Wendlandia
tinctoria (Roxb.) DC. (Rubiaceae), a key nectar source for
butterflies during the summer season in the southern Eastern Ghats, Andhra
Pradesh, India
A.J. Solomon Raju 1, K.
Venkata Ramana 2 & P. Vara Lakshmi 3
1,2,3 Department of Environmental
Sciences, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India
Email: 1 ajsraju@yahoo.com
(corresponding author), 3 varalakshmi83@gmail.com
Date of
publication (online): 26 March 2011
Date of
publication (print): 26 March 2011
ISSN
0974-7907 (online) | 0974-7893 (print)
Editor: K.R. Sasidharan
Manuscript details:
Ms # o2503
Received 06 July 2010
Final received 26 October 2010
Finally accepted 15 February
2011
Citation: Raju,
A.J.S., K.V. Ramana & P.V. Lakshmi (2011). Wendlandia tinctoria (Roxb.) DC. (Rubiaceae), a key nectar source for butterflies during
the summer season in the southern Eastern Ghats, Andhra Pradesh, India. Journal of Threatened Taxa 3(3): 1594-1600.
Copyright: © A.J.
Solomon Raju, K. Venkata Ramana & P. Vara Lakshmi 2011. Creative Commons Attribution 3.0 Unported License. JoTT allows
unrestricted use of this article in any medium for non-profit purposes,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Abstract: Wendlandia tinctoria is a semi-evergreen tree species. It shows
massive flowering for about a month during March–April. The floral characteristics such as the
white colour of the flower, lack of odour, short-tubed corolla with deep seated
nectar having 15–18% sugar concentration are well tailored for visitation
by butterflies. The nectar is hexose-rich and contains the essential amino
acids such as arginine and histidine and the non-essential amino acids such as
alanine, aspartic acid, cysteine, glysine, hydroxyproline, tyrosine, glutamic
acid and serine. The inflorescences with clusters of flowers provide an
excellent platform for foraging by butterflies. The flowers are long-lived and
attractive to butterflies. A variety of butterflies visit the flowers for
nectar and in doing so, they pollinate them. Nymphalids are very diverse and utilize the flowers until
exhausted. The flowers being small
in size with a small amount of nectar compel the butterflies to do a more
laborious search for nectar from a greater number of flowers. But, the clustered state of the flowers
is energetically profitable for butterflies to reduce search time and also
flight time to collect a good amount of nectar; such a probing behaviour is
advantageous for the plant to achieve self- and cross-pollination. Therefore,
the study shows that the association between W. tinctoria and
butterflies is mutual and such an association is referred to as
psychophilous. This plant serves
as a key nectar source for butterflies at the study site where floral nectar
sources are scarce during the summer season.
Keywords:Butterflies, nectar source, psychophily, Wendlandia tinctoria.
This
article is part of the peer-reviewed Proceedings of the 3rd Asian
Lepidoptera Conservation Symposium (3ALCS-2010) jointly organized by the IUCN
SSC South Asian Invertebrate Specialist Group (SAsISG); Department of
Zoology, Bharathiar University; Zoo Outreach Organisation and Wildlife
Information Liaison Development, held from 25 to 29 October 2010 at Coimbatore,
Tamil Nadu, India. http://www.zooreach.org/3alcs2010.html
For figures, images, tables --
click here
Adult
butterflies that visit a wide variety of available flowers are considered to be
opportunistic foragers (Courtney 1986). However, studies conducted to date, indicate that butterfly species show
distinct flower preferences (Erhardt & Thomas 1991). Later, Kunte (2000) also stated that
butterflies do not feed indiscriminately from any flower that they might
find. They prefer certain floral
nectars with specific chemical composition. Their visits to different flowers also depend on other
factors like floral colour, shape, size, position and arrangement in the
inflorescence. For a butterfly, a
flower must offer a reasonable reward, yet may physically restrict access to
the reward. Access may be limited
by a complex flower structure demanding particular foraging skills. Faegri & van der Pijl (1979) stated
that the floral features such as large, red or blue, narrow, tubular flowers
with deep nectaries and often yellow rings or other markings on the petals
which function as nectar guides are important for butterfly visitation. Gunathilagaraj et al. (1998) reported
that butterfly flowers are often regular, tubular and sweet-smelling. Butterfly flower is typified by red,
yellow or blue upright flowers that have diurnal anthesis. Opler (1983) suggested that corolla
colour and shape, positioning of sexual parts, position on plant, presence of
nectar guides, fragrance, and time of anthesis play important roles in the
selection of flower foragers. Baker & Baker (1982, 1983) described two categories of flowers with
reference to flower-butterfly relationships. The first category is “true butterfly flowers” which are
characterized by deep, narrow corolla tubes with relatively copious
sucrose-rich nectar. The second
category is “bee and butterfly flowers” which are characterized by short-tubed
corolla with hexose-rich nectar for which Asteraceae members have been shown to
be excellent examples. The
findings of the present study on the floral biology of Wenlandia tinctoria and its mutual association with butterflies
have been examined in the light of these generalizations in order to adjudicateW. tinctoria as a key nectar resource for
butterflies during the summer season at the study site.
Materials and Methods
Wendlandia
tinctoria trees
occurring at the Seshachalam Hills of the southern Eastern Ghats of Andhra
Pradesh were used for the study during the summer season of 2009. The details of flower morphology such
as flower sex, shape, size, colour, odour, sepals, petals, stamens and ovary
were described. Ten fresh flowers
were used to measure the total volume of nectar/flower. The nectar sugar concentration was
measured by using a Hand Sugar Refractometer (Erma, Japan) as per Dafni et al.
(2005). Nectar analysis for sugar types was done as per the Paper
Chromatography method of Harborne (1973). Nectar analysis for amino acid types was done as per the Paper
Chromatography method of Baker and Baker (1973). Regular observations were made on butterflies visiting the
flowers for nectar to record the number of foraging visits species-wise and
then family-wise in order to assess the importance of W. tinctoria as a key nectar source during the
summer season.
Results
Plant
phenology and Floral biology: Wendlandia tinctoria is a semi-evergreen tree species with
scattered distribution in the forest (Image 1a). The field surveys in the entire forest area covering an
extent of 50km2 showed that the population of this species is
limited to about 25 trees only. The leaves are glabrous and elliptic-lanceolate borne opposite each
other. New leaf flushing occurs
during the rainy season adding a bright green look to the foliage. The flowering occurs from the third
week of March to the third week of April. The flowering is almost synchronous in all individuals. The flowers are borne in clusters of
terminal paniculate inflorescences (Image 1b). The flowers open at 0600 hr (Image 1c–e). The petals
unfold exposing the stigma and stamens beyond the length of the corolla
tube. The flowers are small, 6–7
mm long, tubular, white with a yellow tinge, odourless, regular and
bisexual. The calyx is very small
with five light green fused sepals. The corolla is tubate tipped with five lobes, 5mm long, white and
conceals nectar. The stamens are
five each with dithecous anthers having versatile fixation, very small and
situated below the stigma; the anthers appear star-like at the mature bud stage
but take different postures after anthesis. The style is erect and terminated with spathulate bifid
stigma. Nectar is produced in
minute amounts which stands at 0.6 ± 0.12 µl per flower and is collected at the
base of corolla tube. The nectar
sugar concentration ranged from 15% to 18%; the sugar types include sucrose,
fructose and glucose but the last is more dominant. The nectar contains both essential and non-essential amino
acids. The essential amino acids
are arginine and histidine while non-essential amino acids are alanine,
aspartic acid, cysteine, glysine, hydroxyproline, tyrosine, glutamic acid and
serine. The flowers remain in
place for four days and fall off subsequently.
Foraging
activity of butterflies:
The butterflies foraging for nectar included 25 species representing
Papilionidae, Pieridae, Nymphalidae, Lycaenidae and Hesperiidae (Fig. 1, Table
1). The Papilionidae and Pieridae
each was represented by two species, Lycaenidae by five species, Nymphalidae by
15 species, and Hesperiidae by a single species. The papilionids were Pachliopta hector (Image 1f) and Papilio clytia (Image 1g). The pierids were Catopsilia
pyranthe (Image
1h) and C.
pomona. The
nymphalids were Danaus
genutia (Image
1i),
D. chrysippus, Euploea core(Image 1j),
Tirumala septentrionis(Image 1k),
T. limniace (Image
2a),
Hypolimnas bolina(Image 2b),
H. misippus (Image
2c),
Precis iphita(Image 2d),
Phalanta phalantha(Image 2e),
Neptis hylas (Image
1f),
Junonia lemonias(Image 2g),
J. hierta, Ariadne merione, Acraea violae and Parantica
aglea (Image
2h). The lycaenids were Jamides celeno (Image 2i), Arhopala amantes (Image 2j), Lampides boeticus (Image 2k), Spindasis vulcanus (Image 2l) and Everes lacturnus. The hesperiid was Borbo
cinnara (Image
2m). Of these, the individuals of
nymphalid butterflies were more than those of other families at the flowers
throughout the flowering season. The data collected on the foraging visits of butterflies of each family
showed that nymphalids made 63%, lycaenids 18%, papilionids 9%, pierids 7%, and
hesperiids 3% of total visits (Fig. 2). The aggregated arrangement of flowers provides a comfortable landing
place for butterflies and this arrangement also enables them to probe several
flowers in each visit in succession for nectar before their departure. The clusters of paniculate
inflorescences borne terminally stand out prominently and the butterflies were
found to be attracted to them even from a long distance. All these butterflies stretched out
their proboscis to reach the floral base to access nectar; while doing so the
proboscis invariably contacts the stigmatic lobes and hence effects
pollination. The butterflies
frequently moved between individual plants of W. tinctoria which occur scattered in the forest; this inter-plant
foraging activity was considered to be important in promoting
cross-pollination. Further, the
diurnal hawkmoth, Cephonodes
hylas (Image
2n) also foraged for nectar during dawn hours.
Discussion
Burkhardt
(1964) and Faegri & van der Pijl (1979) characterized butterfly-flowers as
mentioned in the introduction section. Baker & Baker (1983) reported that the short-tubed flowers tend to
be hexose-rich and if grouped in conspicuous inflorescences provide an
excellent standing platform for foragers, and attract, both butterflies and
short-tongued bees. Cruden et al.
(1983) also stated that hexose-richness appears to prevail in the nectar of
short-tubed flowers. These authors
also documented that the nectars of most butterfly-pollinated flowers fall
within the range of 15 to 25% sugar concentration. Kingsolver & Daniel (1979) suggested that the nectar
sugar concentrations of 20–25% optimize the net energy gain by the
butterflies. In W. tinctoria, the floral characteristics such as
the white colour of the flower, lack of odour, short-tubed corolla with deep
seated hexose-rich nectar accounting for 21–26% sugar concentration
characterize psychophily.
Nectar is
a potential source of amino acids for the nutrition of butterflies. Naturally, butterfly nectars are rich
in amino acids (Baker & Baker 1983). Butterflies require ten essential amino acids but all of them are not
normally found in all nectars. Usually, three to four essential amino acids and several non-essential
amino acids are found in floral nectars (Baker & Baker 1982; 1983). Baker & Baker (1986) reported that
the amino acids add taste to the floral nectar and it depends on their
concentration. Their presence
serves as an important cue for butterflies to make flower visits and in the
process effect pollination. In W.
tinctoria, the
nectar contains two essential (arginine and histidine) and eight non-essential
amino acids. Its nectar is an
important source for two of the ten essential amino acids required by
butterflies during adult life for their growth and development (DeGroot 1953). Non-essential amino acids are
metabolized by butterflies from the food they take; however, floral nectar
provides some of these amino acids instantaneously. The nectar of W. tinctoria provides alanine, aspartic acid, cysteine, glysine,
hydroxyproline, tyrosine, glutamic acid and serine. Gardener & Gillman (2002) mentioned that if local soil
conditions favour higher amino acids in the nectar then local populations of
butterflies may derive certain benefits. Adult feeding on amino acid rich food has been shown to increase
longevity and reproductive ability in certain heliconine butterflies (Gilbert
1972; Dunlap-Pianka et al. 1977). A later study on a temperate species Euphydryas editha showed that amino acids in the adult diet led to heavier
eggs (Murphy et al. 1983). Jervis
& Boggs (2005) reported that the butterflies are agents of selection for
higher nectar amino acid production. The requirement of amino acids during adult stage of the butterfly is
related to the larval nutritional condition. The larval food plant has a key role in the evolution of the
flower-butterfly mutualism, and demonstrates that the importance to butterfly
reproduction, and of different nutrient source varies with butterfly
nutritional state. Gardener &
Gillman (2001) reported that soil conditions can affect the amino acid complement
of nectar. This may have
implications for plant-butterfly interactions, as local populations of
butterflies may benefit from the increased amino acid content of the nectar and
preferentially visit plants growing in high nutrient conditions. The fidelity of butterflies to W. tinctoria during the flowering phase attests the
fact that butterflies are in need of amino acids present in this nectar and in
the process of acquiring the amino acids, it is contributing to pollination.
In W. tinctoria, the inflorescences with clusters of
flowers provides an excellent platform for foraging by butterflies. The retention of flowers for four days
appears to be an adaptive trait for the plant to enhance its attractiveness to
butterflies. With these floral,
structural and functional characteristics, W. tinctoria has been found to be foraged by butterflies of all five
families of Lepidoptera. The
short-tubed flowers facilitate butterflies with any length of proboscis to
collect nectar easily. The flowers
being small in size with minute amounts of nectar compel the butterflies to do
a more laborious search for nectar from a greater number of flowers. But, the clustered state of the flowers
is energetically profitable for butterflies to reduce search time and also
flight time to collect a good amount of nectar. Overall, the search for nectar by butterflies due to the
production of minute amounts of nectar at flower level contributes to both
self- and cross-pollination. W. tinctoria attracts more number of individuals
and species of nymphalid butterflies when compared to those of other families
of butterflies suggesting that nymphalid butterflies use this plant as an
important nectar source. The
psychophily is advantageous for the plant because butterflies do not collect
pollen for themselves but only carry pollen on their proboscis and effect
pollination while collecting nectar. Therefore, the study shows that W. tinctoria with massive flowering is quite attractive to butterflies
and it is a keystone tree species for them since it provides them with nectar
for a period of about one month during summer season in the dry deciduous
forest ecosystem of Seshachalam Hills. There are no other plant species in flowering which attract a diversity
of butterflies to this extent during the flowering period of W. tinctoria and hence this tree species plays a
crucial role for the local butterflies for their nutrition for one month during
summer season.
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