Building evidence forconservation globally

10.11609/jott.2022.14.8.21487-21750
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Threatened

26 August 2022 (Online & Print)
14(8): 21487-21750
ISSN 0974-7907 (Online)
ISSN 0974-7893 (Print)

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Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2022 | 14(8): 21642–21650
OPEN
ACCESSISSN 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
COMMUNICATION

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
K. Prathyusha 6, Tebesi Peter Raliengoane 5

&

1,3–6
Department of Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India.
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
2

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.

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.

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INTRODUCTION

MATERIALS AND METHODSIn 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 subtropicalregions of Africa, Asia, Madagascar, Australasia, andOceania (Puttock 1988). It includes a number of wellknown widely cultivated horticultural species for theirfragrant flowers (Smith 1974). This genus is characterized
by hermaphroditic flowers, often large and showy withcorolla 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 intropical belts and the value of its species in horticulture
due to their floral fragrance, there are no systematicstudies on the reproductive ecology of any species.
However, there are sporadic reports on the pollinators of
three Gardenia species, G. tubifera, G. jasminoides andG. 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 hawkmoth 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 thatG. latifolia commonly known as Indian Boxwood is asmall deciduous tree with dense foliage. It occurs in all
deciduous forests of India. Its stem, bark and fruit areused 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 thisbackdrop, 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 withdeeply seated nectar facilitates foraging visits by flower
visitors to collect forage illegitimately and if so, what
would be the role of illegitimate nectar robbing onplant fitness in dry deciduous ecosystem of Idupulapaya
Reserve Forest, Kadapa District, Andhra Pradesh, India.

Gardenia latifolia Ait. trees at Idupulapaya
Reserve Forest representing rocky, rugged terrain withdeciduous forest ecosystem (14.33 °N 78.51 °E, 273m) in Kadapa District, Andhra Pradesh, India, wereselected 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 firsttwo species bear new foliage during the flowering phase
while the third species is completely leafless during theflower phase. In the Indian Boxwood, G. latifolia, theflowering 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 thecharacteristic traits of G. latifolia. Twenty maturingbuds were tagged and followed for recording the timeof anthesis and anther dehiscence. The same buds were
followed at random for the growth and protrusion of styleand stigma in relation to the level of dehisced anthers
through corolla tube to record whether secondary pollen
presentation mechanism is functional or not because thismechanism is the rule in the Rubiaceae family. Further,
the important floral traits of the other simultaneously
blooming tree species were also noted. Nectar volumeof G. latifolia was measured using a graduated pipette
while its sugar concentration was recorded using a handsugar refractometer (Erma, Japan); twenty flowers wereused for recording these two aspects. For the analysis ofsugar types, paper chromatography method describedby Harborne (1973) was followed. Nectar was placedon 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 ofn-butanol-acetone-water (4:5:1), sprayed with aniline
oxalate spray reagent and dried at 120 oC in an electricoven for 20 minutes for the development of spots fromthe nectar and the standard sugars. Then, the sugar
types present were recorded.
The flower visitors were observed on five sunny daysof 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

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bats from 1700 h to 0500 h. The field methods describedin Dafni et al. (2005) were followed for the collection ofdata on foraging visits, foraging schedule, foraging modeand 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 thesevisits, the mean number of total foraging visits made per
day was calculated. The foraging mode employed forforage 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; thenumber of observations made were according to theforaging 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 wascalculated 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 bloomingin the same area were also made to note whether
they were resorting to display illegitimate or legitimate
foraging behaviour to collect nectar. Fruit and seedcharacters were also described.

OBSERVATIONSGardenia latifolia is a medium-sized semi-deciduoustree with grey to light brown colored exfoliating barkdisplaying smooth, concave and rounded depressions.
The leaves are oval to obovate, smooth and arranged
opposite to each other or in whorls with very shortstalks. 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 narrowtube and flaring suddenly into a flat arrangement offive obliquely obovate petals which are abot half as longas 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 stylesprings up from the center of the flower, runs parallel tocorolla tube and gradually protrudes out of the corolla
tube. The stigma is 5-lobed, green, club-shaped, thickand fleshy (Image 1h). Fruit is a 3–5 cm long globose
indehiscent berry with crowned calyx lobes and consists

Image 1. Gardenia latifolia: a—Trunk | b—Leaf flushing and flowering | c–f—Anthesis stages | g—Anther dehiscence by longitudinal slits inbud stage (stigma below the height of anthers) | h—Pistil | i—Brown marks on the corolla indicating bat visit to the flower | j—3rd day flower.
© Prof. A.J. Solomon Raju
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Table 1. List of foragers visiting the flowers of Gardenia latifolia.
Foraging period(h)No. of foraging
visits/day#(N = 5 days)

Mode offoraging

ForagesoughtFlower handlingtime (in seconds)

0700–1200
Peak activity:
0900–1200

42 ± 5.3

Legitimate

Pollen3.2 ± 0.08 (n = 42)

0700–1200
Peak activity:
0900–1200

39 ± 3.5

Legitimate

Pollen2.8 ± 0.05 (n = 37)

0800–1700

Forages
continuously

Legitimate

Pollen +Nectar--

0700–1600

53 ± 3.2

Illegitimate

Nectar2.3 ± 0.8 (n = 31)

Nectarinia zeylonica**

0700–1600

41 ± 2.2

Illegitimate

Nectar2.6 ± 1.4 (n = 36)

Pteropus medius

1830–0300

32 ± 3.7(approx.)

Legitimate

Pollen1.4 ± 0.8 (n = 27)

OrderFamilyInsect species

Hymenoptera

ApidaeXylocopa pubescens*
Xylocopa latipes*

Thysanoptera

Thripidae

Passeriformes

Nectariniidae

Chiroptera

Pteropodidae

Unidentified
Nectarinia asiatica**#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.

of many rugose seeds enclosed by pulp inside (Image2h).
G. latifolia mature buds begin to open by 1600 h andare 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 antherproduces 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 anthersat anthesis and in this process, the stigma is partiallycoated with self-pollen facilitating the occurrenceof autonomous self-pollination. The stigma attains
receptivity about an hour after flower-opening andextends its receptivity until the evening of the next day
with peak receptivity from 1930 h to 1100 h on the nextday. The corolla is milky white emitting strong sweet
fragrance immediately after anthesis but it graduallyfades losing fragrance simultaneously by the eveningof the next day of anthesis. Then, the corolla appears
golden yellow and turns light brown then withers andwilts on the 3rd day. The corolla together with stamens,
style and stigma fall off gradually on 4th day while thecalyx is persistent and provides protection to the apicalpart of the ovary with fertilized ovules throughout fruit
growth, development, and maturation.
G. latifolia flowers initiate nectar secretion bynectaries at the base of the ovary during bud stage andits 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 showedthat 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 andmoved out during and after anthesis. After anthesis, thethrips that moved out of the corolla visited the flowersof the same branch/tree. These thrips were present onlyin day-1 and day-2 flowers despite the availability of fullload or residual pollen and nectar in day-3 (Image 1j)
and day-4 flowers. They collected pollen and nectar andcarried pollen on their body as they were found coated
all over with pollen; this foraging activity could affectpollination 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 peakflowering season (Table 1). This bat foraged for pollen
only as there was no possibility for it to access thenectar which is deeply concealed and protected by along 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 bythis bat can be easily identified by the marks of claws
left on the corolla; the place of marks oxidize graduallyand become prominent as brownish scars by the nextmorning (Image 1i). On the following day, the carpenter

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bees, Xylocopa pubescens Spinola and X. latipes Drury(Image 2c) foraged for pollen collection from 0700 h to1200 h with intense activity at 0900-1100 h (Table 1).
These bees approached the flowers in upright positionand probed from the flower-opening side to collectpollen which is situated at the corolla throat; thepollen collection activity results in the occurrence ofpollination due to the placement of both stamens andstigma 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 andalso never visited day-3 and day-4 flowers. Further, they
never made any attempts to rob nectar illegitimately bymaking a slit into the corolla tube. The Purple Sunbird,
Nectarinia asiatica Latham (Image 2d,e) and the Purplerumped Sunbird N. zeylonica L. (Image 2f) foraged fornectar illegitimately from day-2 flowers from 0700 h to1600 h due to a wide mismatch between the length oftheir beak and the length of the corolla tube to accessnectar location (Table 1). They slit the mid-portion of
the corolla tube from outside with their curved beak toaccess 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 andday-4 flowers. Therefore, the pollination occurs in day1 flowers by pollen collection activity of bats and inday-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 andday-4 flowers indicating that pollination occurs only inwhite-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 partiallythe stigma during the entire flowering season. Several
individuals of this beetle were found on each floweringtree; 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 tobe negatively affecting the reproductive success of theplant.
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.
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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 othertree 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 forcompetition 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 forpollination 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 larvaeof 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 mechanismin 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, andthe stigmas belatedly mature. In this study, G. latifolia
is a hermaphroditic isostylous species with weakprotandry which occurs shortly before anthesis. The
style elongation is not arrested but it continues to growto 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

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Zoophily and nectar-robbing by sunbirds

deposition on the style only. Here, pollen deposition
is strictly on non-receptive surfaces. The stigma andits receptive surfaces is higher up; 2. Pollen depositionon the style and outside of the stigma lobes. Pollen issolely deposited on non-receptive surfaces, but theabaxial 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 typeof pollen presentation mechanism is functional withpartial 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 thefunction of these pollination modes are not absolute.
The secondary pollen presentation increases theefficiency 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 harshambient environmental conditions in the biotope of thisspecies.
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 memberspresent a wide range of flower forms, sizes and colours
indicating the involvement of many different pollinatorsand 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 smallflowered 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, theLong-proboscid Hawk Moth Agrius convolvuli is anextremely 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 abundanceof its individuals (Martins & Johnson 2013; Johnson& Raguso 2016; Johnson et al. 2017). The biotope of
G. latifolia is typically deciduous in nature with rocky

Raju et al.

terrain and a few trees in bloom during the dry season.
Despite the availability of fragrant flowers of thisspecies 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 inthe occurrence of both self- and cross-pollination. The
bat-visited flowers present brownish scars which can betaken as an indicator of bat foraging activity on this tree
species. The G. latifolia flowers may produce tannins andthe marks left by the visiting bats on corolla and stamens
oxidize and appear conspicuous as brownish scars by thenext morning. Jaeger (1961) reported that bats collectnectar and pollen from Adansonia flowers. He foundconsiderable amount of pollen in the digestive tract ofbats. Similarly, the bat visiting the flowers of G. latifolia
collect pollen as a source of protein which would makean excellent balance in its diet with the sugar and waterprovided 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, theyeffect 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 seatednectar and a narrow corolla tube that prevents accessto 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 makeslits 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 orslit in corolla tube tissue to steal nectar bypassing thefloral 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

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Image 2. Gardenia latifolia: a,b—Bat, Pteropus medius collecting pollen | c—Xylocopa latipes collecting pollen | d–f—Sunbirds robbing nectar
by making a slit on the corolla tube from outside | d—Nectarinia asiatica (male) | e—Nectarinia asiatica (female) | f—Nectarinia zeylonica(female) | g—Mylabris phalerata feeding on flowers | h—Fruits. © Prof. A.J. Solomon Raju.

Image 3. Co-blooming tree species in the biotope of Gardenia latifolia: a—Croton scabiosus habit | b—Croton scabiosus –Purple Sunbird
Nectariania asiatica (male) collecting larval instars from the leaves | c,d—Cochlospermum religiosum | e–i—Maerua apetala | e—Tree habit| f—Flowers | g—Carpenter bee Xylocopa latipes collecting pollen | h—Nectarinia asiatica collecting nectar | i—Nectarinia zeylonica (male)perching. © Prof. A.J. Solomon Raju

legitimate probing from the flowers of Maerua apetala
which blooms simultaneously in the same forest.
Castellanos et al. (2003, 2004) documented thatfloral adaptations that promote pollen transport bypollinators are treated as evidence of specialization toa particular pollinator type. Naravvo (2001) reported
21648

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 particularbehaviour to steal nectar. A common form is primarynectar robbing in which the flower visitor makes a hole,

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Zoophily and nectar-robbing by sunbirds

slit, or tear in corolla tissue to steal nectar bypassing thefloral opening used by legitimate pollinators; this form ofrobbing is most common on flowers with hidden nectar.
The flowers with tubular corolla are vulnerable to nectar
robbing. Irwin & Maloof (2002) reported that anotherform of secondary nectar robbing in which the flower
visitor acquires nectar through holes made by primarynectar robbers bypassing the floral opening used bylegitimate 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 abundantnectar 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 generaland 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 nectarin 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 ruledout. 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 unreliabilityof nectariferous floral resources with suitable nectar
chemistry. Nevertheless, the availability of many
flowering trees of G. latifolia during the dry season in thisforest provides the needed levels of nectar for sunbirds
that probe the flowers of this species illegitimately byrobbing. It is interesting to note that bats use new andfresh 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 theseflowers. This discriminatory behavior displayed by theseforagers 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

Raju et al.

that split open at maturity, those that break into oneseeded mericarps and those that remain indehiscent.
The species possessing indehiscent fruits are either
drupes or berry-like. Ornithochory is the most prevailingmode of seed dispersal. In G. latifolia, the fruit is anindehiscent 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 withsmall 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 and4. They produce copious amounts of nectar whichis concealed deep inside at the base of the narrowcorolla 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 forforage 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 theflowers illegitimately. The flower visiting activity of
all these foragers indicates that they do not visit nonfragrant, 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 seeddispersal agents when they break the pericarp and feedon the fruit pulp.
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Dr. George Mathew, Kerala Forest Research Institute, Peechi, India
Dr. John Noyes, Natural History Museum, London, UK
Dr. Albert G. Orr, Griffith University, Nathan, Australia
Dr. Sameer Padhye, Katholieke Universiteit Leuven, Belgium
Dr. Nancy van der Poorten, Toronto, Canada
Dr. Kareen Schnabel, NIWA, Wellington, New Zealand
Dr. R.M. Sharma, (Retd.) Scientist, Zoological Survey of India, Pune, India
Dr. Manju Siliwal, WILD, Coimbatore, Tamil Nadu, India
Dr. G.P. Sinha, Botanical Survey of India, Allahabad, India
Dr. K.A. Subramanian, Zoological Survey of India, New Alipore, Kolkata, India
Dr. P.M. Sureshan, Zoological Survey of India, Kozhikode, Kerala, India
Dr. R. Varatharajan, Manipur University, Imphal, Manipur, India
Dr. Eduard Vives, Museu de Ciències Naturals de Barcelona, Terrassa, Spain
Dr. James Young, Hong Kong Lepidopterists’ Society, Hong Kong
Dr. R. Sundararaj, Institute of Wood Science & Technology, Bengaluru, India
Dr. M. Nithyanandan, Environmental Department, La Ala Al Kuwait Real Estate. Co. K.S.C.,
KuwaitDr. Himender Bharti, Punjabi University, Punjab, India
Mr. Purnendu Roy, London, UK
Dr. Saito Motoki, The Butterfly Society of Japan, Tokyo, Japan
Dr. Sanjay Sondhi, TITLI TRUST, Kalpavriksh, Dehradun, India
Dr. Nguyen Thi Phuong Lien, Vietnam Academy of Science and Technology, Hanoi, Vietnam
Dr. Nitin Kulkarni, Tropical Research Institute, Jabalpur, India
Dr. Robin Wen Jiang Ngiam, National Parks Board, Singapore
Dr. Lional Monod, Natural History Museum of Geneva, Genève, Switzerland.
Dr. Asheesh Shivam, Nehru Gram Bharti University, Allahabad, India
Dr. Rosana Moreira da Rocha, Universidade Federal do Paraná, Curitiba, Brasil
Dr. Kurt R. Arnold, North Dakota State University, Saxony, Germany
Dr. James M. Carpenter, American Museum of Natural History, New York, USA
Dr. David M. Claborn, Missouri State University, Springfield, USA
Dr. Kareen Schnabel, Marine Biologist, Wellington, New Zealand
Dr. Amazonas Chagas Júnior, Universidade Federal de Mato Grosso, Cuiabá, Brasil
Mr. Monsoon Jyoti Gogoi, Assam University, Silchar, Assam, India
Dr. Heo Chong Chin, Universiti Teknologi MARA (UiTM), Selangor, Malaysia
Dr. R.J. Shiel, University of Adelaide, SA 5005, Australia
Dr. Siddharth Kulkarni, The George Washington University, Washington, USA
Dr. Priyadarsanan Dharma Rajan, ATREE, Bengaluru, India
Dr. Phil Alderslade, CSIRO Marine And Atmospheric Research, Hobart, Australia
Dr. John E.N. Veron, Coral Reef Research, Townsville, Australia
Dr. Daniel Whitmore, State Museum of Natural History Stuttgart, Rosenstein, Germany.
Dr. Yu-Feng Hsu, National Taiwan Normal University, Taipei City, Taiwan
Dr. Keith V. Wolfe, Antioch, California, USA
Dr. Siddharth Kulkarni, The Hormiga Lab, The George Washington University, Washington,
D.C., USA
Dr. Tomas Ditrich, Faculty of Education, University of South Bohemia in Ceske
Budejovice, Czech Republic
Dr. Mihaly Foldvari, Natural History Museum, University of Oslo, Norway
Dr. V.P. Uniyal, Wildlife Institute of India, Dehradun, Uttarakhand 248001, India
Dr. John T.D. Caleb, Zoological Survey of India, Kolkata, West Bengal, India
Dr. Priyadarsanan Dharma Rajan, Ashoka Trust for Research in Ecology and the Environment(ATREE), Royal Enclave, Bangalore, Karnataka, India
FishesDr. Neelesh Dahanukar, IISER, Pune, Maharashtra, India
Dr. Topiltzin Contreras MacBeath, Universidad Autónoma del estado de Morelos, México
Dr. Heok Hee Ng, National University of Singapore, Science Drive, Singapore
Dr. Rajeev Raghavan, St. Albert’s College, Kochi, Kerala, India
Dr. Robert D. Sluka, Chiltern Gateway Project, A Rocha UK, Southall, Middlesex, UK
Dr. E. Vivekanandan, Central Marine Fisheries Research Institute, Chennai, India
Dr. Davor Zanella, University of Zagreb, Zagreb, Croatia
Dr. A. Biju Kumar, University of Kerala, Thiruvananthapuram, Kerala, India
Dr. Akhilesh K.V., ICAR-Central Marine Fisheries Research Institute, Mumbai ResearchCentre, Mumbai, Maharashtra, India
Dr. J.A. Johnson, Wildlife Institute of India, Dehradun, Uttarakhand, India
Dr. R. Ravinesh, Gujarat Institute of Desert Ecology, Gujarat, India
Amphibians
Dr. Sushil K. Dutta, Indian Institute of Science, Bengaluru, Karnataka, India
Dr. Annemarie Ohler, Muséum national d’Histoire naturelle, Paris, France
ReptilesDr. Gernot Vogel, Heidelberg, Germany
Dr. Raju Vyas, Vadodara, Gujarat, India
Dr. Pritpal S. Soorae, Environment Agency, Abu Dubai, UAE.
Prof. Dr. Wayne J. Fuller, Near East University, Mersin, Turkey
Prof. Chandrashekher U. Rivonker, Goa University, Taleigao Plateau, Goa. India
Dr. S.R. Ganesh, Chennai Snake Park, Chennai, Tamil Nadu, India
Dr. Himansu Sekhar Das, Terrestrial & Marine Biodiversity, Abu Dhabi, UAE

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Dr. Hem Sagar Baral, Charles Sturt University, NSW Australia
Mr. H. Byju, Coimbatore, Tamil Nadu, India
Dr. Chris Bowden, Royal Society for the Protection of Birds, Sandy, UK
Dr. Priya Davidar, Pondicherry University, Kalapet, Puducherry, India
Dr. J.W. Duckworth, IUCN SSC, Bath, UK
Dr. Rajah Jayapal, SACON, Coimbatore, Tamil Nadu, India
Dr. Rajiv S. Kalsi, M.L.N. College, Yamuna Nagar, Haryana, India
Dr. V. Santharam, Rishi Valley Education Centre, Chittoor Dt., Andhra Pradesh, India
Dr. S. Balachandran, Bombay Natural History Society, Mumbai, India
Mr. J. Praveen, Bengaluru, India
Dr. C. Srinivasulu, Osmania University, Hyderabad, India
Dr. K.S. Gopi Sundar, International Crane Foundation, Baraboo, USA
Dr. Gombobaatar Sundev, Professor of Ornithology, Ulaanbaatar, Mongolia
Prof. Reuven Yosef, International Birding & Research Centre, Eilat, Israel
Dr. Taej Mundkur, Wetlands International, Wageningen, The Netherlands
Dr. Carol Inskipp, Bishop Auckland Co., Durham, UK
Dr. Tim Inskipp, Bishop Auckland Co., Durham, UK
Dr. V. Gokula, National College, Tiruchirappalli, Tamil Nadu, India
Dr. Arkady Lelej, Russian Academy of Sciences, Vladivostok, Russia
Dr. Simon Dowell, Science Director, Chester Zoo, UK
Dr. Mário Gabriel Santiago dos Santos, Universidade de Trás-os-Montes e Alto Douro,
Quinta de Prados, Vila Real, Portugal
Dr. Grant Connette, Smithsonian Institution, Royal, VA, USA
Dr. M. Zafar-ul Islam, Prince Saud Al Faisal Wildlife Research Center, Taif, Saudi Arabia
Mammals
Dr. Giovanni Amori, CNR - Institute of Ecosystem Studies, Rome, Italy
Dr. Anwaruddin Chowdhury, Guwahati, India
Dr. David Mallon, Zoological Society of London, UK
Dr. Shomita Mukherjee, SACON, Coimbatore, Tamil Nadu, India
Dr. Angie Appel, Wild Cat Network, Germany
Dr. P.O. Nameer, Kerala Agricultural University, Thrissur, Kerala, India
Dr. Ian Redmond, UNEP Convention on Migratory Species, Lansdown, UK
Dr. Heidi S. Riddle, Riddle’s Elephant and Wildlife Sanctuary, Arkansas, USA
Dr. Karin Schwartz, George Mason University, Fairfax, Virginia.
Dr. Lala A.K. Singh, Bhubaneswar, Orissa, India
Dr. Mewa Singh, Mysore University, Mysore, India
Dr. Paul Racey, University of Exeter, Devon, UK
Dr. Honnavalli N. Kumara, SACON, Anaikatty P.O., Coimbatore, Tamil Nadu, India
Dr. Nishith Dharaiya, HNG University, Patan, Gujarat, India
Dr. Spartaco Gippoliti, Socio Onorario Società Italiana per la Storia della Fauna “Giuseppe
Altobello”, Rome, Italy
Dr. Justus Joshua, Green Future Foundation, Tiruchirapalli, Tamil Nadu, India
Dr. H. Raghuram, The American College, Madurai, Tamil Nadu, India
Dr. Paul Bates, Harison Institute, Kent, UK
Dr. Jim Sanderson, Small Wild Cat Conservation Foundation, Hartford, USA
Dr. Dan Challender, University of Kent, Canterbury, UK
Dr. David Mallon, Manchester Metropolitan University, Derbyshire, UK
Dr. Brian L. Cypher, California State University-Stanislaus, Bakersfield, CA
Dr. S.S. Talmale, Zoological Survey of India, Pune, Maharashtra, India
Prof. Karan Bahadur Shah, Budhanilakantha Municipality, Kathmandu, Nepal
Dr. Susan Cheyne, Borneo Nature Foundation International, Palangkaraja, Indonesia
Dr. Hemanta Kafley, Wildlife Sciences, Tarleton State University, Texas, USA
Other Disciplines
Dr. Aniruddha Belsare, Columbia MO 65203, USA (Veterinary)Dr. Mandar S. Paingankar, University of Pune, Pune, Maharashtra, India (Molecular)
Dr. Jack Tordoff, Critical Ecosystem Partnership Fund, Arlington, USA (Communities)
Dr. Ulrike Streicher, University of Oregon, Eugene, USA (Veterinary)Dr. Hari Balasubramanian, EcoAdvisors, Nova Scotia, Canada (Communities)
Dr. Rayanna Hellem Santos Bezerra, Universidade Federal de Sergipe, São Cristóvão, Brazil
Dr. Jamie R. Wood, Landcare Research, Canterbury, New ZealandDr. Wendy Collinson-Jonker, Endangered Wildlife Trust, Gauteng, South Africa
Dr. Rajeshkumar G. Jani, Anand Agricultural University, Anand, Gujarat, India
Dr. O.N. Tiwari, Senior Scientist, ICAR-Indian Agricultural Research Institute (IARI), New
Delhi, India
Dr. L.D. Singla, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana, India
Dr. Rupika S. Rajakaruna, University of Peradeniya, Peradeniya, Sri Lanka
Dr. Bahar Baviskar, Wild-CER, Nagpur, Maharashtra 440013, India
Reviewers 2019–2021
Due to pausity of space, the list of reviewers for 2018–2020 is available online.

The opinions expressed by the authors do not reflect the views of the
Journal of Threatened Taxa, Wildlife Information Liaison Development Society,
Zoo Outreach Organization, or any of the partners. The journal, the publisher,
the host, and the partners are not responsible for the accuracy of the politicalboundaries shown in the maps by the authors.

Print copies of the Journal are available at cost. Write to:
The Managing Editor, JoTT,
c/o Wildlife Information Liaison Development Society,No. 12, Thiruvannamalai Nagar, Saravanampatti - Kalapatti Road,
Saravanampatti, Coimbatore, Tamil Nadu 641035, India
ravi@threatenedtaxa.org

The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservation globally by

OPEN ACCESS publishing peer-reviewed articles online every month at a reasonably rapid rate at www.threatenedtaxa.org.

All articles published in JoTT are registered under Creative Commons Attribution 4.0 International License
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ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)

www.threatenedtaxa.org

August 2022 | Vol. 14 | No. 8 | Pages: 21487–21750
Date of Publication: 26 August 2022 (Online & Print)
DOI: 10.11609/jott.2022.14.8.21487-21750

ArticleDietary preference of Assamese Macaque Macaca assamensis McClelland, 1840
(Mammalia: Primates: Cercopithecidae) in Dampa Tiger Reserve, India– Ht. Decemson, Sushanto Gouda, Zothan Siama & Hmar Tlawmte Lalremsanga, Pp. 21487–
21500

Checklist of the orchids of Nokrek Biosphere Reserve, Meghalaya, India– Bikarma Singh & Sneha, Pp. 21660–21695
Morphological assessment and partial genome sequencing inferred from matK and rbcL
genes of the plant Tacca chantrieri– P.C. Lalbiaknii, F. Lalnunmawia, Vanlalhruaii Ralte, P.C. Vanlalnunpuia, Elizabeth Vanlalruati
Ngamlai & Joney Lalnunpuii Pachuau, Pp. 21696–21703

Reviews
Short Communications
Natural history notes on three bat species– Dharmendra Khandal, Ishan Dhar, Dau Lal Bohra & Shyamkant S. Talmale, Pp. 21501–
21507
The checklist of birds of Rajkot district, Gujarat, India with a note on probable local
extinction– Neel Sureja, Hemanya Radadia, Bhavesh Trivedi, Dhavalkumar Varagiya & Mayurdan
Gadhavi, Pp. 21508–21528

Conservation status of freshwater fishes reported from Tungabhadra Reservoir, Karnataka,
India– C.M. Nagabhushan, Pp. 21704–21709
Species diversity and distribution of large centipedes (Chilopoda: Scolopendromorpha)
from the biosphere reserve of the western Nghe An Province, Vietnam– Son X. Le, Thuc H. Nguyen, Thinh T. Do & Binh T.T. Tran, Pp. 21710–21714

Alien flora of Uttarakhand, western Himalaya: a comprehensive review– Shikha Arora, Amit Kumar, Khima Nand Balodi & Kusum Arunachalam, Pp. 21529–21552

Eremotermes neoparadoxalis Ahmad, 1955 (Isoptera: Termitidae: Amitermitinae)
a new record from Haryana, India– Bhanupriya, Nidhi Kakkar & Sanjeev Kumar Gupta, Pp. 21715–21719

Communications

New state records of longhorn beetles (Insecta: Coleoptera: Cerambycidae) from
Meghalaya, India– Vishwanath Duttatray Hegde, Sarita Yadav, Prerna Burathoki & Bhaskar Saikia,
Pp. 21720–21726

New records of Nyctalus leisleri (Kuhl, 1817) and Myotis nattereri (Kuhl, 1817) (Mammalia:
Chiroptera: Vespertilionidae) from National Park “Smolny” and its surroundings, Republicof Mordovia– Dmitry Smirnov, Nadezhda Kirillova, Alexander Kirillov, Alexander Ruchin & Victoria
Vekhnik, Pp. 21553–21560
Avifaunal diversity in unprotected wetlands of Ayodhya District, Uttar Pradesh, India– Yashmita-Ulman & Manoj Singh, Pp. 21561–21578
Can the Sri Lankan endemic-endangered fish Labeo fisheri (Teleostei: Cyprinidae) adapt toa new habitat?
– Dinelka Thilakarathne & Gayan Hirimuthugoda, Pp. 21579–21587
An overview of the fish diversity and their threats in the Gowthami-Godavari Estuary inAndhra Pradesh, India– Paromita Ray, Giridhar Malla, J.A. Johnson & K. Sivakumar, Pp. 21588–21604
DNA barcoding of a lesser-known catfish, Clupisoma bastari (Actinopterygii: Ailiidae) from
Deccan Peninsula, India– Boni Amin Laskar, Harikumar Adimalla, Shantanu Kundu, Deepa Jaiswal & Kailash Chandra,Pp. 21605–21611
Description of the larva of Vestalis melania (Selys, 1873) (Odonata: Calopterygidae)
identified through DNA barcoding– Don Mark E. Guadalquiver, Olga M. Nuneza, Sharon Rose M. Tabugo & Reagan Joseph T.
Villanueva, Pp. 21612–21618
Checklist of Carabidae (Coleoptera) in the Chinnar Wildlife Sanctuary, a dry forest in therain shadow region of the southern Western Ghats, India– M.C. Sruthi & Thomas K. Sabu, Pp. 21619–21641
Zoophily and nectar-robbing by sunbirds in Gardenia latifolia Ait. (Rubiaceae)– A.J. Solomon Raju, S. Sravan Kumar, L. Kala Grace, K. Punny, Tebesi Peter Raliengoane &K. Prathyusha, Pp. 21642–21650
A new population record of the Critically Endangered Dipterocarpus bourdillonii Brandis
from the Anamalai Tiger Reserve, India– Navendu Page, Srinivasan Kasinathan, Kshama Bhat, G. Moorthi, T. Sundarraj, Divya
Mudappa & T.R. Shankar Raman, Pp. 21651–21659

Range extension of lesser-known orchids to the Nilgiris of Tamil Nadu, India– M. Sulaiman, K. Kiruthika & P.B. Harathi, Pp. 21727–21732

Notes
Opportunistic sighting of a Sperm Whale Physeter macrocephalus Linnaeus, 1758 in
Lakshadweep Archipelago– Manokaran Kamalakannan, C.N. Abdul Raheem, Dhriti Banerjee & N. Marimuthu,
Pp. 21733–21735
An unusual morph of Naja naja (Linnaeus, 1758) (Squamata: Serpentes) from Goa, India– Nitin Sawant, Amrut Singh, Shubham Rane, Sagar Naik & Mayur Gawas, Pp. 21736–21738
Drape Fin Barb Oreichthys crenuchoides (Schäfer, 2009) (Cypriniformes: Cyprinidae)
a new fish species report for Nepal– Tapil Prakash Rai, Pp. 21739–21741
New distribution record of Gazalina chrysolopha Kollar, 1844 (Lepidoptera: Notodontidae)
in the Trans-Himalayan region of western Nepal– Ashant Dewan, Bimal Raj Shrestha, Rubina Thapa Magar & Prakash Gaudel, Pp. 21742–
21744
First record of Xanthia (Cirrhia) icteritia (Hufnagel, 1766) (Noctuidae: Xyleninae) from India– Muzafar Riyaz & K. Sivasankaran, Pp. 21745–21748
First report of the mymarid genus Proarescon Huber (Hymenoptera: Chalcidoidea:
Mymaridae) from India– Ayyavu Athithya & Sagadai Manickavasagam, Pp. 21749–21750

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