Honeybee Foraging, Nectar Secretion, and Honey Potential of Wild Jujube Trees, Ziziphus Nummularia
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Neotrop Entomol DOI 10.1007/s13744-015-0279-4 ECOLOGY, BEHAVIOR AND BIONOMICS Honeybee Foraging, Nectar Secretion, and Honey Potential of Wild Jujube Trees, Ziziphus nummularia AS ALQARNI Dept of Plant Protection, College of Food and Agriculture Sciences, King Saud Univ, Riyadh, Saudi Arabia Keywords Abstract Arabian Peninsula, flower phenology, Ziziphus trees are of economic importance due to their aggregated value foraging (source of fruits and timber) and are the most important melliferous plants Correspondence in the Arabian Peninsula. Interaction between honeybees and Ziziphus AS Alqarni, Dept of Plant Protection, College nummularia was investigated by assessing foraging, flower phenology, of Food and Agriculture Sciences, King Saud Univ, Riyadh, Saudi Arabia; [email protected] nectar secretion, and honey potential. It is demonstrate that both the native Apis mellifera jemenitica Ruttner and the exotic Apis mellifera Edited by Fernando B Noll – UNESP carnica Pollmann foraged on Z. nummularia flowers. Bee foraging for Received 10 April 2014 and accepted 1 nectar and pollen was low (2±0.7 workers/200 flowers/3 min) during early February 2015 morning and increased to a peak in the afternoon (100±15 workers/200 flowers/3 min). Remarkable foraging activity was recorded during high * Sociedade Entomológica do Brasil 2015 temperature (35°C) and low humidity (20%) conditions. Foraging for nec- tar collection was more distinct than that for pollen. The flowering of Z. nummularia was gradual, and was characterized by some flowers that opened and secreted nectar early before sunrise, whereas other flowers remained opened until sunrise. The flowers lasted 2 days, with 83% of nectar secreted in the first day. The peak of nectar secretion was recorded at noon under hot and dry conditions. The lowest amount of nectar was secreted during sunrise under mild temperature (24°C) and humidity (31%) conditions. Under optimum conditions, it is assumed that the average sugar mass was 0.321±0.03 mg TSS/flower, while the total sugar mass was 27.65±11 g/tree. The average honey production potential of tested Z. nummularia was approximately 2.998 kg/tree and 749.475 kg/ha in the main flowering season. Introduction the trees can withstand harsh conditions such as drought, salinity, and high temperatures (Hammer 2001). The shrubs Honeybee foraging activity is the most important factor that have been shown to effectively resist wind erosion, help in affects the quantity and quality of honey production (Keasar the deposition of soil, and cause favorable conditions for the &Shmida2009). Honey produced from certain species of growing of perennial grasses. Additionally, they provide Ziziphus is the most expensive in the Middle East ($80–130/ shade and have proven successful in sand dune stabilization kg), and Ziziphus spp. and Acacia spp. are the major honey (Orwa et al 2009). Furthermore, medicinal properties of the plants in Saudi Arabia and in most of the Arabian Peninsula genus Ziziphus are well known, i.e., as an astringent, demul- (Al-Ghamdi 2007,Alqarniet al 2011). cent, diuretic, emmenagogue, expectorant, and tonic (Jain & The genus Ziziphus (Rhamnaceae) is composed of approx- Tarafdar 1970, Dwivedi et al 1987). imately 170 species native to the tropics and subtropics (Tel- The wild jujube Ziziphus nummularia is a shrub that grows Zur & Schneider 2009). Some of these species are multipur- in abundance in sandy and stony soils in the grazing lands of pose economic species valued for their edible fruits and their arid and semi-arid regions. It is important in a horti-pasture use for fencing, fuel, construction, foraging, and furniture. system, particularly in areas with high wind velocities They are well adapted to dry and hot climates. Additionally, (Pandey et al 2010). Ziziphus nummularia generally forms A. Alqarni dense thickets that receive runoff water from adjoining Z. nummularia flowers for nectar or pollen gathering were areas. Dense Z. nummularia vegetation is called “Ziziphus recorded on a branch of approximately 200 flowers/tested basins.” These thickets are considered refuges for birds and tree (total of four trees, 800 flowers) for 3 min using a hand- other wildlife and flora, including palatable annual and pe- held counter and stopwatch. At the colonies, outgoing and rennial herbs (Chaudhary & Al-Jowaid 1999). In arid and incoming foraging workers were recorded for 3 min at the semi-arid regions, such trees are very important environ- same times using a handheld counter and stopwatch. Incom- mental constituents as resources for biodiversity and conser- ing workers were divided into pollen and non-pollen carriers. vation. Trees offer site modification and food resources, such as nectar, pollen, and resin for bees. Bee-visited plants also Plant testing benefit from bees and other visiting insects due to pollination (Hill & Webster 1995). To estimate the Z. nummularia flower ages, 80 flower buds However, no data are available on the flowering phenol- (20 per tree) were labeled with a small tag. Flower buds were ogy, nectar, and pollen presentation in Z. nummularia.In observed every 2 h starting from opening until the end of the addition, information about honeybee foraging on such trees flowering period. Based on previous observations, flowers’ is very limited. Therefore, we aimed to answer the following dehiscence started very early in the morning and continued questions: (1) How do indigenous and exotic honeybees reg- until sunrise; nectar secretion continued until wilting on the ulate their foraging visits on flowers? (2) How are nectar following day. Therefore, the assessment of nectar secretion secretion and bee foraging influenced by certain climatic fac- was performed within this period (2 days). Measurements tors? (3) How does nectar secretion in Z. nummularia fluctu- were conducted exclusively on sunny days. ate during daytime? (4) How can honey production be predicted? Nectar collection Due to the native climatic conditions (high temperature and Material and Methods low humidity), the nectar in flowers was found to be viscous or crystallized and difficult to collect. To overcome this prob- Study site lem, the following procedure was employed: One flowering branch (approximately 30 cm long) near the ground of every The present work was performed in the Rawdhat-Khoraim tree (total of four branches) was labeled, and all opened region (21.0×1.5 km), 120 km Northeast Riyadh, Saudi Arabia flowers were removed. With only flower buds on it, the (25°30′25″N, 47°46′30″E; 557 m above sea level). This region branch was caged with organza bags prior to nectar collec- is a low area oasis where water estuaries from many Wadis tion (Wyatt et al 1992). On the following day, during the early are congregated. In addition to Ziziphus, other trees grow in opening of the flowers, the nectar concentration as total this area, e.g., Acacia spp., and annual plants, e.g., Lavandula soluble solids (TSS) was measured in each flower (20 officinalis and Trigonella hamosa. The study area lies within flowers/branch/tree) using the washing technique (Mallick hot desert climate of accumulated annual precipitation less 2000), as follows: 7 μL of distilled water was carefully depos- than 50% of the potential evapotranspiration and average ited in each flower using a calibrated micropipette. This vol- annual temperature ≥+18°C according to Köppen-Geiger ume was retrieved three times to dissolve the highly concen- climate classification (Kottek et al 2006). Experiments were trated matter. This technique was conducted quickly to avoid conducted during the main flowering season (August– rapid evaporation and consequent concentration of the October) of Z. nummularia in 2012. Four trees of this plant sugars. were randomly selected, and eight equal-in-strength honey- bee colonies (four colonies per subspecies) of the native bee Sugar measurement in flowers Apis mellifera jemenitica (Yemeni) and the exotic bee Apis mellifera carnica (Carniolan) were tested. To estimate the sugar content (TSS) in the 7 μLnectarsolu- tion, an automatically temperature-compensated digital Monitoring of bee foragers handheld refractometer (Reichert®, model 13950000, USA) was used. After each measurement, distilled water was Foraging bees on flowers and at colonies’ entrances were added for washing, the instrument reading was calibrated simultaneously counted during the following times: sunrise, to 0.00, and a new tip was used for each flower. The deter- forenoon, noon, afternoon, and sunset, i.e., at 05:40 am, mination continued for 2 d (flower life) during 29 and 30 08:40 am, 11:40 am, 02:40 pm, and 05:40 pm, respectively, September 2012 at the same previously mentioned daytime according to the local time of the Riyadh region. On flowers, hours for bee foraging. In each flower, the sugar mass in honeybee workers from the two bee subspecies visiting secreted nectar was determined by the volume and Ziziphus nummularia as a bee forage and honey source concentration of the solution measured. Concentration read- Results ings (mass/total mass, g sugar/100 g solution) were convert- ed to mass/volume using the conversion table (Weast 1986). Foraging activity of bees The measured concentration was converted to mg following the equation: TSS (mg/flower)=TSS%×100/7. On flowers, foraging for nectar in both tested honeybee sub- species started in the early morning (5:40 am), while activity Estimation of honey production potential was moderate in the forenoon (26±6 workers/flowers/ 3 min) and noon (30±3 workers/flowers/3 min) periods According to the methods of Masierowska (2003) and Kim and reached its maximum level (99±15 workers/flowers/ et al (2011), the average amount of honey that can be pro- 3 min) during the afternoon (02:40 pm), which showed a ≤ duced from a single tree is equivalent to the average number significant difference (p 0.05) compared to other times of of flowers per tree multiplied by the average mass of sugar day.