biotropia book final.indd 129 POLLINATION EFFECTIVENESS OF APIS CERANA FABRICUS AND APIS MELLIFERA LINNAEUS (HYMENOPTERA: APIDAE) IN JATROPHA CURCAS L. (EUPHORBIACEAE) TRI ATMOWIDI*, PUJI RIYANTI, ANDENG SUTRISNA Department of Biology, Faculty of Mathematics and Natural Sciences, Bogor Agricultural University, Darmaga Campus, Bogor 16680, Indonesia ABSTRACT Pollinators are well known to provide key ecosystem. Animal pollinators are thought to contribute between 15 and 30% of global food production and bees are recognized to be the most important taxon. Th e pollination eff ectiveness of two species of bees, Apis cerana and A. mellifera (Hymenoptera: Apidae) in Jatropha curcas (Euphorbiaceae) was studied. Th ree cages, made of insect screen were set up. Each cage contains three individual plants. One colony of A. mellifera and A. cerana were placed in the fi rst and second cage, while the third cage was used for control plants. Bee colonies were placed during one month in the fi rst and second cages. Fruit set of plants pollinated by A. mellifera, A. cerana, control plants, and open plants were counted and compared. Pollination by honeybees increased the number of fruits per plant and fruits per raceme of J. curcas. Based on measuring of fruit produced by plants, pollination eff ectiveness of A. mellifera was higher than A. carana. Key words: Pollination, eff ectiveness, Apis cerana, A. mellifera, seed set, Jatropha curcas. INTRODUCTION Th e honeybees are the principal species used for crop pollination worldwide (Free 1993). Th e true honeybees (Tribe Apini, genus Apis) consist of nine species i.e. A. mellifera Linnaeus, A. cerana Fabricus, A. dorsata Fabricus, A. laboriosa Smith, A. fl orea Fabricus, A. andreniformis Smith, A. koschevnikovi Buttel-Reepen, A. nigrocincta, dan A. nuluensis. Genus Apis primarily tropical was restricted to the Old World until A. mellifera was introduced worldwide. Both species, A. cerana and A. mellifera consist of medium -sized (10-11 mm) species with multiple combs in cavities, dances on vertical surfaces of combs in the dark (Michener 2000). Th e combs are built under the ceiling of the cavity and attached to the cavity’s walls. Th e arrangement and distribution on the combs are similar in all races of each species (Koeniger 1995). Colonies of A. cerana are relatively small (6000-7000 workers), but A. mellifera colonies consist of 100, 000 or more individuals (Winston 1987). * Corresponding author: atmowidi@ipb.ac.id BIOTROPIA VOL. 15 NO. 2, 2008 : 129 - 134 130 Comparative foraging behaviour of A. cerana and A. mellifera on apple orchard had been reported by Verma (1995). Worker bees of A. cerana started their foraging activity signifi cantly earlier in the morning (06.03 h) than A. mellifera (06.27 h), but duration of foraging trip of A. mellifera (17.92 minutes) was signifi cantly longer than that of A. cerana (11.85 minutes). Th e peak of foraging activities of A. cerana was between 09.00 h and 13.00 h with a temperature range of 15.5-21oC, and that of A. mellifera was between 11.00 h-13.20 h with a temperature range from 21 to 25oC. Worker bees of A. mellifera carried signifi cantly heavier pollen loads than A. cerana throughout the day. A. cerana contacted the stigma on average 3.09 stigmas per visit and spent 5.90 seconds on each fl ower, whereas these values for A. mellifera were 3.33 stigmas per visit and 6.63 seconds on each fl ower, respectively (Verma 1995). Selection for eff ective pollen transfer and receipt has been considered to be the principal force in the evolution of the angiosperm fl ower. Most fl owers, however, allow access to a variety of visitors (Faegri & van der Pijl 1979). Diff erences among visitors in morphology, physiology, and foraging behavior may result in diff erences in their eff ectiveness as pollinators (Young 1988). Wallace et al. (2002) also reported that the natural pollinators were extremely effi cient in producing fertilization and fruit set of Jeff ersonian virgata. In male-sterile oilseed rape (Brassica napus), Steff an-Dewenter (2003) reported that insect pollination can positively aff ect several yield components. However, these eff ects are dependent on cultivar and growing conditions. Total yields are often not increased due to the considerable compensatory capacity of oilseed rape (Westcott & Nelson 2001). Jatropha curcas (Euphorbiaceae) is a perennial, deciduous shrub or treelet. Th e plant produces fl owers in racemose infl orescences, with dichasial cyme pattern. Th e fl owers are unisexual, and male and female fl owers are produced in the same infl orescence. Normally, the infl orescences produce a central female fl ower surrounded by a group of male fl owers. In some cases the female fl owers are substituted by male fl owers. Numerically, 1–5 female fl owers and 25–93 male fl owers are produced per infl orescence. Th e average male to female fl ower ratio is 29 : 1. Each infl orescence, once it begins fl owering, fl owers daily, and the fl owering lasts for 11 days. Th e fl owering pattern showed that the male fl owers are produced earlier (compared to the female fl owers) and will produce fl owers daily until the male buds are exhausted. Th e female fl owers bloom between the second and the sixth day. Th e fl oral base contains nectar in trace amount, which is 0.3 ml per fl ower. Th e fl owers open daily during 0530–0630 h. Th e unpollinated fl owers fall off on the fourth day, while the pollinated ones remain in place. Th e sepals and petals gradually enlarge and protect the growing fruit until the latter reaches its full size (Raju & Ezradanam 2002). Here, we studied the pollination eff ectiveness of two species of honeybees, Apis cerana and A. mellifera in J. curcas. Th e eff ectiveness of the pollinators was measured by the number of seeds set, and seeds weight. MATERIALS AND METHODS Study site Th e study was conducted in Jatropha plantation located at Indramayu district, West Java from May to September 2007. BIOTROPIA VOL. 15 NO. 2, 2008 131 Measuring of the pollination eff ectiveness of honeybees Th e plants selected for measuring pollination eff ectiveness were about three years old. We set up three cages made by of insect screen. Th e size of each cage was 9x3x2.5 m3 and each cage contains three plants of J.curcas. One colony of A. cerana and A. mellifera were placed in the fi rst and second cages for approximately 1 month (June 22 to July 25, 2007) to pollinate the fl owers. Th ird cage was used as a control (no bee application). At this time, bees were fed with honey that placed in a cup. Each infl orescence observed was tagged by color ribbon. After the end of the fruiting period, the number of fruits per plant, fruits per raceme, seeds per fruit, and seed weight were counted. Observation of fl ower visitors Species composition of fl oral visitors was observed visually at Jatropha plantation using scan sampling method (Martin & Bateson 1993) for a few days. After observation, insect visitors were caught by sweep netting for species identifi cation in the laboratory. Data analysis Fruits set of J. curcas pollinated by A. cerana and A. mellifera were compared with control plants and open plants (plants pollinated by natural pollinators). Diff erences in fruit numbers of J. curcas pollinated by bees, control plants, and open plants were analysed by analysis of variance (Anova) and Scheff e test at the 95% level by using Systat 10 for Windows. RESULTS AND DISCUSSION Pollination eff ectiveness of honeybees in J. curcas Pollination eff ectiveness of two species of honeybees in J. curcas varied. Pollination eff ectiveness was shown by the number of fruits produced by plants. Result showed that the mean number of fruits produced per plant as a result of pollination by A. cerana (17 fruits), A. mellifera (19 fruits), and open plants (16 fruits) were higher than that of control plants (5 fruits) (Table 1). Although, based on statistical tests, they were not signifi cantly diff erent. Table 1. Reproductive success of J. curcas pollinated by A. cerana, A. mellifera, open plants, and control plants Plant reproductive success Numbers (+st.dev) Control plants A. cerana A. mellifera Open plants Number of fruits per plant 17a (+7.94) 19a (+11.93) 16a (+12.15) 5a (+5.13) Number of fruits per raceme 2.04a(+1.65) 3.05a (+1.75) 2.45a (+1.47) 2.29a (+1.25) Number of seeds per fruit 2.76a (+0.51) 2.61a (+0.50) 2.47a (+0.63) 2.63a (+0.52) Seed weight (g) 0.47ac (+0.17) 0.39b (+0.14) 0.51a (+0.16) 0.41cb(+0.11) Note: Different lower case letters in the same row indicate different values based on analysis of variance (Anova) and Scheffe test at 95% level (p<0.05). Eff ectiveness of bees to pollination of jatropha – T. Atmowidi et al. 132 Th e number of fruits per raceme of plants pollinated by A. cerana was lowest (2.04 fruits) compared to plants pollinated by A. mellifera (3.05 fruits), open plants (2.45 fruits), and control plants (2.29 fruits). Pollination by bees increased the number of fruits per plant and fruits per raceme of J. curcas. Mean number of seeds per fruit of plants pollinated by A. cerana, A. mellifera, open plants, and control plants were 2.76, 2.61, 2.47, and 2.63 seeds, respectively. Th e number of seeds per fruit ranged from 1 to 3 seeds (Table 1). Results showed that A. mellifera was the superior pollinator compared to A. cerana. In addition, the number of fruits per plant and fruits per raceme of plants pollinated by A. mellifera were higher than that pollinated by A. cerana. Verma (1995) stated that some characteristics of A. mellifera were better than A. cerana, i.e. duration of foraging trip was signifi cantly longer and worker bees carried signifi cantly heavier pollen loads throughout the day. Th e increased yields of J. curcas pollinated by bees was probably caused by cross pollination. As stated by Westcott & Nelson (2001), insect pollination leads to earlier cessation of fl owering and more synchronous pod and seed ripening, thereby possibly increasing the weight of seed harvest. Th e natural pollinators were extremely effi cient in producing fertilization and fruit set of P. virgata (Wallace et al. 2002). In male-sterile oilseed rape (B. napus), Steff an-Dewenter (2003) reported insect pollination could positively aff ect several yield components. However, these eff ects are dependent on cultivar and growing conditions and total yields are often not increased due to the considerable compensatory capacity of oilseed rape (Westcott & Nelson, 2001). Similarly, Atmowidi et al. (2007) reported that mustard (Brassica rapa) pollinated by insects (mostly by bees) increased the number of pods, seeds per pod, and seeds per plant. Lower fruit set of J. curcas plants caged with insect screen could be caused by other factors, such as the number of plants observed, size of plants, and screen eff ect. Th e number of plants observed (three plants for each application) very limited. Size of plants observed was quite uniform, but individual variation in size occurred. Th e screen may be aff ected to plant photosynthetic rate, but most probably this eff ect is small, because the screen transmitted the light intensity easily. Th e natural fruit set rate indicates that J. curcas does not suff er seriously if there are no other pollination agents. Flowers of the species are unisexual, and male and female fl owers are produced in the same infl orescence. Th e production of female fl owers in small number, surrounded by a large number of male fl owers seems to be a strategy to ensure pollination to the maximum extent. Th e stigma receptivity lasting three days also additionally provides opportunities for pollination, if not pollinated on the fi rst and second day. However, the plant with predominant xenogamy requires mostly xenogamous pollen for more fruit set, after selective elimination of growing fruit. Th erefore, pollen transfer between conspecifi c has a great infl uence on the net percentage of natural fruit set (Raju & Ezradanam 2002). Diversity of fl ower visitors Based on fi eld observations, the fl ower-visitors of J. curcas belong to bees and ants (Hymenoptera), butterfl ies and moths (Lepidoptera), beetles (Coleoptera), thrips (Th ysanoptera), and fl ies (Diptera). Bee species belonging to A. cerana, Ceratina sp, Trigona sp., and Hylaeus sp. were found visiting the fl owers. At least, three species of BIOTROPIA VOL. 15 NO. 2, 2008 133 butterfl ies (Nyctemera sp., Eurema hecabe, and Neptis hylas) also visited the fl owers. Snout beetle and some species of Diptera (Syrphus balteatus, Sarcophaga sp., and Musca domestica), and thrips were also found visiting the fl owers. In general, insect pollinators visit the fl owers in the morning. On Brassica rapa (Brassicaceae), the peak abundance of insect pollinators occurred between 08.30-09.30 h (Atmowidi et al. 2007). Similar visitation was shown by two species of pollinators (Trigona carbonari: Apidae and Leiopcoctus speculiferus: Colletidae) visited Persoonia virgata (Proteaceae) occurred before 12.00 h (Wallace et al. 2002). Foraging time of insect pollinators related to plant resources, especially pollen and nectar. Th e increase of plant resources such as during mass fl owering showed an increase in available resources so that the foragers could collect more rewards per unit time. If resources are limited, the foragers require longer searches and travel time (Wesphal et al. 2006). Generally, both pollen and nectar content of most plants are higher in the morning. CONCLUSIONS Pollination by honeybees, A. cerana and A. mellifera increased the number of fruits per plant and fruits per raceme of J. curcas. In J. curcas, pollination eff ectiveness of A. mellifera was higher than that A. cerana. Naturally, fl owers of J. curcas are visited by bees and ants (Hymenoptera), butterfl ies and moth (Lepidoptera), beetles (Coleoptera), thrips (Th ysanoptera), and fl ies (Diptera). ACKNOWLEDGMENTS Th is project was funded by BIOTROP DIPA 2007. We greatly acknowledge Dr. Sih Kahono, Dr. Rosichon Ubaidillah, Dr. Yayuk Rahayuningsih, Woro Nurjito,M.Sc. and Pudji Aswari, M.Sc. of Zoological Museum, Indonesian Institute of Science, Cibi- nong for their help in identifi cation of insect pollinators. We are also grateful to Dian Sari and Sunaryo for the assistance in collecting the data. 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