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1 Original Article Journal of Apiculture 32(3) : 223~235 (2017) DOI: /apiculture Survey of Insect Pollinators Use for Horticultural Crops in Korea, 2016 Hyung Joo Yoon*, Kyeong Yong Lee, Hee Sam Lee, Man Young Lee, Yong Soo Choi, Myeong Lyeol Lee and Gi Hyoung Kim 1 Department of Agricultural Biology, The National Institute of Agricultural Science, RDA, Wanju 55365, Republic of Korea 1 R&D Extension Division, Extension Service Bureau, RDA, Wanju 55365, Republic of Korea (Received 12 September 2017; Revised 20 September 2017; Accepted 20 September 2017) Abstract We have surveyed the current status of insect pollinators use for horticultural crops in The use rate and farm number of insect pollinators for 26 horticultural crops were 25.8% and 55,208, respectively. The colony number of insect pollinators used in this survey was 479,777, which include 344,690 for honeybees, 119,104 for bumblebees, 12,051 for mason bees, 1,317 for flies, and 2,415 for the combination of bumblebees, honeybees, and mason bees. The use rate of insect pollinators was 59.4% for 11 vegetable crops, such as onion (100%), strawberry (99.9%), oriental melon (93.8%), melon (82.8%), water melon (64.8%), tomato (63.6%), pepper (31.8%), paprika (5.9%), zucchini (1.6%), bitter melon (1.2%), and cucumber (0.2%). The colony number of insect pollinators used for 11 vegetable crops was 449,287, which include honeybees (72.3%), bumblebees (25.1%), flies (0.2%), and the combination (2.4%) of bumblebees and honeybees. The use rate of insect pollinators was 9.0% for 15 fruit tree crops, such as mango (100%), raspberry (24.0%), apple (18.3%), persimmon (14.0%), passion fruit (5.5%), boxthorn (4.5%), blueberry (3.8%), Korean raspberry (3.1%), pear (2.7%), cherry (2.2%), pomegranate (1.0%), plum (0.4%), peach (0.2%), kiwi (0.2%), and jujube (0.02%). The colony number of insect pollinators used for 15 fruit tree crops was 30,290, which include honeybees (66.3%), bumblebees (20.2%), mason bees (8.0%), flies (1.6%), and the combination (3.9%) of bumblebees, honeybees, and mason bees. Together, farms of 97.8% showed positive effect for the use of insect pollinators and most of farms (97.0%) planed for the continuous use of insect pollinators. Key words: Insect pollinator, Bumblebee, Honeybee, Mason bee, Horticultural crops, Vegetable crops, Fruit tree crops *Corresponding author. yoonhj1023@korea.kr 223

2 224, (Kearns et al., 1998; Shimizu et al., 2014). 200,000 (Nabhan and Buchnmann, 1997), % (Klein et al., 2007) (Bees) (James and Pitts-Singer, 2008).,,,, (Morandin and Winston, 2005; Greenleaf and Kremen, 2006; Winfree et al., 2007).,, (Free, 1993; Dag and Kammer, 2001). (Batra, 1995; Goulson et al., 2008; Williams and Osborne, 2009; Rao and Stephen, 2010). Gallai et al.(2009) 100 1, %, 1,900 ~3, , (IPBES) 75% 5~8%( 2350~5770 ), ( ),,,, % 16%, 9%, 37%, 31% (IPBES, 2016) ,,,,,,..,, 2015 (,,,,,,,, 9,,,,, 6 ), 2016 (,,,,,,,, 9 ), 2016 ( ), ( )

3 , 1, 8 156,., 2016,,., ( ). 300 / /660m 2 ( 300 /600kg, 5 /kg), 80 / /660m 2 ( 300 /160kg, 5 /kg) , 2016,,,,,,. One-way ANOVA (welch) test, T-test, (Frequencies Analyze) (Multiple response analyze). SPSS PASW 22.0 for windows (IBM, USA). One-way ANOVA (welch) test T-test.,,, ,,,,,,,,,, 11 (Table 1) (Yoon et al., 2013), ,194.0ha, 12,572ha (Statistics Korea, 2015). 8,152.5ha, 6,299.0ha, 4,975.8ha, 4,436.4ha ,851.9ha, 2011 (21,138.1ha) 1.3 (Table 1) %, %. 100%, 99.9%, 93.8%, 82.8%, 64.8%, 63.6% (Table 1). 11,, 4 (Table 1). 26,851.9ha 20,514.1ha(76.4%), 5,383.2ha(20.0%), 899.6ha(3.4%), 55.0ha(0.2%)

4 226 Table 1. Cultural area and rate of insect pollinators use for 11 vegetable crops in 2016 Vegetable crops Cultural area (ha) Water melon 12,572 8, , Tomato 6,976 4, , Strawberry 6,306 6, , Oriental melon 5,305 4, , Pepper 4,878 1, Zucchini 3, Cucumber 3, Melon 1,546 1, , Paprika Bitter melon Onion (seed) Total 45,194 Total 26,851.9 (100%) Area of insect pollinators use (ha) 20,514.1 (76.4%) Honeybees 5,383.2 (20.0%) Honeybee & (3.4%) 55.0 (0.2%) Area rate of insect pollinators use (%) Flies Table 2. The farm number of insect pollinators use for 11 vegetable crops in 2016 Vegetable crops Farm numbers of insect pollinators use Total Honeybees Honeybee & Water melon 11,076 11, Tomato 8, , Strawberry 14,851 12, ,230 0 Oriental melon 6,285 6, Pepper 3,274 1,221 1, Zucchini Cucumber Melon 2,308 2, Paprika Bitter melon Onion (seed) Total 46,194 (100%) 33,610 (72.8%) 10,296 (22.3%) 2,236 (4.8%) 55 (0.1%) Flies (3,009.0ha) %, 27.1%, 24.2%, 5.7%, 3.1%. (Table 1)., %(4,434.7ha), 8.7%, 5.4%, 2.1%., %, % 23.2% (Yoon et al., 2013). 50.0%, 49.5%(445.4ha) 99.5%, 5.0%. 100% (Table 1). Table , (41,916 ) 4,278 (Yoon et al., 2013). 33,610 (72.8%), 10,296

5 227 Table 3. The colony numbers of insect pollinators for 11 vegetable crops in 2016 Vegetable crops Colony numbers of insect pollinators Total Honeybees Honeybee & Water melon 167, , Tomato 100, , Strawberry 93,634 81,519 5,816 6,299 0 Oriental melon 54,750 54, Pepper 15,957 6,802 4,658 4,497 0 Zucchini Cucumber Melon 14,590 13,332 1, Paprika Bitter melon Onion (seed) Total 449,287 (100%) 324,607 (72.2%) 112,974 (25.1%) 10,873 (2.4%) 833 (0.2%) Flies (22.3%), 2,236 (4.8%) %. (38.5%), (33.0%) (18.7%) 90.2% (14,922 ) (9,017 ), (6,173 ) % 8,149, 10.3%(1,056 ), 6.7%(693 ). 55.0%(1,230 ), 44.6%(997 ) %. 100%(55 ) (Table 2) ,287 (Table 3), 2011 (306,856 ) 1.5 (142,431 ) (Yoon et al., 2013). 324, %. 25.1%(112,974 ), 2.4%(10,873 ), 0.2%(833 ) (52,684 ) 2.1.,, %, 25.1%, 16.8% 4.1% % % (Table 3).,, 7, 89.1%, 5.1%, 4.1%, 1.1% %, (57.9%) (41.4%) (Table 3) ,,.,. 0.2%(833 ) (Table 3). 11 3,300m 2

6 228 Table 4. Cultural area and rate of insect pollinators use for 15 fruit tree crops in 2016 Fruit tree crops Apple 31, , , Peach 16, Pear 12, Persimmon 11, , , Plum 5, Blueberry 4, Jujube 2, Korean raspberry 2, Kiwi 1, Pomegranate Raspberry Cherry Boxthorn Mango Passion fruit Total 90,851.7 Cultural area (ha) 8,193.4 (100%) Total 5,490.3 (67.0%) Area of insect pollinators use (ha) 1,788.8 (21.8%) (7.8%) Honeybees Masonbee Honeybee, & Mason-bee (2.9%) 35.5 (0.4%) Area rate of insect pollinators use (%) Flies , Fig. 1 3,300m , (T-test: t(14)=0.548, p=0.592). 2016,,,,,,,,,,,,,,, 15 (Table 4) (Yoon et al., 2013),,,, ,851.7ha, 31,620.0ha, (16,704.0ha), (12,664.0ha) (Statistics Korea, 2015). 5,773.5ha, 1,656.5ha, 336.3ha ,193.4ha, 2011 (12,130.3ha) %(1.5 ) ,193.4ha 11 (26,851.9ha) 3.3 (Table 1 and Table 4). 15 (100%), (24.0%) (18.3%), (14.0%) 10% % 2011 (14.1%) 5.1% (Table 4) (Yoon et al., 2013),, 2.7% 20.3%, 3.8% 19.4%.,,. 15,,, (, ), 5

7 229 Table 5. The farm number of insect pollinators for 15 fruit tree crops in 2016 Fruit tree crops Total Farmer numbers of insect pollinators Honeybees Masonbee Honeybee, & Mason-bee Apple 5,399 2,995 1,595 2, Peach Pear Persimmon 1,976 1, Plum Blueberry Jujube Korean raspberry Kiwi Pomegranate Raspberry Cherry Boxthorn Mango Passion fruit Total 9,014 (100.0%) 6,213 (68.9%) 1,782 (19.8%) 631 (7.0%) 305 (3.4%) 83 (0.9%) Flies 1 (Table 4). 8,193.4ha 5,490.3ha(67.0%), 1,788.8ha(21.8%), 637.7ha (7.8%), (, ) 241.0ha(2.9%), 35.5ha (0.4%). 60.0%, 28.8%, 6.0%. (93.9%),,,. 99.3%., 68.5%, 31.5% , (46,194 ) 5.1 (Table 2 and 5). 6,213 (68.9%), 1,782 (19.8%), 631 (7.0%), (, ) 305 (3.4%) %., (2,995 ) (1,882 ) 78.4% % 1,595, 94, % 626, 5., 183 (60.0%) 122 (40.0%). 83 (Table 5) , (10,721 ) (Table 6). 11 (449,287 ) 14.8., 20, %., 53.6%, 18.4%, 10.6%, 7.0% %. 0.04%(8 ). 6,130 (20.2%) 15,,,, 5. 5, %

8 230 Table 6. The colony number of insect pollinators for 15 fruit tree crops in 2016 Fruit tree crops Total Colony numbers of insect pollinators Honeybees Masonbee Honeybee, & Mason-bee Apple 19,143 10,769 5,266 2, Peach Pear 2,139 2, Persimmon 3,943 3, Plum Blueberry 1, Jujube Korean raspberry Kiwi Pomegranate Raspberry 1,420 1, Cherry Boxthorn Mango Passion fruit Total 30,290 (100.0%) 20,083 (66.3%) 6,130 (20.2%) 2,415 (8.0%) 1,178 (3.9%) 484 (1.6%) Flies, 8.9%, 3.9%. 2,415 (8.0%) % ,346 (75.2%).., 1,178 (3.9%) 59.3%(698 ), 40.7%(480 ). 484 (1.6%) (Table 6). 15 3,300m 2, Fig. 2 3,300m , , ~4.8 (Oneway-ANOVA test: F(2,18)=1.729, p=0.206)., 2016,, , 6 6,,,, % %, 2011, 6. 55,208, ,577, 344,690, 119,104, 2,415,,, 2,415, 1,317.,

9 231 No. of colony/3,300m 2 in vegetable crops Honeybees Insect pollinators Fig. 1. The numbers of average colony of insect pollinators used per 3,300m 2 in vegetable crops, There was significant difference in the number of average colony between honeybees and bumblebees used per 3,300m 2 at T-test. No. of colony/3,300m 2 in fruit crops Honeybees Insect pollinators Mason bees Fig. 2. The colony numbers of insect pollinators per 3,300m 2 for fruit tree crops in There was significant difference in the colony number of insect pollinators per 3,300m 2 at p<0.05 using one-way ANOVA test. A B Fig. 3. Duration (A) and method (B) of insect pollinators use for 26 horticultural crops in A B Fig. 4. Education (A) and care (B) for insect pollinators use.

10 232 (A) 100% a Purchaseprice rate 80% 60% 40% 20% 0% Honeybees Mason bees Insect pollinators (B) 160, , , ,000 80,000 60,000 40,000 20,000 0 Fig. 5. Purchase price rate (A) and purchase price (B) of insect pollinators for 26 horticultural crops in Price (Won) a b Honeybees Insect pollinators b Mason bees A B Fig. 6. Advantage (A) and problem (B) of insect pollinators use. A B Fig. 7. Satisfaction degree (A) and plan (B) of insect pollinators use.

11 233. 1,133 (Fig. 3A), %, 4~6 28.6%, 1 9.2% (Chi-square Test : X 2 = , df=4, p=0.0001). 1,146 Fig. 3B. 36.6%, 43.0%, 18.5% 95.1%. 1,037 (Fig. 4A), 50.7%, 1~2 33.4% 3~7 15.9% 49.3%. 50%,. (Fig. 4B), 33.6%, 31.5%, 15.5%. (Fig. 5), 9~ %. 3~6 22.6%,. 18~24 2.6%. 98,147 39, ,303 11,423, 6~9 85.3%, 3~6 13.8%. 58,888 5,665 6~9 77.8%, 3~6 22.2%.,, (welch's ANOVA test F(2,24.185)= , p<0.0001, (post-hoc analysis : tukey HSD)).,,, (Fig. 6A), (30.5%), (27.3%), (25.8%), (16.4%). 28.4%, 21.0%, 18.6%, 17.3% (Fig. 6B). 1,120 (Fig. 7A), 2.2%,. (Fig. 7B), 39.4%, 57.6%, 3.0% (Fig. 7B). (Yoon et al., 2011a; Yoon et al., 2011b; Yoon et al., 2012).,. 2016,

12 %, 55, ,577, 344,690, 119,104, 12,051, 1,317,,, 2, %, 100.0%, 99.9%, 93.8%, 82.8%, 64.8%, 63.6%, 31.8%, 5.9%, 1.6%, 1.2%, 0.2% , %, 25.1%, 0.2%, 2.4% % 100.0%, 24.0%, 18.3%, 14.0%, 5.5%, 4.5%, 3.8%, 3.1%, 2.7%, 2.2%, 1.0%, 0.4%, 0.2%, 0.2%, 0.02% , %, 20.2%, 8.0%, 1.6%,,, 3.9%. 97.8%, 97.0%. ( : PJ ),. Batra, S.W.T Bee and pollination in our changing environment. Apidologie 26: Dag, A. and Y. Kammer Comparison between the effectiveness of honeybee (Apis mellifera) and bumblebee (Bombus terrestris) as pollinators of greenhouse sweet pepper (Capsicum annuum). Am. Bee. J. 141: Free, J.B Insect pollination of crops. 2nd ed., Academic Press, London. Gallai, N., J.M. Salles, J. Settle and B.E. Vaissiére Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68: Goulson, D., G.C. Lye and B. Darvill Decline and conservation of bumblebees. Annu. Rev. Entomol. 53: Greenleaf, S. S. and C. Kremen Wild bee species increase tomato production and respond differently to surrounding land use in Northern California. Biol. Conserv. 133: Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. (IPBES) Summary for policy makers of the assessment report of the intergovernmental science-policy platform on biodiversity and ecosystem services on pollinators, pollination and food production. IPBES. (deliverable 3 (a)) of the work programme. James, R.J. and T.L. Pitts-Singer Bee pollination in agricultural ecosystems. Oxford University Press, New York. Kearns, C.A, Inouye D.W, Waser N Endangered mutualisms: the conservation of plant? pollinator interactions. Annu. Rev. Ecol. Syst. 29: Klein, A.M., B. Vassiere, J.H. Cane, L. Steffan-Dewenter, S.A. Cunningham, C. Kremen. T. Tscharnkle Importance of crop pollinators in changing landscapes for world crops. Proc. Royal. Soc. London. B. 274: Morandin, L.A. and M.L. Winston Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol. Appl. 15: Nabhan, G.P., Buchmann S.L Services provided by pollinators. pages in G. Daily, editor. Nature s services. Island Press, Washington, D.C. Rao, S. and W.P. Stephen Abundance and diversity of native bumble bees associated with agricultural crops: The Willamette valley experience. Psyche volume 2010, Article ID , 9 pages. Shimizu, A, Dohzono I, Nakaji M, Roff DA, Miller DG III, Osato S, Yajima T, Niitsu S, Utsug N. Sugawara T. Yoshimura J Fine-tuned bee-flower coevolutionary state hidden within multiple pollination interactions. Sci

13 235 Rep. 4: SPSS PASW Statistics PASW Core System User s Guide, SPSS inc. USA. Statistics Korea Crops production statistics, 2012/Fruit vegetable/apple. kor.pi/index.action. Willmer, P. H. and J.L. Osborne Bumblebee vulnerability and conservation world-wide. Apidologie 40: Winfree, R., T. Griswold and C. Kremen Effect of human disturbance on bee communities in a forested ecosystem. Conserv. Biol. 21: Yoon, H.J., K.Y. Lee, M.I. Kim, I.G. Park and Y.C. Choi. 2011a. Current status of insect pollinators use in strawberry crop in Korea. Korean J. Api. 26: Yoon, H.J., K.Y. Lee, M.I. Kim, I.G. Park and Y.C. Choi. 2011b. Current status of insect pollinators use in tomato crop in Korea. Korean J. Apiculture 26: Yoon, H.J., K.Y. Lee, I.G. Park, M.I. Kim, Y.M. Kim and P.D. Kang. 2012a. Current status of insect pollinators use in apple orchards. Korean J. Apiculture 27: Yoon, H.J., K.Y. Lee, I.G. Park., M.I. Kim, Y.M. Kim and P.D. Kang Current Status of Insect Pollinators Use for Horticultural Crops in Korean J. Apiculture 28: 9-18.

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