morning. Jaeger (1961) reported that bats collect nectar and pollen from Adansonia flowers. He found considerable
amount of pollen in the digestive tract of bats. Similarly, the bat visiting
the flowers of G. latifolia collect pollen as
a source of protein which would make an excellent balance in its diet with the
sugar and water provided by nectar collected from other floral sources.
In G. latifolia, thrips by using
the floral buds as breeding site and flowers as pollen and nectar sources as
food could effect autogamy and/or geitonogamy but
their role in pollination is yet to be studied. The carpenter bees, Xylocopa pubescens
and X. latipes visit the flowers for pollen
collection and in this act, they effect both self and cross-pollination but the
flower is not appropriate for nectar collection by these bees as the flower is
highly specialized with deeply seated nectar and a narrow corolla tube that
prevents access to nectar by short-tongued bees such as carpenter bees. These
bees also collect pollen from the simultaneously blooming Cochlospermum
religiosum in the same forest. But, it is not
known whether the same individuals of bees collect pollen from different floral
sources alternately or exhibit fidelity to a particular floral source. Inouye
(1983) reported that among insects, bees, wasps and ants are the most common
primary nectar robbers of which bees make up the vast majority, and include
carpenter bees, bumble bees, and stingless bees, and some solitary bees. They
have some specific morphological structures to make holes on the corolla tube.
Gerling et al. (1989) reported that carpenter bees use their maxillae to make
slits in the sides of the flowers. Despite the copious amount of nectar
produced by the flowers of G. latifolia, the
carpenter bees never attempted to make a hole or slit in corolla tube tissue to
steal nectar bypassing the floral opening used by legitimate pollinators
although there is a dire need for nectar during the dry season. But, these bees
collect nectar which is easily accessible by legitimate probing from the flowers
of Maerua apetala
which blooms simultaneously in the same forest.
Castellanos et al.
(2003, 2004) documented that floral adaptations that promote pollen transport
by pollinators are treated as evidence of specialization to a particular
pollinator type. Naravvo (2001) reported that
specialization in floral architecture is vulnerable to exploitation by flower
visitors which remove or steal nectar without effecting pollination. Rojas-Nossa et al. (2016) stated that nectar robbers display a
particular behaviour to steal nectar. A common form
is primary nectar robbing in which the flower visitor makes a hole, slit, or
tear in corolla tissue to steal nectar bypassing the floral opening used by
legitimate pollinators; this form of robbing is most common on flowers with
hidden nectar. The flowers with tubular corolla are vulnerable to nectar
robbing. Irwin & Maloof (2002) reported that another form of secondary
nectar robbing in which the flower visitor acquires nectar through holes made
by primary nectar robbers bypassing the floral opening used by legitimate
pollinators. Irwin et al. (2010) reported that all flower visitors are not
pollinators. Some visitors rob nectar
bypassing the contact with the anters and/or stigma
and the effects of this nectar robbing behaviour by
robbers range from negative to positive on female and male components of plant
reproduction. Maloof & Inouye (2000) and Irwin et al. (2010) reported that
nectar robbing is very frequent in plant species producing flowers with long
corollas and abundant nectar production. In the present study, the sunbirds are
just robbers of nectar of G. latifolia and
this nectar robbing activity reduces nectar reward and increases variability in
nectar standing crop. Such a situation is expected to promote pollination rate
in general and cross-pollination in particular when legitimate pollinators
visit M. pubescens flowers for nectar. Since
there are no legitimate foragers to collect nectar from G. latifolia except the resident foragers, thrips, the nectar in this species remains in place if not
utilized by sunbirds by robbing and hence the role of nectar in effecting
pollination rate negatively or positively is totally ruled out. The absence of
appropriate legitimate nectar seekers, diurnal hawk moths or nocturnal moths
during the flowering season of G. latifolia
could be attributed to unfavorable ambient temperature and unreliability of nectariferous floral resources with suitable nectar
chemistry. Nevertheless, the availability of many flowering trees of G. latifolia during the dry season in this forest provides
the needed levels of nectar for sunbirds that probe the flowers of this species
illegitimately by robbing. It is interesting to note that bats use new and
fresh flowers as soon as they are available upon anthesis and do not use the
same flowers again on the next day or later while thrips
use day-2 flowers also for forage collection. Bees and sunbirds use day-2
flowers only. All these foragers simply ignore day-3 and day-4 flowers which
are faded by changing corolla color and lacking fragrance despite the
availability of nectar in these flowers. This discriminatory behavior displayed
by these foragers indicate that they use corolla color and strong fragrance as
cues to visit the flowers of G. latifolia.
Puff et al. (2005)
reported that fruits of Rubiaceae are of capsule type
and classified into three types: those that split open at maturity, those that
break into one-seeded mericarps and those that remain indehiscent. The species
possessing indehiscent fruits are either drupes or berry-like. Ornithochory is the most prevailing mode of seed dispersal.
In G. latifolia, the fruit is an indehiscent
berry with seeds enclosed by pulp inside.
But, the pericarp is not very hard to break by birds with their bill,
hence, it is most likely that birds are involved in seed dispersal when they
feed on the pulp along with small seeds.
CONCLUSIONS
Gardenia latifolia is a semi-deciduous hermaphroditic dry season
blooming tree species. The flowers are milky white and strongly fragrant on day
1 and day 2 while they are golden yellow and non-fragrant on days 3 and 4. They produce copious amounts of nectar which
is concealed deep inside at the base of the narrow corolla tube. Thrips use the floral buds as breeding sites and flowers as
pollen and nectar source. As resident foragers, they use day 1 and day 2
flowers only for forage collection. Bats visit only day 1 flowers for pollen
collection while carpenter bees use only day 2 flowers for pollen collection.
Like carpenter bees, sunbirds use only day 2 flowers for robbing nectar by
proving the flowers illegitimately. The flower visiting activity of all these
foragers indicates that they do not visit non-fragrant, golden yellow colored
flowers although they possess nectar. Fruit is an indehiscent berry with seeds
placed in pulp inside; the birds are the most likely seed dispersal agents when
they break the pericarp and feed on the fruit pulp.
Table 1. List of
foragers visiting the flowers of Gardenia latifolia.
|
Order |
Family |
Insect species |
Foraging period (h) |
No. of foraging
visits/day# (N = 5 days) |
Mode of foraging |
Forage sought |
Flower handling
time (in seconds) |
|
Hymenoptera |
Apidae |
Xylocopa pubescens* |
0700–1200 Peak activity:
0900–1200 |
42 ± 5.3 |
Legitimate |
Pollen |
3.2 ± 0.08 (n = 42) |
|
|
|
Xylocopa latipes* |
0700–1200 Peak activity:
0900–1200 |
39 ± 3.5 |
Legitimate |
Pollen |
2.8 ± 0.05 (n = 37) |
|
Thysanoptera |
Thripidae |
Unidentified |
0800–1700 |
Forages
continuously |
Legitimate |
Pollen + Nectar |
-- |
|
Passeriformes |
Nectariniidae |
Nectarinia asiatica** |
0700–1600 |
53 ± 3.2 |
Illegitimate |
Nectar |
2.3 ± 0.8 (n = 31) |
|
|
|
Nectarinia zeylonica** |
0700–1600 |
41 ± 2.2 |
Illegitimate |
Nectar |
2.6 ± 1.4 (n = 36) |
|
Chiroptera |
Pteropodidae |
Pteropus medius |
1830–0300 |
32 ± 3.7 (approx.) |
Legitimate |
Pollen |
1.4 ± 0.8 (n = 27) |
|
#No. of flowers
under observation: Approximately 125 each day on a different tree. *Collecting pollen
from Cochlosperm religiosum
and nectar from Maerua apetala legitimately. **Collecting nectar
from Maerua apetala
legitimately and larvae of an unidentified local butterfly from the leaves of
Croton scabiosus. |
|||||||
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