pollination ecology of rhynchosia minima (l.) dc...

ECOLOGIA BALKANICA2019, Vol. 11, Issue 1 June 2019 pp. 108-126

Pollination Ecology of Rhynchosia minima (L.) DC. (Fabaceae)in the Southern Eastern Ghats, Andhra Pradesh, India

A.J. Solomon Raju1*, K. Venkata Ramana2

Andhra University, Visakhapatnam 530 003, INDIA1 - Department of Environmental Sciences

2 - Department of Botany*Corresponding author: [email protected]

Abstract. Rhynchosia minima is prostrate climbing herb. In India it flowers during September-Marchwith peak flowering during January. The flowers are hermaphroditic, nectariferous, self-compatibleand have explosive pollination mechanism adapted for pollination by bees. They do not fruitthrough autonomous selfing but fruit through manipulated selfing, geitonogamy and xenogamymediated by pollen vectoring bees. The flowers not visited by bees fall off while those visited andpollinated by them set fruit. Seed dispersal occurs by explosive pod dehiscence. Perennial rootstock resurrects back to life during rainy season. Seeds also germinate at the same time but theircontinued growth is subject to the availability of soil moisture content. Therefore, R. minimaexpands its population size and succeeds as a weed in water-saturated habitats only. The plant isused as medicine, animal forage and human food and hence it has the potential for exploitationcommercially.

Key words: economic value, explosive pod dehiscence, explosive pollination mechanism,hermaphroditism, melittophily, Rhynchosia minima.

IntroductionRhynchosia is a genus of the legume

family fabaceae, tribe phaseoleae andsubtribe cajaninae (LACKEY, 1981;JAYASURIYA, 2014). It consists of more than232 species and occurs in both the easternand western hemisphere in warm temperateand tropical regions (GREAR, 1978; JACA et al.,2018; SCHRIRE 2005; TURNER 2011). In theEastern Ghats, twelve species of this genushave been reported to be occurring almost inone region, Seshachalam hills of southernEastern Ghats of Andhra Pradesh. Theyinclude R. albiflora, R. beddomei, R. cana, R.capitata, R. courtollensis, R. densiflora, R.heynei, R. minima, R. rothii, R. rufescens, R.

suaveolens and R. viscosa. These species areeither climbers or shrubs (MADHAVA CHETTY

et al., 2008). Of these, R. minima is apantropical species but it is thought to benative to the Old World and introduced andnaturalized in the New World. It is listed asleast concern in bhutan (LOPEZ POVEDA,2012). Its population is believed to be stableand no real threats are known at present.The population size of this species is notknown, but recent surveys between 1980 and2008 from throughout the range of thespecies in india suggest it occurs in groupsof plants from 30 to 500 individuals (LOPEZ

POVEDA, 2012). In australia, two varietieshave been reported in R. minima based on

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Pollination Ecology of Rhynchosia minima (L.) DC. (Fabaceae) in the Southern Eastern Ghats...

pod hair character, var. minima as havingpods with short fine hairs only and var.australis as having short fine hairs and longtubercular-based hairs on the pods(ANDREWS, 1952; STANLEY & ROSS, 1983).Later, HARDING et al. (1989) reported that R.minima is highly variable and there are fourvarieties in australia, var. amaliae, australis,minima and tomentosa. These authors alsostated that this species with many ecotypesthat vary in their adaptation and growthcharacteristics has the potential to exploit itas a forage plant. Of these infraspecific taxa,R. minima var. minima is studied for itspollination ecology.

Different authors noted that R. minima iswidely used as a medicinal plant. CHUTE &TIWARI (2002) noted that in the indian stateof maharashtra, the tribals of bhandara andgadchiroli district use its seed extract as aneye drop to cure conjunctivitis andinflammation. MUSTAK et al. (2006)mentioned that the whole plant is used forbath of the mother after delivery in pakistan.GUNDIDZA et al. (2009) stated that the plant istraditionally used in skin conditioning andto alleviate boils in zimbabwe. LOPEZPOVEDA (2012) described that the plant isused for medicines such as abortifacients,ecbolics, general healing, medicines to treatsickness such as haemorrhoids, heart,diarrhoea and dysentery. It is also used asfood (sweets) and its seeds are used asmiscellaneous poison or repellents. GILLETT

et al. (1971) mentioned that the plant is usedas animal forage; its palatability has beenbelieved to vary widely with differentecotypes that occur in different habitats.HASSELL (1945) stated that in queensland, theplant is eaten readily by animals whenyoung due to high palatability however,mature plant is not eaten due to fibrous andcoarse nature. BEESTON (1978) listed R.minima as highly palatable for animals in theblackall district of central west queenslandwhile BOYLAND (1973) mentioned this plantas moderately palatable for animals in thefar south-west of queensland. BOGDAN

(1977) stated that in kenya, the plant is

readily eaten by cattle than sheep; however,the cattle stay away during its floweringphase due to slight emission of scent fromflowers. SHUKLA et al. (1970) noted that thisplant is palatable to sheep in india. Despiteits wide use for humans and animals, thisspecies has not been studied for itsreproductive ecology in any part of theworld to understand the factors thatcontribute to the success of this plant as aweed in widely different ecologicalconditions that prevail in the tropicallatitudes.

Franco (1995, Pers. comm., Campinas,University of Campinas) provided floraldetails of Rhynchosia in Brazil. He reportedthat Rhynchosia is autogamous which islimited by spatial segregation betweenstigma and anthers. Levels of out-crossingare maintained by retention of a pollinationmechanism. Hypanthidium sp. and Centris sp.are the primary pollinators and the pollen isdeposited on the ventral part of theirabdomen when the flower is probed.CRAUFURD & PRINS (1979) reported thatRhynchosia sublobata is self-compatible andpollinated by Xylocopa bees. ETCHEVERRY etal. (2011) reported that Rhynchosia edulis andR. senna var. texana display valvularpollination mechanism; the former isfacultative xenogamous while the latter isobligately xenogamous. There is no otherinformation on flowering phenology,breeding systems, pollen presentationmechanisms, pollination mechanisms,pollinators and fruiting ecology of anyspecies of Rhynchosia. It is in this context, thepresent study was contemplated to providethe details of pollination ecology of R.minima to understand the sexualreproduction with which the plant is able topropagate and occupy different ecologicalniches in tropical regions.

Material and MethodsStudy siteThe study region is an integral part of

Southern Eastern Ghats of Andhra Pradeshin Peninsular India. The area is located at

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A.J. Solomon Raju, K. Venkata Ramana

13°40’N latitude and 79°19’E longitude. Theexact study area is the forest cover ofTirumala Hills, a constituent of SeshachalamHill Range in Chittoor District, AndhraPradesh. The entire region represents thedeciduous forest ecosystem. The site ischaracterized by a combination of rocky,undulating and steep terrain with some littercontent formed from grass and otherherbaceous plants. The temperature rangesfrom 40ºC to 42ºC during March to May andat other times varies from 26ºC to 34ºC. Therainfall varies from 975 to 1115 mm. In thisarea, Rhynchosia minima grows as a smallpopulation in open areas of soil rich inmoisture and litter and as isolatedindividuals in open rocky areas with lesssoil, moisture and litter.

Flowering and floral biologyFlowering season was defined based on

regular field trips made. Twentyinflorescences were tagged and followed torecord the length of flowering and thenumber of flowers produced. Anthesis wasinitially recorded by observing twenty fivemarked mature buds in the field. Later, theobservations were repeated five times ondifferent days in order to provide accurateanthesis schedule. Similarly, the maturebuds were followed for recording the time ofanther dehiscence. The presentation patternof pollen was also investigated by recordinghow anthers dehisced and confirmed byobserving the anthers under a 10x hand lens.The details of flower morphology such asflower sex, shape, size, colour, odour, sepals,petals, stamens and ovary were describedbased on twenty five flowers randomlycollected from five plants. Observationsregarding the position and spatialrelationships of stamens and stigma inmature bud, at anthesis and after during theflower-life with reference to self and/orcross-pollination were made very carefully.

Pollen outputThirty mature but un-dehisced anthers

from five different plants were collected and

placed in a Petri dish. Later, each time asingle anther was taken out and placed on aclean microscope slide (75 x 25 mm) anddabbed with a needle in a drop oflactophenol-aniline-blue. The anther tissuewas then observed under the microscope forpollen, if any, and if pollen grains were notthere, the tissue was removed from the slide.The pollen mass was drawn into a band, andthe total number of pollen grains wascounted under a compound microscope (40xobjective, 10x hand lens). This procedurewas followed for counting the number ofpollen grains in each anther collected. Themean pollen output per anther wasmultiplied by the number of anthers in theflower for obtaining the mean number ofpollen grains per flower. The characteristicsof pollen grains were also recorded.

Pollen-ovule ratioThe pollen-ovule ratio was determined

by dividing the average number of pollengrains per flower by the number of ovulesper flower. The value thus obtained wastaken as pollen-ovule ratio (CRUDEN, 1977).

Nectar charactersThe presence of nectar was determined

by observing the mature buds and openflowers. The average volume of nectar perflower was determined and expressed in µlbased; for this ten flowers were used. Theflowers used for this purpose were baggedat mature bud stage, opened after cessationof nectar secretion and squeezed nectar intomicropipette for measuring the volume ofnectar. Nectar sugar concentration wasdetermined using a Hand SugarRefractometer (Erma, Japan). Ten sampleswere used for examining the range of sugarconcentration in the nectar. For the analysisof sugar types, paper chromatographymethod described by HARBORNE (1973) wasfollowed. Nectar was placed on WhatmanNo. 1 filter paper along with standardsamples of glucose, fructose and sucrose.The paper was run ascendingly for 24 hourswith a solvent system of n-butanol-acetone-

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water (4:5:1), sprayed with aniline oxalatespray reagent and dried at 120oC in anelectric oven for 20 minutes for thedevelopment of spots from the nectar andthe standard sugars. Then, the sugar typespresent and also the most dominant sugartype were recorded based on the area andcolour intensity of the spot. The sugarcontent/flower is expressed as the productof nectar volume and sugar concentrationper unit volume, mg/µl. This is done by firstnoting the conversion value for the recordedsugar concentration on the refractometerscale and then by multiplying it with thevolume of nectar/flower. Table 5.6 given inDAFNI et al. (2005) was followed forrecording the conversion value to mg ofsugars present in one µl of nectar.

Stigma receptivityIn visual method, the stigma physical

state (wet or dry) was considered to recordthe commencement of receptivity. H2O2 testas given in DAFNI et al. (2005) was followedfor the confirmation of stigma receptivityperiod.

Breeding SystemsMature flower buds of some

inflorescences on different individuals weretagged and enclosed in paper bags. Theywere tested in the following way and thenumber of flower buds used for each modeof pollination was given in Table 1.

1. The flowers were fine-mesh baggedwithout hand pollination for autonomousautogamy.

2. The stigmas of flowers werepollinated with the pollen of the same flowermanually by using a brush; they werebagged and followed to observe fruit set inmanipulated autogamy.

3. The emasculated flowers were hand-pollinated with the pollen of a differentflower on the same plant; they were baggedand followed for fruit set in geitonogamy.

4. The emasculated flowers werepollinated with the pollen of a differentindividual plant; they were bagged andfollowed for fruit set in xenogamy.

All these categories of flowerpollinations were followed for fruit set. Iffruit set is present, the percentage of fruit setwas calculated for each mode.

Flower-visitorsThe flower foragers included only bees.

The hourly foraging visits of each beespecies were recorded on 3 or 4 occasionsdepending on the possibility and the datawas tabulated to use the same for furtheranalysis. Fully flowering plants wereselected to record the foraging visits of bees.The data obtained was used to calculate thepercentage of foraging visits made by eachbee species per day in order to understandthe relative importance of each bee species.Their foraging behaviour was observed on anumber of occasions for the mode ofapproach, landing, probing behaviour, thetype of forage collected, contact withessential organs to result in pollination,inter-plant foraging activity in terms ofcross-pollination (Solomon Raju & RadhaKrishna, 2017).

Determination of pollen carryover efficiencyof bees

Ten specimens of each bee species werecaptured from flowers and brought them tothe laboratory. The pollen loads if present inthe corbiculae of these bees, they wereremoved prior to pollen analysis. Eachspecimen was washed first in ethyl alcoholand the contents stained with aniline-blue ona glass slide and observed under microscopeto count the number of pollen grains present.From this, the average number of pollengrains carried by each bee species wascalculated to know the pollen carryoverefficiency of different bee species (SOLOMONRAJU & RADHA KRISHNA, 2017).

Natural fruit set, seed dispersal andseedling ecology

A sample of flowers on twenty fiveplants were tagged on different plants priorto anthesis and followed for fruit set rate inopen-pollinations. Fruit maturation period,

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fruit dehiscence and seed dispersal aspectswere observed to the extent possible. Fieldobservations were also made on fruit andseed dispersal modes, seed germination andseedling establishment to the extent possible(SOLOMON RAJU & RADHA KRISHNA, 2017).

Results

PhenologyRhynchosia minima is a perennial

prostrate, climbing herb with slender stemthat grows in open areas. The plant re-growsfrom below ground perennial root stock andfrom the seed during June-August duringwhich growth and leaf flushing occurs. Theplants growing in water saturated soils arerobust when compared to those growing inwater stress soils (Fig. 3a,b). The leaves aretrifoliate with reticulate venation. Theleaflets are petiolate, ovate-rhombic, andpuberulous, especially beneath. Theflowering occurs during September-Marchwith peak flowering in January. The plantswither and disappear in April. The flowersare borne in pedunculate axillary and 50-70mm long lax racemes; individual racemesare 4-6 flowered which open over a period of2-4 days (Fig. 3c).

Flower morphologyThe flowers are pedicellate, small (5.9 ±

0.6 mm long and 6.1 ± 0.5 mm wide), yellow,odorless, papilionaceous, zygomorphic andbisexual. The calyx is green with yellowtinge and consists of 5 free, linear-lanceolate,pubescent, 3-4 mm long sepals. The corolla isbright yellow, pubescent, consists of upperstandard petal, two wing petals and two keelpetals. The standard petal is large (4.9 ±0.3mm long and 5.7 ± 0.4mm wide), yellowstreaked with purple veins outside andinside but prominent at the bottom of theinside mid-region which serves as nectarguide; the petal base is clawed and consistsof two inflexed fingernail auricles. Thestandard petal envelops the rest of the petalsin bud but reflexes when the flower opens.The two adjacent petals (4.7 ± 0.4 mm long

and 2.6 ± 0.4 mm wide), called wing petalssurround the two bottom petals, called keelpetals (4.4 ± 0.4mm long and 2.3 ± 0.4 mmwide). The keel petals form a proximalcylindrical part and a distal part consistingof a pressed angular pouch, with an acuteporate tip in which the stamens and stigmaare housed. The keel and the wing petals areattached by means of two notched folds. Thewing petals serve as alighting platform forinsects visiting the flowers. The stamens areten, 5.6 ± 0.4 mm long, diadelphous; ninefilaments are fused by the basal part into asheath open along the upper side while thetenth filament is free and lies on the others.The distal parts of the filaments are free andcontain 1 mm long uniform dithecousanthers (Fig. 3j). The ovary is sessile, green,villous, 2.3 ± 0.4 mm long and lies in thesheath of the filaments along the cylindricalpart of the keel (Fig. 3l,m). It ismonocarpellary and monolocular with twoovules arranged on marginal placentation(Fig. 3o). It has a long glabrous style with acapitate wet shiny stigma (Fig. 3n), bothtogether account for a length of 3.6 ± 0.4 mm.The stigma is situated at the height of theanthers (Fig. 3j). The distal portion of freefilaments and style and stigma are incurvedand clamped into the keel petals.

Floral biologyMature buds (Fig. 3f) open during 1230-

1530 h with peak anthesis during 1330-1430h (Table 1). Unfolding of the standard petaland wing petals indicates flowering opening.The keel petals do not unfold and remain intheir original position as in mature bud stage(Fig. 3g,h). All the ten anthers in a flowerdehisce at the same time by longitudinal slitsin mature bud stage. The number of pollengrains per anther is 588.6 ± 65.98 and perflower is 5,886. The pollen-ovule ratio is2,943:1. The pollen grains are monads,spheroidal, 17.43 ± 2.49 µm in size, powderyand tricolporate, angulaperturate withreticulate exine (Fig. 3k). A nectariferous discis present at the base of the ovary. Theinitiation of nectar secretion occurs during

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mature bud stage and its cessation occurs anhour after anthesis. Individual flowersproduce 1.2 ± 0.03 µl of nectar with 0.38 mgof sugar. The nectar sugar concentration is28% (Range 26-30%) consisting of sucrose,glucose and fructose with the first asdominant. Nectar is deeply concealed and itis open through two windows between thejoined and the free filaments at the flowerbase. These windows allow access to thenectar. The stigma attains receptivity duringanthesis and remains receptive for aboutthree hours. After three hours of anthesis,the standard, wing and keel petals graduallymove close to each other enclosing thereproductive organs (Fig. 3d,e). The closedflowers remain so even during most part ofthe fruit development.

Pollination mechanismThe reproductive column is held under

pressure within the keel part in openflowers and it is exposed when thepollinator presses against the wing and thekeel petals (Fig. 3i). When insects land onthe wing petals, the latter causes the keelpetals to release the reproductive columnexplosively. Consequently, the reproductivecolumn snaps forward against the standardpetal causing most of the pollen to beinstantly released and the pollen thusreleased comes into contact with the ventralside of the insect body. Since the incurvedstigma is situated above the height of theanthers, it strikes the insect body first dueto which cross-pollination occurs if the

insect visited the other flowers previouslyand carried pollen on its ventral side andalso then the pollen ejected from the antherspowders the ventral side of the insectinstantly. If it is the first visit for the insectto the flower, then it effects self-pollinationupon explosive release of reproductivecolumn from the keel boat. With thedeparture of the insect from the flower, thereproductive column does not return backto its former position but the keel movesforward partly covering the stamens andstigma. The downward movement of keelpetals occurs in each subsequent foragingvisit by appropriate insects. Tripping ofkeel boat can also occur due to heavy rainor high temperature that weaken turgidityof the restraining keel tissues. But, thetripping due to these two factors is ruledout since the plant flowers during winterseason when heavy rains are rare and thetemperatures are usually low (21-26°C). Ifthe flower is untouched or tripping to keeldid not occur, the reproductive column isnever exposed and remain enclosed in thekeel boat. Such flowers fall off subsequentlyupon withering without fruit set.

Breeding systemsIn mature buds, anthers dehisce but

autonomous autogamy does not occur.Fruit set is absent in un-manipulatedautogamy, 16% in hand-pollinatedautogamy, 50% in geitonogamy, 88% inxenogamy and 46% in open-pollination(Table 2).

Table 1. Anthesis as a function of time in Rhynchosia minima.

Time (h) No. of flowers anthesed Percentage of Anthesis

1130 0 01230 11 151330 25 341430 29 401530 8 111630 0 0

No. of mature buds tagged: 73

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Table 2. Results of breeding systems in Rhynchosia minima.

Pollination mode No. of flowerspollinated

No. of fruitsformed Fruit set (%)

Autogamy (un-manipulated and bagged) 50 0 0

Autogamy (hand-pollinated and bagged) 50 8 16

Geitonogamy 50 25 50Xenogamy 50 44 88Open-pollination 351 160 46

Bee pollinators and pollinationThe flowers were exclusively foraged by

three species of bees for both nectar andpollen. The foraging activity began from1100 h onwards and ceased at 1700 h (Table3). The bees started probing the mature budswith partial opening of standard petal andshowed peak foraging activity during 1200-1300 h (Fig. 1). The bees belonged to onlyone order, Hymenoptera, one family, Apidaeand two sub-families, Apinae, andNomiinae. One bee species belonged toApinae and two species to Nomiinae (Fig.3p,q). More individuals of A. florea and a fewindividuals of Ceratina sp. and Nomia sp.were recorded at the flowers. Individually,A. florea made 35%, Ceratina sp. 33% andNomia sp. 32% of total foraging visits (Fig. 2).The body washings of foraging bees showedvariation in the pollen carrying capacity; theaverage pollen recorded on A. florea was174.2, Ceratina sp. 134.3 and Nomia sp. 106.4(Table 3). The flowers were visited severaltimes by bees but new visits lasted shorterthan the first one. With respect to theirbehavior, the bees landed on the wing petalsand the keel, with their head near thestandard petal. They then exerted a certainpressure with legs on the wing petals untilthese and the keel bent downwards, andthen proceeded to collect nectar duringwhich the bee's abdomen appeared pollensmothered (sternotribic pollen deposition).To collect pollen, the bees took "U" turn afternectar collection and proceeded to thestamens to collect pollen.

Fruiting behaviorThe fruit growth and development

begins immediately after pollination andfertilization. The fruits mature within threeweeks (Fig. 4a,b, e-h). The sepals enclose thegrowing fruit initially and the fruit emergesout of the sepals gradually with its gradualgrowth and development. Fruit is greeninitially and brown to dark brown when ripeand dry. It is a non-fleshy, hairy, oblong,13.7 ± 1.0 mm long, 3.9 ± 0.2 mm wide,compressed, rounded and apiculated podwith the remains of the style at the apex andnarrowing towards the base. The podsproduced mostly two seeds but rarely oneseed; it is compressed between two seeds. Incertain 2-seeded pods, one seed is usuallyhealthy and the other is aborted (Fig. 4i).

Seed ecologyMature and dry fruits display explosive

dehiscence to disperse seeds. The pod with bi-valvate configuration dehisce elasticallyejecting the seeds (Fig. 4c,d). The seed isgreyish to brown, compressed, reniform, finelypubescent, shortly beaked, 2.9 ± 0.2 mm long,1.9 ± 0.2 mm wide and shiny withoutstrophiole (Fig. 4j). Seeds germinate duringrainy season which starts from June to August.Seedlings grow continually but their growthrate is subject to the availability of moisturestatus of the soil. In areas where soil issaturated with moisture and contains litter,seeds continue growth and produce matureplants within two months and subsequentlycommence flowering and fruiting.

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Fig. 1. Hourly foraging activity of bees on Rhynchosia minima.

Fig. 2. Percentage of foraging visits of individuals bees on Rhynchosia minima.

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Fig. 3. Rhynchosia minima: a. Luxurious growth in water-saturated soil, b. Individualplant in water-stress soils, c. Flowers, d-e. Closure of standard petal covering the wing andkeel petals, f. Mature bud, g. & h. Flower with stamens and stigma housed in keel petals, I.Explosive release of stamens and stigma from keel petals, j. Stamens and stigma, k. Pollen

grain, l. Pistil, m. Pubescent ovary, n. Capitate stigma, o. Ovules, p. & q. Nomia bees.

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Fig. 4. Rhynchosia minima: a. Fruiting branch with maturing and mature pods, b.Maturing pods, c. Mature and dry pods partly split for seed release, d. Explosive twisting ofpod for seed release , e-h. Different stages of pod development, I. Pod with one healthy seed

and one aborted seed, j. Healthy seeds.

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Table 3. Pollen recorded in the body washings of bee foragers on Rhynchosia minima.

Bee species Sample size(N)

Number of pollen grains

Range Mean S.DApis florea 10 79-276 174.2 72.05Ceratina sp. 10 61-183 134.3 38.21Nomia sp. 10 43-147 106.4 32.43

DiscussionRhynchosia minima grows in diverse

habitats of tropical regions of the world. LOPEZ

POVEDA (2012) documented that this speciesoccurs in grassland, grassland with scatteredtrees, woody bush land, ruderal land,roadside, grazed and human disturbed land,plain land and sandy black soil. HARDING et al.(1989) also stated that this species occurs in avariety of habitats but most often on self-mulching heavy clay soils, from sands andsandy loams. With its ability to grow indifferent habitats, it appears to have evolvedcertain characters that are adaptive to thehabitat(s) where it occurs. Such evolvedcharacters might have led to the origin ofdifferent ecotypes or varieties in this species.In australia, var. minima and var. australis havebeen reported in this species complex based onpod hair character (STANLEY & ROSS, 1983;ANDREWS, 1952). Later in the same country,HARDING et al. (1989) described four varieties -amaliae, australis, minima and tomentosa in thisspecies complex based on variations in theiradaptation and growth characteristics. In thepresent study, R. minima has been found togrow in water-saturated and water stress soils.It grows as a population in water-saturatedsoils while as scattered or isolated individualsin soils experiencing water stress and rockyareas with little soil content. R. minima did notshow any notable variations in their growth ormorphological characters but the plantsgrowing in moist soils are comparativelyrobust to those growing in drought or rockyareas. However, further work in this line indifferent habitats in India may reveal theexistence of ecotypes or varieties in thisspecies.

Rhynchosia minima is a prostrate,climbing herb which grows from perennialroot stock during rainy season. It alsoproduces new plants from seed stock at thesame time. Full leaf flushing is complete bythe end of August and floral bud initiationtakes place in October. The flowering seasonis well defined and is confined to north-eastmonsoon and winter seasons. Individualplants produce a small number of flowersduring their life time due to production of afew inflorescences and each of whichproducing a maximum of only six flowers.The plant during flowering phase does notattract many flower foragers althoughdifferent categories of insects exist in thevicinity; the prostrate habit, display of a fewflowers at ground level and dull banner petal(standard petal) appear to be responsible forthe non-receipt of visits by many insects.

In R. minima, hermaphroditic sexualsystem is functional due to production offertile pollen grains and functional ovary.The flowers display the near synchronoushermaphroditism or homogamy due to theoccurrence of anther dehiscence in maturebud stage and receptivity of stigma duringanthesis. The entire reproductive columnstays inside the keel petals even afteranthesis; in this situation, there is alikelihood of the occurrence autonomousautogamy. But, hand-pollination testsindicated that autonomous autogamy doesnot occur despite self-compatibility but it isfunctional because fruiting occurred whenthis mode of pollination is manipulated bybrushing the stigma with its own pollen.Such a situation suggests that the flowers areessentially dependent on flower foragers for

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fruit set through self- as well as cross-pollination. It appears that the stigmaalthough receptive blocks the germination ofthe self-pollen while it is in keel petals andhence, it essentially requires the rupture ofits surface by a pollinator to allow the self -or cross pollen to germinate. Such astigmatic regulatory function appears tohave evolved to discourage selfing andpromote out-crossing. SHIVANNA & OWENS

(1989) stated that the rupture of the stigmaticsurface by pollinator permits the pollen togerminate in the flowers of phaseoleaemembers with thick stigmatic cuticle. On thecontrary, CASTRO & AGULLO (1998) reportedthat in vigna, a member of the tribephaseoleae, autonomous self-pollinationmay occur by spontaneous rupture of thestigmatic membrane. Similar stigmaticsurface that prevents self-fertilization hasalso been reported in vicia faba (tribe vicieae)(LORD & HESLOP-HARRISON, 1984) and inmedicago scutellata (tribe trifolieae) (KRIETNER& SORENSEN, 1985); however, in these speciesauto-fertile lines have been reported to havethin stigmatic cuticles allowing spontaneousdisruption and self-fertilization. In R.minima, the stigmatic surface appears to havethick cuticle and does not have themechanism of causing spontaneous ruptureto facilitate autonomous self-pollination. Ineffect, the tripping of keel petals appears tobe essential to cause rupture on the stigmaticsurface by the tripping agent due to whichthere is more likelihood of the occurrence ofeither geitonogamy or xenogamy. The fruitset rates recorded in hand-pollinatedgeitonogamy and xenogamy alsosubstantiate that the plant is facultativexenogamous, a breeding system that isflexible and keeps the options open for bothselfing and out-crossing mediated by pollenvectors.

SCHRIRE (1989) stated that the ecologicaland evolutionary success of leguminosae hasbeen related to biotic pollinationmechanisms. The six sub-families within thisfamily have achieved a characteristic floralarchitecture, in which plants within the sub-

family Papilionoideae have developed themost complex floral mechanisms. Plantswithin the papilionoideae have zygomorphicflowers that are mainly bee-pollinated(Westerkamp, 1997; LPWG, 2017) althoughbird pollination and bat pollination havealso been recorded (ORTEGA-OLIVENCIA etal., 2005). In bee-pollinated flowers ofPapilionoideae, each part of the corolla isspecialized for a particular role in pollinatorattraction and the success of pollination. Theflag or standard petal attracts pollinators; thekeel protects androecium and gynoeciumand, together with the wings, provides aplatform for the insects to land on. Thewings also operate as levers that raise orlower the keel (STIRTON, 1981). The flowerstypical of pollination by the bee familyapidae are zygomorphic, bright yellow orblue with nectar guides, and frequently withhidden rewards such as those in thelamiaceae, scrophulariaceae, fabaceae andorchidaceae (FAEGRI & VAN DER PIJL, 1979).In the present study, the Fabaceae member,R. minima has papilionaceous corolla withflag, wing and keel petals; the flag petalserves as a visual attractant, wing petalsprovide landing platform and keel petalsprotect the entire reproductive column. Theflowers are typical of pollination by beessince they are zygomorphic, standard petalwith nectar guide, hidden nectar at thecorolla base and hidden pollen in keel petals.

Within the sub-family Papilionoideae,primary and secondary pollen presentationshave been reported. In plants with primarypollen presentation, pollen is delivereddirectly from the anthers to the vector'sbody. In plants with secondary pollenpresentation, pollen grains are delivered firston a floral part such as the keel petals inpapilionoideae and then on the body of thevector implying an accurate delivery ofpollen on the vector's body (HOWELL et al.,1993). These two pollen presentationpatterns are associated with the four types ofbasic pollination mechanisms - valvular,pump, explosive and brush, all of them areassociated with a particular floral

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architecture and kinetics. In the valvulartype, pollen presentation is primary,whereas in the other three mechanisms, it issecondary (YEO, 1993). In the explosivemechanism, commonly only one pollinationevent occurs and it has evolvedindependently in several tribes (SMALL,1988), while in the other three mechanisms,repeated visitation is possible (WESTERKAMP,1997). In the present study, R. minimaflowers have explosive pollinationmechanism and deliver pollen directly fromthe anthers to the bee's body when keelpetals are tripped by the foraging bee; thistype pollen delivery is the representative ofprimary pollen presentation associated withexplosive pollination mechanism. In theflowers, the staminal column is held underpressure within the keel, and when thetension is released by the forager, the samecolumn snaps forward against the standardpetal causing all the pollen to be instantlyreleased. The reproductive column remainsexposed and does not return back to itsoriginal state but the keel petals return backpartially covering the stamens and stigma.The efficiency of explosive pollinationmechanism depends on the ambient weatherconditions, especially temperature andrelative humidity. Since R. minima flowersduring winter season, it accordinglycommences anthesis from noon onwards bywhich time the ambient air will be relativelydry and hence is conducive for the efficientfunctioning of the explosive pollinationmechanism. Further, the bees also commencetheir foraging activity from around noontime and continue forage collection until theflowers close back. The concealment of thestamens within the keel petals until it istripped is an advantage for the plant tosecure pollen from unusual rains andambient moisture conditions during theflowering season of this plant (PETER et al.,2004).

PERCIVAL (1961) stated that plants withdeep-tubed flowers tend to produce sucrose-rich nectar, whereas those with open orshallow-tubed flowers tend to be hexose-

rich. BAKER & BAKER (1983) stated thatflowers with long corolla tube possess moresucrose in their nectar while those with shorttubes possess more hexoses in their nectar.In the present study, R. minima with shortcorolla tube presents sucrose-rich nectarbecause the nectar is perfectly concealed andhence is not exposed for the breakdown ofsucrose into hexoses. Concealment of nectarin this species is adaptive to protect againstmicroorganisms, particularly yeasts, whosemetabolic activities dramatically changenectar chemistry and the plant gains abenefit from keeping the nectar as sterile aspossible to maintain control over itschemical composition in order to maximizepollination rate by attracting appropriatepollinators (HERRERA et al., 2008). Honeybees prefer the flowers with sucrose as chiefconstituent of nectar (KEVAN, 1995). Theflowers pollinated by long-tongued beesproduce sucrose-rich nectar (BAKER &BAKER, 1990). In line with this, R. minimawith melittophilous pollination syndromealso produces sucrose-rich nectar which isutilized exclusively by long-tongued bees.Apis, ceratina and nomia bees recorded on thisherb have been documented as long-tonguedbees (CRUDEN et al., 1983; ROUBIK, 1992;ROUBIK, 2006). Bee-flowers tend to producesmall volume of nectar with higher sugarconcentration than the nectar of flowerspollinated by other animals (OPLER, 1983;CRUDEN et al., 1983). Honey bees prefersugar concentration of 20 to 40% in thenectar (WALLER, 1972). On the contrary,BAKER & BAKER (1983) noted that honey beesprefer sugar concentration of 30 and 50% inthe nectar. The honey bees have the ability toregurgitate liquid onto concentrated or evencrystallized nectar, in this way, reduce itsconcentration so that it may be imbibed. Thepreferred sugar concentrations of nectar byother categories of bees have not been foundin the literature. But, PYKE & WASER (1981)stated that the nectar sugar concentration offlowers pollinated by bees is generallyhigher than that of those pollinated bybutterflies and hummingbirds; bee-

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pollinated flowers tend to produce nectarwith sugar concentration more than 35%while butterfly or hummingbird pollinatedflowers tend to produce nectar with sugarconcentration ranged between 20 and 25%.In line with these reports, the present studyshows that the flowers of R. minima producea small volume of nectar with 28% sugarconcentration. Further, the energy yield fromnectar appears to be in tune with therequirement of energy by bees. Therefore, R.minima flowers with explosive pollinationmechanism, primary pollen presentation,and hidden nectar and pollen have evolvedto discourage other foragers from visitingthe flowers and to ensure that the bees getthe floral rewards. Accordingly, the flowersof R. minima never received visits from othercategories of insects.

In R. minima, the keel tripping process isnot self-activated to effect pollination. Theflowers depend on bees for tripping of thekeel petals to enable the working ofexplosive pollination mechanism. Theflowers that were not tripped by externalagents subsequently fall off. This situationexplains that the plant is obligatelydependent on bees for pollination. The beesvisiting the flowers seem to be efficient intripping the flowers because the flower sizeand petal strength are commensurate withthe bee size and the force employed todepress the wing petals to access the nectar.MISHRA & RAJESH KUMAR (1997) reportedthat the pollen has great importance for abee colony as pollen provides proteins,which are essential for worker honey bees tosecrete glandular food (royal jelly) forrearing brood. Availability of enough pollendirectly helps in more brood rearing, whichultimately leads to gradual colony build up.R. minima serves also as a pollen source forforaging bees.

CRUDEN (1977) used the pollen-ovule(p/o) ratios as indicators of breedingsystems of plants. He provided P/O ratiosfor different breeding systems - 168.5 + 22.1for facultative autogamy, 798.6 + 87.7 forfacultative xenogamy and 5859.2 + 936.5 for

xenogamy. Several workers followed theseP/O ratios to classify breeding systems ofthe plant species studied by them. ARROYO(1981) stated that the p/o varies according tothe pollination mechanism withinpapilionoideae. These authors suggestedthat the plants with explosive mechanismhave a low P/O because a single pollinatorvisit is needed for efficient transference ofpollen; this low P/O is a consequence of thehighly specialized, irreversible pollinationmechanism, which allows only one effectiveexchange of pollen with pollinators. SMALL(1988) stated that medicago species of thetribe trifolieae with explosive pollinationmechanism displays the lowest pollen-ovuleratios. LOPEZ et al. (1999) recorded explosivepollination mechanism with highest pollen-ovule ratios in certain genera of the fabaceaesuch as cytisus, pterospartum, teline, ulex,stauracanthus and cytisophyllum. ETCHEVERRYet al. (2011) stated that the fabaceae plantswhich they studied with explosivepollination mechanism had intermediatepollen-ovule ratios. These authorsmentioned that Rhynchosia edulis and R.senna var. texana have valvular pollinationmechanism with primary pollenpresentation. Both the species are classifiedas obligate xenogamous based on P/O ratiobut R. edulis has been found to be facultativexenogamous in hand-pollination tests.CRAUFURD & PRINS (1979) reported that r.sublobata is self-compatible and facultativexenogamous in hand-pollination tests; it ispollinated by xylocopa bees. In the presentstudy, r. minima shows highest p/o ratiowhen compared to that of facultativexenogamy used by CRUDEN (1977). Thehighest P/O ratio in this plant speciesappears to be a consequence of pollencollection activity by bees. Therefore, it isinevitable for R. minima to produce high P/Oto compensate the pollen loss caused bypollen collectors and ensure the function ofits vector-dependent facultative xenogamousbreeding system.

TRAN & CAVANAGH (1984) reported thatin leguminosae, seeds of many taxa exhibit

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physical (exogenous) dormancy due to thepresence of a water impermeable seed coat.With this dormancy, they remain viable forlong period of time. ALI et al. (2012) reportedsuch physical dormancy in Rhynchosiacapitata due to which this species issuccessful as a weed. SHAUKAT & BURHAN(2000) described seed characteristics and thefactors regulating germination of r. minimain pakistan; it exhibits differential success indifferent habitats with different micro-climates. RANGASWAMY & NANDAKUMAR

(1985) reported that the seed coat ofRhynchosia minima is composed of threegradative barriers to water uptake a surfacedeposit of waxy material interfused with alipoidal substance, β-sitosterol; a subjacent 3-μm adcrustation of hemicellulose-cellulosecomplex; and a layer of palisade cells inwhich the secondary walls are impregnatedwith arabinan and the lumen contains tanninand phenolic compounds. The micropyleand hilum function as hygroscopic valveswhen seed coat breaks open. In this study, afew seedlings have been sighted and this isnot in tune with the abundant seedproduction through open-pollinations by r.minima; hence this species appears to havephysical dormancy as reported byRANGASWAMY & NANDAKUMAR (1985).Many seeds germinate in the vicinity of theparental plants in areas of water-saturatedsoils during rainy season but their growthsuppressed when long dry spells continuedduring this season. In areas of water stress, afew seeds germinated here and there butthey soon perished due to water stress as aconsequence of long dry spells. In bothwater-saturated and water stress habitats,the perennial root stock of this speciesseasonally resurrects and produces newgrowth during rainy season. The explosivepod dehiscence results in the settlement ofseeds mostly in the parental sites but rainwater may disperse them to new placesduring rainy season. Seed dormancy seemsto be regulating the proliferation of R.minima. It is successful in building uppopulations only in areas where soil is water

saturated and hence there it becomes asuccessful weed in farmlands but certainlynot in areas where soil is deficient inmoisture during rainy season. Therefore, R.minima is not a very widespread speciesbecause it is habitat-specific and requiressufficient moisture and nutrient content inthe soils to establish populations.Nevertheless, r. minima although notsuccessful in establishing populations inwater-stress soils is a hardy plant andtolerant of drought as stated by HARDING etal. (1989).

R. minima is widely used as a medicinalplant. It is used to cure eye conjunctivitisand inflammation (CHUTE & TIWARI, 2002),body care (MUSTAK et al., 2006), skinconditioning and boils (GUNDIDZA et al.,2009), haemorrhoids, heart, diarrhoea anddysentery (LOPEZ POVEDA, 2012). It is alsoused as animal forage (HASSELL, 1945;SHUKLA et al., 1970; GILLETT et al., 1971;BOYLAND, 1973; BEESTON, 1978; BOGDAN,1977). Further, LOPEZ POVEDA (2012) notedthat the seed of this species is used as food,especially in making sweets. In thisconnection, it is pertinent to mention thereport of HARDING et al. (1989) that thisspecies is likely a potential grain cropbecause it is a large seed producer. Sincesignificant variations exist in agronomicattributes such as days to flowering, podindehiscence and seed size of R. minimagrowing in different habitats, there is a hugepotential to identify and select desirablegenotypes to improve grain production inthis species. Therefore, further studies aresuggested to exploit the varieties or ecotypesof R. minima for medicine, animal forage andhuman food.

REMANANDAN (1981) stated thatRhynchosia, being generically related to thegenus cajanus, some of its species can beused to provide substantial contributionstowards crop improvement in pigeon pea.Furthermore, some species of Rhynchosiahave been experimented in India to providephysiological resistance against insect pestssuch as pod-borer and pod-fly in pigeon pea.

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In this study, the seeds of R. minima have notbeen infested by any pod-borer or pod-flyboth in water-saturated and water-stresshabitats suggesting that it has physiologicalresistance against insect pests. Therefore,intensive and extensive research is suggestedto identify and select desirable genotypes ofR. minima that give physiological resistanceagainst pod or seed pests in order to usethem for crop improvement in pigeon pea.

ConclusionRhynchosia minima is a winter blooming

prostrate climbing herb in India. It ishermaphroditic, self-compatible andequipped with explosive pollinationmechanism adapted for melittophily. It isessentially vector-dependent for both self-and cross-pollination. Mature pods dehisceexplosively to disperse seeds whichgerminate during wet season. The seedlingsgrow successfully only in soils withsufficient moisture or else they subsequentlyperish. Therefore, this plant grows as asuccessful weed in farm lands only wheresoil is wet and nutrient-rich. Previousreports indicate that it has medicinal, animalforage and human food values and hencethere is a potential for its exploitationcommercially.

AcknowledgementsWe thank the Andhra University,

Visakhapatnam, India, for providingphysical facilities to carry out this researchwork. We thank Dr. Ch. Prasada Rao,Department of Botany, Andhra University,for providing field assistance.

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