Performance of Apis Mellifera, Bombus Impatiens, and Peponapis Pruinosa (Hymenoptera: Apidae) As Pollinators of Pumpkin Author(S): Derek R

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Performance of Apis mellifera, Bombus impatiens, and Peponapis pruinosa (Hymenoptera: Apidae) as Pollinators of Pumpkin Author(s): Derek R. Artz and Brian A. Nault Source: Journal of Economic Entomology, 104(4):1153-1161. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/EC10431 URL: http://www.bioone.org/doi/full/10.1603/EC10431

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. APICULTURE AND SOCIAL INSECTS Performance of Apis mellifera, Bombus impatiens, and Peponapis pruinosa (Hymenoptera: Apidae) as Pollinators of Pumpkin

1,2,3 1 DEREK R. ARTZ AND BRIAN A. NAULT

Department of Entomology, Cornell University, New York State Agricultural Experiment Station, 630 W. North Street, Geneva, NY 14456

J. Econ. Entomol. 104(4): 1153Ð1161 (2011); DOI: 10.1603/EC10431 ABSTRACT Pollination services of pumpkin, Cucurbita pepo L., provided by the European honey bee, Apis mellifera L., were compared with two native bee species, the common eastern bumble bee, Bombus impatiens (Cresson), and Peponapis pruinosa Say, in New York from 2008 to 2010. Performance of each species was determined by comparing single-visit pollen deposition, percentage of visits that contacted the stigma, ßower-handling time, fruit and seed set, and fruit weight per number of visits. Fruit yield from small Þelds (0.6 ha) supplemented with commercial B. impatiens colonies was compared with yield from those not supplemented. A. mellifera spent nearly 2 and 3 times longer foraging on each pistillate ßower compared with B. impatiens and P. pruinosa, respectively. A. mellifera also visited pistillate ßowers 10Ð20 times more frequently than B. impatiens and P. pruinosa, respectively. Yet, B. impatiens deposited 3 times more pollen grains per stigma and contacted stigmas signiÞcantly more often than either A. mellifera or P. pruinosa. Fruit set and weight from ßowers visited four to eight times by B. impatiens were similar to those from open-pollinated ßowers, whereas ßowers pollinated by A. mellifera and P. pruinosa produced fewer fruit and smaller fruit compared with those from open-pollinated ßowers. Fields supplemented with B. impatiens produced signiÞcantly more pumpkins per plant than nonsupplemented Þelds. B. impatiens was a better pollinator of pumpkin than P. pruinosa and should be considered as a promising alternative to A. mellifera for pollinating this crop.

KEY WORDS European honey bee, common eastern bumble bee, P. pruinosa, foraging behavior, pumpkin

Many economically important crops in the United bumble bees, Bombus impatiens Cresson and Bombus States are pollinated by bees, particularly European terrestris (L.); mason bees (Osmia spp.); and leafcut- honey bees, Apis mellifera L. (Delaplane and Mayer ting bees (Megachile spp.), to augment pollination 2000, Winfree et al. 2007, James and Pitts-Singer 2008). services provided by wild, unmanaged bees for fruit, A. mellifera provides pollination services to a variety of vegetable, and forage crops (Strickler and Freitas fruit and vegetable crops, the most notable being bee- 1999, Benton et al. 2003, Isaacs and Kirk 2010). dependent orchard crops such as almonds (Prunus There is an increasing body of empirical evidence spp.) and apples (Malus spp.) that have relatively brief demonstrating that bumble bees are equivalent to or ßowering periods (Klein et al. 2007, Rader et al. 2009, more effective than A. mellifera for pollinating a Roulston and Goodell 2011). Over the past decade, agricultural crops, including cucurbits (Stanghellini concern about declining A. mellifera populations has et al. 1998, 2002), greenhouse-grown vegetables prompted a surge in efforts to identify alternative, (Fisher and Pomeroy 1989, Dogterom et al. 1998), economically viable nonÐApis pollinators to provide and a variety of fruit (Willmer et al. 1994, Stubbs and pollination services for the worldÕs agriculturally im- Drummond 2001, Ratti et al. 2008). For example, portant crops (Morandin and Winston 2005, Winfree Stanghellini et al. (2002) reported that cucumber, et al. 2008, Potts et al. 2010, Ratnieks and Carreck Cucumis sativus L., and watermelon, Citrullus lana- 2010). As agriculture intensiÞes and habitat conver- tus (Thunb.) Matsum. & Nakai, ßowers visited by B. sion expands worldwide, crop producers are increas- impatiens had lower abortion rates and higher seed ingly relying on a few groups of managed bees, par- production compared with those visited by A. mel- ticularly honey bees, A. mellifera and Apis cerana F.; lifera. Javorek et al. (2002) reported that Bombus spp. queens and workers visited lowbush blueberry, 1 Department of Entomology, Cornell University, New York State Vaccinium angustifolium Aiton, ßowers more fre- Agricultural Experiment Station 630 W. North St., Geneva, NY 14456. 2 quently, pollinated a higher percentage of these Corresponding author, e-mail: [email protected]. Ϸ 3 Current address: USDAÐARS, Pollinating Insects Research Unit, ßowers, and deposited 4 times the amount of pol- Logan, UT 84322. len per visit to ßowers compared with A. mellifera.

0022-0493/11/1153Ð1161$04.00/0 ᭧ 2011 Entomological Society of America 1154 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 4

These results suggested that on a per-bee basis, Materials and Methods bumble bees were more effective pollinators of Study System and Study Site. Cultivated pumpkin blueberry than A. mellifera. Studies that directly (Cucurbita spp.) is a monoecious annual plant that compare the performance of B. impatiens and A. requires insect visitors to transfer pollen among con- mellifera as pollinators of pumpkin in the Northeast speciÞcs for successful pollination. Lasting a single and Great Lakes regions are lacking. Pumpkin is a day, both pistillate and staminate pumpkin ßowers valuable crop in this area (USDAÐNASS 2010) and typically open at dawn and close by noon (Tepedino must get adequate pollination otherwise fruit will be 1981). In New York, pumpkin ßowers typically se- small or misshapen and not be marketable (Dela- plane and Mayer 2000). Because the cost of renting nesce by 1100 hours EDST (D.R.A., unpublished A. mellifera hives has risen as a consequence of data). Staminate ßowers offer nectar and pollen as colony collapse disorder and a suite of other prob- rewards to foraging pollinators, whereas pistillate lems (vanEngelsdorp et al. 2011), pumpkin growers ßowers only provide nectar as a reward; however, are keen to identify and use other effective polli- pistillate ßowers produce nearly three times the nators. amount of nectar as staminate ßowers (Artz et al. In most plantÐpollinator studies, a suite of param- 2011). eters are measured to determine pollinator perfor- This study was conducted at Cornell UniversityÕs mance, such as visitation frequency to pistillate ßow- New York State Agricultural Experiment Station ers, pollen removal and deposition, duration of a ßoral (NYSAES) in the Finger Lakes region of New York Њ Ј Њ Ј visit, and fruit and seed production after a speciÞc (42 52 N, 77 01 W) in 2008, 2009, and 2010. number of ßoral visits (for review, see NeÕeman et al. Depending on the experiment, one or more Þelds Ϸ 2010). In addition, quantifying various parameters ( 0.6 ha) were used each year. All Þelds were such as single-visit pollen deposition, visitation fre- spatially separated (0.5Ð1 km) to minimize inter- quency to pistillate ßowers, and ßower handling time Þeld foraging activity. ÔMystic PlusÕ pumpkin (Cu- help gauge a pollinatorÕs overall contribution to plant curbita pepo L.) seeds were mechanically sown in reproductive success (Inouye et al. 1994, Harder and cultivated Þelds with a row spacing of 1.5 m and Wilson 1998, NeÕeman et al. 2010). in-row spacing of 1 m. Fields were planted on 23 The most common bee species encountered visiting June, 9 July, and 30 June in 2008, 2009, and 2010, pumpkin ßowers in New York are A. mellifera, B. respectively. All Þelds were fertilized and foliar impatiens, and Peponapis pruinosa Say (Artz et al. diseases managed according to standard Þeld prac- 2011). All three species were common in all Þelds tices and application guidelines described for pump- sampled over 2 yr (n ϭ 35); Þelds ranged in size from kin production in New York (Reiners and Petzoldt 0.6 to 26.3 ha. Their study revealed that A. mellifera 2011). Insect pests such as striped and western spot- and B. impatiens visited signiÞcantly more pistillate ted cucumber beetles, Acalymma vittatum (F.), and ßowers than P. pruinosa, a pumpkin specialist, but the Diabrotica undecimpunctata undecimpunctata Man- comparative performance of these three bee species as nerheim, respectively, were rarely encountered in pollinators of pumpkin was not determined. these Þelds; therefore, no insecticides were applied The purpose of this study was to compare the rel- in any of the Þelds in this study. In addition, no Þelds ative effectiveness of A. mellifera, B. impatiens, and P. were irrigated. pruinosa as pollinators of pumpkin. Pollinator effec- Pollen Deposition Experiment. To measure differ- tiveness is deÞned as a measure of a pollinatorÕs ability ences in per-visit pollen deposition among A. mellifera, to deposit pollen on stigmas and to vector pollen more B. impatiens, and P. pruinosa, virgin pistillate pumpkin often to conspeciÞcs, directly resulting in increased ßowers in the bud stage were securely covered using fruit and seed set (Herrera 1987, Fishbein and Venable white nylon mesh (1 mm2) to exclude pollinators the 1996, NeÕeman et al. 2010). Based on previous results day before anticipated anthesis (Wyatt et al. 1992). showing that A. mellifera and B. impatiens visit pistil- During anthesis the following morning, the nylon late pumpkin ßowers more frequently than P. pruinosa mesh was removed and the experiment was initiated. (Artz et al. 2011), we hypothesized that A. mellifera After a single visit and contact of the stigma by either and B. impatiens would be more effective pumpkin A. mellifera, B. impatiens, or P. pruinosa, the stigma was pollinators than P. pruinosa. This hypothesis was removed using a razor blade and transferred to a petri tested by comparing the following parameters for each dish using forceps (n ϭ 20 ßowers sampled per species; species: pollen deposition to virgin pistillate ßowers 60 ßowers total). Because of their large size (stigma per visit, ßower visitation frequency, duration of ßoral diameter ϭ 18.2 Ϯ 0.3 mm; mean Ϯ SEM), whole visits, percentage of visits resulting in contact with stigmas were cut into four manageable sections before stigmas, and the relationship between number of visits the number of pollen grains was counted without to pistillate ßowers and resulting fruit weight and seed staining using a Stemi 2000-C stereomicroscope (Carl production. In addition, we investigated whether fruit Zeiss, Thornwood, NY) at 50Ð80ϫ magniÞcation. Be- yield in pumpkin Þelds supplemented with commer- cause of the wavy architecture of Cucurbita stigmas, cial B. impatiens colonies could be increased com- pollen grain counts were likely underestimated, be- pared with fruit yield in Þelds that were not supple- cause some pollen grains present in the stigmatic pa- mented. pillae were not visible. This study was conducted by August 2011 ARTZ AND NAULT:POLLINATOR PERFORMANCE OF PUMPKIN 1155 sampling ßowers in one of the NYSAES Þelds on 14Au- commercially reared B. impatiens colonies, whereas gust 2008. three Þelds were not supplemented. The stocking den- Pollinator Visitation Experiments. The frequency sity was Ϸ6.6 colonies per ha, which was close to the of pumpkin ßower visitation and foraging behavior in stocking density of Þve colonies per ha recommended each ßower by A. mellifera, B. impatiens, and P. pru- by Koppert Biological Systems. Each B. impatiens col- inosa were assessed using video cameras from morning ony typically contains a reproductive queen and anthesis (0600 hours EDST) to ßower closing (1100 Ϸ200Ð250 workers. B. impatiens colonies were ob- hours EDST). This study involved randomly selecting tained from Koppert Biological Systems, MI. Each groups of pistillate (n ϭ 10) and staminate (n ϭ 10) Þeld was 0.6 ha and separated from the other Þelds by ßowers from four Þelds between July and September 0.5Ð1 km to minimize interÞeld foraging activity. To 2009 and July and August 2010. To assess the period our knowledge, no honey bee hives were located each bee spent foraging on a single pistillate ßower, within 1Ð2 km of each Þeld. the duration of the ßoral visit at the time the bee Before pumpkin Þelds were harvested in 2009 and landed on any ßoral part (e.g., petals, stigma) until its 2010, the number of marketable fruit per plant (i.e., departure was recorded. In addition, the proportion of appropriate fruit weight, size, and shape) was re- stigma contact among bee species was determined by corded along Þve 10-m transects within each Þeld (n ϭ recording whether the bee made contact with any 50 plants sampled per Þeld). In 2009 in each Þeld, all portion of the stigmatic lobes. marketable fruit were harvested and weighed and Pollinator Effectiveness Yield Experiment. To ex- then extrapolated to total fruit yield per hectare (ki- amine the effectiveness among A. mellifera, B. impa- lograms per hectare). Because of minor differences in tiens, and P. pruinosa as pollinators of pumpkin, the shapes of experimental Þelds, the number of rows, row relationships between number of visits to pistillate length, and average number of plants per meter were ßowers and percentage of fruit set, fruit weight and determined to calculate the average fruit weight per seed production per fruit were determined. Each bee plant (kilograms). In 2010, the total number of mar- species was permitted to visit a pistillate ßower either ketable fruit along ten 20-m transects were recorded one, two, four, or eight times from 1 to 15 September within each Þeld (n ϭ 200 plants sampled per Þeld). 2009 and from 11 to 27 August 2010, whereas only the Transects were arranged such that four, two, and four one, two, and four visits per bee species were exam- were located in the lower third, middle third, and ined from 13 to 27 August 2008. This study was con- upper third of each Þeld, respectively. For each Þeld, ducted by Þrst randomly selecting pistillate ßowers in all the marketable fruit along each transect were the bud stage and covering them with nylon mesh the weighed and then the mean weight was extrapolated day before anticipated anthesis, thereby excluding any to total fruit weight per hectare (kilograms per hect- ßoral visitors before initiating the treatments. The are). following morning, the nylon mesh was removed, and each ßower was exposed and the experiment initiated. Data Analyses. For the Pollen Deposition Experi- Because ßowers were not assigned a certain bee vis- ment and Pollinator Visitation Experiment, the num- itation treatment a priori, the goal was to obtain as ber of pollen grains deposited per pistillate ßower many replications of each treatment as possible after a single bee visit and the time each bee spent in (10Ð20 ßowers per treatment). After the number of the ßower were log-transformed and then analyzed visits to a ßower was met by each bee species, ßowers using one-way analysis of variance (ANOVA) to test Ͻ were securely covered again with nylon mesh and for differences among bee species at P 0.05. For the tagged with information including the bee species and pollination effectiveness yield experiment, a ch- number of visits. In every year, replications of each square analysis was used to compare percentage of Ͻ visitation treatment were established to span the en- fruit set among the treatments at P 0.05. Fruit weight tire 2-wk study period (i.e., all of the one-visit treat- and seed set were response variables in the controlled ments were not established at the beginning of the pollination experiments. Because these data did not 2-wk period and all of the eight-visit treatments at the meet normality assumptions and variance homogeneity, end of the 2-wk period), which allowed observers to nonparametric KruskalÐWallis ANOVAs and MannÐ maximize the number of replications based on the Whitney U tests were used to compare bee species and pollinator activity each day through time. In late Sep- pollination treatments (e.g., one, two, four, and eight bee tember or early October, the number of tagged ßowers visits) as well as the proportions of visits resulting in that produced fruit was recorded, and fruit were stigma contacts at P Ͻ 0.05. Data were analyzed using weighed and the number of seeds per fruit counted. SPSS, version 14.0 (SPSS Inc. 2005). Insect voucher specimens have been deposited at the For the bumble bee supplementation yield ex- Insect Collections at Cornell University (CUIC), periment, data from 2009 and 2010 were combined Ithaca, NY. so that each treatment had an n ϭ 6. Mean number Bumble Bee Supplementation Yield Experiment. of fruit per plant and mean fruit weight per ha were Pumpkin yield in Þelds supplemented with commer- analyzed using a mixed model (PROC MIXED) for cial B. impatiens colonies was compared with yield in a randomized complete block design at a signiÞ- Þelds that were not supplemented in 2009 and 2010. In cance level of P Ͻ 0.05 (SAS Institute 2007). Sup- each year, three Þelds were stocked each with one plementation was a Þxed effect and replication was “QUAD” unit (four B. impatiens colonies per box) of a random effect in the model. An F-test was used to 1156 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 4

Fig. 3. Box plots of the proportion of pumpkin stigma Ϯ Fig. 1. Mean number of pollen grains ( SEM) deposited contacts per visit by either A. mellifera, B. impatiens,orP. per pistillate Mystic Plus pumpkin ßower after a single visit by pruinosa (n ϭ 548, 382, and 90, respectively) in New York in ϭ either A. mellifera, B. impatiens,orP. pruinosa (n 20, 20, and 2008 through 2010. The bottom and top edges of box indicate 20, respectively) in New York Þelds in 2009. Means with dif- the 25th and 75th percentiles, with the median marked as a Ͻ ferent letters are signiÞcantly different (P 0.05; ANOVA). horizontal line. The whiskers indicate the 5th and 95th percentiles. determine whether the response variables were sig- niÞcantly impacted by the treatment at P Ͻ 0.05. but B. impatiens spent a signiÞcantly longer period foraging for nectar on pistillate pumpkin ßowers than Results P. pruinosa (Fig. 2). The proportion of visits to pistillate ßowers that resulted in contact with stigmatic Pollen Deposition Experiment. Pollen deposition surfaces signiÞcantly differed among the three bee per single visit to a stigma signiÞcantly differed among species (H ϭ 162.9, df ϭ 2, P Ͻ 0.001) (Fig. 3). B. the three bee species (F ϭ 8.1; df ϭ 2, 27; P Ͻ 0.001) impatiens contacted stigmatic surfaces (99% of visits (Fig. 1). On a per-visit basis, B. impatiens deposited Ϸ3 resulted in stigma contact; n ϭ 382) signiÞcantly more times as many pollen grains as A. mellifera or P. pru- often than A. mellifera (64% of visits; n ϭ 548) (U ϭ inosa. Mean number of pollen grains deposited after a 67,755; P Ͻ 0.001) or P. pruinosa (77% of visits; n ϭ 90) single visit was approximately equal for A. mellifera (U ϭ 13,363; P Ͻ 0.001) (Fig. 3). and P. pruinosa. Individual pistillate ßowers averaged 103.0 Ϯ 12.3 Pollinator Visitation Experiment. Handling time in and 18.1 Ϯ 2.8 (mean Ϯ SE) visits by A. mellifera and pistillate ßowers also signiÞcantly differed among the B. impatiens, respectively, over the life span of each three bee species (F ϭ 36.2; df ϭ 2, 554; P Ͻ 0.001) ßower during the 2009 and 2010 seasons (Table 1). (Fig. 2). Mean handling times for A. mellifera were Individual pistillate ßowers received on average only signiÞcantly greater than B. impatiens and P. pruinosa, 5.5 Ϯ 0.8 visits by P. pruinosa. Individual staminate ßowers averaged 37.7 Ϯ 12.1, 11.5 Ϯ 2.4, and 27.8 Ϯ 4.3 visits by A. mellifera, B. impatiens, and P. pruinosa, respectively (Table 1).

Table 1. Number of visits by A. mellifera, B. impatiens, and P. pruinosa to pistillate and staminate Mystic Plus pumpkin ﬂowers during the life of each ﬂower (0600–1100 hours) in 2009 and 2010 in New York

Mean no. visits per ßower (Ϯ SEM) Time (h) A. mellifera B. impatiens P. pruinosa Pistillate ßowers (n ϭ 10) 0600Ð0700 17.4 Ϯ 4.7 1.7 Ϯ 0.6 0.4 Ϯ 0.3 0700Ð0800 23.7 Ϯ 3.3 3.0 Ϯ 0.3 0.8 Ϯ 0.4 0800Ð0900 26.7 Ϯ 5.6 6.0 Ϯ 1.7 1.5 Ϯ 0.5 0900Ð1000 22.7 Ϯ 2.6 5.3 Ϯ 1.2 1.1 Ϯ 0.2 1000Ð1100 11.8 Ϯ 3.1 1.9 Ϯ 0.7 0.6 Ϯ 0.3 Total visits/ßower 103.0 Ϯ 12.3 18.1 Ϯ 2.8 5.5 Ϯ 0.8 Staminate ßowers (n ϭ 10) 0600Ð0700 3.5 Ϯ 2.4 0.6 Ϯ 0.4 1.3 Ϯ 0.3 Fig. 2. Mean ßower-handling time (ϮSEM) for pistillate 0700Ð0800 12.7 Ϯ 3.4 3.6 Ϯ 0.6 1.6 Ϯ 0.4 Mystic Plus pumpkin ßowers during a single visit by either A. 0800Ð0900 11.5 Ϯ 4.3 4.5 Ϯ 1.6 7.1 Ϯ 3.3 ϭ 0900Ð1000 7.4 Ϯ 2.9 1.9 Ϯ 0.6 10.3 Ϯ 1.9 mellifera, B. impatiens,orP. pruinosa (n 302, 231, and 24, Ϯ Ϯ Ϯ respectively) in New York in 2008 and 2010. Means with dif- 1000Ð1100 1.4 3.2 1.1 0.7 1.2 0.5 Total visits/ßower 37.7 Ϯ 12.1 11.5 Ϯ 2.4 27.8 Ϯ 4.3 ferent letters are signiÞcantly different (P Ͻ 0.05; ANOVA). August 2011 ARTZ AND NAULT:POLLINATOR PERFORMANCE OF PUMPKIN 1157

Pollination Effectiveness Yield Experiment. Too few P. pruinosa individuals visited pistillate ßowers to be included in the analyses in 2008. More P. pruinosa individuals visited ßowers in the 2009 and 2010 experiments, but only in the one, two, and four visit treat- 0.001 (60.60, 11) ments (Table 2; Fig. 4aÐf). Ͻ Fruit set. Percentage of fruit set tended to increase as the number of bee visits to a ßower increased ) 2010 fruit set (%) (Table 2). Percentage of fruit set signiÞcantly differed n among the treatments in 2008 (␹2 ϭ 35.9, df ϭ 6, P Ͻ 0.001), 2009 (␹2 ϭ 62.7, df ϭ 12, P Ͻ 0.001), and in 2010 (␹2 ϭ 60.6, df ϭ 11, P Ͻ 0.001) (Table 2). Percentage of fruit set for ßowers visited a single time by A. ) Fruit ( n mellifera was greater than percentage of fruit set for ßowers visited a single time by B. impatiens. In contrast, percentage of fruit set for ßowers visited two in New York in 2008 through 2010 times by B. impatiens was greater than percentage of fruit set for ßowers visited two times by A. mellifera. Percentage of fruit set for ßowers visited four times by

A. mellifera and B. impatiens was similar (Table 2). In P. pruinosa 2009 and 2010, percentage of fruit set for ßowers vis- or ited by B. impatiens was signiÞcantly greater than

percentage of fruit set for ßowers visited by A. mel- 0.001 (62.74, 12) SigniÞcance lifera and P. pruinosa for all visitation treatments (Ta- Ͻ ble 2). Percentage of fruit set for ßowers visited two or fewer times by A. mellifera and P. pruinosa were ) 2009 fruit set (%) Flowers ( n test, was used. 2 similar, but percentage of fruit set for ßowers visited ␹ four or more times by A. mellifera tended to be greater

than that visited by P. pruinosa (Table 2). A. mellifera, B. impatiens, values and degrees of freedom in parentheses.

Fruit weight. Pumpkin weights tended to increase 2

) Fruit ( ␹ as the number of bee visits to a ßower increased (Fig. n

4a, c, and e). Mean fruit weights signiÞcantly differed 896770 0 8 00 1 1 0 1 100.0 11.1 16.7 14.3 11 5 4 2 11 1 0 1 100.0 20.0 0 50.0 among pollination treatments in 2008 (H ϭ 39.0, df ϭ

6, P Ͻ 0.001), 2009 (H ϭ 75.0, df ϭ 12, P Ͻ 0.001), and SigniÞcance in 2010 (H ϭ 102.6, df ϭ 11, P Ͻ 0.001) (Fig. 4a, c, and e). In 2008, mean pumpkin weights for ßowers visited four times by A. mellifera were similar to those in the open pollinated treatment (U ϭ 145.5, P ϭ 0.003) (Fig. (35.86, 6) c

4a) and for ßowers visited four times by B. impatiens 5, and FisherÕs Exact test, rather than a and the open pollinated treatment (U ϭ 35.0, P ϭ Ͻ 0.001

0.002) (Fig. 4a). In 2009, mean fruit weight for ßowers Ͻ

visited eight times by A. mellifera was signiÞcantly (fruit set) among all treatments, with 2 lower than fruit weight in the open pollinated treat- ␹ ) 2008 fruit set (%) Flowers ( ment in 2009 (U ϭ 28.0, P ϭ 0.019) (Fig. 4c) and in n 2010 (U ϭ 11.5, P Ͻ 0.001) (Fig. 4e). In contrast, there

were no signiÞcant differences in fruit weight be- values for tween ßowers visited eight times by B. impatiens and P Ͼ the open pollinated treatment in 2009 (P 0.05) (Fig. ) Fruit ( 4c) or in 2010 (P Ͼ 0.05) (Fig. 4e). In 2009 and 2010, n fruit weights for ßowers visited four or fewer times by 25 22 88.017 12 0 12 0 100.0 7 24 0 24 0 100.0 11 0 P. pruinosa and A. mellifera were similar. There was SigniÞcance only one pistillate ßower in the P. pruinosa eight-visit Flowers ( treatment and this ßower aborted. Number of seeds. The mean number of seeds per b a fruit tended to increase as the number of visits to a 1248124 218 181 232 4 158 18 5 9 9 18 2 11 23.8 7 50.0 78.3 13.3 61.1 77.8 13 8 7 9 7 11 1 7 0 2 4 6 7 7 7.7 0 28.6 44.4 85.7 63.6 100.0 13 16 15 17 16 14 3 13 8 4 11 12 12 12 23.1 50.0 26.7 64.7 75.0 85.7 92.3 OP ßower increased (Fig. 4b, d, and f). Mean number of NEG treatment seeds produced per fruit differed among pollination Pollination treatments in 2008 (H ϭ 29.9, df ϭ 6, P Ͻ 0.001), 2009 (H ϭ 77.2, df ϭ 12, P Ͻ 0.001), and 2010 (H ϭ 106.6, df ϭ 11, P Ͻ 0.001) (Fig. 4b, d, and f). In 2008, fewer NEG, ßowers always bagged (negative control). OP, open-pollinated ßowers (positive control). In one case, a cell in the contingency table had an expected count of seeds were produced when A. mellifera visited ßowers Table 2. Fruit set resulting from varying numbers of visits to Mystic Plus pumpkin ﬂowers by either a b c The signiÞcance row (bottom of table) displays Bee species four times compared with the open pollinated treat- A. mellifera B. impatiens P. pruinosa 1158 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 4

Fig. 4. Mystic Plus pumpkin fruit weights (a, c, and e) and seed production (b, d, and f) resulting from controlled pollination by either A. mellifera, B. impatiens, and P. pruinosa after visiting pistillate ßowers one, two, four, or eight times in New York in 2008 through 2010. Bars with different letters are signiÞcantly different (P Ͻ 0.001; MannÐWhitney U tests). OP, open-pollinated ßowers (positive control); NEG, ßowers always bagged (negative control). ment (U ϭ 155.5, P ϭ 0.006) (Fig. 4b); however, no Discussion signiÞcant difference in seed set occurred between B. impatiens was a highly effective pollinator of four B. impatiens visits and the open pollinated treat- pumpkin and performed better than A. mellifera and ment (P Ͼ 0.05) (Fig. 4b). In 2009 and 2010, fewer P. pruinosa in several of the pollinator performance seeds were produced when A. mellifera visited ßowers categories. For example, B. impatiens deposited Ͼ3 eight times compared with the open pollinated treat- ϭ Ͻ ϭ Ͻ times the amount of pollen grains per stigma per visit ment (2009: U 19.0, P 0.01; 2010: U 97.0, P than the other species, nearly always contacted the 0.05) (Fig. 4d and f). In contrast in 2009, mean seed set stigma during a visit (99% of the time) compared with for ßowers visited four to eight times by B. impatiens the other species (Ͻ78% of the time), and spent Ϸ33% did not differ from seed set in the open pollinated longer foraging in pistillate ßowers than P. pruinosa. Ͼ treatment (P 0.05) (Fig. 4d). Similarly in 2010, seed We observed B. impatiens foragers landing directly on set for ßowers visited eight visits did not differ from stigmas, whereas A. mellifera workers often landed on Ͼ seed set in the open pollinated treatment (P 0.05) ßower petals and then crawled down into the nectary, (Fig. 4f). Overall, these results indicate that pumpkin sometimes not making contact with stigmas. Pollina- fruit set, fruit weight and seed set for ßowers visited tion by B. impatiens also was shown to signiÞcantly four to eight times by B. impatiens tended to be similar improve pumpkin yields. Fruit set, fruit weight, and to those that had no restrictions on the number of bee seed set tended to be greater for ßowers visited four visits in a Þeld. to eight times by B. impatiens compared with those Bumble Bee Supplementation Yield Experiment. visited by the other species at the same frequency. Although pumpkin fruit weight in Þelds supplemented A. mellifera also was an effective pollinator of pump- with commercial B. impatiens did not differ signiÞ- kin. A. mellifera visited pistillate ßowers 10Ð20 times cantly from fruit weight in Þelds not supplemented more frequently than B. impatiens and P. pruinosa, (P Ͼ 0.05) (Fig. 5a), mean fruit yield in Þelds sup- respectively. A. mellifera spent nearly 2 and 3 times plemented with B. impatiens colonies was nearly twice longer foraging on each pistillate ßower compared that in nonsupplemented Þelds. The mean number of with B. impatiens and P. pruinosa, respectively. Wal- fruit per plant was signiÞcantly greater in bumble ters and Taylor (2006) demonstrated that A. mellifera bee-supplemented Þelds than nonsupplemented was an effective pollinator of cultivated C. pepo, Cu- Þelds (t ϭϪ3.27, df ϭ 5, P ϭ 0.011) (Fig. 5b). curbita maxima Duchesne, and Cucurbita moschata August 2011 ARTZ AND NAULT:POLLINATOR PERFORMANCE OF PUMPKIN 1159

our study, we recorded few P. pruinosa visits to pistillate pumpkin ßowers during early morning (0600 hours EST) when their activity is purported to be higher than late morning hours (Willis and Kevan 1995). Also, we were not able to observe P. pruinosa visit a pistillate ßower more than four times at our Þeld sites, and these ßowers often aborted or produced small fruit. Nesting resources, nest site availability and land management practices are important factors that can inßuence the abundance of wild bee populations, including P. pruinosa, in agroecosystems (Potts et al. 2005, Julier and Roulston 2009, Roulston and Goodell 2011). For example, Shuler et al. (2005) found that P. pruinosa density was three times higher in no-tillage pumpkin and squash Þelds compared with tilled Þelds in the Mid-Atlantic region. Below-ground nests of P. pruinosa and other ground-nesting bees in conven- tionally tilled pumpkin Þelds are likely to be destroyed in the disking and turnover of the soil, hence reducing local populations. All Þelds in our study were tilled and probably had low populations of P. pruinosa. More- over, our Þelds were planted a few weeks later (late June to mid-July) than most commercial pumpkin Þelds (late May to early June), which would have reduced the time P. pruinosa had to establish nests in the pumpkin Þelds and increase the size of their pop- ulation. Perhaps, both of these factors contributed to the relatively few P. pruinosa we observed visiting pistillate ßowers. Flower and fruit production in plants can be inßu- Fig. 5. (a) Mean Mystic Plus pumpkin fruit weight (ki- enced by a variety of biotic and abiotic factors includ- lograms per hectare) from Þelds supplemented with com- ing quantity and quality of pollinators, pest injury, mercial B. impatiens colonies (n ϭ 6) and nonsupplemented temperature, and particularly, limitation of resources Þelds (n ϭ 6) in 2009 and 2010. (b) Mean number of fruit per (e.g., light, water, and nutrients) (Stephenson 1981, plant from Þelds supplemented with commercial B. impatiens El-Keblawy and Lovett-Doust 1996, Juenger and Ber- and nonsupplemented Þelds in 2009 and 2010. Means with gelson 1997). In our study, abiotic factors did not seem Ͻ different letters are signiÞcantly different (P 0.05; to be limiting factors in either ßower or fruit produc- ANOVA). tion. Rather, our results indicated that pollination was a limiting factor for pumpkin because fruit yield in- Duchesne ex. Poir. The number of fruit produced by creased when Þelds were supplemented with B. im- C. maxima and C. moschata increased and fruit weight patiens colonies. of all three species increased when Þelds were sup- Fruit set and seed production are strongly inßu- plemented with A. mellifera hives. enced by bee visitation rates (Young and Stanton 1990, P. pruinosa, a Cucurbita specialist, was the least MayÞeld et al. 2001, Karron et al. 2009). In the polli- effective pollinator of pumpkin in our 3-yr study. P. nation effectiveness yield experiment, percentage of pruinosa visitation to pistillate ßowers was very low fruit set, fruit weight, and seed production were all relative to the other species and there was a poor affected by the number of bee visits and bee species. relationship between number of visits to pistillate As the number of bee visits increased by B. impatiens ßowers and fruit set, fruit weight, and seed set. Our and A. mellifera, fruit weight and seed set generally results differ from those that show P. pruinosa to be an increased. In two of the three Þeld seasons (2009 and effective pollinator of cucurbit crops (Hurd et al. 1971, 2010), we found that pumpkin fruit weight and seed Tepedino 1981, Cane 2004). Below, we discuss some of set resulting from visits by B. impatiens were signiÞ- these differences and potential explanations for our cantly higher than A. mellifera on a per-visit basis. Our results. Þndings are consistent with other studies comparing Past studies have shown that P. pruinosa is an early pollinator performance in cucurbit crops. Stanghellini morning specialist that visits ßowers earlier in the et al. (2002) found that B. impatiens was more effective morning than A. mellifera and Bombus spp. (Tepedino than A. mellifera at pollinating cucumber, Cucumis 1981, Kevan et al. 1988). In addition, Cane et al. (2011) sativus L., and watermelon, Citrullus lanatus (Thunb.) found that within the Þrst hour after dawn, male P. Matsum. & Nakai. Floral visitation rates and pollen pruinosa bees effectively pollinated C. pepo, requiring deposition were greater for B. impatiens than for A. only seven successive visits to maximize fruit set. In mellifera on both cucurbit crops. 1160 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 104, no. 4

Depending on the size and growth of the colony, A. Cane, J. H. 2004. Importance of squash bees (Peponapis & Xe- mellifera foragers specialize on collecting pollen, nec- noglossa) as pollinators of domestic Cucurbita in the Ameri- tar, or both, and individuals use information on colony cas. Squash Pollinators of the Americas Survey. (http://www. resource storage levels to regulate pollen and nectar fao.org/ag/AGP/AGPS/C-CAB/Caselist.htm). foraging activity (Fewell and Winston 1992, Oldroyd Cane, J. H., B. J. Sampson, and S. A. Miller. 2011. Pollination et al. 1992). Nectar is the principal energy source for value of male bees: the specialist bee Peponapis pruinosa metabolic activity for individual A. mellifera in the (Apidae) at cultivated summer squash (Cucurbita pepo). Environ. Entomol. 40: 614Ð620. colony and must be collected throughout the year, Delaplane, K. S., and D. F. Mayer. 2000. Crop pollination by whereas pollen is the primary resource for brood de- bees. CABI Publishing, New York. velopment and colony expansion and is needed at Dogterom, M. H., J. A. Matteoni, and R. C. Plowright. 1998. varying times throughout the year based on the colony Pollination of greenhouse tomatoes by the North Amer- state (Houston et al. 1988, Fewell and Winston 1992). ican Bombus vosnesenskii (Hymenoptera: Apidae). J. In this study, 98% of all A. mellifera visits to pumpkin Econ. Entomol. 91: 71Ð75. ßowers were nectar-collecting visits. El-Keblawy, A., and J. Lovett-Doust. 1996. Resource re-al- Bombus spp. are highly effective pollinators of var- location following fruit removal in cucurbits: patterns in ious fruit and vegetable crops such as apple (Thomson two varieties of squash. New Phytol. 133: 583Ð593. and Goodell 2001), lowbush blueberry (Stubbs and Fewell, J. H., and M. L. Winston. 1992. Colony state and Drummond 2001, Javorek et al. 2002), raspberries (Ru- regulation of pollen foraging in the honey bee, Apis mel- bus spp.) (Willmer et al. 1994, Lye et al. 2011), and lifera L. Behav. Ecol. Sociobiol. 30: 387Ð393. Fishbein, M., and D. L. Venable. 1996. Diversity and tem- tomato (Solanum spp.) (Dogterom et al. 1998, Mo- poral change in the effective pollinators of Asclepias tu- randin et al. 2001). Furthermore, commercially reared berosa. Ecology 77: 1061Ð1073. Bombus spp. have been developed for pollination of Fisher, R. M., and N. Pomeroy. 1989. Pollination of green- various forage and Þeld crops. In our study, mean house muskmelons by bumble bees (Hymenoptera, Api- pumpkin fruit weight in Þelds supplemented with dae). J. Econ. Entomol. 82: 1061Ð1066. commercial B. impatiens colonies was numerically Harder, L., and W. G. Wilson. 1998. Theoretical conse- greater than fruit weight in nonsupplemented Þelds. quences of heterogeneous transport conditions for pollen In addition, signiÞcantly more fruit per plant were dispersal by animals. Ecology 79: 2789Ð2807. produced in Þelds supplemented with B. impatiens Herrera, C. M. 1987. Components of pollinator “quality”: than in nonsupplemented Þelds, indicating that more comparative analysis of a diverse insect assemblage. Oikos ßowers were successfully pollinated and set fruit in B. 50: 79Ð90. impatiens-supplemented Þelds. In regions where pop- Houston, A. I., P. Schmid-Hempel, and A. Kacelnik. 1988. Colony growth, worker mortality and foraging strategies ulations of Bombus spp. and P. pruinosa and feral pop- in social insects. Am. Nat. 131: 107Ð114. ulations of A. mellifera are locally abundant, it may be Hurd, P. D., E. G. Linsley, and T. W. Whitaker. 1971. cost-effective to reduce the number of commercial A. Squash and gourd bees (Peponapis, Xenoglossa) and ori- mellifera hives that are rented for pollination, because gin of cultivated Cucurbita. Evolution 25: 218Ð234. the wild bees may provide a substantial portion of the Inouye, D. W., D. E. Gill, M. R. Dudash, and C. B. Fenster. pollination services needed. More speciÞcally, be- 1994. A model and lexicon for pollen fate. Am. J. Bot. 81: cause B. impatiens was a better pollinator of pumpkin 1517Ð1530. than P. pruinosa, B. impatiens should be considered as Isaacs, R., and A. K. Kirk. 2010. Pollination services provided a promising alternative to A. mellifera for pollinating to small and large highbush blueberry Þelds by wild and this crop. managed bees. J. Appl. Ecol. 47: 841Ð849. James, R. R., and T. L. Pitts-Singer. 2008. Bee pollination in agricultural ecosystems. Oxford University Press, New York. Acknowledgments Javorek, S. K., K. E. MacKenzie, and S. P. VanderKloet. 2002. We thank E. Abbott, M. Bekauri, C. Boutard-Hunt, M. 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