The Effect of Nest Box Distribution on Sustainable Propagation of Osmia lignaria (Hymenoptera: Megachilidae) in Commercial Tart Cherry Orchards

The Effect of Nest Box Distribution on Sustainable Propagation of Osmia lignaria (Hymenoptera:... The blue orchard bee, Osmia lignaria (Say), is a solitary bee that is an excellent pollinator of tree fruit orchards. Due to the annual rising costs of honey bee hive rentals, many orchardists are eager to develop management tools and practices to support O. lignaria as an alternative pollinator. Establishing O. lignaria pollination as a sustainable industry requires careful consideration of both bee and orchard management. Here, we test the effect of artificial nest box distribution on in-orchard propagation of O. lignaria in Utah commercial tart cherry orchards. Two nest box distributions were compared across three paired, 1.2-ha plots. One distribution, traditionally employed by O. lignaria consultants, included a centrally located tote for mass-nesting with smaller, surrounding ‘satellite’ nest boxes at orchard margins. The other distribution was composed of smaller, more equally distributed nest boxes throughout the 1.2-ha plots. Significantly higher propagation of O. lignaria was observed in the latter nest box distribution, although all treatments resulted in bee return exceeding the number of bees initially released. These findings provide support for the use of O. lignaria in tart cherry orchards, and demonstrate how simple changes to bee set-up and management can influence propagation efforts. Key words: blue orchard bee, commercial pollination, dispersal, Prunus cerasus, solitary bee Recent declines in honey bee colonies (Seitz et al. 2016), combined with honey bees significantly increases fruit set, and provides meas- with increasing demands for pollination services in agriculture (Aizen urable increases in nut yield (Artz et al. 2013, Brittain et al. 2013, and Harder 2009), have elicited renewed enthusiasm to develop man- unpublished data). Furthermore, O. lignaria show a strong prefer- agement strategies for alternative pollinators in many agricultural sys- ence for foraging on fruit trees (Bosch and Kemp 1999), highlighting tems. The blue orchard bee, Osmia lignaria (Say) (Hymenoptera: great potential for this species to contribute to pollination in Megachilidae), is a solitary, cavity nesting bee that has proven success- orchards. ful in providing pollination to spring-blooming orchard trees, including At present, current best management practices (BMPs) for using O. lignaria as pollinators of conventional, commercial orchards gen- apple, pear, almond, and cherry (Torchio 1979, 1985; Bosch and Kemp 1999; Sheffield 2014). Native across most of the United States erally fail to provide details concerning how to optimally arrange nesting sites and deploy the bees, based on orchard structure and its andSouthernCanada(Rust 1974)adult O. lignaria females reside in naturally occurring tunnels located in wood or hollow stems, but will management needs. For example, nesting site visibility and fre- readily nest in various artificial substrates, including cardboard tubes, quency may curtail the high rates of bee dispersal away from or- chards, which limits the number of in-orchard nesting females and paper straws, and drilled wood laminates in agricultural settings (re- viewed in Bosch and Kemp 2001; Fig. 1). retrieval of bee offspring for use the following year. Consequently, Osmia lignaria emergence can be manipulated to occur in syn- orchardists typically do not recover the same number of bees that chrony with bloom through the use of standardized temperature- they initially release (Artz et al. 2013, 2014). Pollination using O. controlled incubation practices. The combined ease of in-orchard lignaria in orchards often requires that a new bee supply is pur- management and flexibility with timing adult bee emergence makes chased annually, which in most cases is not economically feasible at O. lignaria particularly attractive as a possible alternative, commer- current costs. Developing BMPs that result in nesting rates that cially managed pollinator (Bosch et al. 2000, Bosch and Kemp match or exceed the initial number of bees released in commercial 2001). In almond orchards, the use of O. lignaria in combination orchards can dramatically decrease or eliminate the cost of Published by Oxford University Press on behalf of the Entomological Society of America 2017. This work is written by US Government employees and is in the public domain in the US. 1 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 2 Journal of Insect Science, 2017, Vol. 17, No. 2 Fig. 1. Three completed and X-radiographed O. lignaria nests. Adult female O. lignaria provision individual eggs with a mass of pollen and nectar, separated by mud partitions. Females (‘F’) are typically laid before males (‘M’) and can be identified by their large body size and the shape of their cocoon. Completed nests are easy to discern from the mud ‘plug’ visible at the end of the nest (end of nest on right side). Pollen ball (‘P’; nest 107) occurs when an individual fails to de- velop and the provision mass remains uneaten. replenishing annual O. lignaria populations. Identifying practices were released at the center of each plot from Styrofoam and plastic that improve annual in-orchard retention would have substantial emergence boxes (40  25  20 cm), situated 12 cm above implications for the economic viability of using this bee for commer- ground. The emergence boxes each had a small, 2-cm exit hole at cial pollination. Furthermore, sustainable in-orchard management the bottom from which adult bees could crawl through and fly of bee populations would reduce the need to collect additional bees away. Plastic, corrugated nest boxes were distributed in one of two from native wildlands, which has unknown impacts on wild different layouts (or treatments) within each experimental block O. lignaria populations. concurrently with O. lignaria bee releases: (1) A ‘Mail Tote/ Presently, some solitary bee suppliers recommend providing nest- Satellite’ (MTS) treatment and (2) a ‘Uniform’ (UF) treatment (Fig. ing cavities for O. lignaria from a centrally located, corrugated plas- 3). The MTS treatment consisted of a large, centrally located mail tic ‘mail tote’ (Cane 2006; Fig. 2a) along with smaller ‘satellite’ nest tote (described in Cane 2006; Fig. 2a) that supported 600 nesting boxes (Artz et al. 2013; Fig. 2b) placed on the field margins of the cavities. This layout included four small corner satellite nest boxes space requiring pollination (J. Watts, personal communication). as well (boxes described in Artz et al. 2013; Fig. 2b), each containing Previous studies that evaluate O. lignaria nesting in almond or- 100 cardboard nest tubes (15.3 cm in length  7 mm inner diameter, chards report higher nesting rates when many nest boxes, partially each lined with paper straw inserts) and situated 86 m from the cen- filled with nest tubes, are placed uniformly throughout the orchard tral tote. The UF treatment consisted of 10 small nest boxes, distrib- than when fewer nest boxes completely filled with nest tubes are uted evenly across two central rows within each replicate and uniformly provided (Artz et al. 2013, 2014). Nesting preference by containing 100 nesting cavities each (same as the previously O. lignaria females is also affected by other physical attributes such described satellite boxes; Fig. 2b). All nest boxes were blue in color as nest box color, height, orientation, and nest cavity diameter and installed at breast height with southeast-facing entrances. Both (Bosch et al. 2000, Artz et al. 2014, Boyle et al., unpublished data). treatments provided the same number of cavities (n ¼ 1000) to O. Thus, nest box style and distribution are simple and relatively inex- lignaria females in this experiment. A patented spray-on attractant pensive modifications that can have significant impacts on O. ligna- (Pitts-Singer et al. 2015), which was identified from O. lignaria co- ria reproduction in orchard environments (Artz et al. 2013, 2014). coons, was applied at a rate of 100 cocoon equivalents (105.77 mg The purpose of this study was to evaluate the use of O. lignaria as active ingredient ¼ one cocoon equivalent) per nest box by spritzing an alternative pollinator of tart cherry orchards in Utah while also it directly onto the outer ends of the cardboard tubes. Composed of sustaining, or enhancing, in-orchard populations. More specifically, a free fatty acid mixed into an ethyl acetate solvent, this attractant our interests were (1) whether O. lignaria populations can be sus- has been demonstrated to increase nesting when sprayed onto va- tainable in this system and (2) how changing the distribution of arti- cant cardboard tubes (Pitts-Singer et al. 2015; unpublished data). ficial nest boxes in cherry orchards can influence overall nesting Cherry bloom began 15 April 2016 and senesced around 30 success. April 2016. However, O. lignaria were permitted to mate and pro- vision their nests in the orchard through post-bloom until 17 May 2016 so that delicate, immature larvae would be able to develop Materials and Methods to less vulnerable stages prior to their removal (manipulation of This study took place in a 101-ha tart cherry (var. Montmorency on early instar O. lignaria can dislodge them from their provision 0 00 Mahelab root) orchard in Santaquin, Utah (GPS: 39 59 28.84 N, mass, resulting in mortality due to starvation; Bosch and Kemp 0 00 111 48 21.20 W). Within the orchard, two nest-box distributions 2001). No pesticide applications were made while the bees were (treatments; described below) were established across six 1.2-ha nesting, and nest boxes were removed from the orchards prior to plots (treatments were paired across three geographically distinct application of the first post-bloom nutritional spray (19 May ‘blocks’; Fig. 3). Because the typical foraging range of O. lignaria is 2016). In addition to introduced O. lignaria, honey bees were about 60 m (Rust 1974) radius from the nest site, each treatment present in the orchard at a standard rate of one hive per acre for was separated by at least 75 m to minimize bee drift into neighbor- the duration of bloom. ing experimental plots. Bees were provided by Watts Bees (Bothell, Upon their removal in mid-May, nest boxes were disassembled WA) in spring 2016 as loose-cell, overwintering adults in cocoons. and the cardboard tubes were evaluated immediately for occupancy They were stored at the USDA-ARS Pollinating Insects Research by visual inspection. Fully or partially completed nests were deter- Unit in darkness at 4 C until their release. At the onset of bloom (15 mined to be ‘occupied’, and occupancy was compared between nest April 2016), 825 female and 1,230 male just-emerging O. lignaria box distributions. Starting 9 June 2016, the nests with developing Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 Journal of Insect Science, 2017, Vol. 17, No. 2 3 Fig. 2. Two types of corrugated plastic nest boxes were used in this study: (a) a large, centrally located mail tote in the MTS treatment (600 cavities) and (b) smaller nest boxes that comprised ‘satellite’ boxes in the MTS treatment and all boxes in the uniformly distributed (UF) treatment (100 cavities). bees in cocoons from each treatment were X-radiographed to deter- cells were created from the original 5,000 females released into the mine the number of successfully completed live cells (or healthy co- orchards. Overall, an average 1.11 male to female sex ratio was ob- tained, which did not vary significantly by treatment (F ¼ 0.78; coons), and offspring sex ratio (by visual inspection of nest position and size; Fig. 1). Statistical comparisons between treatments were df ¼ 5; P ¼ 0.47). While cavity occupancy did not reveal significantly conducted using one-way ANOVAs, blocked by replicate (JMP, SAS higher nesting between treatments (F ¼ 3.71; df ¼ 2; P ¼ 0.194), we Institute 2015). did observe significantly more live cells (F ¼ 18.79; df ¼ 1; P ¼ 0.0494) produced in UF treatment over the MTS treatment (Table 1). This discrepancy results from a combination of a slightly Results and Discussion higher number of cells per nest in the UF treatment (4.73 average Despite the short bloom time of cherries (about 2 wk in this or- cells per nest) over the MTS treatment (4.34 cells per nest) and nu- chard), O. lignaria nested successfully and in large numbers. merically higher occupancy in UF (Table 1). Block did not affect Regardless of treatment, reproduction of female O. lignaria sur- nesting occupancy (F ¼ 1.34; df ¼ 2; P ¼ 0.43) or live cell production passed the initial number of bees released into the orchard, resulting (F ¼ 13.94; df ¼ 2; P ¼ 0.067). In cherries, it appears best to distrib- in a 1.6-fold increase in bees across treatments. In total, 19,336 live ute nest boxes uniformly throughout the orchard rather than rely on Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 4 Journal of Insect Science, 2017, Vol. 17, No. 2 Fig. 3. Nest box placement throughout tart cherry orchards in Santaquin, UT. Each white marker indicates the location of a small nest box. Orange markers indi- cate mail tote locations. Solid lines outline the MTS treatment (n ¼ 3). Dashed lines outline the uniform (UF) nest box distribution treatment (n ¼ 3). O. lignaria fe- males were released at the center of each plot. a central nesting location with satellite boxes on orchard block in cases where pesticides are routinely applied during or just after margins. bloom. Previous attempts to incorporate O. lignaria as cherry orchard Because the native range of O. lignaria overlaps with our study pollinators have reported extremely successful nesting of in-orchard site, there is a possibility that some of the bees nesting in these or- bee populations and significantly increased cherry yield where they chards were from local, wild populations. However, due to the in- are used (Bosch et al. 2006), although these earlier trials were lim- tensive management strategies employed in conventional ited to one small 1.4-ha orchard over several years. In addition, this commercial orchards (including frequent agrochemical applications) smaller orchard received limited chemical inputs and was located in and short cherry bloom window, it is improbable that the local en- a semi-agricultural area. To our knowledge, our study is the first sci- vironment would be capable of sustaining large, stable populations entific report of successful O. lignaria propagation in conventional, of O. lignaria over time. commercially managed tart cherry orchards in Utah, suggesting that On the day of nest removal from the orchard, no adult O. ligna- it could be an excellent target crop for future O. lignaria ria were observed. This is likely a consequence of limited available application. forage to the bees immediately following bloom. In the presence of As with many tart cherry varieties that are commercially pro- alternative floral resources (combined with careful pesticide use), duced, Montmorency cherries are not entirely reliant on insect pol- the foraging window for O. lignaria can extend beyond crop bloom, lination, as they are partially self-compatible and capable of setting which has been shown to have positive impacts on bee propagation fruit without cross-pollination. However, this variety, along with (Sheffield et al. 2008, unpublished data). many others that are grown commercially in the United States do Presently, the greatest challenge in using O. lignaria for commer- benefit substantially from bee visitation (Lansari and Iezzoni 1990), cial pollination is their limited supply. O. lignaria are primarily ob- which is why honey bee hives are frequently interspersed throughout tained by wild trapping, in which ‘trappers’ place artificial nest these orchards. Considering the use of an optional (Scott-Dupree cavities in regions where they are known to aggregate (predomin- et al. 1999) stocking rate of one hive per acre, O. lignaria may be a antly in high elevation areas of Utah, Idaho, and Washington). At viable alternative or complimentary candidate for providing pollin- the end of nesting, wild-caught bees are sorted and processed for ation services in this system. However, due to the sensitivity of O. storage at 3–5 C over the winter months as adults in cocoons. lignaria to pesticide exposure (e.g., Biddinger et al. 2013, Artz and Subsequently, they are sold and distributed to local farm stores or directly to orchardists. Management practices to date are labor- Pitts-Singer 2015) and the practicalities concerning the timing of nest removal from orchards, the use of this pollinator requires care intensive and expensive, which results in impractically high retail Table 1. Mean (6 SE) nest occupancy and live cell count of O. lignaria reproduction by treatment N Mean nest occupancy, % 6 SE Mean live cells, 6 SE Average cells per nest Uniform treatment 3 80.6 6 8.2 3,812.0 6 562.5 4.73 MTS treatment 3 60.7 6 2.1 2,633.3 6 501.6 4.34 Percent occupancy is a total percentage of all nest straws available at each site (n ¼ 1,000 per site). Male-to-female ratio did not vary between treatments. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 Journal of Insect Science, 2017, Vol. 17, No. 2 5 Bosch, J., and W. P. Kemp. 1999. Exceptional cherry production in an orchard prices of O. lignaria for pollination (typical 2016 costs were upwards pollinated with blue orchard bees. Bee World. 80: 163–173. of $1 per female USD; J. Watts, personal communication) on a com- Bosch, J., and W. P. Kemp. 2001. How to manage the Blue Orchard bee as an mercial scale. With a suggested stocking rate of 250 females per acre orchard pollinator. Sustainable Agricultural Network, Handbook No. 5, (618 females per ha) (Bosch and Kemp 2001), commercial O. lignaria Beltsville, MD. pollination will only be economically feasible if sustainable year-to- Bosch, J., W. P. Kemp, and S. S. Peterson. 2000. Management of Osmia ligna- year reproduction within orchards is achieved. This study provides ria (Hymenoptera: Megachilidae) populations for almond pollination: the kind of nuanced detail in O. lignaria management needed for im- methods to advance bee emergence. Environ. Entomol. 29: 874–883. proving BMPs that will lead to sustainable O. lignaria reproduction Bosch, J., W. P. Kemp, and G. E. Trostle. 2006. Bee population returns and within tart cherry orchards. Overall, results obtained from this study cherry yields in an orchard pollinated with Osmia lignaria (Hymenoptera: are provocative, and further evaluation to examine pollination effi- Megachilidae). J. Econ. Entomol. 99: 408–412. Brittain, C., N. Williams, C. Kremen, and A.-M. Klein. 2013. Synergistic ef- cacy of O. lignaria in commercial cherry orchards is needed. fects of non-Apis and honey bees for pollination services. Proc. R. Soc. Lond. . 280: 20122767. Cane, J. 2006. The Logan BeeMail Shelter: a practical, portable unit for man- Acknowledgments aging cavity-nesting pollinators. Am. Bee J. 146: 611–613. This study would not have been possible without incredible support and as- Lansari, A., and A. Iezzoni. 1990. A preliminary analysis of self- sistance provided by Jim Watts, who provided the bees and the premise for incompatibility in sour cherry. Hort. Sci. 25: 1636–1638. this study, and Ray Rowley who allowed us to work in his cherry orchards. Pitts-Singer, T. L., W. P. Kemp, D. Moreland, S. Peterson, J. S. Buckner, and We would also like to thank ARS laboratory technicians and science aids, M. Hagen. 2015. U.S. Patent. Bee Attractants. Approved December. Ellen Klomps, Jenna Hanson, Hannah Jarvis, Penina Meatoga, and Matthew Rust, R. W. 1974. The systematics and biology of the genus Osmia, subgenera Treasure for help in executing the study and processing much of the data dis- Osmia, Chalcosmia, and Cephalosmia (Hymenoptera: Megachilidae). cussed in this manuscript. Wasmann J. Biol. 32: 1–93. SAS Institute 2015. JMPV, Version 12. SAS Institute, Cary, NC. Scott-Dupree, C., M. Winston, G. Hergert, S. C. Jay, D. Nelson, J. Gates, B. References Cited Termeer, and G. Otis. 1999. A guide to: managing bees for crop pollination. Aizen, M. A., and L. D. Harder. 2009. The global stock of domesticated honey Canadian Association of Professional Apiculturalists, Vancouver, British bees is growing slower than agricultural demand for pollination. Curr. Biol. Columbia. 19: 915–918. Seitz, N., K. S. Traynor, N. Steinhauer, K. Rennich, M. E. Wilson, J. D. Ellis, Artz, D. R., and T. L. Pitts-Singer. 2015. Effects of fungicide and adjuvant R. Rose, D. R. Tarpy, R. R. Sagili, D. M. Caron, et al. 2016. A national sur- sprays on nesting behavior in two managed solitary bees, Osmia lignaria vey of managed honey bee 2014–2015 annual colony losses in the USA. J. and Megachile rotundata. PLoS One. 10: e0135688. Apic. Res. . 54: 292–304. Artz, D. R., M. J. Allan, G. I. Wardell, and T. L. Pitts-Singer. 2013. Nesting Sheffield, C. S. 2014. Pollination, seed set and fruit quality in apple: studies site density and distribution affects Osmia lignaria (Hymenoptera: with Osmia lignaria (Hymenoptera: Megachilidae) in the Annapolis Valley, Megachilidae) reproductive success and almond yield in a commercial or- Nova Scotia. Can. J. Poll. Ecol. 12: 120–128. chard. Insect Conserv. Divers. 6: 715–724. Sheffield, C. S., S. M. Westby, R. F. Smith, and P. G. Kevan. 2008. Potential of Artz, D. R., M. J. Allan, G. I. Wardell, and T. L. Pitts-Singer. 2014. Influence bigleaf lupine for building and sustaining Osmia lignaria populations for of nest box color and release sites on Osmia lignaria (Hymenoptera: pollination of apple. Can Entomol. 140: 589–599. Megachilidae) reproductive success in a commercial almond orchard. J. Torchio, P. F. 1979. Use of Osmia lignaria Say as a pollinator of caged almond Econ. Entomol. 107: 2045–2054. in California. Md. Agric. Exp. Stat. Spec. Misc. Publ. 1: 285–293. Biddinger, D. J., J. L. Robertson, C. Mullin, J. Frazier, S. A. Ashcraft, E. G. Torchio, P. F. 1985. Field experiments with the pollinator species, Osmia Rajotte, N. K. Joshi, and M. Vaughan. 2013. Comparative toxicities and lignaria propinqua Cresson in apple orchards: V, (1979–1980), method of synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cor- introducing bees, nesting success, seed counts, fruit yields (Hymenoptera: nifrons (Radoszkowski). PLoS One. 8: e72587. Megachilidae). J. Kans. Entomol. Soc. 58: 448–464. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Insect Science Oxford University Press

The Effect of Nest Box Distribution on Sustainable Propagation of Osmia lignaria (Hymenoptera: Megachilidae) in Commercial Tart Cherry Orchards

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Abstract

The blue orchard bee, Osmia lignaria (Say), is a solitary bee that is an excellent pollinator of tree fruit orchards. Due to the annual rising costs of honey bee hive rentals, many orchardists are eager to develop management tools and practices to support O. lignaria as an alternative pollinator. Establishing O. lignaria pollination as a sustainable industry requires careful consideration of both bee and orchard management. Here, we test the effect of artificial nest box distribution on in-orchard propagation of O. lignaria in Utah commercial tart cherry orchards. Two nest box distributions were compared across three paired, 1.2-ha plots. One distribution, traditionally employed by O. lignaria consultants, included a centrally located tote for mass-nesting with smaller, surrounding ‘satellite’ nest boxes at orchard margins. The other distribution was composed of smaller, more equally distributed nest boxes throughout the 1.2-ha plots. Significantly higher propagation of O. lignaria was observed in the latter nest box distribution, although all treatments resulted in bee return exceeding the number of bees initially released. These findings provide support for the use of O. lignaria in tart cherry orchards, and demonstrate how simple changes to bee set-up and management can influence propagation efforts. Key words: blue orchard bee, commercial pollination, dispersal, Prunus cerasus, solitary bee Recent declines in honey bee colonies (Seitz et al. 2016), combined with honey bees significantly increases fruit set, and provides meas- with increasing demands for pollination services in agriculture (Aizen urable increases in nut yield (Artz et al. 2013, Brittain et al. 2013, and Harder 2009), have elicited renewed enthusiasm to develop man- unpublished data). Furthermore, O. lignaria show a strong prefer- agement strategies for alternative pollinators in many agricultural sys- ence for foraging on fruit trees (Bosch and Kemp 1999), highlighting tems. The blue orchard bee, Osmia lignaria (Say) (Hymenoptera: great potential for this species to contribute to pollination in Megachilidae), is a solitary, cavity nesting bee that has proven success- orchards. ful in providing pollination to spring-blooming orchard trees, including At present, current best management practices (BMPs) for using O. lignaria as pollinators of conventional, commercial orchards gen- apple, pear, almond, and cherry (Torchio 1979, 1985; Bosch and Kemp 1999; Sheffield 2014). Native across most of the United States erally fail to provide details concerning how to optimally arrange nesting sites and deploy the bees, based on orchard structure and its andSouthernCanada(Rust 1974)adult O. lignaria females reside in naturally occurring tunnels located in wood or hollow stems, but will management needs. For example, nesting site visibility and fre- readily nest in various artificial substrates, including cardboard tubes, quency may curtail the high rates of bee dispersal away from or- chards, which limits the number of in-orchard nesting females and paper straws, and drilled wood laminates in agricultural settings (re- viewed in Bosch and Kemp 2001; Fig. 1). retrieval of bee offspring for use the following year. Consequently, Osmia lignaria emergence can be manipulated to occur in syn- orchardists typically do not recover the same number of bees that chrony with bloom through the use of standardized temperature- they initially release (Artz et al. 2013, 2014). Pollination using O. controlled incubation practices. The combined ease of in-orchard lignaria in orchards often requires that a new bee supply is pur- management and flexibility with timing adult bee emergence makes chased annually, which in most cases is not economically feasible at O. lignaria particularly attractive as a possible alternative, commer- current costs. Developing BMPs that result in nesting rates that cially managed pollinator (Bosch et al. 2000, Bosch and Kemp match or exceed the initial number of bees released in commercial 2001). In almond orchards, the use of O. lignaria in combination orchards can dramatically decrease or eliminate the cost of Published by Oxford University Press on behalf of the Entomological Society of America 2017. This work is written by US Government employees and is in the public domain in the US. 1 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 2 Journal of Insect Science, 2017, Vol. 17, No. 2 Fig. 1. Three completed and X-radiographed O. lignaria nests. Adult female O. lignaria provision individual eggs with a mass of pollen and nectar, separated by mud partitions. Females (‘F’) are typically laid before males (‘M’) and can be identified by their large body size and the shape of their cocoon. Completed nests are easy to discern from the mud ‘plug’ visible at the end of the nest (end of nest on right side). Pollen ball (‘P’; nest 107) occurs when an individual fails to de- velop and the provision mass remains uneaten. replenishing annual O. lignaria populations. Identifying practices were released at the center of each plot from Styrofoam and plastic that improve annual in-orchard retention would have substantial emergence boxes (40  25  20 cm), situated 12 cm above implications for the economic viability of using this bee for commer- ground. The emergence boxes each had a small, 2-cm exit hole at cial pollination. Furthermore, sustainable in-orchard management the bottom from which adult bees could crawl through and fly of bee populations would reduce the need to collect additional bees away. Plastic, corrugated nest boxes were distributed in one of two from native wildlands, which has unknown impacts on wild different layouts (or treatments) within each experimental block O. lignaria populations. concurrently with O. lignaria bee releases: (1) A ‘Mail Tote/ Presently, some solitary bee suppliers recommend providing nest- Satellite’ (MTS) treatment and (2) a ‘Uniform’ (UF) treatment (Fig. ing cavities for O. lignaria from a centrally located, corrugated plas- 3). The MTS treatment consisted of a large, centrally located mail tic ‘mail tote’ (Cane 2006; Fig. 2a) along with smaller ‘satellite’ nest tote (described in Cane 2006; Fig. 2a) that supported 600 nesting boxes (Artz et al. 2013; Fig. 2b) placed on the field margins of the cavities. This layout included four small corner satellite nest boxes space requiring pollination (J. Watts, personal communication). as well (boxes described in Artz et al. 2013; Fig. 2b), each containing Previous studies that evaluate O. lignaria nesting in almond or- 100 cardboard nest tubes (15.3 cm in length  7 mm inner diameter, chards report higher nesting rates when many nest boxes, partially each lined with paper straw inserts) and situated 86 m from the cen- filled with nest tubes, are placed uniformly throughout the orchard tral tote. The UF treatment consisted of 10 small nest boxes, distrib- than when fewer nest boxes completely filled with nest tubes are uted evenly across two central rows within each replicate and uniformly provided (Artz et al. 2013, 2014). Nesting preference by containing 100 nesting cavities each (same as the previously O. lignaria females is also affected by other physical attributes such described satellite boxes; Fig. 2b). All nest boxes were blue in color as nest box color, height, orientation, and nest cavity diameter and installed at breast height with southeast-facing entrances. Both (Bosch et al. 2000, Artz et al. 2014, Boyle et al., unpublished data). treatments provided the same number of cavities (n ¼ 1000) to O. Thus, nest box style and distribution are simple and relatively inex- lignaria females in this experiment. A patented spray-on attractant pensive modifications that can have significant impacts on O. ligna- (Pitts-Singer et al. 2015), which was identified from O. lignaria co- ria reproduction in orchard environments (Artz et al. 2013, 2014). coons, was applied at a rate of 100 cocoon equivalents (105.77 mg The purpose of this study was to evaluate the use of O. lignaria as active ingredient ¼ one cocoon equivalent) per nest box by spritzing an alternative pollinator of tart cherry orchards in Utah while also it directly onto the outer ends of the cardboard tubes. Composed of sustaining, or enhancing, in-orchard populations. More specifically, a free fatty acid mixed into an ethyl acetate solvent, this attractant our interests were (1) whether O. lignaria populations can be sus- has been demonstrated to increase nesting when sprayed onto va- tainable in this system and (2) how changing the distribution of arti- cant cardboard tubes (Pitts-Singer et al. 2015; unpublished data). ficial nest boxes in cherry orchards can influence overall nesting Cherry bloom began 15 April 2016 and senesced around 30 success. April 2016. However, O. lignaria were permitted to mate and pro- vision their nests in the orchard through post-bloom until 17 May 2016 so that delicate, immature larvae would be able to develop Materials and Methods to less vulnerable stages prior to their removal (manipulation of This study took place in a 101-ha tart cherry (var. Montmorency on early instar O. lignaria can dislodge them from their provision 0 00 Mahelab root) orchard in Santaquin, Utah (GPS: 39 59 28.84 N, mass, resulting in mortality due to starvation; Bosch and Kemp 0 00 111 48 21.20 W). Within the orchard, two nest-box distributions 2001). No pesticide applications were made while the bees were (treatments; described below) were established across six 1.2-ha nesting, and nest boxes were removed from the orchards prior to plots (treatments were paired across three geographically distinct application of the first post-bloom nutritional spray (19 May ‘blocks’; Fig. 3). Because the typical foraging range of O. lignaria is 2016). In addition to introduced O. lignaria, honey bees were about 60 m (Rust 1974) radius from the nest site, each treatment present in the orchard at a standard rate of one hive per acre for was separated by at least 75 m to minimize bee drift into neighbor- the duration of bloom. ing experimental plots. Bees were provided by Watts Bees (Bothell, Upon their removal in mid-May, nest boxes were disassembled WA) in spring 2016 as loose-cell, overwintering adults in cocoons. and the cardboard tubes were evaluated immediately for occupancy They were stored at the USDA-ARS Pollinating Insects Research by visual inspection. Fully or partially completed nests were deter- Unit in darkness at 4 C until their release. At the onset of bloom (15 mined to be ‘occupied’, and occupancy was compared between nest April 2016), 825 female and 1,230 male just-emerging O. lignaria box distributions. Starting 9 June 2016, the nests with developing Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 Journal of Insect Science, 2017, Vol. 17, No. 2 3 Fig. 2. Two types of corrugated plastic nest boxes were used in this study: (a) a large, centrally located mail tote in the MTS treatment (600 cavities) and (b) smaller nest boxes that comprised ‘satellite’ boxes in the MTS treatment and all boxes in the uniformly distributed (UF) treatment (100 cavities). bees in cocoons from each treatment were X-radiographed to deter- cells were created from the original 5,000 females released into the mine the number of successfully completed live cells (or healthy co- orchards. Overall, an average 1.11 male to female sex ratio was ob- tained, which did not vary significantly by treatment (F ¼ 0.78; coons), and offspring sex ratio (by visual inspection of nest position and size; Fig. 1). Statistical comparisons between treatments were df ¼ 5; P ¼ 0.47). While cavity occupancy did not reveal significantly conducted using one-way ANOVAs, blocked by replicate (JMP, SAS higher nesting between treatments (F ¼ 3.71; df ¼ 2; P ¼ 0.194), we Institute 2015). did observe significantly more live cells (F ¼ 18.79; df ¼ 1; P ¼ 0.0494) produced in UF treatment over the MTS treatment (Table 1). This discrepancy results from a combination of a slightly Results and Discussion higher number of cells per nest in the UF treatment (4.73 average Despite the short bloom time of cherries (about 2 wk in this or- cells per nest) over the MTS treatment (4.34 cells per nest) and nu- chard), O. lignaria nested successfully and in large numbers. merically higher occupancy in UF (Table 1). Block did not affect Regardless of treatment, reproduction of female O. lignaria sur- nesting occupancy (F ¼ 1.34; df ¼ 2; P ¼ 0.43) or live cell production passed the initial number of bees released into the orchard, resulting (F ¼ 13.94; df ¼ 2; P ¼ 0.067). In cherries, it appears best to distrib- in a 1.6-fold increase in bees across treatments. In total, 19,336 live ute nest boxes uniformly throughout the orchard rather than rely on Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 4 Journal of Insect Science, 2017, Vol. 17, No. 2 Fig. 3. Nest box placement throughout tart cherry orchards in Santaquin, UT. Each white marker indicates the location of a small nest box. Orange markers indi- cate mail tote locations. Solid lines outline the MTS treatment (n ¼ 3). Dashed lines outline the uniform (UF) nest box distribution treatment (n ¼ 3). O. lignaria fe- males were released at the center of each plot. a central nesting location with satellite boxes on orchard block in cases where pesticides are routinely applied during or just after margins. bloom. Previous attempts to incorporate O. lignaria as cherry orchard Because the native range of O. lignaria overlaps with our study pollinators have reported extremely successful nesting of in-orchard site, there is a possibility that some of the bees nesting in these or- bee populations and significantly increased cherry yield where they chards were from local, wild populations. However, due to the in- are used (Bosch et al. 2006), although these earlier trials were lim- tensive management strategies employed in conventional ited to one small 1.4-ha orchard over several years. In addition, this commercial orchards (including frequent agrochemical applications) smaller orchard received limited chemical inputs and was located in and short cherry bloom window, it is improbable that the local en- a semi-agricultural area. To our knowledge, our study is the first sci- vironment would be capable of sustaining large, stable populations entific report of successful O. lignaria propagation in conventional, of O. lignaria over time. commercially managed tart cherry orchards in Utah, suggesting that On the day of nest removal from the orchard, no adult O. ligna- it could be an excellent target crop for future O. lignaria ria were observed. This is likely a consequence of limited available application. forage to the bees immediately following bloom. In the presence of As with many tart cherry varieties that are commercially pro- alternative floral resources (combined with careful pesticide use), duced, Montmorency cherries are not entirely reliant on insect pol- the foraging window for O. lignaria can extend beyond crop bloom, lination, as they are partially self-compatible and capable of setting which has been shown to have positive impacts on bee propagation fruit without cross-pollination. However, this variety, along with (Sheffield et al. 2008, unpublished data). many others that are grown commercially in the United States do Presently, the greatest challenge in using O. lignaria for commer- benefit substantially from bee visitation (Lansari and Iezzoni 1990), cial pollination is their limited supply. O. lignaria are primarily ob- which is why honey bee hives are frequently interspersed throughout tained by wild trapping, in which ‘trappers’ place artificial nest these orchards. Considering the use of an optional (Scott-Dupree cavities in regions where they are known to aggregate (predomin- et al. 1999) stocking rate of one hive per acre, O. lignaria may be a antly in high elevation areas of Utah, Idaho, and Washington). At viable alternative or complimentary candidate for providing pollin- the end of nesting, wild-caught bees are sorted and processed for ation services in this system. However, due to the sensitivity of O. storage at 3–5 C over the winter months as adults in cocoons. lignaria to pesticide exposure (e.g., Biddinger et al. 2013, Artz and Subsequently, they are sold and distributed to local farm stores or directly to orchardists. Management practices to date are labor- Pitts-Singer 2015) and the practicalities concerning the timing of nest removal from orchards, the use of this pollinator requires care intensive and expensive, which results in impractically high retail Table 1. Mean (6 SE) nest occupancy and live cell count of O. lignaria reproduction by treatment N Mean nest occupancy, % 6 SE Mean live cells, 6 SE Average cells per nest Uniform treatment 3 80.6 6 8.2 3,812.0 6 562.5 4.73 MTS treatment 3 60.7 6 2.1 2,633.3 6 501.6 4.34 Percent occupancy is a total percentage of all nest straws available at each site (n ¼ 1,000 per site). Male-to-female ratio did not vary between treatments. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018 Journal of Insect Science, 2017, Vol. 17, No. 2 5 Bosch, J., and W. P. Kemp. 1999. Exceptional cherry production in an orchard prices of O. lignaria for pollination (typical 2016 costs were upwards pollinated with blue orchard bees. Bee World. 80: 163–173. of $1 per female USD; J. Watts, personal communication) on a com- Bosch, J., and W. P. Kemp. 2001. How to manage the Blue Orchard bee as an mercial scale. With a suggested stocking rate of 250 females per acre orchard pollinator. Sustainable Agricultural Network, Handbook No. 5, (618 females per ha) (Bosch and Kemp 2001), commercial O. lignaria Beltsville, MD. pollination will only be economically feasible if sustainable year-to- Bosch, J., W. P. Kemp, and S. S. Peterson. 2000. Management of Osmia ligna- year reproduction within orchards is achieved. This study provides ria (Hymenoptera: Megachilidae) populations for almond pollination: the kind of nuanced detail in O. lignaria management needed for im- methods to advance bee emergence. Environ. Entomol. 29: 874–883. proving BMPs that will lead to sustainable O. lignaria reproduction Bosch, J., W. P. Kemp, and G. E. Trostle. 2006. Bee population returns and within tart cherry orchards. Overall, results obtained from this study cherry yields in an orchard pollinated with Osmia lignaria (Hymenoptera: are provocative, and further evaluation to examine pollination effi- Megachilidae). J. Econ. Entomol. 99: 408–412. Brittain, C., N. Williams, C. Kremen, and A.-M. Klein. 2013. Synergistic ef- cacy of O. lignaria in commercial cherry orchards is needed. fects of non-Apis and honey bees for pollination services. Proc. R. Soc. Lond. . 280: 20122767. Cane, J. 2006. The Logan BeeMail Shelter: a practical, portable unit for man- Acknowledgments aging cavity-nesting pollinators. Am. Bee J. 146: 611–613. This study would not have been possible without incredible support and as- Lansari, A., and A. Iezzoni. 1990. A preliminary analysis of self- sistance provided by Jim Watts, who provided the bees and the premise for incompatibility in sour cherry. Hort. Sci. 25: 1636–1638. this study, and Ray Rowley who allowed us to work in his cherry orchards. Pitts-Singer, T. L., W. P. Kemp, D. Moreland, S. Peterson, J. S. Buckner, and We would also like to thank ARS laboratory technicians and science aids, M. Hagen. 2015. U.S. Patent. Bee Attractants. Approved December. Ellen Klomps, Jenna Hanson, Hannah Jarvis, Penina Meatoga, and Matthew Rust, R. W. 1974. The systematics and biology of the genus Osmia, subgenera Treasure for help in executing the study and processing much of the data dis- Osmia, Chalcosmia, and Cephalosmia (Hymenoptera: Megachilidae). cussed in this manuscript. Wasmann J. Biol. 32: 1–93. SAS Institute 2015. JMPV, Version 12. SAS Institute, Cary, NC. Scott-Dupree, C., M. Winston, G. Hergert, S. C. Jay, D. Nelson, J. Gates, B. References Cited Termeer, and G. Otis. 1999. A guide to: managing bees for crop pollination. Aizen, M. A., and L. D. Harder. 2009. The global stock of domesticated honey Canadian Association of Professional Apiculturalists, Vancouver, British bees is growing slower than agricultural demand for pollination. Curr. Biol. Columbia. 19: 915–918. Seitz, N., K. S. Traynor, N. Steinhauer, K. Rennich, M. E. Wilson, J. D. Ellis, Artz, D. R., and T. L. Pitts-Singer. 2015. Effects of fungicide and adjuvant R. Rose, D. R. Tarpy, R. R. Sagili, D. M. Caron, et al. 2016. A national sur- sprays on nesting behavior in two managed solitary bees, Osmia lignaria vey of managed honey bee 2014–2015 annual colony losses in the USA. J. and Megachile rotundata. PLoS One. 10: e0135688. Apic. Res. . 54: 292–304. Artz, D. R., M. J. Allan, G. I. Wardell, and T. L. Pitts-Singer. 2013. Nesting Sheffield, C. S. 2014. Pollination, seed set and fruit quality in apple: studies site density and distribution affects Osmia lignaria (Hymenoptera: with Osmia lignaria (Hymenoptera: Megachilidae) in the Annapolis Valley, Megachilidae) reproductive success and almond yield in a commercial or- Nova Scotia. Can. J. Poll. Ecol. 12: 120–128. chard. Insect Conserv. Divers. 6: 715–724. Sheffield, C. S., S. M. Westby, R. F. Smith, and P. G. Kevan. 2008. Potential of Artz, D. R., M. J. Allan, G. I. Wardell, and T. L. Pitts-Singer. 2014. Influence bigleaf lupine for building and sustaining Osmia lignaria populations for of nest box color and release sites on Osmia lignaria (Hymenoptera: pollination of apple. Can Entomol. 140: 589–599. Megachilidae) reproductive success in a commercial almond orchard. J. Torchio, P. F. 1979. Use of Osmia lignaria Say as a pollinator of caged almond Econ. Entomol. 107: 2045–2054. in California. Md. Agric. Exp. Stat. Spec. Misc. Publ. 1: 285–293. Biddinger, D. J., J. L. Robertson, C. Mullin, J. Frazier, S. A. Ashcraft, E. G. Torchio, P. F. 1985. Field experiments with the pollinator species, Osmia Rajotte, N. K. Joshi, and M. Vaughan. 2013. Comparative toxicities and lignaria propinqua Cresson in apple orchards: V, (1979–1980), method of synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cor- introducing bees, nesting success, seed counts, fruit yields (Hymenoptera: nifrons (Radoszkowski). PLoS One. 8: e72587. Megachilidae). J. Kans. Entomol. Soc. 58: 448–464. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/17/2/41/3074742 by Ed 'DeepDyve' Gillespie user on 17 July 2018

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Journal of Insect ScienceOxford University Press

Published: Mar 30, 2017

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