The Carpenter Bee Xylocopa Pubescens As an Agricultural Pollinator in Greenhouses Adi Sadeh, Avi Shmida, Tamar Keasar

The Carpenter Bee Xylocopa pubescens as an Agricultural Pollinator in Greenhouses Adi Sadeh, Avi Shmida, Tamar Keasar

To cite this version:

Adi Sadeh, Avi Shmida, Tamar Keasar. The Carpenter Bee Xylocopa pubescens as an Agricultural Pollinator in Greenhouses. Apidologie, Springer Verlag, 2007, 38 (6), pp.508-517. hal-00892288

HAL Id: hal-00892288 https://hal.archives-ouvertes.fr/hal-00892288 Submitted on 1 Jan 2007

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 38 (2007) 508–517 Available online at: c INRA, EDP Sciences, 2007 www.apidologie.org DOI: 10.1051/apido:2007036 Original article

The Carpenter Bee Xylocopa pubescens as an Agricultural Pollinator in Greenhouses*

Adi Sadeh,AviShmida, Tamar Keasar

Department of Evolution, Systematic and Ecology, the Hebrew University, Jerusalem 91904, Israel

Received 24 December 2006 – Revised 6 May 2007 – Accepted 22 May 2007

Abstract – Many greenhouse crops depend on bees for pollination. Global declines of honeybee populations, and their limited efficiency in pollinating some greenhouse food-plants, motivate the search for additional pollinators. We evaluated the carpenter bee X. pubescens, a local species to Israel, as a pollinator of greenhouse-grown honeydew melons, in comparison to honeybees. We recorded the bees’ daily and seasonal activity patterns in relation to floral nectar levels, frequencies and durations of flower visits, and fruit quantity and quality. The bees’ daily foraging schedule on melon did not correlate with nectar yield and nectar production patterns by the flowers. Visit durations per flower were shorter for X. pubescens than for honeybees. Pollination by both bees resulted in similar fruit mass and seed numbers, but X. pubescens pollination increased fruit set threefold as compared to honeybee pollination. We conclude that X. pubescens can effectively pollinate melons in enclosures. carpenter bee / greenhouse / honeybee / honeydew melon / pollination

1. INTRODUCTION Pollination is thus one of the most im- portant ecosystem services provided to agriculture. This critical ecosystem service has Agricultural pollination is the ﬁrst indis- been degrading in recent years, as honeybee pensable step in a process that results in colonies are declining in abundance because of the production of fruit, vegetables, nuts and habitat loss, diseases, pesticides, and other im- seeds. Agriculture is highly dependent on in- pacts (Kremen et al., 2002). An expert review sect pollination, in particular by the honeybee, panel recently conﬁrmed that the last years of Apis mellifera L. (Cunningham et al., 2002). losses of honeybee colonies in North Amer- The economic value of insect pollination to ica leave us with fewer managed pollinators agriculture can be estimated on the basis of than at any time in the past 50 years, and that the abundance and market value of insect- the management and protection of wild polli- pollinated crops. In the United States, for ex- nators is an issue of paramount importance to ample, the value of crop pollination by insects the food supply system (Allen-Wardell et al., is estimated at US$14.6 billion (Morse and 1998). Calderone, 2000). $3 billion’s worth of this Native bee communities also provide pollination service is provided by native polli- pollination services, but the extent of these nator species (Losey and Vaughan, 2006), and services, and how they vary with land man- the remaining agricultural output is due to pol- agement practices, are largely unknown. In lination by honeybees. a pioneering study, Kremen et al. (2002) documented the individual species and ag- Corresponding author: T. Keasar, gregate community contributions of native [email protected] bees to crop pollination, on farms that var- * Manuscript editor: Jacqueline Pierre ied both in their proximity to natural habitat

Article published by EDP Sciences and available at http://www.apidologie.org or http://dx.doi.org/10.1051/apido:2007036 Carpenter bees for greenhouse pollination 509 and in management type (organic versus con- ley (Gerling et al., 1989; Hogendoorn and ventional). Native bee communities provided Leys, 1993; Leys et al., 2000, 2002). Fe- full pollination services on organic farms near males of this species typically dig branched natural habitat even for a crop with heavy nests in dead wood (Ben Mordechai et al., pollination requirements (e.g., watermelon, 1978). They hibernate in the nests from the Citrullus lanatus). All other farms, however, end of October until the middle of March. Dur- experienced greatly reduced diversity and ing the activity season (March–October), fe- abundance of native bees, resulting in insuf- males are engaged in preparing brood cells, ficient pollination services. While this study while males form non-resource mating terri- demonstrates the importance of native bees to tories (Gerling et al., 1983). X. pubescens is crop pollination, only three species of native multivoltine, and may produce 4–5 genera- solitary bees (Nomia melanderi, Megachile ro- tions per year. Females are extremely long- tunda and Osmia cornifrons) are produced on lived and may be reproductively active for up a commercial scale to provide pollination ser- to 120 days (Gerling et al., 1981). Ovipositing vices. These pollinators are mainly used for females provision each brood cell with nectar alfalfa and orchard crops (Velthuis and van and pollen, lay a single egg in the cell, seal it Doorn, 2006). and proceed to construct the next cell. The de- In recent decades, insect pollinators have velopment from egg to adult takes 27–35 days. been actively introduced into greenhouses and Young adults that remain in the maternal nest nethouses. This effort was initiated in the before dispersal are provisioned with pollen by Netherlands, where honeybees were first in- their mother (Velthuis and Gerling, 1983; Van troduced into tomato greenhouses to replace der Blom and Velthuis, 1988), and obtain nec- hand pollination (de Ruijter, 1999). Honey- tar by trophallaxis (Gerling et al., 1983). bees were also shown to efficiently pollinate In natural habitats, X. pubescens foragers sweet peppers in enclosures (de Ruijter et al., feed on a wide variety of flower species, and ◦ 1991). Additional experiments demonstrated remain active at temperatures up to 40 C the superiority of bumblebees over honeybees (Gerling et al., 1989). This heat resilience in pollinating greenhouse tomatoes and egg- makes X. pubescens an attractive candidate plants (Pessarakli and Dris, 2004; Velthuis and pollinator for greenhouses in hot climates, van Doorn, 2006). Honeybees remain the main where temperatures often exceed the thermal greenhouse pollinator for crops that do not re- window of honeybees and bumblebees (Corbet quire mechanical buzzing of the anthers. In- et al., 1993). Initial favorable results, regard- sect pollination in greenhouses is now prac- ing the success of native Australian Xylocopa ticed worldwide, but is generally limited to in pollinating greenhouse tomatoes, provide an honeybees and bumblebees. The domestica- additional incentive for a quantitative evaluation and use of additional pollinator species in tion of their performance (Hogendoorn et al., enclosures is desirable as a countermeasure to 2000). the decreases in honeybee populations. In the present research, we tested the feasibility of adding the carpenter bee Xylocopa pubescens 2. MATERIALS AND METHODS (L.) to the arsenal of agricultural greenhouse pollinators. We compared X. pubescens’ polli- 2.1. General methods nation efficiency with that of the honeybee, the standard pollinating insect. Observations were conducted in a small (8 × The genus Xylocopa consists of about 469 4 × 4 m) greenhouse between April and October, species (Michener, 2002), predominantly dis- 2005. Temperature in the greenhouse ranged 11– tributed in tropical and subtropical climates, 38 ◦C during the study period, relative humidity and occasionally in temperate areas (Hurd and ranged 5–86%, and radiation levels were between Moure, 1963). X. pubescens, a local species 3 and 353 lux. The greenhouse was not illuminated, to Israel, is of Ethiopian origin, and has and provided no humidity control. We grew hon- reached Israel via the Syrian-African rift val- eydew melons in the greenhouse, and introduced X. 510 A. Sadeh et al.

pubescens and honeybees in alteration into it (11 in- observation session, depending on the availability troductions of X. pubescens, 7 introductions of hon- of active, single-female nests. eybees). Preliminary observations indicated that X. pubescens foragers seem to behave normally within a few hours of introduction into the greenhouse. The 2.2.2. Apis mellifera condition of honeybee colonies, on the other hand, started deteriorating after a few days in the enclo- Honeybees are the standard pollinators of green- sure. These factors favoured short observation ses- house melons in Israel, and were therefore used as sions within the greenhouse. We therefore started a reference for the evaluation of pollination per- observing the bees on the morning following intro- formance. Two mini-nucleus honeybee colonies, duction, with no period of acclimation. We recorded originally developed for queen-rearing, were used nectar yields in the flowers, bee activity, and crop for observations. These colonies typically contain yields for both types of visitors. a queen and ca. 400 workers. They survive up to several months with high levels of worker foraging, and are as effective as regular-sized honey- 2.2. Bees bee colonies in pollinating honeydew melons in enclosures (Keasar et al., in press). Their advan- tages include their small population size (suitable 2.2.1. Xylocopa pubescens for the low carrying capacity of the experimental greenhouse), low weight, ease of handling, and low We collected palm branches containing wild worker aggression. We monitored the mini-hives nesting X. pubescens from four locations in Israel once a week for stored honey and pollen, presence in 2004 and 2005. We number-marked and trans- of eggs and brood, and queen activity. Dead queens ferred the nests to the experimental greenhouse. The were replaced. The bees were fed once a week, or nests were housed outside the greenhouse between as needed, with ca. 100 mL of 62% inverted sucrose observation sessions, and the bees were allowed to solution. exit and reenter the nests without restriction. Nests The bees were allowed to forage without restric- were moved into- and out of the greenhouse at tion outside the greenhouse before and after obser- night only, to minimize disturbance to the bees. vation sessions. Observation sessions in the green- We introduced the nests into the greenhouse for house lasted 2–3 days, and were alternated with observation periods of 2–3 days. Preliminary ob- observations on X. pubescens. The bees were un- servations revealed that females forage more in- marked. tensively than males, therefore only females were observed (Sadeh, 2006). X. pubescens is unique in having intra-specific plasticity in social organi- 2.3. Forage plants zation, which changes according to environmental conditions. That is, both solitary and social nests Cucumis melo (L.) var. Gallia (honeydew mel- often coexist in a population (Gerling et al., 1981; ons), Ocimum basil (L.), Portulaca oleracea (L.), Hogendoorn and Leys, 1993). Solitary nests con- Leucophyllum frutescens (Berland) and Solanum tain a single adult female, while social nests con- rantonnetii (C.) were grown in the greenhouse tain a reproductive foraging female, and a helper throughout the study period. 150 melon plants were female that guards the nest entrance. Despite dif- maintained throughout the experimental period as ferences in foraging behavior, pollination of honey- the model crop. This was done by removing plants dew melons by both nesters results in similar fruit that have stopped blooming, and adding blooming mass, fruit seed numbers and fruit set (Keasar et al., plants in replacement, throughout the experimen- 2006). To reduce behavioral variability arising from tal period. Portulaca oleracea and Solanum ranton- differences in social organization, we included only netii supplemented the bees’ diet with pollen (pre- solitary nesters in the greenhouse observations. We liminary observations showed that no pollen was observed the nests for the presence of a guard one collected from melon flowers). Ocimum basil and day before each introduction into the greenhouse, Leucophyllum frutescens provided an additional and subsequently introduced only nests without a nectar supply when melon blooming was insuffi- guard. Individual bees were not marked, because cient. When the blooming of nectariferous plants in the marking procedure causes some mortality. We the greenhouse was insufficient, we also placed a introduced 4–10 nests into the greenhouse in each 40% sucrose solution feeder inside the greenhouse. Carpenter bees for greenhouse pollination 511

Melon flowers are either male or hermaphrodite, 2.5. Bee behavioral parameters and their sex can be easily determined morpho- logically. Hermaphrodite flowers have receptive ovaries and viable pollen, therefore self-pollination We sampled the bees’ daily and seasonal flight is possible. However, self-pollination does not oc- activity by counting the number of active individu- cur spontaneously, as hand- or insect-pollination is als that were outside the nests at ten haphazardly de- required for successful fertilization (Orr, 1985). In- termined time points every hour. The data were col- dividual flowers bloom for 24 hours. They open in lected at two-week intervals throughout the study early morning, and remain receptive throughout the period. We alternated between a whole-day obser- day. This feature allowed us to determine whether vation (0500 h–1800 h), and an observation at peak a flower has been pollinated by Xylocopa or honey- activity hours only. We selected the observation bee, depending on the visitor species that was intro- hours for the peak activity record based on the bees’ duced into the greenhouse on the day of its bloom. daily activity pattern in the previous whole-day ob- We used tags of different colors to mark flowers that servation. We also recorded the total number of bee bloomed during observations on X. pubescens and exits from the nests for 15 minutes at hourly in- observations on honeybees. tervals, once a month. We used these data to estimate nest exit rates per foraging individual (see Data Analysis section). 2.4. Nectar measurements We assessed the bees’ daily pattern of foraging on melon flowers by counting the number of vis- We tested for correlations between the bees’ pat- its of all the active bees in 100 melon flowers in terns of foraging activity and the amount of nec- a ten-minute observation period. These data were tar available to them in melon flowers. Nectar pro- recorded once a month, between 0600 h and 1200 h duction is the total volume secreted by a flower in at two-hour intervals. the absence of exploitation of nectar by insects. To For pollination to occur, bees must fly and trans- measure production, we depleted 40 randomly se- fer pollen from male to hermaphrodite flowers. We µ lected flowers of nectar (using 1 L pipettes), and tested whether X. pubescens bees (a) have a prefer- covered them with a fine mesh net. The netting al- ence for one of the flower sexes, and (b) switch be- lowed air and light, but not insects, to get through. tween flowers of different sexes at random. To this Netting was performed at dawn (0600 h), before the end, we recorded the sex of flowers visited by a sin- start of bee foraging. At 0900 h, 1200 h and 1500 h gle bee during 45–312 consecutive visits in melon we measured the nectar content of one third of the flowers. We recorded eight visit sequences, each by initial sample (i.e., 13–14 flowers per sample). The adifferent bee. We tested for goodness of fit be- flowers were picked after the second nectar sam- tween the bee’s flower selection of male vs. female pling, which was therefore a destructive sample. We flowers and the proportions of male and female repeated this sampling procedure once a month, be- flowers in the greenhouse on the day of observation. tween April and October, 2005. We also tested whether the frequencies of the pos- Nectar yield is the volume of nectar available sible transitions between flower sexes (male-male, to bees, and depends on nectar production by the male-female, female-female and female-male) con- plant and its consumption by insects. To determine formed to the product of the proportions of males yield, we measured nectar from 20 randomly se- and females in the greenhouse. lected uncovered flowers per sample, using 1 µL pipettes. The first measures were conducted before the bees started foraging. Sampling was repeated at two-hour intervals between 0600 h and 1200 h with- 2.6. Crop yield parameters out destruction of flowers. The sex of each sampled flower was recorded. Nectar yields were recorded 2–3 times a month throughout the study period. We weighed the melons and counted their seeds Nectar concentrations were determined in sam- when the fruits became yellow, as measures of yield ples taken for determination of nectar yield and quality (McGregor, 1976). We calculated the pro- nectar production, using a hand-held Refractometer portion of flowers, pollinated by different bee types, (Bellingham-Stanley). Only nectar volumes higher which set fruit as a quantitative and comparative than 0.17 microliters could be used for concentra- measure of the bees’ pollination success in the tion measurements. greenhouse. 512 A. Sadeh et al.

2.7. Data analysis 1,2 1

0,8

Most of the observations were combined into 0,6 seasons, deﬁned as spring (March–May), summer 0,4

(June–August), and autumn (September–October). 0,2 Exits / hour / foraging bee Each season includes 2–4 observation periods of 0 each bee species. The number of individual bees Spring Summer Autumn monitored varied greatly between observations: the Xylocopa Apis honeybee colonies contained several hundred individuals (albeit not all of them foraging at once), Figure 1. Mean (+SE) number of bee exits from the while each Xylocopa nest only contained one fe- nests for X. pubescens and A. mellifera. The ﬁgures male. The number of Xylocopa nests introduced are based on 266 observations, of 15 minutes each, into the greenhouse varied between observations as of nest exits. well. To allow comparisons between observations, we standardized them in two ways: 3. RESULTS

(a) When calculating daily activity patterns, we 3.1. General activity patterns calculated an hourly frequency distribution of / all individuals visits recorded in an observation Both X. pubescens and A. mellifera were ac- day (no matter by how many bees), such that tive in the greenhouse between April and Oc- all frequencies summed up to 1. We then calcu- tober, 2005. The frequency of exits from the lated average frequency distributions for each season and each bee species. nest per foraging bee increased for both bee species from spring to autumn, and was con- (b) When calculating nest exit frequencies, we sistently higher for X. pubescens than for A. counted the number of exits observed in a 15- melllifera (Fig. 1). These trends were only par- minute observation period, and multiplied the tially statistically significant: The frequency of count by four to obtain an estimate of the num- nest exits per forager was significantly affected ber of exits per hour. We then divided this es- by season for A. mellifera (ANOVA: F2,129 = timate by the mean number of active bees ob- . = . served outside the nest during the same hour, 4 613, P 0 012), but not for X. pubescens = . = . to obtain a nest exit rate per foraging bee. This (ANOVA: F2,129 1 415, P 0 247). The fre- estimate is independent of the number of bees quency of nest exits per forager did not dif- introduced into the greenhouse. After checking fer significantly between bee species in any for homogeneity of variances, we used two-way season (ANOVA: spring, F1,88 = 1.212, P = ANOVA to test the effects of bee species and 0.274, summer, F1,90 = 1.049, P = 0.361, season on nest exit rates. autumn, F1,79 = 0.083, P = 0.774). Neither was the difference significant when data from all seasons were combined (ANOVA: F1,262 = We used the Z-test to check whether the proportion 1.041, P = 0.309). of male flowers visited by a X. pubescens female differs from the proportion of males in the greenhouse. We used χ2 tests for independence to check whether the frequency of male- female flower tran- 3.2. Foraging on melon flowers sitions within a series of visits is consistent with random choice of flower sex. We obtained a P- Although both visitor species showed a value for each of the eight sequences of visits, and wide seasonal and daily activity range, they combined them using Fisher’s combined probabil- foraged on melon plants only part of the time. ity test. Both X. pubescens and honeybees foraged on We used SPSSTM version 13 for statistical anal- melon only during the morning hours (0600 h– yses, such as ANOVAs, correlations, t-tests, and χ2 1200 h). In spring, X. pubescens started forag- tests. ing earlier than the honeybees. Foraging rates Carpenter bees for greenhouse pollination 513

100% 80% 60% 40% 0,15 20% Visits (%) 0% 0,10 06:00 08:00 10:00 12:00 0,05

Hour 0,00 Nectar volume (µL) volume Nectar Xylocopa Apis mellifera 6:00-7:00 9:00-10:00 12:00-13:00 15:00-16:00 Hour 100% 80% 25,00 60% 20,00 40% 15,00 10,00 20% % Sucrose

Visits (%) 5,00 0% 0,00 06:00 08:00 10:00 12:00 6:00-7:00 9:00-10:00 12:00-13:00 15:00-16:00 Hour Hour Xylocopa Apis mellifera Figure 3. Mean (+SE) nectar production rates (top) 100% 80% and sucrose concentrations (bottom) of male (black 60% 40% bars) and female (white bars) flowers. Nectar pro- 20% Visits (%) 0% duction was recorded in 240 flowers. Concentra- 06:00 08:00 10:00 12:00 tions were determined in 101 flowers. Hour XylocopaXylocopa Apis mellifera 20

Figure 2. Frequency distribution of visits to melon 16 flowers along the activity hours, for X. pubescens 12 and A. mellifera, in spring (top), summer (middle) 8 and autumn (bottom). Data are based on 18, 28 and 16 observation days in spring, summer and autumn, 4 respectively. 0 Visit duration per flower (s) Spring Summer Autumn Xylocopa Apis varied significantly between hours of observa- Figure 4. Mean (+SE) duration of visits of X. tion, but were not significantly affected by bee pubescens (dark bars) and A. mellifera (white bars) species (GLM: Bee: F1 = 0.092, P = 0.764, on a melon flower (seconds) in each season. Data Hour: F3 = 6.941, P = 0.001, Fig. 2). Neither are based on 497 recorded visits. hour nor bee species affected foraging rates in melon in summer and in autumn (GLM: sum- . < . = mer: Bee: F1 = 2.298, P = 0.145, Hour: F5 = 245 07, P 0 001 for flower sex, F2,245 . = . 0.444, P = 0.812; autumn: Bee: F1 = 0.059, 0 481, P 0 696 for season). Flower sex and ff P = 0.812, Hour: F3 = 1.249, P = 0.812). season did not significantly a ect nectar con- Combined over both bee species, the daily dis- centration (two-way ANOVA: F1,97 = 0.696, tribution of visits did not differ between sea- P = 0.41, F2,97 = 0.181, P = 0.83 for season). sons (ANOVA: F2,21 = 0.000, P = 1.000). Average visit duration per flower was sig- The daily distribution of visits to melon nificantly higher for A. mellifera than for X. flowers was not significantly correlated with pubescens (GLM: F1 = 31.990, P < 0.001). nectar yield at any season, for either of the bee The differences in visit durations between the species. Nectar production rates were max- bees were less marked in autumn than in imal at 6 am, and somewhat decreased to- spring and summer (Fig. 4). Accordingly, the wards noon, while nectar concentrations did interaction between bee and season was highly not show a clear trend over the morning hours significant (GLM: F2 = 5.524, P = 0.004). (Fig. 3). Thus, the timing of bee foraging activ- Visit durations of A. mellifera were signifi- ity did not coincide with peak periods of nec- cantly affected by season (GLM: F2 = 6.250, tar secretion or concentration. Nectar produc- P = 0.002), but the effect of season on visit tion was significantly affected by flower sex, durations for X. pubescens was not significant but not by season (two-way ANOVA: F1,245 = (GLM: F2 = 2.849, P = 0.059). 514 A. Sadeh et al.

90 80 comparison to honeybees. Both species were 70 60 active in the greenhouse for several hours a 50 day throughout spring, summer and autumn. 40 30 Exit frequencies were consistently higher for No. flowers & fruit 20 51.4% X. pubescens than for A. mellifera in each sea- 10 17.1% 0 ff Xylocopa Apis son, but these di erences were not statistically significant. Figure 5. Number of ripening fruits (shaded part Thus, comparison of general activity in the of bars) as a percent of the total number of flowers greenhouse does not reveal a clear advantage available (whole length of bars) for pollination by of either of the pollinators over the other. X. pubescens and A. mellifera. Records of visits to melon flowers revealed that A. mellifera spent significantly more time visiting each flower than X. pubescens. Visit The proportions of foraging visits made by duration to melon flowers is expected to corre- X. pubescens to male flowers did not devi- late positively with pollination efficiency, be- ate significantly from the proportions of male cause bees may collect more pollen from a flowers in the greenhouse (Z7 = −0.33, P = . flower the longer they stay in it (Castellanos, 0 63). The bees’ selection of flower sex in a 2003; Kudo, 2003). The difference in visit du- series of successive visits was independent of ration thus suggests a possible advantage to their previous selection (χ2 = 18.31, P = . 16 A. mellifera in pollination. Contrary to this 0 31). This indicates that the bees switched prediction, however, fruit set was three times randomly between male and female flowers higher in flowers that were pollinated by X. during successive visits. pubescens than by A. mellifera. This highly significant difference suggests that honeybees are less efficient pollinators than X. pubescens, 3.3. Melon crop despite their longer durations of visits in flowers, and the large workforce in the colony. It Mean (±SD) fruit mass was 206.37 ± 60.44 should be noted, however, that the fruit set (n = 37) and 201.53 ± 73.72 (n = 14) for mel- due to both pollinator species in our study was ons arising from pollination by X. pubescens much lower than in commercial melon green- and A. mellifera, respectively. The mean seed houses. This is probably due to a large number number per fruit was 59.14 ± 48.87 for mel- of arthropod pests (mites, aphids and white- ons arising from X. pubescens pollination, and flies), which infested the greenhouse and re- 39.86±44.37 for fruit arising from A. mellifera duced plant vigor. pollination. These yield parameters were not Several explanations for X. pubescens’ ff = significantly a ected by pollinator type (t49 greater success in pollination come to mind. − . = . = 0 240, P 0 811 for fruit mass and t49 First, X. pubescens’ larger body size may en- − . = . 1 288, P 0 204 for seed number). Melon able better dusting with floral pollen. Sec- fruit set was, however, significantly higher for ond, X. pubescens may orient and navigate flowers that were pollinated by X. pubescens in enclosures better than honeybees. We ob- than for flowers that were pollinated by A. mel- served many disoriented honeybee foragers χ2 = . < . lifera ( (1) 13 702, P 0 0001, Fig. 5). outside the colony, while disorientation was only rarely observed in X. pubescens (unpubl. data). Third, honeybees accumulate excessive 4. DISCUSSION amounts of pollen, which may cause clogging of the stigmas in the pollen recipients. Finally, Apis mellifera is well known as an agricul- honeybees may remove pollen accumulated on tural pollinator of many crops (Cunningham their bodies while cleaning themselves, while et al., 2002). In the present study we evaluated X. pubescens’ grooming may be less efficient. X. pubescens as an alternative/additional polli- It is less likely that X. pubescens’ success owes nator for greenhouse crops in hot climates, in to their adaptation to the climatic conditions in Carpenter bees for greenhouse pollination 515 the greenhouse, because both species were ac- ison between honeybees and carpenter bees to tive at similar hours and seasons. other types of agricultural enclosures, and to The temporal distribution of visits did not open fields. Owing to its large body size, X. correlate with the patterns of floral nectar pro- pubescens mayalsoprovideeffective pollina- duction and yield for both pollinators, sug- tion to flowers that require sonication of the gesting that the bees’ activity schedule was anthers, such as tomatoes. Its pollination effi- not affected by the temporal pattern of food ciency should be compared to other buzz pol- available to them. Possibly, the bees’ activ- linators, such as Bombus terrestris. ity pattern is affected by abiotic factors, such The present study extends previous work as temperature, humidity and light intensity that demonstrates the feasibility of using local (Gottlieb et al., 2005). An additional possi- pollinator species for agricultural greenhouse bility is the bees’ activity patterns are regu- pollination (Hogendoorn et al., 2000, 2006; lated by an intrinsic circadian rhythm, as was Cauich et al., 2004; Del Sarto et al., 2005). A already demonstrated for honeybee foragers major obstacle to the commercial use of na- (Bloch and Robinson, 2001). It is also possible tive pollinators in agriculture is the need to that the bees were not allowed enough time to mass-rear them, rather than collect them from learn optimal timing for collection of nectar, as nature. Devising efficient and cost-effective they were introduced into the greenhouse for mass-rearing protocols for X. pubescens is a 2–3 days only in each observation session. necessary step in this direction. We also observed no preference for male or female melon flowers, and no tendency to visit flowers of the same sex in succession. ACKNOWLEDGEMENTS Such random foraging in respect to flower sex should enable pollen transfer from male to fe- This research was supported under Grant No. C21-046 funded by the U.S.-Israel Coop- male flowers, and thus increase the plants’ re- erative Development Research Program, Bureau productive success. for Economic Growth, Agriculture, and Trade, Our observations spanned X. pubescens’ U.S. Agency for International Development. Shauli annual activity period. The bees hibernate in Aviel generously supplied the melon plants. Two winter (Ben Mordechai et al., 1978; Gerling anonymous referees commented on a previous ver- et al., 1983), and therefore could not be com- sion of the MS. We thank Dan Weil, Ally Harari, pared with honeybees during this period. Pos- Michal Segoli, Daphna Gottlieb and Michal Shilo sible future domestication and commercial for helpful discussions. rearing of X. pubescens may lead to changes in the bees’ pattern of activity. A similar change L’Abeille charpentière Xylocopa pubescens in activity pattern was achieved for Bombus comme pollinisateur des cultures sous serre. terrestris: queens of this species hibernate in winter under natural conditions, but domes- Xylocopa pubescens / Apis mellifera / pollinisa- / / ticated queens can be induced to reproduce tion culture protégée Cucumis melo year-round (de Ruijter, 1999; Velthuis and van Doorn, 2006). Similar modification of X. Zusammenfassung – Die Holzbiene Xylocopa pu- pubescens’ activity pattern is likely possible, bescens als landwirtschaftlicher Bestäuber in because females occasionally break their hi- Gewächshäusern. Viele Nutzpflanzen sind von bernation on warm winter days in their natural Bienen als Bestäubern abhängig, besonders in Ge- wächshäusern. Die Populationen von Honigbienen habitat (Michener, 1990). Year-round activity, haben über die vergangenen Jahrzehnte durch den if feasible, may further increase X. pubescens’ Verlust von Habitaten, Krankheiten, Bekämpfungs- usefulness for agricultural pollination. mittel und andere Einwirkungen abgenommen. Als We conclude that X. pubescens and A. mel- Folge leiden viele landwirtschaftliche Pflanzen we- lifera are similar in many of their foraging pa- gen unzureichender Bestäubung unter verminder- ter Menge oder Qualität des Ertrags. Die begrenzte rameters, but the bottom line is that X. pub- Bestäubungsleistung von Honigbienen bei vielen scens was the better pollinator in terms of Gewächshauspflanzen ist ein zusätzlicher Anstoß, crop yield. We propose to extend the compar- weitere potentielle Bestäuber zu untersuchen. Die 516 A. Sadeh et al.

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