Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 October 2022 | 14(10): 22001–22007
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.8023.14.10.22001-22007
#8023 | Received 20 May 2022 | Final received
12 October 2022 | Finally accepted 15 October 2022
Nectar robbing by
bees on the flowers of Volkameria inermis (Lamiaceae) in Coringa Wildlife Sanctuary, Andhra Pradesh, India
P. Suvarna Raju
1, A.J. Solomon Raju 2, C. Venkateswara
Reddy 3 & G. Nagaraju 4
1 Department of Health,
Safety and Environmental Management, International College of Engineering and
Management, Muscat, Sultanate of Oman, Oman.
2–4 Department of
Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh
530003, India.
1 suvarnarajup@rediffmail.com,
2 solomonraju@gmail.com (corresponding author), 3 cvreddy1980@gmail.com,
4 nagaraju_gattu@yahoo.com
Abstract: Floral traits that
shape the floral architecture are important to allow or disallow flower
visitors to access nectar and effect pollination. Specialization in floral
architecture is vulnerable to flower visitors that exploit nectar by robbery
without effecting pollination. In Coringa Wildlife
Sanctuary in Andhra Pradesh, India, studies on the exploitation of nectar by
robbery in plant species with specialized flowers are completely lacking. We
carried out a study on the foraging activity of insect foragers and nectar
robbing by bees on the specialized nectariferous
flowers of an evergreen shrub, Volkameria inermis growing in the landward side of this sanctuary.
Field observations indicated that the flowers of this species facilitate
legitimate probing only by butterflies and diurnal moths which while seeking
nectar effect pollination. However, two bee species Anthophora
dizona and Xylocopa
pubescens seek nectar illegitimately as primary
nectar robbers by making a slit/hole into the corolla tube from outside
bypassing the flower front. Additionally, A. dizona
gathers pollen legitimately from the stamens which are exposed and placed
outside the corolla tube. The stigma is also placed outside the corolla tube
but this bee indiscriminately makes attempts to collect pollen from the stigma,
as a result of which pollination occurs. Nectar robbing by these bees leads to
a reduction in nectar volume in robbed flowers and brings about variability in
the standing crop of nectar. As a result, the pollinating butterflies increase
the number of nectar foraging visits and shuttle between populations of V. inermis in quest of more nectar to meet their daily
metabolic requirements. Such a foraging behavior increases pollination rate in
general and cross-pollination in particular, which in turn increases plant
fitness in V. inermis. Therefore, the nectar
robbing by bees appears to have a positive effect on plant fitness through
change in seed set rates.
Keywords: Anthophora
dizona, butterflies, nectariferous
flowers, plant fitness, tubular corolla, Xylocopa
pubescens.
Editor: A.K. Sreekala, Jawaharlal Nehru Tropical Botanic Garden and
Research Institute, Trivandrum, India. Date
of publication: 26 October 2022 (online & print)
Citation: Raju, P.S., A.J.S.
Raju, C.V. Reddy & G. Nagaraju (2022). Nectar robbing by
bees on the flowers of Volkameria inermis (Lamiaceae) in Coringa Wildlife Sanctuary, Andhra Pradesh, India. Journal of Threatened
Taxa 14(10): 22001–22007. https://doi.org/10.11609/jott.8023.14.10.22001-22007
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: Dr.
P. Suvarna Raju is Assistant Professor, Department of Health, Safety and
Environmental Management, International College of Engineering and Management,
Muscat, Sultanate of Oman, Oman.
Prof. A.J. Solomon Raju,
Department of Environmental Sciences, Andhra
University, Visakhapatnam, India
Ch. Venkateswara Reddy and G. Naga Raju 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, India, for providing physical facilities for
carrying out this research work.
INTRODUCTION
Floral adaptations
that promote pollen transport by pollinators are treated as evidence of
specialization to a particular pollinator type (Castellanos et al. 2003, 2004).
Specialization in floral architecture is vulnerable to exploitation by flower
visitors which remove or steal nectar without effecting pollination which in
turn may show detrimental effects on plant fitness (Navarro 2001). 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 (Rojas-Nossa et al.
2016). Another form is 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 & Maloof 2002). 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.
Rojas-Nossa et al. (2021) reported that nectar
robbing behavior has negative, neutral and positive consequences according to
life history traits of the interacting animals and the ecological mechanisms
involved. These authors reported that nectar robbing has neutral effects on the
reproduction of Lonicera etrusca. In this
species, the nectar robbers act as pollinators and decrease the visitation
rates of legitimate foragers.
The available
information on the foraging activity and pollination in mangrove plant species
of Coringa Wildlife Sanctuary indicates that different
insect species act as pollinators there. Ceriops
decandra is pollinated by bees and wasps, C. tagal by flies and honey bees (Raju & Karyamsetty 2008), Avicennia
alba, A. marina, A. officinalis by insects (Raju et al. 2012), Caesalpinia crista by bees (Raju & Raju
2014), Derris trifoliata by bees (Raju & Kumar 2016a), Scyphiphora hydrophyllacea
by bees and wind (Solomon Raju & Rajesh 2014), Suaeda
maritima, S. monoica, S. nudiflora by wind and insects (Raju & Kumar 2016b),
Brownlowia tersa
by carpenter bees and honey bees (Raju 2019a), Sarcolobus
carinatus by insects (Raju 2019b), Xylocarpus granatum
and X. moluccensis by hawk moths (Raju 2020).
In all these plant species, none of the insects have been reported as nectar
robbers. 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, stingless bees, and some solitary
bees. These bees also act secondary nectar robbers. These bees use their
mouthparts to pierce the floral tissues.
Bumble bees use their maxillae, proboscis, or toothed mandibles to make
holes. Gerling et al. (1989) reported that carpenter bees use their maxillae to
make slits in the sides of the flowers. The insects that act as nectar robbers
in some plants pay legitimate visits to the flowers of others growing in the
same area and act as pollinators.
The aim of the
present study was to carry out field studies on legitimate and illegitimate
foraging visits to the flowers of a mangrove associate, Volkameria
inermis L. (Lamiaceae)
to collect nectar in Coringa Wildlife Sanctuary,
Andhra Pradesh, India.
MATERIALS AND METHODS
The Coringa Wildlife Sanctuary is a wildlife sanctuary and
estuary situated near Kakinada (16.716 0N, 82.245 0E) in
Andhra Pradesh State, India. It is the second largest expanse of mangrove
forest ecosystem in India with several viviparous, crypto-viviparous, oviparous
mangrove plant species, and also with several mangrove associate plant species.
In this sanctuary, Volkameria inermis is a mangrove associate that grows well with
bushy habit in landward locations. It is a perennial with leaf shedding taking
place year-long but this phenological event is quite prominent during summer
season (March–May). The flowering occurs during rainy season from August to
October but prolific flowering occurs during September. The study was carried
out during the flowering season of 2019 and 2020 to observe the foraging
activity of flower visitors in the collection of pollen and/or nectar. The
flower visitors were observed on five sunny days in each month of the flowering
season for their flower approaching, probing and forage collection behaviour. Nectar volume was measured by using a graduated
pipette while its sugar concentration was recorded by 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 foraging activity
was observed from sunrise to sunset to record the flower-visiting schedules of
individual species. Bee species visiting the flowers were captured and
identified by Zoological Survey of India, Howrah. Butterfly species visiting
the flowers were identified instantaneously by consulting the book of Kunte (2007). The field methods described in Dafni et al.
(2005) and Suvarnaraju & Raju (2014) were
followed for the collection of data on foraging visits made, foraging schedule,
foraging mode and flower handling time. The number of foraging visits made by
each insect species were recorded for 10 minutes at each hour throughout the
day from 0600 to 1800 for five days at random in July and August 2019 and again
for five days at random in August and September 2020. Based on these visits,
the mean number of total foraging visits made per day were calculated. The
foraging mode employed for forage collection were also recorded while the
insects were probing the flowers. The time spent for probing and collecting the
floral reward by each insect species was counted in seconds by using a stop
watch; the number of observations made was 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 insect species was
calculated to understand the flower to flower mobility rate. Among the flower
visitors, bees were found to exhibit nectar robbing behaviour;
this behaviour was carefully observed in the field in
order to quantify the number of flowers robbed from the total standing stock of
flowers. A sample of 650 flowers from five populations was observed for
recording the percentage of unrobbed and robbed
flowers. The flower morphological characters were also noted to evaluate their
specialized traits that contribute to the exploitation by nectar robbing bees.
Further, the observations on the foraging activity of these bees on other plant
species growing in the same area were also made to note whether they are
resorting to display illegitimate or legitimate foraging behaviour
to collect nectar.
RESULTS
Volkameria inermis flowers throughout
the year with intense flowering during rainy season from July to September
(Image 1a). It produces 3-flowered cymes in leaf axils (Image 1b) which open on
the same day (Image 1c) or in 2–3 days, between 1500–1800 h depending on the
stage of the bud development. The flowers are pedicellate, large, fragrant,
zygomorphic and functionally hermaphroditic. Calyx is green, cup-shaped at base
and valvate apically. Corolla is white and tubular with 4–5 lobes separated from
each other and reflexed. The stamens are 4 or 5, epipetalous and protrude out
of the corolla mouth at flower-opening. The ovary is bicarpellary with 2–4
ovules and extended into a long style tipped with stigma. The flowers initiate
nectar secretion soon after flower-opening but its secretion continues until
the noontime of the third day. Individual flowers produce 3.6 ± 1.3 µl of
nectar with 17 ± 2.13% (sugar concentration made up of three sugar types,
sucrose, glucose and fructose, and it is stationed around the ovary which is
completely concealed due to tubular corolla.
The floral
architecture is highly specialized and the stamens and stigma are exposed far
beyond the rim of the corolla tube in synchrony with the unfolding of the
petals. A diurnal hawk moth, Macroglossum gyrans Walker began visiting the flowers for nectar
almost immediately after flower-opening (1530 h) and continued its activity
until sunset (1800 h), again started visiting the flowers the next day during
dawn hours from 0430 h to 0600 h and stopped its foraging activity thereafter;
its foraging activity favors both self- and cross-pollination. The butterflies Pareronia valeria
Cramer (Image 1d), Danaus genutia Cramer
(Image 1e), & Borbo cinnara
Wallace (Image 1f), the digger bee Anthophora
dizona Engel (Image 2a,b), and the carpenter bee Xylocopa pubescens Spinola (Image 2c), visited the flowers regularly during
day time (Table 1).
Of these, only
butterflies probed the flowers legitimately from the flower-opening side to
insert their proboscis to reach the location of nectar; their proboscis length
facilitated to access and collect nectar with great ease (Table 1). In bees, A.
dizona foraged for both pollen and nectar while X.
pubescens foraged for nectar only. Both bee
species rob nectar by making a slit/hole into the corolla tube from outside
bypassing the flower front. This nectar robbing behavior indicates that they
are primary nectar robbers. A. dizona slit the
corolla tube tissue nearly at the flower base to rob nectar during which the
flower did not bend downwards due to its light body weight. On the contrary, X.
pubescens made a hole in the middle portion of
the corolla tube to rob nectar; the hole is usually at the origin point of the
epipetalous stamens which are covered by short hairs. During this activity, the
flower hangs downwards due to its heavy body weight. In the standing crop of
flowers, the flowers that were not robbed accounted for 61% while the robbed
flowers accounted for 39%. A. dizona had
collected pollen from individual anthers and in doing so they did not
discriminate the stigma from the anthers and hence invariably made attempts to
collect pollen from the stigma. The inability of this bee to distinguish the
anthers from the stigma was considered to be effecting pollination. Butterflies
being large in size were able to contact both anthers and stigma with their
wings/abdomen and effect self- and cross-pollination while collecting nectar
from the flower-opening side on clear sunny days. Flower-handling time (in
seconds) for forage collection varied with each insect species (Table 1). X.
pubescens had collected nectar only legitimately
from the flower-opening side from other plant species growing in the same area
(Table 1); they include Acanthus ilicifolius
L. (Acanthaceae) (Image 2d), Caesalpinia
crista L. (Fabaceae) (Image 2e), Malachra
capitata (L.) L. (Malvaceae)
(Image 2f) and Cucumis maderaspatanus
L. (Cucurbitaceae) (Image 2g). The flowers of all
these species are nectariferous but not specialized
and facilitated legitimate foraging behaviour by all
insects that seek nectar.
DISCUSSION
Specialized flowers
are vulnerable to exploitation by other flower visitors (Mainero
& del Rio 1985) by removing nectar without pollinating (Navarro 2001).
Nectar robbing takes place in nectariferous flowers
with morphological restrictions for illegitimate foragers but nectar robbing
foragers overcome these restrictions with their behavioural
and physical capacity to rob indicating that this nectar robbing activity is an
outcome of the ability of some flower foragers to rob nectar without effecting
pollination (Inouye 1980; Maloof & Inouye 2000). However, the flower
foragers that act as nectar robbers pay legitimate visits and pollinate the
flowers of other species growing in the same area indicating that the floral
traits of some plants are responsible for triggering this behaviour
in some flower foragers (Newman & Thomson 2005).
In the present study,
it is found that Volkameria inermis flowers are highly specialized as they possess
long corolla and abundant nectar with moderate sugar concentration containing
all the three common sugars and restrict the nectar access to illegitimate
foragers. The flowers are morphologically adapted for visits by moths and
butterflies which act as legitimate foragers-cum-pollinators while collecting
nectar. Since the long corolla tube of the flowers restricts access to nectar
for bees, A. dizona and X. pubescens, they resort to rob nectar by making slit or
hole into the corolla tube from outside bypassing the flower front. Both bee
species act as primary robbers as they do not acquire nectar from the slit/hole
made by the other bee. Further, the place where each bee species makes slit on
the corolla tube is different. A. dizona slits
at the base of the corolla tube while X. pubescens
at the middle part of the corolla tube; the selection of the place on the
corolla tube appears to be related to the physical strength they exert to cause
the nectar to flow to the place where the bees make slit. A. dizona is relatively small-bodied when compared to X.
pubescens; the landing of the former on the
corolla tube does not change the orientation of the latter to cause the nectar
to flow downwards for its collection while that of the latter changes the
orientation of the corolla tube causing the nectar to flow downwards which is
then easy for its collection. Since A. dizona
is unable to bring down the corolla tube by landing, it is compelled to move to
the flower base to make a slit to rob nectar. On the contrary, X. pubescens is able to bring down the corolla tube
considerably by landing due to which there is a rapid flow of nectar from the
flower base to the point where slit is made by it. These findings agree with
Inouye (1980) and Maloof & Inouye (2000) who stated that the nectar robbing
foragers overcome the morphological restrictions imposed by nectariferous
flowers for illegitimate foragers by changing their legitimate flower foraging behaviour and by using their physical capacity. Further, X.
pubescens is using certain other plant species
located in the same area, Acanthus ilicifolius,
Caesalpinia crista, Malachra
capitata and Cucumis
maderaspatanus as nectar sources by probing the
flowers legitimately. Such a flower-probing behaviour
displayed by X. pubescens indicates that it
has the ability to use physical capacity and employ legitimate and illegitimate
foraging behaviours to exploit the standing crop of
nectar from different nectariferous flowers with
different floral morphologies for its survival.
Newman & Thomson
(2005) reported that the pollinators may need to increase the number of flowers
they visit to meet their daily metabolic requirements if they visit the
nectar-robbed flowers in which there is usually a reduction in nectar volume.
Maloof & Inouye (2000) and Irwin et al. (2001) reported that changes in
pollinator behaviour due to nectar robbing may have
positive, negative and neutral effects on plant fitness through change in seed
set rates. The present study finds that nectar robbing by bees reduces nectar
reward and increases variability in nectar standing crop which in turn may make
the pollinating butterflies to increase the number of foraging visits and
shuttle between populations of V. inermis
frequently. Further study is needed to evaluate the effect of primary nectar
robbing by bees on pollination rate, genetic variation and plant fitness in V.
inermis.
CONCLUSIONS
In Volkameria inermis,
the pollinators are butterflies and diurnal moths. However, bees, Anthophora dizona
and Xylocopa pubescens
act as primary nectar robbers. A. dizona is
also a pollen gatherer and its attempts to probe the stigma for pollen results
in pollination. Nectar robbing by bees reduces nectar volume in robbed flowers
and at the same time brings about variability in the standing crop of nectar.
As a result, the pollinating butterflies increase the number of nectar foraging
visits and shuttle between populations of V. inermis
in quest of more nectar to meet their daily metabolic requirements. Such a
foraging behavior may promote pollination rate in V. inermis.
Further study is recommended to evaluate the effect of nectar robbing by bees
on the reproductive success and plant fitness in V. inermis.
Table 1. List of
insect foragers on Volkameria inermis.
Order |
Family |
Insect species |
Foraging period |
No. of foraging
visits/day* (n = 10 days) |
Mode of foraging |
Forage sought |
Flower handling
time (in seconds) |
Hymenoptera |
Apidae |
Xylocopa pubescens* Spinola |
08:30–17:00 |
35 ± 5.3 |
Illegitimate Primary nectar
robber |
Nectar |
2.8 ± 0.09 (n = 42) |
|
|
Anthophora dizona Engel |
08:00–17:00 |
28 ± 4.2 |
Illegitimate Primary nectar
robber |
Nectar + pollen |
3.2 ± 0.06 (n = 38) |
Lepidoptera |
Pieridae |
Pareronia valeria Cramer |
09:00–16:30 |
54 ± 3.4 |
Legitimate |
Nectar |
2.5 ± 1.2 (n = 32) |
|
Nymphalidae |
Danaus genutia Cramer |
09:30–16:00 |
42 ± 2.5 |
Legitimate |
Nectar |
2.1 ± 1.1 (n = 39) |
|
Hesperiidae |
Borbo cinnara Wallace |
09:00–15:30 |
32 ± 1.9 |
Legitimate |
Nectar |
2.8 ± 1.3 (n = 27) |
|
Sphingidae |
Macroglossum gyrans Walker |
15:30–18:00;
04:30–06:00 |
63 ± 6.7 |
Legitimate |
Nectar |
2.1 ± 0.04 (n = 46) |
No. of flowers
under observation: Approximately 150 each day on a different population in
each flowering season. *Collecting nectar
legitimately from the flowers of Acanthus ilicifolius,
Caesalpinia crista, Malachra capitata,
and Cucumis maderaspatanus. |
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