Pollination ecology of Solanum sysimbrifolium Lamk.
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1 Proc. lndian Acad. Sci. (Plant Sci.), Vol. 97, No. 4, August 1987, pp ,~~ Printed in India. Pollination ecology of Solanum sysimbrifolium Lamk. G V SARAT BABU*, S C BHATT and S C PANDEYA Department of Bioscience, Saurashtra University, Rajkot , India *Land Resources Division, Remote Sensing Atea, Space Application Centre (ISROI, Ahmedabad , India MS received 24 February 1986; revised 17 June 1987 Abstraer. Pollination ecology of Solanum sysimbrifolium was studied. Two species of Xylocopa and one species of Anthophora ate the active pollinators. AII the visitors are diurnal and only larger bees ate the effective pollinators. It can be concluded that male flowers are advantageous to Solanum and have developed from the close insect-plant dependence. Keywords. Solanum sysimbrifolium; X ylocopa fenestrata;, X ylocopa pubescence; Anthophora confusa; pollination ecology. I. Introduction Anthecology or pollination ecology is an environmental and evolutionary discipline concerned with the dynamics of pouination mechanism. Flower insect co-adaptation is considered a continuing process in which changing inter-relationships establish and remove reproductive barriers in the breeding systems at the vital link of pollen transfer (Macior 1971). The mechanism by which the stigma recognizes and accepts or rejects the pollen is yet incompletely understood for major plant species. The nature of the pouinators and their behavioural patterns, flowering time, nectar production, anthecological strategies and co-adaptations of plants and pouen vectors have received considerable interest from several workers. In studies of ecological behaviour of plant species, it is essential to observe the mechanism of reproduction and the possible role of insect vectors in pollination. The present study is an attempt to record with precision the operaticn of pollination mechanism of Solanum sysimbrifolium at Rajkot. The evidence that many species of bees and syrphids can manipulate the poricidal anthers of Solanum flowers is now extensive, although close species dependence is less frequently documented (Linsley 1962; Linsley and Cazier 1963, 1972; Macior 1964; Michener 1962; Bowers 1975; Symon 1979). The present study was undertaken to determine the vectors of pollen transfer, the mechanism of pollination and the role of male flowers in reproductive biology of this species. 2. Material and methods During the summers of 1980 and 1981, casual observations were made on a naturally growing population of S. sysimbrifolium in the Saurashtra University campus. Similar observations were also made in the precinct of the Rajkot airport 5 km away from the University campus. Floral phenology and morphology were observed, information obtained included 295
2 296 G V Sarat Babu, S C Bhatt and S C Pandeya the time of flower opening and closing, time of anthesis and the size and position of stamens. In order to understand the necessity of insects in pollination, the flowers were enclosed in polyethylene bags and fruit set was checked. Pollen grains were stained with lactophenol aniline and examined for fertility. More than 60 h were spent in making detailed observations and noting down the frequency, periodicity and behaviour of insect visitation. Insects were collected, identified and the position, composition and quantity of pollen loads carried by them were examined. 3. Results 3.1 Phenology and.floral morphology At Rajkot, S. sysimbrifi~lium grows naturally along road sides and waste places and it flowers throughout the year. The flowers ate borne on simple bractless cymes with a few to 13 flowers in one inflorescence. The portion of the cyme distal from the open flower is strongly decurved so that each open flower appears superficially terminal. Generally, the flowers are hermaphrodite (figure 1), but in some instances the distal flowers were found to be female sterile (figure 2). There are no clear differences in sepals, petals and stamens and in pollen grains between the hermaphrodite flowers and female sterile flowers. But the ovaries of female sterile flowers are abortive and the styles are greatly reduced. In some cases even the first borne flowers of the inflorescence were female sterile and in others, complete male inflorescences were observed (figure 3). The bright liliac corolla is regular and the 5 united petals forma bowl type of blossom (18 mm in diam) (Faegri and van der Pijl 1971). AII stamens in both hermaphrodite and male flowers are equal in size averaging 7 to 8 mm in length and 1"5 mm in diameter at the widest point near the base. The stamens ate yellow and perpendicular to the corolla. The filaments of the stamens are 1 mm or less in length. Dehiscence occurs with the initial opening of flower and the pollen is available through two apical pores. Flower opening occurs immediately after dawn and the flowers usually remain open upto 18 h. On hot days (temperature 30~ and above) blossoms may close before noon. Individual flowers remain open for 2-3 days. The flowers have no nectar but the stamens emita distinct fragrance which disappears within 3-4 h of floral opening. The slender green style in hermaphrodite flowers averages 15 mm in length. Few flowers are enantiostylous (the style is projected from the side of the anther cone) but in the majority of flowers, the style is projected from the centre of the anther cone. The smallest plants may have 5-10 open flowers in a day but in big plants the number of open flowers in a day varied from lnsect visitation and behaviour Records of insect visits to S. sysimbrifotium included carpenter and mining bees. Two genera and three species of bees were observed collecting pouen from the plants. AII visitors were diurnal. The most abundant, earliest, frequent and regular visitors to the flowers were members of Xylocopa. There were two species of Xylocopa,
3 Pollination ecology of S. sysimhr!]blium 297 Figures 1-3. I. Hermaphroditc flowers of S..sysiml~rili;lium with incurved green style. 2. Female sterile flowers devoid of long slender grecn style. 3. A c~~mpletc male inflorescence.
4 298 G V Sarat Babu, S C Bhatt and S C Pandeya X. fenestrata and X. pubescence. The mining bees included Anthophora confusa. The peak visitation time for all the bees was 0630 to 0930 h. The earliest collection during entire study period was on 8 April 1981 at 0545 h. Occasionally Xylocopa could be found on the blossoms even in the noon and in the early hours of evenings, provided there was no gale and temperature did not exceed 30~ When foraging on pollen from the flowers of S. sysimbrifoliurn the bigger insects landed and curled their body over the tips of the anthers. The bee grasped the base of each anther with its mandibles and in a series of short strokes directed towards the apex and milked the anther. This was aceomplished with a high pitehed humm clearly audible at a distance of 1"5 m which was quite different from the normal flight sound. The introrse anthers begin dehiscence at their tips and the probing by insects release pollen through apical pores at the apex. Abundant hairs on the ventral surface and on the legs of the bees facilitated storage of collected pollen. While the bee collected the pollen in this manner the incurved style comes in contact with either abdominal portion of lateral surface of its body and pollen transfer takes place. Early morning visits lasted for more than s per flower but the subsequent visits were much shorter. On April 8, 1981 one individual of X.fenestrata arrived at 0620 h with empty corbiculae and collected pollen continuously for 10ruin visiting 68 flowers on 4 plants. Each flower visit lasted for not more than 15 s. The pollen collection by bee was interrupted only by a short flight from flower to flower. Captured while still collecting pollen, this insect revealed heavy homogeneous corbicular loads of pollen of S. sysimbrifolium. Hairs on the ventral side of the thorax and on abdomen also held pollen of S. sysimbrifolium, exclusively. A second Xylocopa visited 25 flowers on 3 plants in 2 ruin and 20 s. In contrast to larger bees, smaller ones (Anthophora confusa) did not have any contact with the stigma. Tbey curled their bodies over each of the stamens and vibrated them one at a time allowing pollen to be deposited on the ventral portion of the bee. The declined position of the style virtually ruled out the possibility of pollination by these smaller pollen collectors. However, accidentally sometimes these insects touch the surface of the stigma and may help in pouination. 4. Diseussion The anthers of many species of Solanum are poricidal, i.e. the pollen is shed through small pores at the apex of the anther. They ate either loosely or firmly erect forming a cone above the style. Very little pollen is ever displayed at orifice and some manipulation of the anther by vibration or 'milking' is necessary to release pollen. Michener (1962) has described in detail about the ability of bees to buzz or vibrate t, he anthers to release pollen. His observations were also supported by those of Linsley (I 962) and Linsley and Cazier (1963, 1972) and also the present investigation. The lack of berry production in the bagged flowers and abundant berry development in the open flowers suggest the necessity of the insects in the pollination of S. sysijnbr(]bliun~. Although the probability for autogamy exists, it rarely occurs because of the morphology of the fiowers. Due to large number of open flowers on a plant, the possibilities of Xenogamy and Geitonogamy ate equal, depending upon the flight pattern of the insects.
5 Pollination ecology of S. sysimbrifolium 299 In the early summers the regular visitors were the two species of Xylocopa. The large foraging bees alight on the central stamens and milk pollen on to their venter. This pollen is transferred to the scopae and is later utilised by the bees as brood food. Due to vibration of thorax, some pollen grains fall down on the hairy abdomen which touches the surface of the stigma and pollination takes place. This normal manner of pollination appears to be a behavioural pattern of the bee closely related to the form, function and orientation of flowers (Macior 1964). During pollen collection Xylocopa vibrates its thorax presumably with the indirect flight muscles (Heinrich 1972; Simpson 1964) causing no observable wing motion. The mechanism is very similar to that described for Xylocopa in Melastoma malabathricum (Percival 1965) and that of honey bee queen piping (Simpson 1964) and for Bombus on Solanum rostratum (Bowers 1975). Linsley and Cazier (1963) reported almost a comparable behaviour of bees on S. elaeagnifolium and S. rostratum in Arizona. The examination of pollen loads of all the 3 bees revealed that mining bees (A. confusa) were carrying pure S. sysimbrifolium pollen, whereas, carpenter bees had some foreign pollen other than that of S. sysimbrifolium. Consistency in the collection of pollen is characteristic of bees in genera/(linsley 1958). The term oligolecty is used for those bees which collect pollen from a few species and this is reflected in physiological and morphological adaptations which sharply limit the number of kinds of pollen sources normally utilized by bees with this inherited character (Faegri and van der Pijl 1971). Malyshev (cf. Linsley 1958) considered that majority of solitary bees are oligolectic. There ate fewer oligolectics in the tropics and more in arid arcas where competition for pollen is more intense. The present study lends further support to Malyshev's observations that Rajkot is an arid to semi-arid region and the preponderance of these bees is a striking feature. Two types of ftowers (hermaphrodite and male flowers) were observed in the present study. Symon (1979) reported 3 different types of inflorescences (hermaphrodite, andromonoecious and androdioecious) in the genus Solanum. In S. sysimbrifolium both hermaphrodite and andromonoecious types occurred. Though, pure male inflorescences were observed (figure 3), exclusively male plants were not recorded in S. sysimbrifolium. Thus, by producing male inflorescence, S. sysimbrifolium may be in the way of achieving androdioecious nature. Self-ste alleles are wide spread in the genus Solanum and D'Arcy (1972) has reported self incompatibility in S. sysimbrifolium. Symon (1979) further reported that true dioecism ensures outcrossing and the maintenance of considerable heterozygosity in the population was ah evolutionary advantage in the genus Solanum. For pollination, the flowers obviously depend upon the insects. Now the question is what is the advantage of the production of male flowers? Some advantages may accrue by producing extra pollen. The male flowers set no seed and do not contribute directly to the seed supply. The flowers have no nectar and the only attraction they have for insects is the pollen they produce. Even if the incompatibility is not present, the presence of pure male inflorescence at least ensures a proportion of outcrossing while still retaining the possibility of selfing. If the flowers were female only, they could not have attracted the insects. It can be concluded that male flowers are advantageous to the genus Solanum and have developed from the close insect-plant dependence.
6 300 G V Sarat Babu, S C Bhatt and S C Pandeya References Bowers K A W 1975 The pollination ecology of Solanum rostratum (Solanaceae); Aro. J. Bot D'Arcy W G 1972 Solanaceae studies. II. Typification of subdivisions of Solanum; Arre. M. Bot. Gard Faegri K and van der Pijl L 1971 The principles vfpollination ecology 2nd edition; (New York: Pergamon Press) Heinrich B 1972 Temperature regulation in the bumble bee Bombus va~trans: a field study; Science Linsley E G 1958 The ecology of solitary bees; Hil~lardia Linsley E G 1962 The colletid Ptiloglossa arizonensis (timberlake) a matinal pollinator of Solanum; Pan- Par. Emomol Linsley E G and Cazier M A 1963 Further observations on bees which take pollen from plants of the genus Solanum; Pan-Pac. Entomol Linsley E G and Cazier M A 1972 Diurnal and seasonal behaviour patterns among adults of Protoxaea.qloriosa (Hymenoptera, Oxacidae); Aro. Mus. Novit I Macior L M 1964 Ah experimental study of the floral ecology of Dodecatheon meadia;, Aro. J. Bot Macior L M 1971 Co-evolution of plants and animals; systematic insights from plant-insect interactions; Ta.xon Michener C D 1962 Ah interesting method of pouen collection by bees from flowers with tubular anthers; Rey. Bi,l. Trop Percival M S 1965 Floral biology (Oxford, New York: Pergamon Press) Simpson J 1964 The mechanism of honey-bee queen piping; Z. Vgl. Physiol Symon D E 1979 Sex forms in Solanum and the role of pollen coll~ting insects; in The Biology and Taxonomy of Solanaceae (eds) J G Hawkes, R N Lester and A D Skelding (London: Academic Press lnc. Ltd.) pp
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