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1 Current Status of Honeybee Production for Pollination Service in 2013 Kyeong Yong Lee, Seung Geu Lee 1, Young Bo Lee, Nam Jung Kim, Jung Hwa Kim 1, Yong Soo Choi, Pil Don Kang and Hyung Joo Yoon* Department of Agricultural Biology, The National Academy of Agricultural Science, RDA, Wanju, , Republic of Korea 1 R&D Extension Division, Extension Service Bureau, RDA, Jeonju, , Republic of Korea (Received 3 October 2014; Revised 23 October 2014; Accepted 2 November 2014) Abstract Recently, the importance of insect pollinators is a significant and growing for efficient pollination of the crop. We surveyed current status of production of honeybee for pollination service in Total 2,224 beekeepers produce 216,846 honeybee colonies for pollination in 2013 survey. This account 13.2% of beekeepers and 12.1% of honeybee colony in Korea. In the province-wise, Gyeongbuk was number one with 898 beekeepers (20.0%) and 74,180 colonies (17.2%), followed by Chungnam (16.3%, 14.8%), Gyeongnam (15.4%,16.0%), and Jeonnam (15.0%, 10.0%). The Annual gross income of honeybee pollination service was 23.1 billion won (USD 21.7million) and was 5.8% of total gross income of beekeeping with billion won (USD 355 million). Among 7 gross income category of beekeeping industry, honey was the highest with 67.4%, followed by bee venom with 17.3% and then pollination service. The rental price and sale price of colony for pollination service were 82,892 2,819 won (USD 77.8) and 130,586 4,118 won (USD 122.6). The ratio rental to sale was In survey that asked the beekeeping income of beekeeper producing pollination colony, honey was higher with 67.4% followed by pollination service with 23.4%. Most beekeeper expressed a positive intention as 92.8% in produce and providing colonies for pollination service. Key words: Current status, Honeybee pollination, Pollination service, Pollination colony (Free, 1970). 65%,, (Pollinator) (Barth, 1985). *Corresponding author. yoonhj1023@korea.kr 245

2 246 2 (Lebuhn et al., 2013), % (Richards, 1993)., 80~85% (Free, 1970; Delaplane and Mayer, 2000; Klein et al., 2003). 90% (Allsopp et al., 2008). 146 (Morse and Calderone, 2000), 189, 143 (Levin, 1983) (Potts, 2004). 35, 17 (RIRDC, 2010). Jung(2008) 5.9, 1 18., Seo et al.(2011) 7,559, 1,838., 19, 99% (Yoon et al., 2011; Yoon et al., 2013).,, (Kim et al., 2008; Lee et al., 2008; Kim and Jung 2013; Ahn et al., 2013), (Lee et al., 2006; Lee et al., 2008; Lee et al., 2010),., (Lee et al., 2007; Yoon et al., 2008; Yoon et al., 2011; Yoon et al., 2012; Yoon et al., 2013).,.,,,,,,,,,, (2012, MAFRI),,. 2013, (RDA, 2014). ( ), ( ) (RDA, 2014) , 1, ,,,,.

3 .,,,. Chi-square test.,, (purposive sampling) ,.,,,,,,,,,,,,., 1 2,000, 2,000. PASW 18 (IBM Inc., 2009) One-way(welch s) ANOVA test, T- test, (Correlation Analysis), (Frequencies Analyze) (Multiple response analyze). One-way ANOVA test,,, Tukey HSD Duncun method. T- test. 40%,, (Table 2), 2,244, 216, ,877 1,795, %, 12.1% (RDA, 2014)., 10% 20 (Koapis, 2007), %. (Table 2), %, 375 (16.7%), 244 (10.9%). 74,180 (34.2%), 36,060 (16.6%), 32,970 (15.2%). 23 (1%) 1,690 (0.8%),. (Table 2), %, % %, %, % 247

4 248 Table 1. The number of beekeepers providing pollination service in survey of producing honeybee colonies for pollination in 2013 Province Surveyed city or county Number of counties Bee keepers Suwon (2), Namyangju (3), Anseong (1), Gyeonggi-do Yangpkeong (3), Hwaseong (1), Gwangju (1), 8 17 Icheon (3), Yangju (3) Gangwon-do Chungju (3), Jwcheon (1), Jincheon (1), Chungcheongbuk-do Cheongwon (3), Okcheon (1), Goesan (1), 9 17 Eumseong (3), Danyang (2), Boeun (2) Chungcheongnam-do Seocheon (3), Hongseong (3), Taean (3), Dangjin (3) 4 12 Jeollabuk-do Iksan (1) 1 1 Jeollanam-do Boseong (3), Jangheung (-), Yeongwang (3), Hwasun (1), Gokseong (3) 5 10 Sangju (1), Gumi (2), Yeongju (1), Gyeongsangbuk-do Chwongsong (3), Goryeong (3), Chilgok (3), 8 19 Yecheon (3), Seongju (3) Gyeongsangnam-do Gimhae (5), Haman (3), Changnyeong (3), Goseong (2) 4 13 Jeju-do ) Metropolitans Daegu (3), Incheon (2), Daejeon (1) 3 6 Total ) Metropolitans is included following cities: Seoul, Busan, Daegu, Gwangju, Incheon, Daejeon, Ulsan, Sejong. Table 2. Current beekeeper, colonies and rate of beekeepers and colonies for crop pollination in 2013 Province No. of beekeepers No. of colonies Colonies/ beekeepers Honeybee for crop pollination No. of beekeepers No. of colonies Rate of beekeepers Rate of colonies for for pollination pollination (%) (%) Gyeonggi-do 1, , ab 65 8, ab abc Gangwon-do , ab 23 1, b c Chungcheongbuk-do 1, , a 46 19, b abc Chungcheongnam-do 1, , ab , ab ab Jeollabuk-do 1, , b 86 5, ab bc Jeollanam-do 1, , b , ab abc Gyeongsangbuk-do 4, , ab , a a Gyeongsangnam-do 2, , ab , ab ab Jeju-do ,969 1) Metropolitans 1, , b , ab abc Total 16,877 1,795, , , ) Metropolitans is included following cities: Seoul, Busan, Daegu, Gwangju, Incheon, Daejeon, Ulsan, Sejong. 2) The rate of beekeepers, colonies and colonies per beekeepers for pollination service are significantly different among province and metropolitans (Oneway ANOVA test, p<0.05).. Table %, %., %, % %, %,.

A Royaljelly 109 Propolis 2.7% 160 4.0% Pollen 99 2.5% Beeswax 14 0.3% B Royaljelly 955 3.1% Bee venom, 474 1.6% Pollination 231 5.8% Vee venom, 69 17.

5 A Royaljelly 109 Propolis 2.7% % Pollen % Beeswax % B Royaljelly % Bee venom, % Pollination % Vee venom, % Annual gross income of beekeeping n=158 (100 million won) Honey 2, % Beeswax 2, % Pollen 2, % Pollination service 2, % No. of beekeepers selling bee products and pollination service n=30, 573 Propolis 5, % Honey 15, % Fig. 1. Annual gross income of beekeeping (A) and number of beekeepers selling bee products and pollination service (B) (Welch s ANOVA test:, F=3.385, df=8,55.071, p=0.003;, F=5.351, df=8,52.189, p=0.000). 27.4%, 22.2% 8 (RDA, 2014), (81.2%) (17.8%) (Yoon et al., 2013; Statistics Korea, 2013)., (99.9%) (45.8%) (Yoon et al., 2013; Statistics Korea, 2013). 40%,,, (Correlation analysis: r=0.913), ( ), 2.3 (Table 2).,,,,,,. (One-way ANOVA F=2.365, df=8,85, p=0.024) (7, 3,783 ) 5.8%, (67.4%, 2,707 ) (17.3%, 694 ) (5.8%, 231 ) (Fig. 1A). 15, % (18.7%, 5730 ), (9.5%, 2917 ), (9.0%, 2,741 ), 7.3% (Fig. 1B).,,, 8.5%..,,,,,. 94 Table ,

6 Table 3. Current state of production and marketing of honeybees as pollinator for crop pollination in Province Beekeepers Gyeonggi-do ,344 7,241 a 91,250 7, Gangwon-do ,250 14,738 b Chungcheongbuk-do , ab 82,778 4, Chungcheongnam-do ,818 9,635 b 70,000 10, Jeollabuk-do ,857 34,206 a 77,142 7, Jeollanam-do ,000 8,548 ab 79,000 9, Gyeongsangbuk-do ,125 6,239 ab 89,166 7, Gyeongsangnam-do ,000 4,899 ab 85,909 5, Jeju-do 1) Metropolitans ,333 19,734 b 82,000 11, Total 2, ,586 4,118 82,891 2, ) Metropolitans is included following cities: Seoul, Busan, Daegu, Gwangju, Incheon, Daejeon, Ulsan, Sejong 2) The Average sale price is significantly different among province and metropolitans (One-way ANOVA test, p<0.05) 4,118, 82,892 2, ,857 34,206, 147,344 7,241 12~17%.,, (Table 3).,,, 9% 23%. (One-way ANOVA F=2.047, df=8,77, p=0.05)., 10% 91,250 7,388.,, 82,000. 5~16%, % (Table 3)., 11% %.,,, 4~7% Sale Average price Rental The ratio of rental to sale (%) 91,354 16,932 (Yoon et al., 2011), ,937 51,675 (Yoon et al., 2012), 107,162 40,396 10,000~20,000,.,,, (Yoon et al., 2013),.,. 95 (Table 1), (Fig. 2) % %, %, 1,000 7%., 88.2%

7 colonies 4.7% colonies 3.5% colonies 4.7% colonies 3.5% colonies 9.4% No. of colonies providing pollination service n= colonies 32.9% More than 3000 colonies 3.5% Below 100 colonies 37.6% Fig. 2. The number of colonies providing crop pollination service., 11.8% (Fig. 3A). (120 ) 48.7%, 21.8%, 16.8%, 6.7%, 2.5%.,,, (Fig. 3B). (17 ), 41.2%, 17.6%, 11.8%,,, 5.9% (Fig. 3C). 2011, 43.3%(14,749 ), 25.8%(8,801 ), 17.2%(5,869 ), 8.6%(2,932 ), 4.5%(1,532 ), (Fig. 3B)(Yoon et al., 2013). 34.1%(3,932 ), 31.9%(3,675 ), 17.9%(2,056 ), 5.6%, 4.3%, 2.9%, 2.3% (Yoon et al., 2013). 17., 59%, 50%, 65% (Fig. 4)., %, 46.8% (Yoon et al., 2011). (87 ), 54.3%, 45.7% 10% (Fig. 5A). Fig. 5B., %, % 67.7% 3~4 Fruits 11.8% Crop provided pollination service n=137 Vegetables 88.2% Melon 2.5% Oriental melon 16.8% Pumkin 0.8% Vegetables Crop provided pollination service n=120 Strawberry 48.7% Rasberry 5.9% Cherry 5.9% Blueberry 5.9% Peach 11.8% Fig. 3. The rate of crop (A), vegetable crop (B) and fruit crop (C) provided colonies for pollination service in Pepper 6.7% Daicon 0.8% Eggplant 0.8% A B C Chinese cabbage 0.8% Fruit tree crop provided pollination service n=17 Sweet persimmon 11.8% Water melon 21.8% Pear 17.6% Apple 41.2% 251

252 Ratio of sale to rental (%) 100 80 60 40 20 0.0 40.7 59.3 Oriental melon Fig. 4. The providing ratio of sale between rental in 3 vegetable crops in 2013.

,,. 2,000 80.9% (Yoon et al., 2011). 49.7 50.3 Strawberry Vegetable crops Rental Sale 65.0 35.0 Water melon, 57.5%, 31.0% 11.5% (Fig. 5C). 88.5%,, (RDA, 2009).., 58.4%, 37.7%, 3.9% (Fig. 6A).,,. 225 93.

8 252 Ratio of sale to rental (%) Oriental melon Fig. 4. The providing ratio of sale between rental in 3 vegetable crops in There is statistically no significant difference in the ratio of sale to rental among 3 vegetable crops (Oneway ANOVA, p>0.05) % %, 3, 4 3.4%. 93.2% (Fig. 5B) ~5 60.7%.,,. 2, % (Yoon et al., 2011) Strawberry Vegetable crops Rental Sale Water melon, 57.5%, 31.0% 11.5% (Fig. 5C). 88.5%,, (RDA, 2009).., 58.4%, 37.7%, 3.9% (Fig. 6A).,, %, 1~2 54.3%, 3~4 39.0%, (Fig. 6B). 92 (Fig. 7A), 1 Providing method n=87 3 combs, weak 3.4% 5 combs, strong 20.3% 2 combs, strong 10.2% 4 combs, weak 3.4% A B C Rental 45.7% Sale 54.3% Colony strength n=92 4 combs, strong 32.2% In the province 31.0% Out of the province 11.5% Seles area n=113 In the City country and district 57.5% 3 combs, strong 30.5% Fig. 5. The providing method (A), colony strength (B) and sales (C) of colonies for crop pollination service in 2013.

A Plastic 3.9% B No care 7.1% 3 times/month 14.2% 1 time/month 27.6% Wood 37.7% Structure of beehive n=154 Styrofoam 58.4% Over 4 times/month 24.4% Colony care after sale n=225 2 times/month 26.

9 A Plastic 3.9% B No care 7.1% 3 times/month 14.2% 1 time/month 27.6% Wood 37.7% Structure of beehive n=154 Styrofoam 58.4% Over 4 times/month 24.4% Colony care after sale n=225 2 times/month 26.7% Fig. 6. The structure of beehive (A) and colony care after sale (B) for pollination service, %, 23.4%, 17.7%, 13.2%, 8.0%, 3.2%, 1.9%. 10~ %, 10% 23.1%, 20~30% 17.6%, 40% 17.6%, 30~40% 12.1% 10~40% 59.4% (Fig. 7B).,., 5.8%,, 5~20%.. (Fig. 8A), %. (28.8%), (15.4%), (10.6%). 35.6%,. (Fig. 8B), 69.6%, 12%. 24.1%, 20.0%, 19.9%, 18.1%, 14.9%, 3.1% (Fig. 8C).,,. Choi(1987) 94.4%, Kim and Jung(2013) , 72%. 40% (Choi and Lee, 1986), 34% (Jung and Kim, 2013) % (Yoon et al., 2013),.,, 253

254 A Saleing colonies 13.2% Propolis 17.7% Contribution apiculture income n=92 Pollination 23.4% Honey 32.6% More than 40% 17.6% Pollination total income n=92 Fig. 7.

2% Royaljelly 8.0% Etc. 1.9% Satisfaction degree n=92 B 20-30% 17.6% 30-40% 12.1% Beekeeper cooperative union Very low Very high 1.1% A 2.9% B 3.3% C Beekeeper society 10.

10 254 A Saleing colonies 13.2% Propolis 17.7% Contribution apiculture income n=92 Pollination 23.4% Honey 32.6% More than 40% 17.6% Pollination total income n=92 Fig. 7. Distribution of annual income of beekeepers who provide pollination service (A) and the proportion of income from pollination service (B). Education experience and institution n=104 Bee venom 3.2% Royaljelly 8.0% Etc. 1.9% Satisfaction degree n=92 B 20-30% 17.6% 30-40% 12.1% Beekeeper cooperative union Very low Very high 1.1% A 2.9% B 3.3% C Beekeeper society 10.6% Agricultural Extension Agencies 15.4% Universty 7.7% Beekeeping association 28.8% Inexperience 34.6% Low 15.2% High 10.9% Medium 69.6% Manual of honeybee pollination 18.1% Below 10% 23.1% Production of colony for pollination 14.9% 10-20% 29.7% Etc.3.1% Problem of colony production n=95 Education shortage 19.9% Pesticide damege 24.1% Sales route 20.0% Fig. 8. The education experience of production of colony (A), the satisfaction degree of production of colony (B) and the problem of colony production (C) for pollination service, (Fig. 9A), 74.7% (Chi-square test: x 2 =46.449, df=4, p=0.0001), 97 (Fig. 9B), 92.8% (Chi-square test: x 2 =61.733, df=3, p=0.0001).,,.,,,,.,,,.., ,244, 216,846.

11 A B Very unnecessary 2.1% Reduce 7.2% Unnecessary 11.6% Maintain 46.4% Plan for provide of pollination colony n=95 Increase 46.4% Maintain 11.6% Necessity for research of pollination colony n=95 Very Unecessary 38.9% Necessary 35.8% Fig. 9. The future plan for pollination business (A) and the need of pollination research. 13.2% 12.1%., 898 (20.0%), 74,180 (17.2%), (16.3%, 14.8%), (15.4%, 16.0%), (15.0%, 10.1%) % (67.4%) (17.3%). 82,892 2,819, 130,586 4,118 65%., 32.6%, 23.4%. 92.8%. ( : PJ ). Ahn, K.S., C.M., Yoon, K.H. Kim, S.Y. Nam, M.G. Oh and G.H. Kim Evaluation of acute and residual toxicity of insecticides registered on strawberry against honeybee (Apis mellifera). Korean J. Pestic Sci. 17(3): Allsopp, M.H., W.J. De Lange and R. Veldtman Valuing insect pollination services with cost of replacement. PLos Biol. 3: 1-8. Barth, F.G Insects and flowers. The Biology of a Partnerships. Georgte Allen and Unwin. pp Betty, J.N Honeybees: market for pollination dervices grows. Region Focus. 2009: Choi, S.Y Questionnaire survey on the pesticide injury of mellifera honey bees. Korean J. Apic. 2: Choi, S.Y. and M.L. Lee A questionary survey on the injury to honey bees by pesticide poisonings in Korea. Korean J. Apic. 1: Delaplane, K.S and D.F. Mayer Crop pollination by bees. CABI Publishing. New York. Free, J.B Insect pollination of crops. Academic Press. New York. pp IBM PASW Statistics PASW Core System User s Guide, IBM inc. USA. Jung, C Economic value of honeybee pollination on major fruit and vegetable crops in Korea. Korean J. Apic. 23(2): Kim, B.S., Y.K. Park, Y.H. Lee, M.H. Jeong, A.S. You, Y.J. Yang, J.B. Kim, O.K. Kwon and Y.J. Ahn Honeybee acute and residual toxicity of pesticides registered for strawberry. Korean J. Pestic Sci. 12: Kim, D.W. and C.E. Jung Comparative analysis of the perception on honeybee damage by the pesticides between beekeepers and apple growers. Korean J. Apic. 28(1): Korapis Korean Beekeeping Association Hompage. Lebuhn, G., S. Droege, E.F. Connor, B. Gemmill-Herren, S.G. Potts, R.L. Minckley, T. Griswold, R. Jean, E. Kula, D.W. Roubik, J.H. Cane, K.W. Wright, G. Frankie and F. Parker Detecting insect pollinator declines on 255

12 256 regional and global scales. Con. Biolo. 27(1): Lee, M.L., K.H. Choi, S.W. Lee and J.B. Kim Physical symptoms of honeybees, Apis mellifera L., after contact with residual acephate on apple trees. Korean J. Apic. 23: Lee, S.B., H.J. Yoon, I.K. Park, Y.S. Kim, M.Y. Lee and M.L. Lee Comparion on the pollinating activities of bumblebee, Bombus terrestris L. and honeybee, Apis mellifera (Hymenoptera : Apidae) in the strawberry house. Korean J. Apic 21: Lee, S.B., Y.S. Kim, M.L. Lee, M.Y. Lee and H.J. Yoon The foraging activity and the effect of honeybee, Apis mellifera L. (Hymenoptera: Apidae) in the watermelon houses. Korean J. Apic. 21(1): Lee, S.B., K.Y. Lee, N.G. Ha, H.J. Yoon, I.G. Park, S.J. Hwang and H.S. Gang The status of the pollinator uses on major economical crops in Korea. Korean J. Apic. 22(1): Lee, S.B., H.S. Sim, W.T. Kim, K.H. Park, S.J. Hwang and Y.C. Choi Characteristics of pollinating activities by Bombus terrestris worker, drone and Apis mellifera worker at the oriental melon houses. Korean J. Apic. 25(4): Levin, M.D Value of bee pollination to U.S. Bull. Entomol Soc Am. 29(4): Ministry of Agriculture Food and Rural Affairs (MAFRA) Domestic animals statistics pp. MAFRA Press, Sejong, Korea. Morse, R.A. and N.W. Calderone The value of honey bees as pollinators of US crops in Bee Culture. 128:1-15 Potts, S.G European pollinator initiative: assessing the risks of pollinator loss. in: solitary bees and their role in pollination. (eds. B. Freitas and V. Fonseca). Proceedings of the International Workshop on solitary bees and their role in pollination pp , Fortaleza, Brazil Richards, K.W Non-Apis bees as crop pollinators. Rev. Suisse Zoo.l 100: Roger, A.M., W.C. Nicholas The value of honey bees as pollinators of U.S. Crops in Bee Culturw. 128: special pullout supplement. Rural Development Administration (RDA) Current status of pollinators use for tomato pp. RDA Press, Jeonju, Korea. Rural Development Administration (RDA) The current status of apiculture in pp. RDA Official paper. Jeonju, Korea. Rural Industries Research and Development Corporation (RIRDC) Pollination aware: the real value of pollination in australia. RIRDC Pub. 2010: Seo, D.K., S.B. Lee, S.Y. Lee, S.H. Park, D.S. Kim, W.T. Kim, K.H. Park and Y.C. Choi An economic analysis of pollinator s activities on the production of major fruit trees in Korea. Korean J. Apic. 26(4): Statistics Korea Crops production statistics, Yoon, H.J., K.Y. Lee, S.B. Lee, I.G. Park, S.J. Jang, Y.C. Choi, Y.S. Choi and G.G Lee Research on the current status of insect pollinator use in Korea. Korean J. Apic 23: 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. Apic. 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. Apic. 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. Apic. 28(1): 9-18.

DBPIA-NURIMEDIA

DBPIA-NURIMEDIA Original Article Journal of Apiculture 32(3) : 223~235 (2017) DOI: 10.17519/apiculture.2017.09.32.3.223 Survey of Insect Pollinators Use for Horticultural Crops in Korea, 2016 Hyung Joo Yoon*, Kyeong Yong