Flowers often attract a broader spectrum of visitors than 2010), Psychotria nilgiriensis (Malleshappa and Richard what predicted from their respective syndromes so that many 2011) and Wenlandia tinctoria (Raju et al. 2011).plants have more than one type of pollinators (Waser et al. MATERIALS AND METHODS1996, Fenster et al. 2004, Waser and Ollerton 2006, Ollerton

For this investigation, observations on various factors et al. 2009). Plant-pollinator community oriented interaction

have been made on naturally growing population of P. is the first step for defining pollinator and plant ‘guilds’ 0dicoccos in the Madras Christian College campus (12 55’ relationship mainly for assessing specialisation and

06.79" N 800 07’ 14.86" E) Chennai, Tamil Nadu, India.generalisation trend among them (Smith-Ramírez et al. Floral morphology—The morphological characters of 2005). Studies like this have a wide application in ecosystem

restoration & conservation and also helps in understanding flower such as sex expression, floral colour, scent, shape and the complexity as well as the organisation of pollinator symmetry were observed. Corolla length and diameter and relationship (Johnson and Ster 2000, Kremen and Rickett the stigma height were measured in fixed flowers (10 flowers) 2000, Kirk and Gilbert 2009).According to Shatz (1990), that are collected from 10 different plants. Individual flower community level characterisation of pollinators for any production was estimated by counting the number of tropical region has not been comprehensively investigated. inflorescence and flowers per inflorescence of 10 individuals

The present investigation was carried out by studying the (Virillo et al. 2007, Malleshappa and Richard 2011).floral structure, pollination mechanism and the fruit-set of Floral anatomy – The normal opened flowers were cut and Psydrax dicoccos belonging to family Rubiaceae. Psydrax removed carefully from the inflorescence and fixed in 5% dicoccos is a small unarmed evergreen tree growing up to 15 m FAA (5 ml of formalin, 5 ml of acetic acid and 90 ml of 70% tall with inflorescence in densely umbellate cymes and

ethanol). After 24 hrs of fixing, the specimens were pentamerous florets. This species is commonly distributed in

dehydrated with graded series of tertiary-Butyl alcohol open areas of tropical dry evergreen forest of peninsular India,

(TBA). Infiltration of the specimens was carried by gradual Nepal, China, Malaysia and Sri Lanka. The family Rubiaceae 0addition of paraffin wax (melting point 58–60 C). Then the shows a great variety in pollination syndromes, including

specimens were casted into paraffin blocks and sectioned at pollination by bees & butterflies (Hamilton 1990), moth 8μm thickness using Rotary Microtome followed by a (Nilsson et al. 1990) and birds (Sobrevilla et al. 198, Ree standard dewaxing protocol (Johansen 1940; Sass 1940). The 1997, Castro and Araújo 2004). Similar studies have been sections were stained with Toluidine blue O (Brien et al. conducted in various taxa of Rubiaceae such as Ferdinan dusa 1964). Photomicrographs at different magnifications were speciosa (Castro et al. 2001), Palicourea padifolia (Ornelas et taken with Nikon Labophot II microscopic Unit. al. 2004 a,b), Psychotria tenuinervis (Ramos and Santos Magnifications of the figures are indicated by the scale-bars. 2006), Chiococca alba (Castro et al. 2008), Hamelia patens Descriptions of floral anatomical features were made as per (Chauhan and Galetto 2009), Psychotria poeppigiana (Valois-the standard format (Esau 1964).Cuesta et al. 2009) and Palicourea rigida (Machado et al.

The International Journal of Plant Reproductive Biology 8(2) July 2016, pp.173-185DOI 10.14787/ijprb.2016 8.2.173-185

Floral structure and the fruit-set in Psydrax dicoccos Gaertn. (Rubiaceae) in relation to foraging behaviour of floral visitors

Subha V and Selva Singh Richard*

Department of Botany, Madras Christian College, Tambaram, Chennai-600059, India

*e-mail : *

Received : 15.11.2015; Revised: 12.02.2016; Accepted and Published on line: 01.07.2016

ABSTRACT

This study explains the floral structure and fruitset in Psydrax dicoccos in relation to the visit and behavioural pattern of the floral visitors. The morphological and anatomical features of P. dicoccos flowers are highly complex and specially designed for the broader spectrum of floral visitors. The flowers are hermaphrodite, actinomorphic, pentamerous with light-green calyx and white or greenish-white short tubular corollahaving dense ring of hairs in the internal part of the corolla tube, producing weak pleasant odour. In between the style and corolla occurs a thick circular nectariferous disc which secretes small quantity of nectar. Nectar and pollen are the major floral rewards for the floral visitors. Investigation on the floral visitors of P. dicoccos flowers has revealed 38 species of various functional groups such as butterfly, wasp, bee, moth, fly, ant, bug, spider and a reptile. Breeding experiment showed significant difference between the fruit-set of netted inflorescence (25.6%) and open inflorescence (80.6%). This highlights the influence of floral visitors in the process of pollination and the fruit-set of P. dicoccos.

Keywords : Floral structure, floral visitors, pollen, nectar, fruit-set.

ssrichard2001@gmail.com

EPR R OT DN UAL CP T IF VEO BYT IOEI L

C O

O G

S I SE TH ST

Histochemical studies— Both the entire flower and free-hand blue stain, the total pollen count was carried out on10 sections of P. dicoccos were used for histochemical staining undehisced anthers (Subba Reddi and Reddi 1986).especially for the localization of various histochemical Pollen/Ovule ratio — Pollen /ovule ratio was calculated by compounds. Fresh open flowers were immersed in 0.1% aqueous counting pollen grains (stained using Lactophenol-aniline Neutral Red stain (Effmert et al. 2005) for the localisation of blue stain) ofentire anthers from ten flowers and all the ovules Volatile aromatic compounds (floral scent) and 1% Sudan III belonging to ten pistils. In both the cases single flower was stain (1g in 100 ml of 70% ethanol) for the localisation of lipids. used per plant and observations were made under a light Stained flowers were examined with hand lens and the sections microscope.were examined under Nikon Labophot II microscopic Unit.

Pollen load on stigmatic surface— pollen grains on the Fresh sections were also stained with Toluidine blue O (Brien et

stigmatic surface were counted by mounting the entire stigma al. 1964) for the localisation of the protein bodies.

in Lactophenol-aniline blue stain and examined under the Pollen histochemistry— Pollen grains of the P. dicoccos microscope.were subjected to histochemical studies usingfreshly dehisced

Fruit Set — Fruit set was observed by counting all the flowers and undehisced anthers separately by following the standard

in the netted and open inflorescence of 10 individuals of each staining procedures.

set. This is to estimate the average number of flowers per Starch— Pollen I KI were treated with I KI reagent (2g of 22 inflorescence of both netted and open type. After a period of 15 Potassium Iodide and 0.2g of Iodine in 100 ml distilled water)

days interval, the developed fruits were counted from both for one minute, mounted in glycerine and observed under the

netted and open inflorescences. light microscope. The starch grains appeared blue to black in

Floral visitors— Floral visitors and their behaviour were colour (Jensen 1962). nd stobserved between 2 September 2011 and 21 September

Lipid— 0.7% Sudan IV stain was prepared by dissolving 0.7g 2011 from 6.00 am to 6.00 pm i.e. 12h/day during the peak

of Sudan IV in 100 ml of 95% ethanol and filtered using flowering period. Similar observations were conducted

Whatman No.1 filter paper before staining. The pollen grains throughout that flowering period but on different days and

were stained with Sudan IV stain for five minutes, mounted in covering a total of about 54 hours of field observation. Based

95% ethanol and observed under the light microscope. Lipids on the frequency of visits, visiting time and the behaviour of

stained red in colour (Gomori 1952).floral visitors on the flower, they were categorised as

Protein— Coomassie Brilliant Blue stain was prepared by pollinators, robbers or visitors. Pollinators were determined dissolving 0.25g of Coomassie Brilliant Blue dye in a mixture on the basis of their frequent contacts with the floral consisting of 45 ml methanol and 10ml acetic acid. This stock reproductive parts. Photographs of each visiting species were solution was filtered before usage. To 2ml of this stock taken for identification purpose. These visitors were identified solution, 4ml of 40% sucrose was added to give final dye and authenticated using standard references (Chapman 1969, concentration. Protein bodies appeared blue in colour

Mani1982) and also with the help of an entomologist.(Howlett et al. 1973).

RESULTS AND DISCUSSIONPollen morphology— Polliniferous material (mature flower

Psydrax dicoccos is distributed in the exposed areas of buds) was collected and stored in the sample vials containing tropical dry evergreen forests along with other native species 70% acetic acid. Pollen samples were subjected to standard such as Atlantia monophylla, Diospyros buxifolia, Grewia acetolysis method (Erdtman 1960) and then mounted in orbiculata, Memecylon umbellatum, Hemidesumus indicus unstained glycerin jelly, for permanent slide preparation and etc. P. dicoccos produce axillary cymose inflorescence. The microscopic observation. 50 pollen grains were measured and number of inflorescence per individual branch varies from 4 – the minimum, maximum and mean values were recorded. 29 (15) and the number of flowers per inflorescence varies Observation, measurements and photomicrographs were from 24 – 122 (50). The anthesis was diurnal and the flowers taken using Carl Zeiss microscope fitted with Canon EOS normally open at c. 07.00hrs. Immediately after blooming, the 450D digital SLR camera. Acetolysed pollen grains were anthers dehisce and the stigma is well receptive. Similar also coated with gold using HITACHI E-1010 ion sputter anthesis period was reported in Psychotria tenuinervis by and observed under HITACHI-S3400N Scanning Electron Virillo et al. (2007).Microscope from Central workshop, Department of

Mechanical Engineering, Anna University, Chennai. Floral morphology— The flowers of P. dicoccos are mostly hermaphrodite, actinomorphic, pentamerous, producing Pollen production— For the determination of the pollen weak pleasant scent, characterized by light-green calyx and productivity, mature and undehisced anther samples were white or greenish white short tubular Corolla (Co) of 3 – 4 collected (preferably from different conspecific individuals) (3.1) mm long and 2 mm in diameter. The inner part of the during the peak blooming period. Using Lactophenol-aniline

The International Journal of Plant Reproductive Biology 8(2) SUBHA AND RICHARD174

corolla tube bears dense Epidermal Trichomes (ET), which of lower tubular part and upper four free, triangular lobes. In are long, wide, thin walled and sinuous. The trichomes are between the style and corolla occurs a thick circular distributed in the upper dilated region and not in the lower nectariferous disc that secretes small quantity of nectar. The narrow region of the corolla tube (Figs. 1 B, C).The stamens nectar disc is c. 150 µm in height and 200 µm wide. It is are epipetalous attached along the mouth of the corolla. The hemispherical at the apex and it closely encircles the basal anthers deflected in between the petal rows about 1.3 mm in part of the style. These floral characters resemble the length (Fig. 1A). The base of the corolla tube has a thick characteristics features of bee, butterfly & wasp-visited cylindrical epigynous bilocular ovary of 700 µm in width. flowers (Proctor et al. 1996; Stone 1996; Taylor 1996; Castro The style arises from the central part of ovary and protruded and Oliveira 2002). The functional longevity of the flowers out from the corolla tube. The style is usually thin, narrow and was approximately over 12 hrs, after which the corolla lost its terminated with a capitate bilobed stigma, ranging from 9 – 10 shine by forenoon of the next day. Table 1 summarizes the (9.6) mm in length (Figs. 1A & B).The Corolla (Co) consists floral characters of P. dicoccos.

Table 1 – Floral characters of Psydrax dicoccos Gaertn.

Floral Characters

Floral type Hermaphrodite Floral Symmetry ActinomorphicFloral shape Tubular-shapedFloral colour Calyx green and corolla greenish whiteFloral scent Weak pleasantSepals 5 (conate)Petals 5 (conate) Anthers 5 Carpels 2Number of Ovule/flower 2

Minimum Maximum Mean

Number of inflorescence/branch 4 29 15

Number of florets/inflorescence 14 122 50

Number of pollen per anther 912 1228 1019

Pollen production per flower 3610 6140 5093

Pollen ovule ratio 1805:1 3070:1 2546:1

Floral anatomy: and appears to be 3-porate showing protruded Germ Tubes

(GT) (Figs. 2 D – G). Corolla—The inner epidermis of the lower part of the corolla

tube consists of radially elongated compact papillate cells. Nectar disc—The Nectariferous Disc (ND) of the mature The cells along the outer surface of the corolla tube are also floweris circular with regular ridges and shallow furrows. The

radially elongated, thin walled and vacuolated (Fig. 2 C). In Epidermal Cells (EC) are thick walled and possess dense

cytoplasm. The inner cavity of the disc also has small short between the two epidermal layers occur three or four layers of oblong cells that are secretary in nature (Figs. 2 A, B). Whereas angular compact parenchyma cells.The petal lobes have in the transverse section of young flower bud, the nectar disc small, thick walled outer epidermis, loosely arranged consists of a thick epidermal layer of radially elongated, spherical mesophyll ground tissue and the inner epidermal palisade-like cells (Ep). The interior ground tissue comprises of cells are papillate (Figs. 2 D, E). In transversal section of the compactly arranged parenchymatous cells with darkly stained flower at level of the nectariferous disc, five petals are seen as cell inclusions probably containing tannin. These tannin circular tube, their lateral margins are seen interlocking with containing cells are sparsely seen in the ground tissue. From the the marginal trichomes of adjacent petal lobes (Figs. 2 D & E).centre of the tubular nectar disc occurs the style (St) which is

Anther— Dithecous and the anther lobes are two chambered. circular and parenchymatous in nature (Fig. 2 D).

The anther wall consists of thick, wide radially oblong Ovary—The bi-carpellary epigynous ovary with anatropous Endothecium (Et). The endothecial cells have annular ovules on axile placentation. The ovary wall is thick, lignified thickenings called Stomium (ST). The inner and vascularised and have parenchymatous tissue, with scattered

outer walls are disintegrated at the time of dehiscence. The tannin containing cells (Figs. 2 H & I).

Pollen grains (Po) are deeply stained with Toluidine blue O

July 2016] 175FLORAL STRUCTURE AND THE FRUIT-SET IN PSYDRAX DICOCCOS GAERTN

The International Journal of Plant Reproductive Biology 8(2) SUBHA AND RICHARD176

Floral Histochemistry—The histochemical analysis of P. nectar disc and the inner layer of papillate cells (Pa) of the dicoccos entire flower and the floral parts revealed the corolla tube show intense staining. The ovules (OVL) also presence of various compounds such as starch, lipid and stained well with Sudan III and Neutral Red (Figs. 3 B & C). proteins (Table 2). Fresh flowers immersed in Sudan III stain The longitudinal sections of fresh flowers treated with I KI 2

exhibit the following reactions. The staining pattern indicated reagent showed the less number of starch grains in ovary and the presence of lipids in the petal lobes, anther and as well in nectar disc (Fig. 3D).the stigma (Fig. 3A).The flowers immersed in Neutral Red The qualitative localisation of major food reserves in the stain showed red colour staining only in small patches on the anther wall as well as in the pollen grains of both dehisced and petal lobes and deep staining on the anthers and stigma. These undehisced anthers show only the presence of lipids and the small patches of staining on the petal lobes indicated the starch and protein bodies are mostly lacking or present in presence of aromatic substances in the petal lobes. The negligible amounts. The presence of starch deposits were longitudinal sections of the mature flowers were stained with noticed only in the pollen grains of undehisced anthers (Fig. Neutral Red and Sudan III dyes shows that the cells of the

Fig. 1– Psydrax dicoccos, A. An axillary cymose inflorescence; B - D. Toluidine Blue O stained L.S. of flower showing the Sepals (SP), Corolla (Co), Epidermal Trichomes (ET), Nectar Disc (ND) and Style (St).

Fig. 2—Toluidine Blue O stained flower sections of Psydrax dicoccos. A & B. L.S. of Nectar Disc (ND) showing secretary Epidermal Cells (EC); C. T. S. of Ovary (OV) at the centre surrounded by a broad Nectar Disc (ND) followed by the Corolla (Co) and Calyx (Ca); D. T. S. of flower at the anther level showing central Style (St), surrounded by nectar disc with elongated Epidermal cells (EP), anther locules with Pollen grains (Po) and the Corolla (Co) as the outer most layer; E – G.T. S. of anther showing Anther Locule (Al) with Pollen (Po) and the anther wall showing Stomium (St); H & J. T. S. of Ovary (OV) showing anatropus Ovules (OVL)

July 2016] 177FLORAL STRUCTURE AND THE FRUIT-SET IN PSYDRAX DICOCCOS GAERTN

Table 2 –Histochemical localisation and distribution of biochemical substances in Psydrax dicoccos flower

Biochemical Stains/ Structural parts of the flower

substances Reagents

Corolla Tric Anther Ovary Style Stigma Nectar Pollen Pollen

home disc (UA) (DA)

Starch I KI - - - ++ - - ++ ++ -2

* * *Lipid Sudan III & IV +++ - +++ ++ + +++ + +++ +++

* *Protein Toluidine blue +++ + +++ ++ ++ +++ +++ ++ ++

O & Coomassie

Brilliant Blue

Aromatic Neutral Red ++ ++ ++ - + +++ - + ++

substances

‘-’: absent, ‘+’: present, ‘++’: moderate staining, ‘+++’: intense staining, UA: undehisced anther, DA: dehisced anthes

3E). The pollen grains of both undehisced and dehisced pollen production of an inflorescence is c. 85400 – 749080

anthers showed the presence of more lipid bodies and (249004) pollen grains.

comparatively less amount of protein (Fig. 4 A). The proteins Pollen loads on the stigmatic surface — The pollen load on in the aperture region of the pollen grains are deeply stained the stigmatic surface of the open inflorescence shows when compared to the other regions. Pankow (1957) observed considerable amount of pollen 61 – 123 (86), which is mainly the lipoidal coatings on the Brassica pollen wall surface and due to the contributions of pollinators. This shows the analysed that during the final period of pollen wall importance of pollinators in depositing the pollen grains on the development these additional lipoidal and pigmented stigma surface.substances may be accumulated on and between the outer Fruit set— In this study, the fruit set between the open and exine. This deposit is called as “Pollenkitt”. netted inflorescences shows significant variation. The netted Pollen morphology—The pollen grains of P. dicoccos are inflorescence showed the poor fruit set and unhealthy fruits

monad; radial symmetry; isopolar; 3(4)-porate; amb sub- ranges from 9 – 36 (26) %, this is due to the act of self-pollination whereas the open inflorescence show normal and triangular; P = 39 – 50 (43.8) ± 3.6 μm; E = 49 – 57 (52) ± 3.1 healthy fruit ranges from 22 – 81 (54) %. The higher fruit set in μm; P/E ratio: 0.84; suboblate; aperture porate, pore circular, the open inflorescences highlight the influence of pollinators poral membrane psilate, costae pori; exine 4 – 5 (4.8) ± 0.4 μm in the process of fertilization and the fruit set. Sakai and thick; equal at the pole and the midpoint of intercolpium; Wright (2008) on studying the reproductive ecology of 21 sexine coarsely reticulate; heterobrochate; intraluminal Psychotria species, reported that the heterostylous species set elements granulate (SEM); tectate; infratectum columellate; few fruits when flowers were bagged. In Hamelia patens, sexine > nexine (Figs. 4 B – F). Tilney and Van Wyk (1997) Chauhan and Galetto (2009) observed that cross-pollination classified this pollen as Canthium subtype C. The presence of produce higher fruit developed and larger heavy seeds when columellae with coarsely reticulated wall ornamentation as compared to self-pollination.well as granulated intra-luminal spaces in P. dicoccos pollen is Floral visitors— According to Castero and Oliveira (2002) highly useful in accommodating the lipid bodies (Fig.4 F). several species of Rubiaceae are visited by one or two This accumulation of lipoidal substance on the pollen wall dominant flower-visitors. We observed that the flowers of P. surface promotes the adhesiveness of the pollen that aid in dicoccos recorded visits of 38 floral visitors of which 37 insect pollination. Similarly, Ferguson and Skvarla (1982) species of insects, predominantly butterflies (13 species), bees stated that one of the functions of tectal columellae is the (6 species), moth (3 species), flies (2 species), ants (1 species), accumulation of pollen surface loadings. wasp (10 species), bug (1 species), spider (1 species) and one

Pollen production and Pollen-Ovule ratio—The number of reptile (Calotes versicolor) (Fig. 5). The visiting frequency of

pollen production of P. dicoccos was 722 – 1228 (1019) floral visitors, their preferable floral reward and their

pollen/ anther. Therefore, the total pollen production of a estimated pollinator type are provided in Table 3. Our data

single flower was calculated to 5093 pollen grains with a demonstrated that; the floral visit is mostly for nectar reward

pollen: ovule ratio (P: O) equivalent to 2546:1.The estimated

The International Journal of Plant Reproductive Biology 8(2) SUBHA AND RICHARD178

Fig. 3—Psydrax dicoccos. A. Neutral Red stained entire flower showing the presence aromatic compounds; B. Neutral Red stained L. S. of Ovary (OV) and nectar disc showing the presence of aromatic substances; C. Sudan III stained L. S. of Ovary (OV) and nectar disc showing the presence of Lipid droplets (Li); D. I KI stained L. S. of 2

Ovary (OV) and the nectar disc showing the Starch Grains (SG); E. I KI 2

stained pollen from the undehisced anther showing the presence of starch grains.

Fig. 4—Psydrax dicoccos. A. Sudan IV stained pollen grains in the anther locule showing the presence of lipid bodies; B – D. Light microscopic (LM) photomicrographs of acetolysed pollen (10 µm scale bar); E & F. Scanning Electron Microscopic (SEM) photomicrographs of pollen showing the porate aperture (10 µm scale bar) and a reticulate sexine with granulated lumina; G – N : Floral visitors of P. dicoccos G. Species of ant feeding nectar; H. Amegilla sp.; J. Apis dorsata; K. Apis indica; M.Thyreus sp.; N.Plautia sp.

and not for pollen. Similarly, Sakai & Wright (2008) also Euphorbia santapaui and Viburnum punctatum blossoms and reported that the floral visitors mostly visited for nectar and observed that these visitors may be the pollinators due to the the pollen-collecting behaviour was a rare phenomenon. presence of pollen deposits on their body surface.

Ants— In this study, single species of ant (Oecophylla sp.) Bee— Bees are the most frequent floral visitors and contributes 1.56% of total visits on the blossoms of P. dicoccos pollinators in tropical forests (Cane 2001, Ramos and Santos (Fig. 6). This ant belongs to the family, Formicidae and they 2006). In this study, bees are contributing about 33% of are frequent or sometimes the most frequent visitors to flowers visiting frequency of the floral visitors in P. dicoccos (Fig. 6). with accessible nectar (Corlett 2004). This ant species is small The flowers of P. dicoccos are mostly visited by bees such as and they can easily access the nectar without disturbing the Amegilla (Fig. 4 H), Apis dorsata (Fig. 4 J), Apis indica (Fig. anther or stigma. Hence this species is considered as nectar 4 K), Thyreus sp. (Fig. 4 M), Trigona sp. and Lassioglossum thieves (Fig. 4 G) (Inouye 1980 and Barth 1985). Reddi and sp. Among these bee species Apis dorsata and Thyreus sp. are Reddi (1984) reported, instead, the species of Camponotus considered to be an effective pollinators based on their size pollinating the blossoms of Euphobia geniculata. Recently and their frequent contact with the anther and stigma. Apis Richard et al. (2011) mentioned the visitation of ant species in dorsata is the most frequently visited bee species in this study.

Table 3 – List of observed floral visitors of P. dicoccos with their functional group, frequency, preferable floral reward and the estimated pollinator type.

S. No. Floral visitors and their Functional groups Frequency of visit Frequency % Preferable floral Pollinator/Robber/ reward Visitor

ANT

1. Oecophylla sp. 6 1.56 Nectar Robber

BEE

2. Amegilla sp. (Blue banded bee) 5 1.29 Nectar Robber

3. Apis dorsata 43 11.16 Nectar Pollinator

4. Apis indica 36 9.35 Nectar Robber

5. Thyreus sp. (Cuckoo bee) 2 0.51 Nectar Pollinator

6. Lasioglossum sp. 13 3.37 Nectar Robber

7. Trigona sp. 27 7.01 Pollen & Nectar Robber

BUG

8. Plautia sp. (Green bug) 2 0.51 Nectar Robber

BUTTERFLY

9. Anaphaeis aurota (Pioneer/Capperwhite) 19 4.93 Nectar Pollinator

10. Castalius rosimon (White zebra) 6 1.55 Nectar Pollinator

11. Catopsilia pomona (Common /Lemon emigrant) 6 1.55 Nectar Robber

12. Danaus chrysippus (Plain tiger) 4 1.03 Nectar Robber

13. Euploea core (Common crow) 23 5.97 Nectar Robber

14. Graphium sp. (Common blue bottle) 14 3.63 Nectar Pollinator

15. Junonia lemonias (Lemon pansy) 7 1.81 Nectar Robber

16. Pachliopta hector (Crimson rose) 7 1.81 Nectar Robber

17. Papilio polytes (Common mormon) 6 1.55 Nectar Robber

18. Phalanta phalantha (Common leopard) 6 1.55 Nectar Pollinator

19. Ratinda amor (Monkey puzzle) 3 0.77 Nectar Pollinator

20. Tirumala limniace (Blue tiger) 7 1.81 Nectar Robber

21. Zizina sp. (Grass blue) 35 9.09 Nectar Pollinator

FLY

22. Melagyna sp. (Syrphid fly) 2 0.51 - Visitor

23. Eristalinus megacephalus (Hover fly) 11 2.85 Pollen Robber

MOTH

24. Macroglossum sp. 1 1 0.25 Nectar Robber

25. Macroglossum sp. 2 17 4.41 Nectar Robber

26. Macroglossum sp. 3 2 0.51 Nectar Robber

REPTILE

27. Calotes versicolor (Oriental Garden Lizard) 1 0.25 - Visitor

SPIDER

28. Thomisus sp. (Crab spider) 1 0.25 - Visitor

WASP

29. Eumenes sp. 5 1.29 Nectar Pollinator

30. Eumenes flavopicta (Yellow potter wasp) 11 2.85 Nectar Pollinator

31. Isodontia elegans 17 4.41 Nectar Pollinator

32. Isodontia sp. 18 4.67 Nectar Pollinator

33. Phimenes flavopitus 3 0.77 Nectar Pollinator

34. Rhynchium sp. 1 2 0.51 Nectar Pollinator

35. Rhynchium sp. 2 6 1.55 Nectar Pollinator

36. Sceliphron sp. 5 1.29 Nectar Pollinator

37. Vespa tropica 4 1.03 Nectar Pollinator

38. Unidentified (Black wasp with 2 0.51 Nectar Pollinator

orange striped abdomen)

Based on the observations, the flowers of this plant are predominantly visited by butterflies, wasps and bees (Table 3). This confirms that species of the family Rubiaceae are mainly pollinated by hymenopterans and lepidopterans (Taylor 1996).

July 2016] 179FLORAL STRUCTURE AND THE FRUIT-SET IN PSYDRAX DICOCCOS GAERTN

The International Journal of Plant Reproductive Biology 8(2) SUBHA AND RICHARD180

Fig. 5—Contribution of different functional groups to the pollinators guild of Psydrax dicoccos

Fig. 6— Percentage of floral visiting frequency of functional groups on P. dicoccos

This giant honeybee is found throughout the Indomalayan study, Trigona sp. contributes about 7% of total visits and this

region (Corlett 2004). Deposition of pollen grains was also is the only genus that was harvesting both nectar and pollen.

observed on the head and thorax region of Apis dorsata (Fig. 4 Though Trigona sp. was harvesting pollen, it was not

J).Similar observations were made by Rasheed and Harder considered as an effective pollinator due to its size. Earlier

(1997), Richard et al. (2011). Apis dorsata colonies were studies show that many species of stingless bees, the genus

present only during the mass-flowering periods that occur at Trigona in particular are known to rob flowers (Almeda 1977,

irregular, multi-year intervals (Itioka et al. 2001). In the Roubik 1982, Renner 1983, Valois-Cuesta et al. 2009).

rainforests of Western Ghats, Apis cerana is an important Butterfly— Butterflies are usual visitors of open or tubular canopy pollinator along with A. dorsata (Devy and flowers and their role in the pollination are rarely studied in Livingstone 2001, Devy and Davidar 2003). Likewise small- India (Balasubramanian 1989, Devy and Davidar 2003). In sized bee species such as Amegilla, Lassioglossum and Apis Palicourea padifolia, Ornelas et al. (2004) reported 10% of indica did not make any significant contact with the stigma visits were by butterflies, whereas in this study, 13 species of while probing for nectar and these bees were considered as butterflies were observed to be visiting the blossoms of P. robbing nectar alone. Amegilla has been recorded throughout dicoccos which accounted for 37% of total species. Among the Indomalayan region, visiting a variety of flower types in these, Zizina sp. (Fig. 7 M) was the most frequently visited both open and forested habitats (Raju 1989, Raju and Reddi butterfly species (9.09%), followed by Eupolea core (5.97%)

(Fig. 7 E) and Anaphaeis aurota (3.64%) (Fig. 7 A). Based on 1989, Reddy and Aruna 1990, Atluri et al. 2000, Kato 2000, the size, frequency of visits and the behavioural pattern, Raju and Rao 2002). However, it appears to be most important butterflies such as Anaphaeis, Castalius (Fig. 7 B), Graphium as a pollinator in the understorey strata of evergreen forests (Fig. 7 F), Phalanta (Fig. 7 H), Tirumala (Fig. 7 K) and Zizina (Kato et al. 1989, 1991, Kato 1996, 2000, Momose et al. 1998, were considered to be the effective pollinators of P. dicoccos. Sakai et al. 1999). Amegilla species can extract pollen from Large butterfly species such as Catopsilia (Fig. 7 C), Danaus porose anthers by buzzing but their smaller size must make (Fig. 7 D), Euploea, Junonia (Fig. 7 G), Pachliopta, Papilio them less effective pollinators. Malleshappa and Richard and Tirumala were not considered as effective pollinators as (2011) recently observed a species of small Halictidae bee, they probe nectar by maintaining distance away from the Lasioglossum sp. accounted for 5.93% of total visits and blossoms and avoiding any contact with the essential considered as one of the pollinators of Psychotria nilgiriensis. reproductive parts. Valois-Cuesta et al. (2009) highlighted the Like wasps, bees visit flowers for nectar but, unlike wasps behaviour of butterfly species on the blossoms of Psychotria most bees also gather pollen as a high-protein to feed their poeppigiana. In the rain forest of Western Ghats, butterflies larvae (Corlett 2004). Bees rarely collect pollen and nectar visit many flower and they are considered major pollinators of simultaneously because the most efficient collecting four woody genera such as Callicarpa, Clerodendrum, behaviours are different (Rasheed and Harder 1997). In this

Spider0.26%Reptile0.26%

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Fig. 7—Floral visitors of Psydrax dicoccos: A. Anaphaeis aurota; B. Castalius rosimon; C. Catopsilia pomona; D. Danaus chrysippus; E. Euploea core; F. Graphium sp.; G. Junonia lemonias; H. Phalanta phalantha; J. Ratinda amor; K.Tirumala limniace; M. Zizina sp.; N. Melagyna sp.

Fig. 8—Floral visitors of Psydrax dicoccos : A. Eristalinus megacephalus; B – D. Macroglossum spp.; E. Eumenes sp.; F. Eumenes flavopicta; G. Isodontia elegans; H. Isodontia sp.; J. Rhynchium sp.; K. Sceliphorn sp.; M. Vespa tropica; N. Thomisus sp.

Trichilia and Vernonia (Devy and Davidar 2003). Species of Isodontia species (Figs. 8 G & H). The height of these wasp Mussaenda and Ixora are apparently pollinated by butterflies species are such that the thorax region can come in direct have sucrose-dominated nectars (Freeman et al. 1991). The contact with the stigma and thereby enabling the act of Nymphalidae have been implicated in the pollination of pollination. In India, Ropalidia was considered a major Syzygium species in Malaysian rainforest (Appanah 1990). pollinator of Zizyphus mauritiana (Devi et al. 1989), Ropalidia

and Rhynchium were considered major pollinators of Alangium Wasp—In this study, 10 species of wasps were recorded to be lamarkii (Reddy and Aruna 1990); Rhynchium and Vespa were visiting the flowers of P. dicoccos, contributing 18.96% of total considered important vector for moving pollen between visits (Fig. 6); all the wasp species were observed to be patches in Cardiospermum halicacabum (Das et al. 1997). collecting nectar. Similarly earlier studies reported that wasps Wasps in several genera are apparently major pollinators of were the common visitors of flowers that are with exposed Santalum album (Jyothi et al.1991); In Vitex negundo, species nectar and often some species were attracted to prey on other of Rhynchium and Ropalidia punctured the corolla tubes to get visitors (Faegri and van der Pijil 1979, Reddi and Reddi 1985, nectar greatly reducing fruit set in perforated compares with Dayanandan et al. 1990, Corlett 2001, Ramos and Santos 2006, non-perforated flowers (Reddy et al. 1992).Consolaro et al. 2011, Malleshappa and Richard 2011). Based

on the size and the behaviour, most of the wasp species are Moths— Three species of Macroglossum were observed visiting the floral blossoms of P. dicoccos (Figs. 8 B – D). The considered to be the pollinators of P. dicoccos. Large numbers contributions of these moths in pollination are meagre and of pollen grain were deposited on the thorax region of both

their visitation was mainly for nectar. Balasubramanian The results show that all the species of wasps especially the (1990) reported that the white scented tubular flowers of species of Isodontia and the butterfly genera such as Anaphaeis, Pavetta indica, are pollinated by hawkmoths. Similarly Castalius, Graphium, Phalantha, Ratinda and Zizina and bees Richard et al. (2011) observed a diurnal moth species of Apis dorsata and Thyreus sp. were considered to be the effective Arctiidae, Amata sp. was observed to be feeding nectar from pollinating agents.the flowers of Syzygium mundagam and considered this may

Acknowledgements—The authors wish to thank the Head, be a pollinator.

Department of Botany, Madras Christian College for Other floral visitors—A species of Syrphid fly, Melagyna providing infrastructural facilities during this study, Dr. R. (Fig. 7 N) was observed to be laying eggs on the blossoms of

Raveen, Associate Professor and Dr. Samuel Tennyson, P. dicoccos and apart from this no other significant

Assistant Professor, Department of Zoology, Madras observations were made on this species. A species of Crab

Christian College for their support in identifying floral spider, Thomisus (Fig. 8 N) and Garden lizards (Calotes visitors, Prof. P. Jayaraman, Director, Plant Anatomy versicolar) were attracted to the blossoms of P. dicoccos Research Center (PARC) for his help rendered towards mainly for the opportunity to prey up on these floral visitors. Anatomical studies and Mr. Sreenivasan, Central Workshop, Similarly, Anushuya (2011) observed a crab spider predating Dept. of Mechanical Engineering, Anna University for SEM on Apis dorsata on the flowers of Ventalago maderaspatana.studies.The floral visitors started their visits early in the morning

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