Table Of Content

POLLINATION ECOLOGY OF CASSIA ALATA (CAESALPINIACEAE) L. 1 C. Bhaskara Rao, C. Subba Reddi, Raju J.S. Aluri2 J.B. Atluri3 , (With one text-figure ) Key words: Cassia alata, heteranthery, enantiostyly, carpenter bees, pollination. Cassia alata blooms annually during October-February. The flowers are borne on typical racemes, and are yellow and devoid ofnectar. They exhibit enantiostyly and heteranthery with feeding as well as pollinating anthers. In the biotope ofthe study area, the carpenter bees consisting ofXylocopa latipes andX. pubescens are the exclusive visitors to C. alata. They collect pollen by buzzing. During the vibratile movement ofthe visitor’s body, the pollen grains are discharged from pollinating anthers on to the sides ofthe insect visitor’s thorax and abdomen. Simultaneously, the pollen grains are also transferred to the stigmas oriented to the right or to the left. Heteranthery and enantiostyly, complemented by the buzzing behaviour of the pollinating carpenter bees, promote geitonogamy as well as xenogamy in C. alata. , I•' Introduction styled and left-styled flowers on the same inflorescence. This floral dimorphism has been Buchmann (1983) gave a complete list of treated as a device for enhancing outbreeding anthecological work on Cassia species which (Bahadur et al. 1990). However, Dulberger include C. fasciculata, C. fistula, C. glauca, C. (1981) cautions that itneed notbe connected with bacillaris, C. multijuga, C. didymobotrya, C. outcrossing. auriculata, and C. alata. Those works not Carpenter bees are the only insects mentioned by Buchmann (1983) have been pollinating Cassia sp. so far studied. The bees touched upon by Gottsberger and Gottsberger collect pollen from feeding anthers by rapidly (1988). These studies show thatpollen discharge contracting the indirect flight muscles, thus by releaselbfa small cloud ofpollen occurs from producing strong vibrations that are trans- apical pores ofthe anthers by vibratile behaviour mitted directly to the anthers and indicated by of the bees collecting pollen. The genus Cassia audible buzzing of the bees. This vibration is known to exhibit heteranthery and rapidlyproduces a directed streamorpollencloud enantiostyly. Heteranthery means that the from the anther pores that primarily strikes the androecium of the same flower is functionally venter ofthe bee, and sometimes the pleural and differentiated into short stamens with feeding dorsal areas also. During this act, the pollen from anthers, which provide food for the pollinator, pollinating anthers situated over the dorsal side and longer stamens with pollinating anthers or lateral sides of the bee is discharged and which provide pollen for pollinating the stigma. deposited on the head-thorax region of the Enantiostyly refers to the occurrence of right- foragingbee, resulting innototriby orpleurotriby. The stigma ofthe flower simultaneously strikes the pollen-laden head-thorax region ofthe bee. 1AcceptedMay, 1997 departmentofEnvironmental Sciences,AndhraUniversity, Fiji (1954) has provided fragmentary Visakhapatnam 530003. information on the floral biology of C. alata in departmentofBotany,Andhra University, Java. He suggests that C. alata has a similar Visakhapatnam530 003 454 JOURNAL BOMBAYNATURALHISTORYSOCIETY, 95(3) DEC 1998 POLLINATION ECOLOGY OF CASSIA ALATA L. floral mechanism and is pollinated by carpenter Breeding behaviour was studied through bees. The available information on this medici- controlled pollination. Fruit set, seed set and nally valuable plant is highly inadequate to fecundity rates in controlled pollination were understand its unique form of pollination, and measured following the procedure described by the information is from Java, where meteo- Aluri and Subba Reddi (1994). The flower and rological conditions may differ from those of fruit abortions were expressed in percentages. India. Complete details of the floral ecology of Flower visitors were carpenter bees oftwo C. alata are necessary for its commercial species of Xylocopa only. Foraging activity of cultivation. these bees, their foraging behaviour, forage resource sought, pollination potential, etc. was Material and methods investigated in detail. The pollen carrying capacity of the bees was also determined by Cassia alata L. is abundant in counting the pollen grains obtained from body N Visakhapatnam (17° 42' and 82° 18' E). The washings in aniline-blue. The duration offlower studies were carried out in 1989 and 1990. To visit and flowers foraged in a unit time by the determine flowering phenology, ten flower-visitors were noted to assess the foraging inflorescences selected at random were tagged speed. before the initiation of blooming and observed for the daily opening of flowers. The Results inflorescences were then removed to avoid recounting the next day. Tagged inflorescences Flowering phenology: The plants of C. were observed until they ceased flowering to alata grow from new seeds every year following obtain data on the duration offlower production the first rains of the monsoon and continue to and also the daily rate of flowering. Flower grow until late September. Then they start morphometries were observed in detail. Daily producing inflorescence stalks and flower buds. anthesis rate was noted from ten randomly The mature flower buds begin to open from A selected inflorescences marked before anthesis. October through February. plant flowers for Time of anther dehiscence was recorded by an average period of 88 days (range 61-106). observing the anthers with a 1Ox hand lens before Inflorescence phenology: The inflores- and after the flowers opened. Undehiscedmature cence is a typical terminal raceme. An anthers, immersed separately in a drop of inflorescence produces a mean number of 88 lactophenol aniline-blue were observedunderthe flowers (range 40-1 17) anthesing overan average microscope, and the number ofpollen grains per period of 24 days (range 16-29). Each day the anther was counted to determine pollen output. number of newly opened flowers of an Pollenproduction per anther was then multiplied inflorescence varies from 2-5. Flowerproduction by the number ofanthers to estimate total pollen ceases in February, then the plants start to dry grains per flower. Structural characters ofpollen up and wither. grains were observed and their size wasmeasured Flower morphology: The flowers are with a calibrated ocularmicrometer. Pollen-ovule bisexual, showy but lack fragrance. The calyx ratio was determined by dividing the number of consists of5 sepals, each 1.5 cmlong. The yellow pollen grains per flower by the number ofovules corolla is ovate and divided into 5 petals. The per flower. Pollen viability was tested by hand- clawed and imbricated petals are first involute pollination experiments using relatively fresh and later become spread. Stamens are 10. The stigmas, and stigma receptivity by hand- uppermost (adaxial) three stamens have sterile pollination using relatively fresh pollen. anthers. The remainder possess fertile anthers JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 95(3), DEC. 1998 455 POLLINATION ECOLOGY OF CASSIA ALATA L. Fig. 1 Enantiostyly in Cassia alata L. a. Left-styled flower; b. Right-styled flower : which can be grouped into three categories. The production per anther in the three categories of top central group of4 stamens have filaments 3 fertile stamens is different. It averages 32,600 mm mm long and anthers 4 long. The second (range 29,000-37,000) in the top central group group composed of2 large lateral stamens having of stamens. The corresponding figures for the mm mm filaments 4 long and anthers 10 long, second andthe third group ofstamens is 2,47,000 are situated below the top central group. The (range 2,10,640-2,86,000) and 22,410 (range A anthers of this group are thick, hard, curved, 18,550-25,460) respectively. few grains are tapering and slightly twisted. The third group sterile in all the three groups ofstamens (3-5%). represents one lower-most (abaxial) median The pollen-ovule ratio is 9,880:1. mm mm stamen with a 7 long filament and a 5 Pollen viability and stigma receptivity: long anther. The ovary has 60 ovules (range 50- C. alata pollen germinated well in 50% sugar 63) arranged in a linear fashion. The upwardly concentration. The germination percentage bending sickle-shapedpistil emerges between the obtained for fresh pollen is 90%, 24 h old pollen bases ofthe second group ofstamens and above 68% and for 100 h old pollen 6%. The pollen the median stamen ofthe third group. The pistil viability tested through fruiting ability showed projects to the right or to the left in the flowers that the stigma pollinated with fresh pollen of the same inflorescence (Fig. 1), but without produced 84% and those with 96 h old pollen any regular pattern. The ratio ofright-styled and gave 20% fruiting. left-styled flowers in an inflorescence is nearly The tests conducted for fruiting ability of 1:1. The style is terminated with a simple stigma the stigmas of different maturing periods from having a cavity-like opening. anthesis to the flower life up to 36 h showed that Anthesis and anther dehiscence: The the stigma favours pollen germination and later flowers open daily during 0300-0400 h. Anthers gives fruit for 30 h. This condition ofthe stigma dehisce by pores; a pore is formed at the apical is takenas stigmareceptivityperiod. The fruiting appendage ofeach anther lobe. Dehiscence takes ability ofthe stigma, however, was not the same place about3 hafteranthesis. The corolla, together throughoutthe receptivityperiod. Thepercentage with stamens, falls offin 36-48 h after anthesis. offruiting obtained with fresh stigmas was 84%. Pollen characters: Pollen grains are With advancement in the age ofthe stigma, there triangular, tricolporate, with a smooth exine. The was reduction in fruiting, it being 12% with pm grains are 43-51 in diameter. Pollen 30 h old stigmas. 456 JOURNAL, BOMBAYNATURALHISTORYSOCIETY, 95(3)DEC 1998 POLLINATION ECOLOGY OF CASSIA ALATA L. Breeding behaviour: The results of vibrates its body and collects pollen from the top breeding tests show that the plant is not central and third group of anthers. A buzzing apomictic, but reproduces through xenogamy and sound is heard and the pollen is deposited all geitonogamy. The xenogamic fruiting, seeding over the ventral side ofthe bee, where it is greatly and fecundity values obtained were 84,100 and accessible for grooming and for subsequent 84%, respectively. The agreeing values for ingestion. Added to this, the stigma does not geitonogamy were 68,100 and 68%. make contact with the ventral side of the bee. Natural flower and fruit abortions: The The four stamens of the top central group and recorded natural flower and fruiting pattern show the single stamen of the third group constitute that about halfofthe flowers fall offwithout any the feeding anthers. The second group, with signs of fruit development, in the remainder, larger stamens orientedlaterally, discharge pollen about 25% initiate fruit development and then onto the sides ofthe thorax and abdomen ofthe abort. The remaining flowers ranging from 19- bee. Washings ofthe thorax revealed 180 to 325 25% develop mature fruit. The mature fruits are pollen grains, while those of the abdomen area largely produced at the basal part of the showed 180-260 grains. The pollen deposited in inflorescence. this area may be totally inaccessible for grooming Flower visitors: The flowers of C. alata or for ingestion. The stigma of the right- and are foraged exclusively by Xylocopa pubescens left-styled flowers touches the dorsal side ofthe and X. latipes. The foraging visits of these bees thorax and the abdomen, where pollen from are, however, significantly disproportionate. X. lateral anthers is deposited. The second category latipes made 64-70% of foraging visits while X. of stamens, the lateral ones, thus constitute the pubescens only 30-36%. Butthe two species were pollinating anthers. equally mobile. Both foraged 13 flowers (range 7-20) in one minute and spent 2-4 seconds at a Discussion flower. The bees usually foraged on fresh flowers and occasionally on day-old flowers. The As early as 1909, Burkill considered foraging speed ofthe two species was greater on Xylocopa sp. to be the most important flower- sunny days compared to cloudy days. On sunny visiting insects in the plains of tropical India, days, the bees started foraging at 0800 h and and largely responsible for the pollination of stopped at 1600 h. The activity was more brisk sunhemp, Indian pulses and Cassias. From other around noon. The foraging schedule of the bees tropical regionsXylocopa sp. have been reported was delayed by two hours and stopped early by as pollinators of several Cassia species. Knuth an hour on cloudy days. (1906) reported that in South Asia, the main Foraging behaviour: The yellow corolla pollinators ofCassia spp. with large and medium appears to attract and direct carpenter bees to sized flowers are X. latipes and X. aestuans. the pollen source in the flower. On approaching Fiji 1954) describes three large-flowered tropical ( the flower, the bee lands on the top central and species ofCassia with typicalXylocopa flowers; We the third group ofstamens situated in the middle one ofthese species is Cassia alata. observed of the flower. While landing, it curls its body that the flowers of C. alata in Visakhapatnam over the anthers and produces a high-pitched are visited and pollinated exclusively by X. buzzing sound which is quite different from the latipes and X. pubescens. flight sound. The head and thorax ofthe buzzing C. alata flowers are nectarless, and the bee are now covered over by the upper involute floral reward is only pollen. The male carpenter petals, while the lower petals are pressed bees do not forage forpollen (Buchmann, 1983). downward by the weight of the bee. The bee Then successful pollination in C. alata should JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 95(3), DEC. 1998 457 POLLINATION ECOLOGY OF CASSIA ALATA L. result from the activity offemale carpenter bees. be having different races in different The captured pollinators in the present study geographical regions, with differing breeding were female. systems. On the basis ofP/O ratio (9880: 1), C. alata Heteranthery and enantiostyly in Cassia may be treated as highly xenogamous (Cruden, species mightbe taken as a device forpromoting 1977). However, breeding experiments revealed outcrossing (Bahadur et al. 1990). Efficacy of that both xenogamy and geitonogamy operate this strategy in promoting outcrossing in C. alata with equal success in seed formation. Cruden and is poor. The flowers have their pollinating Jensen (1979) suggest that P/O ratios may reflect anthers oriented on both sides ofthe flower and pollination efficiency, and the lower P/O ratio the stigma, whether in R and L flowers, can makes more efficient delivery of pollen. Thus, invariably receive pollen of the two pollinating in C. alata the high P/O ratio may indicate anthers. Since the flowers are compatible to both inefficient delivery ofpollen. geitonogamous and xenogamous pollen, and the However, the 100% seed set and the pollinator visits all the 2-5 flowers that open in nototribic and/or pleurotribic transfer of pollen a day, the situation may enhance geitonogamous suggest that the pollination mechanism in C. pollination, irrespective of the presence of alata is efficient. The high pollen production enantiostyly. However, considering the flight which resulted in the high P/O ratio compensates pattern ofcarpenterbees which involve interplant the pollen wastage/loss from pollinator feeding. and interpopulation flights, it is likely that Further, the small size of the stigma, compared xenogamous pollination is also promoted, though to the area of pollen spread on the body of the the incidence of such pollination relative to bee, may also necessitate the production oflarge geitonogamy can onlybe assessedthroughpollen amounts of pollen. These interpretations agree tagging tests. Dulberger (1981), while with those of Dulberger (1981) who also found interpreting the functions of various unusually high P/O in C. didymobotrya and C. morphological characters of C. auriculata and auriculata. C. didymobotrya, concluded that the main Flower function andbee behaviour suggest function of enantiostyly need not be connected that geitonogamy cannot be eliminated. When with outcrossing. He says that its primary role the bee lands on an inflorescence, it visits all the may be that ofclearing access ofthe insect to the fresh flowers that range from 2-5. In every visit feeding anthers, at the same time protecting the of the bee, its dorsal thorax or abdomen, female parts from injury by insect vibrations. powdered with pollen grains makes contact with Possible injury may be prevented by the the stigma. Then, the pollen grains are trans- presentation ofstigma and style from the median ferred to the stigma. The pollen thus transferred plane ofsymmetry, so that it comes into contact may be geitonogamous or xenogamous. with the back or side ofthe insect rather than its Contrary to the present observations, Pijl ventral part. As revealed by the extensive studies (1954) observed in Java that isolated plants of of vibratile pollination (Buchmann, 1983), the C. alata are sterile. He writes that the flowers of intensity of buzzing increases with the size of an old specimen of C. alata have been setting the insect. Carpenter bees are the giants of the fruit to almost 100%. After clearing the bee world (Meeuse 1961) and are to be treated surrounding vegetation in the whole field no as powerful buzzers (Roubik, 1989). Therefore, fruit was formed. As soon as the neighbour- it is reasonable to assume that in flowers ing young plant, which had also been spared, exhibiting the buzz-pollination syndrome started flowering, the inflorescence of the first discussed at length by Buchmann (1983), the one produced fruits again. Perhaps, C. alata may style deflections may have evolvedtogether with 458 JOURNAL BOMBAYNATURAL HISTORYSOCIETY, 95(3) DEC 1998 , POLLINATION ECOLOGY OF CASSIA ALATA L. changes in stamen orientation and a division of Even if there is direct contact, as seen in the androecium into upper and lower anthers. It may present study ofC. alata, electrostatic forces are be noted that the female part deflected away from necessary to push or pull pollen into the hollow the flowercentre is the whole carpel. Enantiostyly style tip wherein the stigmatic surface is located. might be a safeguarding device from the damage As stated by Buchmann (1983) and Gottsberger that may result from the weight ofthe pollinator and Gottsberger (1988), there would be a lot of and intensity of its vibrations. pollen dispersal and loss into the air but for the Gottsberger and Gottsberger (1988) state electrostatic field around a visiting bee. In the that in their study on the flower adaptation and absence of electrostatic field around the evolution of the Cassinae in relation to pollination vector, the cloud of pollen released pollination events, there was often no real contact during vibration should become airborne and of the bee body with the stigma and/or anther pollen trapping in the atmosphere should reveal openings, but that there occurred close high concentrations. However, pollen trapping approximation. Then, to explain the deposition in the ambient air has revealed low ofpollen on the stigma, they relied on the concept concentrations of Cassia pollen. The probable of Corbet et al. (1982) that electrostatic forces importance of electrostatic forces in buzz- play an important role in pollen transfer via pollination has also been recognised by insects. Electrostatic potentials enable pollen to Buchmann (1978) and Buchmann and Hurley jump from anther to bee and from bee to stigma. (1978). References & Aluri,J.S.R. C. Subba Reddi (1994): Pollination ecology CellEnviron. 5: 125-129. and mating system of the weedy mint Leonotis Cruden, R.W. (1977): Pollen-ovule ratio: A Conservative nepetaefolia R.Br. in India. Proc. Indian natn. Sci. indicator ofbreeding systems in flowering plants. Acad. B60 255-268. Evolution 31: 32-46. : Bahadur, B., A. Chaturvedi & N. Ramaswamy (1990): Cruden, R.W. & K.G. Jensen (1979): Viscin threads, SEMstudiesonpollen in relation toenantiostyly and pollinationefficiencyandlowpollen-ovuleratios.Am. heteranthery in Cassia (Caesalpiniaeeae). hr. Current J. Bot. 66: 875-879. Perspectives in Palynological Research, pp. 7-22. Dulberger, R. (1981): The floral biology of Cassia C SilverJubilee Commemoration Volume,J. Palynol. didymobotrya and auriculata (Caesalpiniaeeae). (India). Am. J. Bot. 68: 1350-1360. & Buchmann, S.L. (1978): Vibratile “buzz” pollination in Gottsberger, G. S.I. Gottsberger(1988): Evolution of angiospermswithporicidallydehiscentanthers. Ph.D. flower structures and pollination in neotropical Dissertation, Entomology, University ofCalifornia, Cassinae(Caesalpiniaeeae)species. Phyton (Austria) Davis. 28: 293-320. Buchmann, S.L. (1983): Buzz-pollination in angiosperms. Knuth, P. (1906): Handbook of Flower Pollination. In: HandbookofExperimental Pollination Biology. Transl. Ainsworth Davis, J.R. Clarendon Press. r C.E.JonesandR.J. Littleeds. Scientific and Academic (Oxford). Editions (New York), pp. 72-1 13. Meeuse, B.J.D. (1961): The Story ofPollination, Ronald Buchmann, S.L. & P.V. Hurley (1978): A biophysical Press (New York). model forbuzz-pollination in angiosperms.J. Theor. Pul, L. Van Der (1954): Xylocopa and flowers in the Biol. 72: 639-657. tropics I-III. Proc. Kon. Ned. Ak. Wet. Ser. C. 57: 413- Burkill, I.H. (1909): Insects and flowers in India. In: 423,514-562. Maxwell-Lefroy, Indian Insect Life, pp. 222-223. Roubik, D.W. (1989): Ecology and natural history of Corbet, S.A., J. Beament & D. Eisikowitch (1982): Are tropical bees. Cambridge University Press, electrostatic forces involved in pollen transfer?Plant Cambridge,New York. ill JOURNAL, BOMBAYNATURAL HISTORYSOCIETY, 95(3), DEC. 1998 459