Effectiveness of the bumble bee, Bombus impatiens Cr. (Hymenoptera: Apidae), as a pollinator of greenhouse sweet pepper

SClENTIA HORTICULTUR~ ELSEVIER

Scientia Horticulturae, 57 (1994) 29-39

Effectiveness of the bumble bee, Bombus impatiens Cr. (Hymenoptera: Apidae), as a pollinator of greenhouse sweet pepper J.L. Shipp*'a, G.H. Whitfield b, A.P. Papadopoulos ~ aAgriculture Canada, Research Station, Harrow, Ont. NOR 1GO, Canada bAgriculture Canada, Research Station, Delhi, Ont. N4B 2W9, Canada

(Accepted 14 September 1993 )

Abstract The bumble bee, Bombus impatiens Cr., was evaluated for its effectiveness as a pollinator of greenhouse sweet pepper, Capsicum annuum L. (cultivars 'Cubico' and 'Plutona'). Four pollination trials lasting 2-5 weeks were conducted in three greenhouses from midMarch to the end of August 1991. Bees were introduced once a week for 24 h into each greenhouse. At the same time, a pollination cage was placed over a block of plants in each greenhouse to establish a control (no bees). For 'Plutona', the effect of bumble bees as pollinators was significant ( P < 0.05 ) for fruit weight, fruit width, fruit volume, pericarp volume, seed weight and days from fruit set to harvest. Bee pollination also improved fruit grade, resulting in a greater percentage of extra-large and large fruit, and fruit with four locules. For 'Cubico', pollination by bumble bees significantly ( P < 0.05) reduced the number of days from fruit set to harvest and increased the percentage of extra-large and large fruit. A simple cost-benefit analysis has shown that the use of B. impatiens as pollinators o f greenhouse sweet pepper is likely to increase the profitability for both cultivars. Key words: Bumble bee; 'Cubico'; Insecta; Pollination; 'Plutona'; Sweet pepper

1. Introduction Insects are i m p o r t a n t pollinators o f agricultural crops. K e v a n ( 1 9 8 9 ) r e p o r t e d that the value o f insect pollination to C a n a d i a n agriculture was $1.5 billion. In the Urfited States, the annual benefit has b e e n e s t i m a t e d at $1.6-8.3 billion *Corresponding author. 0304-4238/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved SSDI 0304-4238 (93) 00590-X

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J.L. Shipp et al. / Scientia Horticulturae 57 (1994) 29-39

(Southwick and Southwick, 1992). Insect pollinators include bees, flies, moths, butterflies and beetles (McGregor, 1976); bees are considered to be the most important insect pollinators of crops worldwide. Bumble bees are regarded as one of the most efficient pollinators of many crops such as red clover, cotton, alfalfa, sainfoin and berry crops (Heinrich, 1979; Richards and Edwards, 1988; Berger et al., 1988). However, natural population densities of bumble bees can fluctuate greatly from year to year, making them unpredictable in value as pollinators (Free, 1970). As a result, colonized populations of honey bees and leafcutter bees are primarily used in managed pollination of crops (Heinrich, 1979 ). Only in the last few years has it become possible to mass-rear colonies of bumble bees; this has been achieved through the efforts of Dr. R.C. Plowright (Bees-Under-Glass Pollination Services, Cantley, Que.) and the Ambrosiushoeve Center in the Netherlands (J.L. Shipp, personal communication, 1994). Dr. Plowright and the Ambrosiushoeve Center were the first to establish mass-rearing techniques for native species of bumble bees in their respective countries and this has led to the widespread commercial use of bumble bees for pollination of greenhouse tomatoes (Van den Eijnde, 1990; Steidman, 1991). In Europe, the bumble bee, Bombus terrestris L. is used to pollinate greenhouse tomato (Van den Eijnde, 1990). Previously, greenhouse tomato was pollinated using electric pollinators. This procedure is labor-intensive, requiring approximately 12 h to pollinate 1 ha (25 000 plants). Also, to maximize labor usage, the vibration of flower clusters is often practiced when conditions for pollination are not ideal. In contrast, bumble bees are present 24 h per day and can thus visit flowers at the optimal time for pollination. Encouraging results with greenhouse tomato have led to the growers of greenhouse sweet pepper in Europe expressing interest in using bumble bees for pollination (Van den Eijnde, 1990). Bombus terrestris is not an indigenous species of North America, and because of regulations preventing the importation of non-native bees, it cannot be imported for use in Canada or the United States. However, Bombus impatiens Cresson is native to eastern North America (Heinrich, 1979 ) and can be mass-reared for use in greenhouses. This species has already been shown to be as effective as the electric pollinator in terms of yield per plant and fruit grade for greenhouse tomato in Ontario (Kevan et al., 1991 ). North American growers of greenhouse sweet pepper have also shown an interest in using bumble bees for pollination, although sweet pepper is a self-pollinating crop. Rasmussen (1985 ) evaluated the use of hand-pollination, electric pollination and the solitary bee Megachile rotundata F. and found that all three methods resulted in better fruit set and higher yield than natural self-pollination. The objective of our study was to determine the effect of bumble bee pollination on fruit quality and yield of greenhouse sweet pepper, and ultimately, to assess the cost-effectiveness of bumble bees in the commercial production of greenhouse sweet peppers.

J.L. Shipp et al. / Scientia Horticulturae 57 (1994) 29-39

31

2. Materials and methods

2.1. Study site The study was conducted in three glasshouses (9.6 m × 15.6 m) at the Agriculture Canada Research Station in Harrow, Ontario, Canada. Equal numbers of sweet pepper, Capsicum annuum L., cultivars 'Cubico' and 'Plutona' were transplanted into the soil in each greenhouse (312 plants per greenhouse) on 12 February 1c~91 at a density of three plants m -2. A plot plan for one of the three greenhouses is presented for the two cultivars in Fig. 1. The cultivars were rotated for each of the greenhouses. The crop was maintained according to standard commercial practices (Ontario Ministry of Agriculture and Food, 1988 ).

2.2. Bumble bees All bees used in this study belonged to the species B. impatiens. The number of bees in a hive varied from 24 to 77, depending upon the length of time that the hive was used. One hive was placed in the same location in each greenhouse during the pollination treatment and a shade cover was constructed over the hive to prevent possible over-heating. The bumble bees were provided with a continuous source of sucrose solution (50% w / v ) and supplemental pollen, in the form of

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Fig. 1. Plot plan of the greenhouse planting arrangement for greenhouse sweet pepper cultivars 'Cubico' and ' Plutona'. The non bee-pollinated plants are shown as the two boxed areas.

32

J.L. Shipp et al. / Scientia Horticulturae 57(1994) 29-39

pellets, when the bees were prevented from exiting the hive for more than 24 h. Hives were replaced after 35 days of use to maintain consistency in the number of bees between treatment periods.

2.3. E x p e r i m e n t a l design

The design was a stratified random block with two treatments, non-bee-pollinated (control) and bee-pollinated, in each of three greenhouses. The control consisted of a bee-proof, fine-mesh screen (20 × 20 mesh), pollination cage (3.7 m × 3.7 m × 1.8 m) (Sullivan and Brampton, San Leandro, CA) which enclosed three double rows of plants with seven plants per row and was rotated weekly in each greenhouse between two sites that were at opposite sides and ends of the greenhouse. The control cage enclosed either 18 'Plutona' and 24 'Cubico' plants, or vice versa, for a total of 42 plants of each cultivar in each greenhouse for each pollination test. The outside perimeter row in the cage was considered to be a guard row and was not used in the study. The study consisted of four trials commencing on 19 March, 22 May, 23 July and 20 August. Within a trial, each greenhouse was exposed to bumble bees for a 24 h period once a week for 2-5 continuous weeks; the same hive was used in all greenhouses within each trial. The side and ridge vents of each greenhouse were screened, which prevented the bees from leaving the greenhouses. Twenty-four hours before each test, a maximum of 150 partially opened flowers of each cultivar per treatment were tagged and labeled. The outside perimeter rows and the end plant of each row were considered guard plants and thus, no flowers from these plants were tagged. The tagged flowers were chosen on the basis of their not being pollinated, but would open and produce pollen within 24 h. All tagged flowers that were exposed to bumble bees were bee-pollinated. Bee-pollinated flowers were easily identified by the complete removal of pollen from the anthers by the bees. In contrast, self-pollinated flowers always had a noticeable amount of pollen present on the anthers. The control cages were kept in the greenhouse for an extra 2-3 days to ensure the flowers on the non bee-pollinated plants had sufficient time to be pollinated and as a precaution in case any bees were left in the greenhouse after the hive was removed. After this time period, the cage was removed to ensure uniform exposure to light, regardless of the method of pollination. All tagged fruit were harvested on a weekly basis by cultivar and treatment in each greenhouse when the fruit was 80-90% red in color. Harvested fruit was placed individually in paper bags and stored at 10 °C until examined for fruit quality and yield. Each fruit was individually examined and observations recorded. Fruit assessment criteria were divided into discreet variables (grade and number of locules) and continuous variables (fresh weight, length, width, volume of whole fruit, pericarp volume, seed weight and days from fruit set to harvest).

281.04 117.45 19.72 140.03 -

~GH, greenhouse. -, not included in the model. *'**Significant at P--- 0.05 or P = 0.01, respectively.

36.75** 1.06 1.55 2.73*

24549.62 258.41 378.49 668.10

Cultivar "Cubico'

Trial 3 Pollination 1 Trial x Pollination 3 Week (Trial) 9 W e e k x G H ( T r i a l ) ] 35

331.35 309.36 5.90 130.84 .

2.01 5.93* 1.00 7.06**

2.51 14.53" 0.28 6.15**

F

MS

MS

F

Days to harvest

Fruit weight

13182.58 37.60** 2395.97 6.83* 571.13 1.63 . . .

d.f.

Trial 3 Pollination 1 Trial×Pollination 3 Week (Trial) 9 W e e k x G H ( T r i a l ) ~ 35

Cultivar ' Plutona'

Source of variation

1222.40 46.18 12.02 . 54.44

782.01 121.79 19.65 57.24

MS

189.28 63.64 81.37

MS

0.19 0.85 . -

8.89**

7.46* 2.51 3.21" -

F

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22.45** 743.00 3.98 49.15 1.04 71.06 . . . 4.69** -

13.55" 6.93* 1.12 3.26* -

F

Fruit width

63893.43 855.78 1505.84 . 3173.85

36391.53 5409.98 1838.95 2021.43

MS

34.10"* 0.48 1.13 2.75*

748.57 2.28*

:

31.65"* 5.86* 1.21

F

25529.44 130.44 307.69

:

13171.30 2439.39 503.37

MS

Pericarp volume

20.13"* 0.61 1.08

18.14"* 7.86* 2.67 2.94*

F

Fruit volume

Analysis of variance for fruit assessment criteria for bee-pollinated and non bee-pollinated greenhouse sweet pepper

Table 1

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J.L. Shippet aL / Scientia Horticulturae 57 (1994) 29-39

34

Table 2 Mean values (_+ SE) for fruit assessment variables that were significantly affected by bumble bee pollination for greenhouse sweet pepper ('Plutona') Treatment

n2

Fruit assessment variables~ Fruit weight (g)

Days to harvest

Fruit width (mm)

Whole fruit volume

Pericarp volume (cc)

Seed weight (g)

183.6_+5.4 170.8_+6.1

2.1+0.1 1.8_+0.1

(cc) Bee-pollinated Non bee-pollinated

829 469

177.6+5.1 167.5_+5.8

72.9+1.1 77.0_+1.3

80.4+1.1 77.9_+1.3

318.3+8.0 303.6_+9.5

~AIIvariables presented were significant when subjected to a random analysis of variance (P< 0.05 ). 2Total number of fruit harvested over four trials.

2.4. Data analysis For each cultivar, continuous-variable data were analyzed using a four-factor mixed-model analysis of variance (ANOVA) with fixed trial and pollination effects and random date-within-a-trial, greenhouse, and two-way interaction effects (Statistical Analysis Systems Institute, 1989 ). Any random effect terms that were not significant in the initial analyses were pooled with the error term in the final model. The data were determined to be normally distributed following examination of the residual plots. Discreet fruit assessment variables were compared using frequency histogram plots as these variables did not have a continuous normal distribution.

3. Results

3.1. 'Plutona' Fruit quality assessments for the cultivar 'Plutona' were done for a total of 1298 fruit over the four trials. The effect of bumble bee pollination was significant for fruit weight, days from fruit set to harvest, fruit width, fruit volume, pericarp volume and seed weight ( P < 0.05 ) (Table 1 ). The mean values ( + SE) of fruit weight, width, whole fruit and pericarp volume and seed weight over the four trials were greater for the bee-pollinated versus non bee-pollinated treatments (Table 2). Days from fruit set to harvest were 4.1 days (5.3%) fewer for bee-pollinated compared with non bee-pollinated fruit. This difference was significant throughout the complete experiment as indicated by the lack of a significant trial X pollination interaction. Frequency histograms of grade for each of the four trials showed that bee pollination resulted in a greater mean percentage of extra-large and large fruit ( 61.7 _+ 12.7% ) compared with non bee-pollinated fruit (41.5 ___16.3% ) for three of four trials and equal percentages (approximately 87%) for the trial starting on 22 May (Fig. 2 ). The mean percentage of fruit with four locules in the bee-polli-

J.L. Shipp et al. / Scientia Horticulturae 57 (1994) 29-39

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Fig. 2. The percentage of fruit of bee-pollinated and non bee-pollinated greenhouse sweet pepper cultivar 'Plutona' (A) of EX (extra-large), L (large), M (medium), S (small) or U (unmarketable) grade; (B) with different numbers of locules for four pollination trials.

36

J.L, Shipp et al. / Scientia Horticulturae 57 (1994) 29-39

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Fig. 3. The percentage of fruit of bee-pollinated and non bee-pollinated greenhouse sweet pepper cultivar 'Cubico' (A) of EX (extra-large), L (large), M (medium), S (small) or U (unmarketable) grade; (B) with different numbers oflocules for four pollination trials.

J.L. Shipp et al. /Scientia Horticulturae 57 (1994) 29-39

37

nated fiafit was 15.5 -+ 3.5% compared with 9.5 _+3.2% from non bee-pollinated fruit (Fig. 2 ). The use of bumble bees also resulted in a small increase in the mean percentage of fruit with one or two locules ( 17.1 _+ 1.6%) compared with non beepollinated fruit ( 14.9 _+2.8%).

3.2. 'Cubico ' For the cultivar 'Cubico', 1518 fruit were assessed over the four trials. The effect of bumble bee pollination was only significant for days from fruit set to harvest ( P < 0 . 0 5 ) (Table 1 ). The mean days from fruit set to harvest was 75.1 -+ 1.0 days for bee-pollinated fruit compared with 77.4_+ 1.1 days for non bee-pollinated fruit over the four trials. The difference in days from fruit set to harvest for the two treatments was significant over all trial periods as indicated by the lack of a significant trial × pollination interaction (Table 1 ). Frequency histograms of fruit grade for the different trials showed that beepollinated plants again had a greater mean percentage of extra-large and large fruit (73.6_+ 10.4%) for three of four trials compared with non bee-pollinated fruit (65.0_+ 11.0%) and equal percentages (94%) for the trial initiated on 22 May (Fig. 3 ). The mean percentage of fruit with four locules was approximately the same for both treatments (17%) over the four trials (Fig. 3 ). The mean percentage of bee-pollinated fruit with two locules, however, was slightly greater ( 15.0 _+2.9% ) compared with the non bee-pollinated treatment ( 11.6 _+2.9% ).

4. Discussion

Although sweet pepper is widely considered a self-pollinating plant, it is not 100% self-pollinated (McGregor, 1976; Rasmussen, 1985 ). In Europe, studies of pollinaLion of greenhouse sweet pepper with the solitary bees, Osmia cornifrons (Radoszkowski) and M. rotundata, and the honey bee, Apis mellifera L., found that bee pollination increased fruit weight and the percentage of extra-large and large fruit compared with self-pollinated fruit (Rasmussen, 1985; Kristjansson and Rasmussen, 1991; De Ruijter et al., 1991 ). The sweet pepper cultivars evaluated in Europe were 'Delphin', 'Doria', 'Novi' and 'Trophy'. In our study, the use of .0. impatiens for pollination of sweet pepper improved fruit quality and yield more for 'Plutona' than for 'Cubico'. For 'Plutona', fruit weight was increased by 6.0%, while there was no significant increase in fruit weight for 'Cubico'. The increased percentage of extra-large and large fruit, and fruit with four locules was also greater with 'Plutona'. To our knowledge, this is the first documented evidence of significant improvement in fruit quality and yield in greenhouse sweet pepper with the use of bumble bees as pollinators. These improvements in fruit weight of 'Plutona' were significant for pollination dates from March to August. Variability in percentage increase in fruit weight was high among the trials beginning in March (9.0%) and July (23%) compared with May (1.8%) and August (1.9%). Kristjansson and Rasmussen (1991) re-

38

J.L. Shipp et al. /Scientia Horticulturae 57 (1994) 29-39

ported that the effect of pollination by the solitary bee, O. cornifrons, on fruit quality and weight was significantly greater for fruit harvested from 3 May to mid-June, but after this time there was no significant difference. In this study, a 33% increase in bee-pollinated fruit weight during May was observed for extralarge and large fruit compared with non bee-pollinated fruit. The use of honey bees has also been shown to increase fruit yield for an autumn crop (planted 24 July) and spring crop (planted 9 February) (De Ruijter et al., 1991 ). Fruit weight increased by 10.4% for the spring crop and 3.4% for the autumn crop. It would seem, on the basis of our findings and the findings of others, that the benefits of mechanical and bee pollination compared with self-pollination are likely to be greater when plants are under stress (i.e. low light conditions in March, high temperature and relative humidity in July) and depleted of photosynthates. Under such conditions, flower development and pollination are hindered (Picken, 1984). Accordingly, the small improvements in fruit size with bumble bee pollinators in May and August could be the result of unhindered flower development and pollination under the favorable environmental conditions for photosynthetic productivity at that time. Conversely, low increases in fruit weight during May and August could be related to changes in the population dynamics of the bee colonies. In the present study, the reduction in the length of time from fruit set to harvest makes the use of bumble bees cost-effective for both cultivars. The initiation of flowers and fruit set with sweet pepper is a continuous process and, at any one time, the plant contains flowers and fruit at various stages of development (Smith, 1981 ). Thus, this reduction (4.1 days and 2.3 days for 'Plutona' and 'Cubico', respectively) translates into a potential corresponding increase in production of 2.7 and 1.5 fruit per plant. This is based upon a standard harvest period from March to October that includes six flushes of fruit production. Each flush of production consists of an average of eight fruit per plant. By multiplying the number of flushes of fruit production in a crop by the anticipated saving in days from fruit set to harvest, we estimate that bumble bee pollination resulted in an extra flush of fruit production. In Ontario, the average price of greenhouse sweet pepper was $4.11 kg- 1 during the harvest period in 1992 (Agriculture Canada, 1992 ). Based upon a mean weight for bumble bee pollinated fruit of 177.6 g for 'Plutona' and 199.7 g for 'Cubico', this would result in an increased profit margin of $55 K h a - ~ and $34 K h a - 1 for the two cultivars, respectively. For 'Plutona', the 6.0% increase in fruit weight would have resulted in an additional $53.5 K ha-1. In 1992, the rental cost for bumble bees was $1 K month-1 ha-l; bees are usually required for approximately 10 months. On the basis of this simple comparison of costs and benefits, B. i m p a t i e n s is a cost-effective pollinator for greenhouse sweet pepper in eastern North America.

Acknowledgments We thank L. Barlow, J. Blackburn, J. Gavloski, R. Mitaut, P. Timmins and K. Ward for their technical assistance, and N. Zariffa for assisting with the statistical

J.L. Shipp et al. /Scientia Horticulturae 57 (1994) 29-39

39

analyses. The bumble bees were provided by Bees-Under-Glass Pollination Services, Cantley, Que., Canada. This study was supported in part by a grant from the Ontario Greenhouse Vegetable Producers' Marketing Board. References Agriculture Canada, 1992. Publ. ISSN-0833-1332, Markets Information and Intelligence Unit, Ottawa, Ont. Berger, L.A., Vaissi~re, B.E., Moffett, J.O. and Merritt, S.J., 1988. Bombus spp. (Hymenoptcra: Apidae ) as pollinators of male-sterile upland cotton on the Texas high plains. Environ. Entomol., 17" 789-794. De Ruijter, A., van den Eijnde, J. and van der Steen, J., 1991. Pollination of sweet pepper (Capsicum annuum L.) in greenhouses by honey bees. Acta Hortic., 288: 270-274. Free, J.B (Editor), 1970. Insect Pollination of Crops. Academic Press, New York, 544 pp. Heinrich, B. (Editor), 1979. Bumblebee Economics. Harvard University Press, Cambridge, 245 pp. Kevan, F'.G., 1989. Crop pollination at the cross-roads: I. The immediate problems. In: National Work.shop on Bee and Pollination Research. Agriculture Canada, Research Branch, Research Program Service, Ottawa, pp. 160-167. Kevan, P.G., Strayer, W.A., Offer, M. and Laverty, T.M., 1991. Pollination of greenhouse tomatoes by bumble bees in Ontario. Proc. Entomol. Soc. Ont., 122: 15-19. Kristjansson, K. and Rasmussen, K., 1991. Pollination of sweet pepper ( Capsicum annuum L. ) with solitary bee Osmia cornifrons (Radoszkowski). Acta Hortic., 288:173-179. McGregor, S.E. (Editor), 1976. Insect Pollination of Cultivated Plants. Agricultural Handbook No. 496. USDA, ARS, Washington, DC, 411 pp. Ontario Ministry of Agriculture and Food, 1988. Growing greenhouse vegetables. Publ. 526, Toronto, Ont., 54 pp. Picken, A.J.F., 1984. A review of pollination and fruit set in the tomato (Lycopersicon esculentum Mill.i~. J. Hortic. Sci., 59: 1-13. Rasmussen, K., 1985. Pollination of pepper: Results from two years experiment. Gartner Tidende, 101: 830-831. Richards, K.W. and Edwards, P.D., 1988. Density, diversity, and efficiency of pollinators of sainfoin, Onobrychis viciaefolia Scop. Can. Entomol., 120:1085-1100. Smith, D., 1981. Peppers and aubergines. Grower Guide No. 3. Grower Books, London, 91 pp. Southwick, E.E. and Southwick, Jr., L., 1992. Estimating the economic value of honey bees (Hymenopte ra: Apidae) as agricultural pollinators in the United States. J. Econ. Entomol., 85:621-633. Statistic~tl Analysis Systems Institute, 1989. SAS Guide for Personal Computers, Version 6.03. SAS Institute, Cary, NC, 1290 pp. Steidman, B., 1991. Bumblebees in the greenhouse. Greenhouse Can., 11: 26-27. Van den Eijnde, J., 1990. Method for continuous rearing of Bombus terrestris and the production of bumblebee colonies for pollination purposes. Apidologie, 21:330-331.