Neotrop Entomol DOI 10.1007/s13744-015-0279-4

ECOLOGY, BEHAVIOR AND BIONOMICS

Honeybee Foraging, Nectar Secretion, and Honey Potential of Wild Trees, nummularia

AS ALQARNI

Dept of 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 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 () 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. After that, foraging activity decreased (20±6 workers/ per flower. The average number of flowers per tree=mean flowers/3 min) until sunset (05:40 pm). Pollen-gathering ac- number of flowers/m2×average surface area of canopy. To tivity was low compared to nectar-gathering activity. It calculate this, opened flowers were counted in five random started with low levels (1.8±0.5 workers/flowers/3 min) in 1-m2 areas of canopy surface per tree (a total of four trees), the early morning (05:40 am) and then increased to its max- and the mean number of flowers/m2 was obtained. The av- imum level (7.5±2.5 workers/flowers/3 min) in the forenoon ≤ erage surface area of the canopy was calculated by measur- (08:40 am) with significant differences (p 0.0001) com- ing 10 trees’ canopies manually using a rectangular (2 m× pared to other times of day. This activity decreased to its 3 m) wooden frame divided into equal 1-m2 units by grid minimum level (0.5±0.3 workers/flowers/3 min) in the noon wires. The top surface area of the canopy=πr2,where“r” is (11:40 am), afternoon (0.0 workers/flowers/3 min) (02:40 the diameter of the top of the canopy. pm), and sunset (0.0 workers/flowers/3 min) (05:40 pm) periods without significant differences between these pe- riods (Fig 1). Meteorology The average numbers of bees per subspecies collecting nectar and pollen were 34.9±8.00 and 1.9±0.80 To study the effect of some climatic factors on the tested workers/200 flowers/3 min, respectively. Workers parameters, air temperature (°C) and relative humidity (RH (outgoing) of A. m. jemenitica and A. m. carnica colonies %) values were recorded. A Tylor® digital wireless started foraging early (before sunrise) in low numbers. This thermohydrometer was used. activity increased over time and reached its peak (60±10 workers/flowers/3 min) in the afternoon (Fig 2)duringhigh Statistical analysis temperature (35°C) and low relative humidity (20%) condi- tions (Fig 3). Notably, the activity of A. m. jemenitica workers To analyze the foraging of worker bees on flowers, four trees continued until sunset, while this activity decreased sharply in randomized complete blocks were tested. Two variables for A. m. carnica in the afternoon to the sunset. The average were studied: (1) pollen-gathering and (2) nectar-gathering. daily number of foraging (outgoing) A. m. jemenitica workers The factor tested was the time of day. In these two experi- (41.7±7.00) was significantly (p≤0.0001) higher than that of ments, one-way ANOVA was applied, and Duncan’stestwas A. m. carnica (25.50±5.00). Among the incoming foragers, used for comparison between levels. Pearson’s correlation (t the non-pollen-gathering activity was significantly (p≤ tailed) was also applied. For foraging workers, outgoing and 0.0001) higher than that of pollen gathering in the two bee incoming to the hives, three variables were studied: (1) out- groups. The average numbers of non-pollen-gathering going bees, (2) incoming pollen-gathering bees, and (3) in- workers coming into the hives were 34.9±6.27 and 22.6± coming non-pollen-gathering bees. Two factors were tested: 5.30, whereas numbers of pollen-gathering workers aver- (1) time of day (one-way ANOVA and Duncan’s test were aged 6.8±2.00 and 2.5±1.00 for A. m. jemenitica and A. m. applied) and (2) bee subspecies, for which t test and carnica, respectively. Duncan’stest(t tailed) were used for comparison between Nectar collection was active during daytimes and reached levels. For nectar secretion, trees were in randomized com- its peak in the afternoon for A. m. carnica, whereas this plete blocks. The variable was the mass of secreted nectar, activity continued to a peak during the sunset for A. m. and the factor was the flower age (times of day during the jemenitica (Fig 4). In colonies, foraging activity was negatively first and second days). For computing, the software pro- correlated with humidity (r=−0.591, p≤0.01, n=40) and was grams Microsoft Excel 2010 and SPSS (Statistical Package positively correlated with temperature (r=0.614, p≤0.01, n= for the Social Sciences), ver. 20, 2012 for Windows Vista® 40). Pollen-gathering activity showed a weak correlation with were used. temperature (r=0.259, p≤0.01, n=40) and a weakly negative A. Alqarni

Fig 1 Daytime nectar and pollen gathering activities (average number±SE) of workers from Apis mellifera jemenitica and Apis mellifera carnica honeybee colonies recorded on flowers of Ziziphus nummularia in Riyadh, Saudi Arabia. Different letters indicate significant differences at p≤0.0001.

correlation with humidity (r=−0.160, p≤0.01, n=40). How- 33.25 μg/flower) and noon periods (mean 20.48; range ever, non-pollen-gathering activity was negatively correlated 13.00–28.00 μg TSS/flower). Nectar secretion decreased in with humidity (r=−0.588, p≤0.01, n=40), but the correlation the afternoon (mean 9.80; range 5.00–13.65 μg TSS/flower) was highly positive with temperature (r=0.590, p≤0.01, n= and reached its lowest level (mean 6.56; range 5.00–8.40 μg 40). On flowers, nectar collection was positively correlated TSS/flower) during the sunset period. The recorded air tem- with temperature (r=0.640, p≤0.01, n=20) and highly neg- perature and relative humidity values (Fig 6)weresimilarin atively correlated with humidity (r=−0.711, n=20). Nectar the 2 days of flowering. Nonetheless, it was observed that collection was also weakly negatively correlated with pollen nectar secretion increased to its peak with the increase of gathering (r=−0.406, p≤0.01, n=20). Nectar secretion was temperature (40.3°C) and the decrease of relative humidity positively correlated with temperature (r=0.647, p≤0.01,n= (20.0%). Statistically, nectar secretion was negatively corre- 20). Meanwhile, this correlation was negative with humidity lated with flower age (r=−0.353, p≤0.01, n=800) and hu- (r=−0.518, p≤0.01, n=20) and weakly negative with pollen midity (r=−0.304, p≤0.01, n=800), while it was positively gathering (r=−0.234, p≤0.01, n=20). By contrast, pollen correlated with air temperature (r=0.307, p≤0.01, n=800). gathering showed a negative weak correlation with temper- ature (r=−0.08, n=20), nectar collection (r=−0.406, p≤ 0.076, n=20), and nectar secretion (on flowers) (r=−0.234, Honey production potential p≤0.01, n=20). Morphologically, Z. nummularia has a wide canopy area and Dynamic of nectar secretion thick branches. It produces numerous flowers on branchlets. According to the obtained data (daily values), the average As shown in Fig 5, on the first day of flowering (main nectar number of flowers/m2 of canopy surface was 1914±129. secretion), nectar secretion started early before sunrise The canopy surface area was 45±8 m2. Therefore, the aver- (05:40 am) but in small amounts (mean 3.50; range 2.80– age number of flowers/tree was 86,130±300. The average 5.00 μg TSS/flower). Nectar secretion increased gradually sugar mass was 0.321±0.03 mg TSS/flower, and the total (mean 56.07; range 44.73–72.00 μg TSS/flower) until fore- sugar mass was 27.65±11 g/tree. Assuming that 1 kg of honey noon (08:40 am); its peak (mean 208.86; range 144.00– has, on average, 17% water and contains 830 g of sugar (TSS), 236.00 μg TSS/flower) was recorded at noon (11:40 am), the total potential sugar mass/tree is 33.31 g honey (approx- and then, secretion levels decreased again. The afternoon imately 0.03331 kg honey) daily and 2998.193±119 g (approx- (02:40 pm) and the sunset (05:40 pm) periods were substan- imately 2.998 kg honey) in the main flowering season tial for nectar secretion (means 114.63 and 148.14 and ranges (90 days). According to Adgaba et al (2012), the required land 63.00–138.95 and 86.00–187.60 μg TSS/flower for the two area for one Ziziphus tree is approximately 40 m2, including periods, respectively). On the second day of flowering (sec- spacing between trees. Consequently, the total number of ondary nectar secretion), it was noted that the sunrise period trees/hectare is approximately 250. The daily average of was a remarkable time, as nectar secretion reached its peak honey production potential of Z. nummularia is 8.3275 kg (mean 48.30; range 36.00 μg TSS/flower). Secretion de- honey/hectare and 749.475 kg of honey during the main creased in the forenoon (mean 25.20; range 12.00– flowering season. Ziziphus nummularia as a bee forage and honey source

Fig 2 Daytime foraging activity (average number±SE) of outgoing workers from Apis mellifera jemenitica (Yemeni) and Apis mellifera carnica (Carniolan) honeybee colonies in Riyadh, Saudi Arabia. Different letters indicate significant differences at p≤0.0001.

Discussion in A. m. carnica but continued in A. m. jemenitica to the late afternoon. The foraging activity pattern of A. m. jemenitica was Foraging activity of bees noticeably more frequent than that of A. m. carnica, i.e., the native honeybee subspecies appeared to be better than the The results indicated that the foraging activity in both tested imported subspecies in foraging on Z. nummularia flowers. As bee subspecies was low in early morning and then gradually observed in nectar secretion dynamics, the foraging activity increased to a peak in the afternoon. Then, it decreased sharply peaks were recorded during high temperature and low A. Alqarni

Fig 3 Air temperature (°C) and relative humidity (RH %) values during observations of honeybee foraging on Ziziphus nummularia flowers in Riyadh, Saudi Arabia.

humidity. Generally, the nectar collection foraging was more Dynamics of nectar secretion distinct than that of pollen, which may be due to low pollen content in flowers. The distinction of the native bee subspecies Observations revealed that Z. nummularia flowers bloom on may be due to its acclimatization with the harsh local environ- the sides of new branchlets of the same year. Some flowers mental conditions compared with the imported bee species start opening and secreting nectar early before sunrise and (Ali 2011,Alqarniet al 2011), including a better tolerance of high subsequent flowers continue to open until sunrise. Flowers summer temperatures (Alqarni 2006). Additionally, under ex- last for 2 days and then stop nectar secretion. It was ob- treme in vitro conditions at elevated temperatures or low hu- served that Z. nummularia flowers secreted approximately midity, the native honeybees showed higher tolerance than 83% of their nectar in the first day, while 17% of nectar was Carniolan honeybees (Abou-Shaara et al 2012). secreted on the second day. The peak of nectar secretion Balhareth (2012) showed that although foraging activity was at noon (11:40 am) on the first day of flowering with was negatively affected by decreased temperature, A. m. significant differences (p≤0.0001) with other times of flower jemenitica workers exhibited obvious activity compared to age. Additionally, three significantly different peaks (p≤ A. m. carnica workers. Forager honeybees apparently assess 0.0001) were recorded in the first day, while in the second the profitability of nectar rewards by evaluating a number of day, the nectar secretion was markedly low. Pham (2012) factors, including sugar concentration, nectar volume, flight noted that longevity of Z. mauritiana flower was approxi- distance from the hive, weather conditions, wind speed and mately 1.0–1.5 days. He added that nectar volume and sugar direction, level of difficulty in obtaining nectar from the concentration are important factors attracting pollinators to flowers, abundance of nectar within the patch, and nutrition- most entomophilous plants. However, most studies of forag- al status of the colony (Seeley et al 1991). Because honey ing behavior in bees have been performed under artificial yield primarily depends on the availability of nectar- conditions. providing flora, maximum honey production could be imper- One highly neglected research area is the daily nectar ative to establishing a balanced bee forage system. Simulta- secretion rhythm in flowers, including how nectar properties neously, forager bees schedule their visits to the flowers with mayvarywithtimeofday(Edgeet al 2012). Unfortunately, high nectar secretion rates. The potential of a bee plant can detailed information on flora and nectar secretion with re- be assessed by recording activities of honeybees on its spect to time of day has rarely captured the attention of flowers (Pham-Delegue et al 1986,Jones&Yates1991,Al- researchers (Nepi et al 2001). Anthesis of different jujube Ghamdi 2007). There is a significantly positive linear correla- species occurred from 12:00 pm to 13.00 pm and produced tion between honey production and colony attributes, e.g., small amounts of nectar (1.47–3.70 μL) at the base of the colony strength, brood rearing, comb building, and foraging flowers at different times of day. Sugar concentration was activity (Bhusal & Thapa 2006). Nadia et al (2007) reported quite variable (12–65%) (Pham 2012). For another species, that A. mellifera has the highest frequency of visits (77.5%) on Nadia et al (2007)showedthatZ. joazeiro flowers last ap- Ziziphus joazeiro followed by wasps (20.4%), and both act as proximately 12 h and produce high-sugar nectar (75%) in a effective pollinators. In the present findings, no honeybees small amount (1 μL). In the present findings, nectar secretion were observed visiting flowers of Ziziphus spina-christi in the was low in early morning (05:40 am), coinciding with high afternoon between 14:00 h and 18:00 h (Adgaba et al 2012). relative humidity (33.0%) and decreased air temperature Ziziphus nummularia as a bee forage and honey source

Fig 4 Daytime non-pollen and pollen-gathering activities (average number±SE) of incoming workers to the tested Apis mellifera jemenitica (Yemeni) and Apis mellifera carnica (Carniolan) colonies in Riyadh, Saudi Arabia. Different letters indicate significant differences at p≤0.0001.

(24.2°C), but increased to a peak with increasing tempera- access to some underground water, and they can also sur- ture (40.3°C) and decreasing relative humidity (20.0%) vive during flooding (Chaudhary & Al-Jowaid 1999). The same around noon (11:40 am) and in the subsequent times of mea- trend was noticed for Z. spina-christi in the same region, as surement. This is related to the Ziziphus species’ high adap- nectar secretion was positively correlated with temperature tation to dry-hot climates. Higher values than those obtained (Adgaba et al 2012). Even during controlled conditions in in the present study were found by Adgaba et al (2012), who three clones of Trifolium repens (Jakbson & Kristjánsson reported 0.79±0.54 (range 0.09–2.48 mg of sugar/flower) 1994) and in some Mediterranean plants, e.g., Thymus for Z. spina-christi. The same authors attributed this wide capitatus and Ballota acetabulosa, nectar secretion rate range to the variations among trees sampled. was temperature-dependent (Petanidou & Smets 1996). By Flower-to-flower differences are due to variations in mi- contrast, nectar production for Allium cepa was significantly croclimate within a flower patch (Corbet et al 1979). Ziziphus and inversely related to relative humidity while the effects of species are highly adapted to desert conditions as they have temperature, evapotranspiration, wind speed, and solar A. Alqarni

Fig 5 Dynamics of nectar secretion as total soluble solids (TSS) of Ziziphus nummularia (average number±SE) during flower lifetime (2 days) in Riyadh, Saudi Arabia. Different letters indicate significant differences at p≤0.05.

radiation were not significant (Silva & Dean 2004). It was Honey production potential noted that Z. spina-christi has two flowering seasons annu- ally. The first and less important season starts during June. It The observations of the present work indicated significant occurs over a short period and probably does not occur dur- differences (p≤0.0001) among trees tested for nectar pro- ing some years, depending on rainfall. The second season duction, which could be an effective factor when selecting (the main flow) occurs from August to October and repre- trees for honey production. According to the obtained re- sents the main source for the production of Ziziphus honey sults, during optimum environmental conditions and exclud- (Adgaba et al 2012). ing other factors (e.g., competitors of honeybees, available

Fig 6 Daytime air temperature (°C) and relative humidity (RH) (%) values during nectar measurements of Ziziphus nummularia in Riyadh, Saudi Arabia. Ziziphus nummularia as a bee forage and honey source nectar to be collected, and consumed nectar for bee energy), Adgaba N, Awad MA, Al-Ghamdi AA, Alqarni AS, Radloff SE (2012) Nectar the average honey production potential of tested of Ziziphus spina-christi (L.) Wild (Rhamnaceae): dynamics of secre- tion and potential for honey production. J Apic Sci 56(2):5–15 Z. nummularia could be approximately 2.998 kg/tree and Al-Ghamdi AA (2007) Evaluation of various honeybee foraging activities 749.475 kg/ha in the main flowering season (September– for identification of potential bee plants in Riyadh, Saudi Arabia. Ann October). The present values are less than those (3.6 kg/tree Agric Sci Fac Ain Shams Univ 52(2):487–499 and 900 kg/ha) obtained by Adgaba et al (2012)forZ. spina- Ali MAM (2011) Comparative study for evaluating two honey bee races, Apis mellifera jemenitica (indigenous race) and Apis mellifera carnica christi. This may be due to the morphological and physiolog- (Carniolan race) in brood production, population development and ical variations between the two Ziziphus species, including foraging activity under the environmental conditions of the central average intensity of flowers on trees and nectar amount in region of the Kingdom of Saudi Arabia. Ann Agric Sci Fac Agric Ain – flowers. Depending on the number and intensity of trees, Shams Univ 56(2):127 134 Alqarni AS (2006) Tolerance of summer temperature in imported and number of honeybee colonies and honey yield per colony, indigenous honeybee, Apis mellifera L. races in Central Saudi Arabia. one Ziziphus tree produced 3.5–5.8 kg of honey and one Saudi J Biol Sci 13(2):123–127 colony produced 1.1–3.8 kg/colony. However, a significant Alqarni AS, Hannan MA, Owayss AA, Engel MS (2011) The indigenous negative correlation was found between numbers of honey- honey bees of Saudi Arabia (Hymenoptera, Apidae, Apis mellifera jemenitica Ruttner): their natural history and role in beekeeping. bee colonies/tree and amount of honey yielded (Khanbash ZooKeys 134:83–98 2003). The same author attributed these variations to envi- Balhareth HM (2012) Comparative studies of queens and colonies of ronmental conditions including rainfall as well as locality and native and imported honeybees, Apis mellifera L. M. Sc. Thesis. size of the tree. College of Food and Agriculture Sciences, King Saud University, p 102 (in Arabic), p 103–104 (English abstract) For nectar secretion, the obtained measurements were Bataher AS, Al-Kathery MA (2001) Non-wood products of Sidr, Ziziphus far lower than those of Bataher & Al-Kathery (2001), who spina-christi, tree. Scientific Symposium about honey and Sidr tree. reported 0.2–2.6 mg/flower/day. According to nectar secre- Hadramout University for Science and Technology, Faculty of Applied ’ – tion and sugar concentration in the flower, it has been pos- Sciences, Se oun, Yemen. March 22 24, (In Arabic) p 9 Bhusal SJ, Thapa RB (2006) Response of colony strength to honey pro- sible to estimate the honey production potential (kg of hon- duction: regression and correlation analysis. J Inst Agric Anim Sci 27: ey/ha/flowering season) of the following plants: Z. spina- 133–137 christi (Christ’s thorn) (approximately 900 kg of honey/ha, Chaudhary SA, Al-Jowaid AA (1999) Vegetation of the Kingdom of Saudi range 550–1300 kg; Adgaba et al 2012); Asclepias syriaca Arabia. National Agriculture & Water Research Center, Ministry of – Agriculture & Water, Kingdom of Saudi Arabia, p 800 (milkweed) (500 600 kg; Farkas & Zajácz 2007); Trifolium Corbet SA, Willmer PG, Beatment JWL, Unwin DM, Prys-Jones OE (1979) pratense (red clover) (883 kg; Szabo & Najda 1985); Post-secretory determinants of sugar concentration in nectar. Plant Phaceliata nacetifolia (60–360 kg; Farkas & Zajácz 2007); Cell Environ 2:293–308 and Tilia (lime) (90–1200 kg; Crane et al 1984). The high Crane E, Walker P, Day R (1984) Directory of important world honey sources. International Bee Research Association London, pp 384 nectar secretion potential of Ziziphus trees could be due to Dwivedi SPD, Pandey VB, Shah AH, Eckhardt G (1987) Cyclopeptide al- its flowering pattern, which is distributed throughout the kaloids from Ziziphus nummularia. J Nat Prod 50(2):235–237 flowering period (few flowers/cyme/day for up to 3 months). Edge AA, Van Nest BN, Johnson JN, Miller SN, Naeger N, Boyd SD, This pattern could be due to an adaptation of the plant to Moore D (2012) Diel nectar secretion rhythm in squash (Cucurbita pepo) and its relation with pollinator activity. Apidologie 43:1–16 attract sufficient pollinators for flowers. The extended Farkas Á, Zajácz E (2007) Nectar production for the Hungarian honey flowering pattern could also be due to the plant’smechanism industry. Eur J Plant Sci Biotech 1(2):125–151 to generate sufficient sugar for nectar preparation of daily Hammer K (2001) Rhamnaceae. In: Hanelt P, Institute of Plant Genetics photosynthesis in the leaves. Additionally, the very deep- and Crop Plant Research (eds) Mansfeld’s encyclopedia of agricultural and horticultural crops, vol 3. Springer, Berlin, pp 1141–1150 rooted nature of the plant is an adaptation to use deep Hill DB, Webster TC (1995) Apiculture and forestry (bees and trees). ground water, so that it can produce nectar without Agrofor Syst 29:313–320 experiencing moisture stress (Adgaba et al 2012). Jain SK, Tarafdar CR (1970) Medicinal plant lore of the Santhals. Econ Bot 24(3):241–278 Jakbson HB, Kristjánsson K (1994) Influence of temperature and floret age on nectar secretion in Trifolium repens L. Ann Bot 74:327–334 Acknowledgments The author extends his appreciation to the Dean- Jones D, Yates BD (1991) Beekeeping study notes, 2nd edn. Bee Books ship of Scientific Research at King Saud University for funding this work New and Old Tapping Wall Farm, Burrowbridge, Bridgewater TA7 through the research group project No. RGP-189. ORY, Somerset, UK Keasar T, Shmida A (2009) An evaluation of Israeli forestry trees and shrubs as potential forage plants for bees. Isr J Plant Sci 57:1–16 Khanbash MS (2003) Relationship between the density of Sidr trees, References Ziziphus spina-christi, and honey production. The 3rd international conference of Arab Beekeepers Union, 28–31 December, Tanta, Egypt, p 101–108 (in Arabic), p 109 (English abstract) Abou-Shaara HF, Al-Ghamdi AA, Mohamed AA (2012) Tolerance of two Kim MS, Kim SH, Han J, Kang MS, Park YK (2011) Honeybee visit and honey bee races to various temperature and relative humidity gradi- nectar secretion characteristics of the Chinese Hawthorn, Crataegus ents. Environ Exp Biol 10:133–138 pinnatifida Bunge. J Apic Apic Soc Korea 26(1):11–14 A. Alqarni

Kottek MJ, Grieser, Beck C, Rudolf B, Rubel F (2006) World map of the Pham HD (2012) Pollination biology of and longans and the Köppen-Geiger climate classification updated. Meteorol Z 15:259– importance of insects in the pollination of crops in Vietnam. Ph.D. 263. doi:10.1127/0941-2948/2006/0130 Thesis. University of Guelph, Canada Mallick SA (2000) Technique for washing nectar from the flowers of Pham-Delegue MH, Masson C, Etievant P, Azar M (1986) Selective olfac- Tasmanian leatherwood (Eucryphia lucida, Eucryphiaceae). Austral tory choices among sunflower aromas, a study by combined olfactory Ecol 25:210–212. doi:10.1046/j.1442-9993.2000.01010.x conditioning and chemical analysis. J Chem Ecol 12:781–793 Masierowska ML (2003) Floral nectaries and nectar production in brown Seeley TD, Camazineand S, Sneyd J (1991) Collective decision-making in mustard (Brassica juncea) and white mustard (Sinapis alba) honey bees: how colonies choose among nectar sources. Behav Ecol (Brassicaceae). Plant Syst Evol 238:97–107 Sociobiol 28:277–290 Nadia TL, Machado IC, Lopes AV (2007) Fenologiareprodutiva e sistema Silva EM, Dean BB (2004) Patterns of floral nectar production of onion de polinização de Ziziphus joazeiro Mart. (Rhamnaceae): atuação de (Allium cepa L.) and the effects of environmental conditions. J Am Soc Apis mellifera e de visitantes floraisautóctones como polinizadores. Hort Sci 129(3):299–302 – Acta Bot Bras 21(4):835 845 Szabo TI, Najda HG (1985) Flowering, nectar secretion and pollen pro- Nepi M, Guarnieri M, Pacini E (2001) Nectar secretion, reabsorption, and duction of some legumes in the Peace River Region of Alberta, sugar composition in male and female flowers of Cucurbita pepo.IntJ Canada. J Apic Res 24(2):102–106 Plant Sci 162:353–365 Tel-Zur N, Schneider B (2009) Floral biology of Ziziphus mauritiana Orwa C, Mutua A, Kindt R, Jamnadass R, Simons A (2009) Agroforestree (Rhamnaceae). Sex Plant Reprod 22:73–85 database: a tree reference and selection guide version 4.0 (http:// www.worldagroforestry.org/af/treedb/) Weast R (ed) (1986) CRC handbook of chemistry and physics, 67th edn. Pandey A, Singh R, Radhamaniand J, Bhandari DC (2010) Exploring the CRC Press, Inc., Boca Raton potential of Ziziphus nummularia (Burm. f.) Wight et Arn. from drier Wyatt R, Broyles SB, Derda GS (1992) Environmental influences on nec- regions of . Genet Resour Crop Evol 57:929–936 tar production in milkweeds (Ascelapias syriaca and A. exaltata). Am J – Petanidou T, Smets E (1996) Does temperature stress induce nectar Bot 79:636 642 secretion in Mediterranean plants? New Phytol 133:513–518 本文献由“学霸图书馆-文献云下载”收集自网络，仅供学习交流使用。

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