2010. 11. 9

Yoon, Hyung Joo

National Academy of Agricultural Science, Rural Development Administration, KOREA Contents

Introduct io n Commercially managed - Establishment of year-round rearing of Korean native B. ignitus - Bumblebee as a pollinator Honeybee as a pollinator

Osmia mason bee as an orchard pollinator Conclusion Introduction

Bees are important for , and the most important activity of bees is their pollination of natural vegetation and agricultural plants.

Bees are diverse and abundant, with 16,325 species identified throughout the world (Michener, 2000).

ItInsect pollinati on is bthboth an ecosystem service and aprodtiduction practice used extensively by farmers all over the world for crop production.

We rely on bees to pollinate 70% of most valuable crops used directly for human consumption (Klein et al., 2007).

The production of 84% of crop species cultivated in Europe depends directly on pollinators, especially bees (Williams, 1994). Introduction

Worldwide, bees pollinate more than 400 crop species, and in the United States more than 130 crop species (James and Pitts-Singer, 2008).

Commercially managed bees are also available for pollination services and are used in large commercial fields, small gardens, or enclosures such as greenhouses and screen houses.

Although the general public gives honeybees much of the credit for pollination, managed bumblebees and solitary bees also have a great impact on certain commodities (Free, 1993; Dag and Kammer, 2001).

Thus the economic benefit of insect pollination is clear for farmers, and the market for colony rental is now well developed and organized for honeybees in the United States (Sumner and BiBoriss, 2006) and Europe (CkCarreck and Williams, 1998) as well as for bumblebees all over the world (Velthuis and van Doorn, 2006). Introduction

For the 100 crops used for human food worldwide, the total economic value of pollination throughout the world amounted to € 153 billion in 2005, which was about 9.5% of the value of the world agricultural production used for human food (Gallai et al., 2009).

Here, we discuss the current status and agricultural utilization of commercial bees such as bumblebees, honeybees, and mason bees as pollinators in Korea.

We also describe year-round techniques for rearing the Korean native bumblebee Bombus ignitus. Commercially managed bumblebees

The introduction of bumblebees into greenhouses for pollination has become widespread in recent years and demand increases annually.

The large bumblebee, , which is indigenous to Europe, has been artificially introduced in several parts of the world.

Since 1988, colonies of B. terrestris have been imported into many countries, including Korea, Japan, China, Taiwan, Mexico, Chile, Argentina, Uruguay, South Africa, Morocco, and Tunisia.

It has been estimated that the bumblebees sold in 2004 consisted of approximately 1,000,000 colonies world Commercially managed bumblebees

There has been some anxiety associated with the introduction of B. terrestris into greenhouses because it is highly invasive could possibly escape from greenhouses and could have negative effect s through competition or geneticcontititamination by hybridization with native bumblebees.

The competitive displacement of native pollinators and the invasion of native vegetation by B. terrestris have already been recorded in Tasmania.

In Israel, there has been a decline in the numbers of honeybees and solitary bees with the range expansion of B. terrestris.

B. terrestris has also colonized Japan, where it escaped from greenhouses in 1996 after its introduction in 1991 Commercially managed bumblebees

For this reason, the governments of Canada and the USA prohibit the introduction of foreign bumblebee species, and at present a native bumblebee B. impatiens is used for commercial pollination in North America.

In Korea, B. terrestris was first introduced in 1994 and in early May 2002 to 2008, B. terrestris overwintering queens were caught in several regions.

We are studying the artificial year-round mass rearing of B. ignitus, a Korean native bumblebee, because this species is the most reliable native bumblebee for crop pollination (Yoon et al., 1999, 2002, 2003, 2004). Year--roundround rearing of B. ignitus

Temperature and humidity favorable for colony development of B. ignitus Feed (Sugar solution, Pollen) Facilitating effects of helper Developmental characteristics of B. ignitus by the first ovipositon period

The effect of CO2 – treatment Artificial hibernation method Optimum temperature of B. ignitus

100 23℃ 80 27℃ 30℃ 60

Rate (%) 40

20

0 Colony Colony Progeny- initiation foundation queen production Development stage

Fig. 1. Colony development of B. ignitus reared at different temperatures. For the statistical analyy,sis, Chi-squared test was used in each developmental stage: X2=18.13, P<0.001 in colony initiation, X2 =13.88, P<0.001 in colony foundation, and X2=10.32, P<0.05 in progeny-queen production. Twenty four queens were allotted to every experimental regimes for temperature. Optimum temperature of B. ignitus

Table 1. Number of adults produced from foundation queens of B. ignitus indoor-reared at different temperatures

Number of adults produced Temperature Total 1) 2) number of Worker n Male n Queen n queens/ colony

23℃ 150.5± 2.1 2 355.5±103.9 2 1.5± 0.7 2 3/2 27℃ 163.7±33.3 9 552.7±174.1 10 32.7±47.9 11 360/11 30℃ 123.5±29.9 4 583.3±254.2 4 22.0±25.8 4 88/4

1) The units stand for means±SD. 2) There were no significant differences in the numbers of adults produced and longevity of foundation queen in either temperature or humidity factor at p<0.05 by Tukey’s pairwise comparison test. Optimum humidity of B. ignitus

100 50% 80 65% 80%

) 60 %%

Rate ( 40

20

0 Colony Colony Progeny- initiation foundation queen production Development s tage

Fig. 2. Colony development of B. ignitus reared at different humidities. For the statistical analysis, Chi-squared test was used in each developmental stage: X2=9.91, P<0.05 in colony initiation, X2 =8.17, P<0.05 in colony foundation, and X2=5.55, P>0.05 (N.S.) in progeny-queen production. Twenty queens were allotted to every experimental regimes for humidity. Optimum humidity of B. ignitus

Table 2. Number of adults produced from foundation queens of B. ignitus indoor-reared at different humidities

Number of adults produced Humidity (R.H) TtlTotal 1) 2) number of Worker n Male n Queen n queens/ colony 50％ 166.7±44.1 6 606.2±256.4 5 35.9±38.5 7 251/7 65％ 180.1±30.2 6 578.0±187.9 7 35.4±37.9 10 354/7 80％ 127. 0±56. 7 3 493. 7± 89. 2 3 13. 3±21. 4 3 40/3 1) The units stand for means±SD. 2) There were no significant differences in the numbers of adults produced and longevity of foundation queen in either temperature or humidity factor at p<0.05 by Tukey’ s pairwise comparison test . Facilitating effects of helper

100 Oviposition rate 50 Preoviposition period

80 40 (days) %) (( dd 60 30

siton rate 40 20 ition perio oo ss

Ovip 20 10 Preovipo 0 0 Con BiYW BtYW BtOW BtWC BtMC DC HW EC

Helper

Fig. 6. Oviposition rate and preoviposition period of B. ignitus cohebited with several kinds of helper. Abbreviations: Con, without helper; BiYW, Bombus ignitus young worker; BtYW, Bombus terrestris young worker; BtOW, B. terrestris old worker narcotized with CO2; BtWC, B. terrestris worker cocoon; BtMC, B. terrestris male cocoon; DC, dried cocoon; HW, honeybee worker; EC, egg cup. For the statistical analysis, oneway ANOVA and Duncan's multiple range test were used: p<0.05 for oviposition rate; p<0.001 for preoviposition period. Effect of colony by the first ovipositon period

Table 3. Colony development of collected foundation queen of B. ignitus by preovipositon period

Rate of Periods of Rate of Preoviposition Number of colony colony progeny-queen queens foundation n production period surveyed foundation (%) (days) (%)

E 65 93.8 52.8±5.4 51 75.4 M 55 94.5 52.9±6.8 43 65.5 L 20 60.0 54.3±9.9 9 50.0 VL 29 20.7 69.5 ±10.6 2 24.1

1) DtiDuration up to firs t oviitiiposition after collec ting queen : E; 1∼ 5days, M; 6∼10days, L; 1∼20 days, VL; over 21days. Abbreviations : E, early; M, middle; L, late; VL, very late. 2) n : Number of colony surveyed 3) Statistical analysis : Rate of colony foundation; Chi-square test, df=3, p<0.001 ; Periods of clony foundation; one-way ANOVA test, F=4.37,p<0.05; Rate of progeny-queen production; Chi-square test, df=3, p<0.001 Effect of colony by the first ovipositon period

Table 4. Number of adults ppqroduced from foundation queens of B.ignitus foundation queen by preovipositon period

Number of adults produced Preoviposition period Worker1) n2) Male n Queen n

E 169.6±56.7 60 556.1±195.5 60 36.4±44.8 53 M 175.8±63.3 52 565.3±201.5 52 29.1±38.4 48 L 151.3±43.6 10 505.3±270.1 11 35.1±38.3 16 VL 96. 6±74. 2 9 433. 8±297. 7 6 616.1 ±858.5 29

1) For abbrevation, see legend to Table 3. 2) Statistical analysis : No. of worker produced, one-way ANOVA test , F=4.77 , p<0. 05. Effect of CO2 – treatment

Oviposition rate 100Preoviposition period 40 )

80 yy 30

60 rate (%) rate 20 period (da nn 40

10 20 viposition viposition Oviposito oo

0 0 Pre Con 65% 99%

CO2 concentitraion

Fig. 8 Oviposition rate and preoviposition period of B. ignitus by different CO2 concentrations. For the statistical analysis, oneway ANOVA and Tukey test were used: p<0.05 for oviposition rate; p<0.001 for preoviposition period. Effect of CO2 – treatment

Oviposition rate Preoviposition peridod 100 30

80 ) days) (( %% 20 60 ition rateition ( ition period ition

ss 40 10

Ovipo 20 Preovipos

0 0 1st 2nd 3rd 4th

Time of of CO CO2 treatment after after mating mating (days) (days)

Fig. 9. Oviposition rate and preoviposition period of B. ignitus by the time of CO2 treatment after mating. For the statistical analysis, oneway ANOVA and Tukey test were used: significant differences at p<0.05 for oviposition rate; no significant differences at p<0.05 for preoviposition period. Artificial hibernation of B. ignitus

100 97 97 87 87 -2.5 0 2.5 5 80 70 ) 63 %%

60 53 50 50

43 val rate ( rate val 40 27 Survi

20 13 10 10 10

3 0 1234 Periods of cold teratment (month)

Fig. 10. The survival rates of B ignitus at temperatures and periods for artificial hibernation. Time of cold treatment : 12 days after adult eclosion Artificial hibernation of B. ignitus

100

1 month 80 2 month ) 60 ival rate (%

vv 40 Sur

20

0 8 days 12 days 16 days Time of cold treatment (days after adult eclosion)

Fig. 12. Survival rate after chilling of queen of B. ignitus according to time of cold treatment. Temperature of cold treatment : 2.5℃ Year-round rearing method of B. ignitus

27℃, 65% Food: 40%sugar solution, pollen Queen ↓ ← Input helper (two worker) Oviposition ↓ Colony initiation Larva (4 instar) ↓ Pupa ↓ Worker ( 25~30days after oviposition) Colony foundation ↓ ( 60days after oviposition) Worker < 50 ↓ Colony maturation (80~90days Worker < 100 after oviposition) ( emergence of male and queen) CO2 ↓ treatment Matiing Period : 0ne week, (30min, one Temperature: 23~25℃ time/dayⅩ2)

Temperature : 2 .5℃ Artificial hibernation Time of chilling : 10~12days after eclosion Mass-production rearing system Establishment of bumblebee rearing

In 1994, 2,300 B. terrestris colonies were first introduced into Korea. We transferred more than 10 patents and 20 bumblebee rearing techniques to farmers for commercial rearing of bumblebees from 2004 until. Since then, many more producers have started commercial rearing of bumblebees. There are over 10 producers in Korea today. The total number of bumblebee colonies produced in 2009 was over 600,000,of which 70% colilonies were proddduced by Korean bumblebee companies and 30% colonies imported from foreign sources (Yoon, H.J., personal communication, 2010). In 1994, the value of a bumblebee colony was $ 167. Now, 15 years later, is $ 67, which is more than 60% cheaper than in 1994. Bumblebee as a pollinator

2000 100

1800 Acreage 1600 80 Use rate 1400 ops (ha) es (%) rr 1200 60.9 60

1000

800 39.7 40 f bumblebe creage of c oo AA 600 Use 400 20 16.2 200 525.2 0 0.4 0.0 0.0 0.0 0.0 0.0 0

Crops

Fig. 13 . A creage and use rat e of b umbl eb ees used f or th e polli nati on of 10 major horticultural corps in greenhouses, 2009. Bumblebee as a pollinator

100,000 90, 000 80,000 Bumblebee 70,000 ny used ny

oo 60, 000 50,000

40,000 31,406 ler of col

bb 30, 000

20,000 13,780 Num 10,000 3,632 1,352 1,230 0 0 000 0

Crops

Fig. 14. Numbers of colonies of bumblebees used for the pollination of 10 major horticultural corps in greenhouses, 2009. Bumblebee as a pollinator

10,000 100 9,000 Acreage 8,000 80

Use rate (%) (ha)

7, 000 ss 6,000 60 5,000 of crops umblebee ee

4, 000 40 bb 3,000

Acreag 1,709

2,000 20 Use of 1,000 6.1%55 29 10 0 0.5% 0.9% 0.1% 0.0% 0.0% 0.0% 0.0% 0.0% 0.0%0

Crops

Fig. 15. Acreage and use rate of bumblebee used for the pollination of 10 major fruit trees in 2009. Bumblebee as a pollinator

20,000 18,000 16,000 14,000 Bumblebee

ny used ny 12, 000 11,501 oo 10,000 8,000 er of col

bb 6, 000

Num 4,000

2,000 1,018 339 87 0 0 0 0 0 0 0

Crops

Fig. 16. Numbers of colonies of bumblebee used for the pollination of 10 major fruit trees in 2009. Honeybee as a pollinator

The most widely used pollinator, and the one with the longest hi story of dtitidomestication, is the hbhoneybee (Crane, 1990),probblbably utilized for at least 90% of managed pollination services. The main features that place honeybees ahead of other and other bees as pollinators are flower constancy, colony size, and recruitment behavior (Corbet et al., 1991). The acreages and values of insect-pollinated crops and the demand for insect pollinators are increasing year by year. RtlRecently, however, the unexplilained loss of hbhoneybee colilonies, referred to as colony collapse disorder, aroused considerable concern about managed bees and natural wild bees for crop pollination. We investigated the current status of Korean beekeeping and the role of honeybees as pollinators. Honeybee as a pollinator

60,000

A. cerana A. mellifera Total 52,555 50,000

40,000 er pp

28,490 34,102 30,000 27,438 of beekee

rr 20, 684 20,219 20,000 Numbe

13,883 10,000

0 19891990199119921993199419951996199719981999200020012002200320042005200620072008

year

Fig. 17 . The number of beekeepers in Korean apiculture over 20 years (Ministry of Food, Agriculture, Forest and Fisheries, Korea, 2008). Honeybee as a pollinator

2,500

A. cerana 2,089,762 A. mellifera 2,000 1,858,574 Total

,000) 1,720,074 11

× 1,500 1,544,063

of hive ( 1, 000

636,094 Number 500 436, 247 404, 495

199,847 314,511

19891990199119921993199419951996199719981999200020012002200320042005200620072008

Year

Fig. 18 . The number of hives in Korean apiculture over 20 years (Ministry of Food, Agriculture, Forest and Fisheries, Korea, 2008). Honeybee as a pollinator

Table 5 . Comparison of beekeepers and hives involved in fixed and moved management of the honeybee Apis mellifera in Korean apiculture

BBeekeepereekeeper (%) HivHivee (%) Year Fixed Moved Fixed Moved

1990 84. 7 15. 3 62. 1 37. 9

1995 80.2 19.8 54.6 45.4

2000 75.3 24.7 43.6 56.4

2005 68. 9 31.1 39.2 60. 8

2008 62.7 37.3 42.1 57.9

Source: Ministry of Food, Agriculture, Forest and Fisheries, Korea, 2009. Honeybee as a pollinator

7000 100.0% 100

6000 Acreage 80 5000 Use rate s (%) ps (ha) 66.5% ee oo 60 4000 51.8% 3000

age of cr 40 f honeybe

ee 36. 9% 2000 30.0% Acr

20 Use o 1000

0 0.2% 0.2% 0.0% 0.0% 0.0%0

Crops

Fig. 19 . A creage and use rat e of h oneyb ees used f or th e polli nati on of 10 major horticultural corps in greenhouses, 2009. Honeybee as a pollinator

100,000 96,733 90,000 85,538 81,363 Honeybee 80,000 70,000 used 60,000 50,000

er of hive 40,000 30,451 bb 30,000

Num 20,000 10,977 10,000 130 25 0 0 0 0

Crops

Fig. 20. Numbers of hives of honeybees used for the pollination of 10 major horticultural corps in greenhouses, 2009. Honeybee as a pollinator

10,000 100 9, 000 8,000 80 Acreage 7,000 Use rate s (ha) es (%) pp 6,000 60 ee 5,000 4,000 40 ge of cro f honeyb aa 3,000 oo 2,242 2,209 Acre 2,000 20 Use 16.3% 1,000 7.9% 387 121 3.4% 43 0 1.5% 1.3% 0.0% 0.0% 0.0% 0.0% 0.0%0

Crops

Fig. 21. Acreage and use rate of honeybees used for the pollination of 10 major fruit trees in 2009. Honeybee as a pollinator

20,000 18,000 16,000 Honeybee 13,893 14,000 used 12, 042 12,000 10,000 8,000 er of hive bb 6,000 5,104

Num 4,000 2,000 984 362 0 0 0 0 0 0

Crops

Fig. 22. Numbers of hives of honeybees used for the pollination of 10 major fruit trees in 2009. in ment crops Japan g d ar td t from . mus d Korea crops into mason bees to au f egume an l . d ) blooming - cage an in the 1960s. 2000 introduced p d spring ener, firstly comprises more than 300 species, mostly in h , the horn-faced bee, was developed as an c ouse an species have been developed in different parts of h (Mi h was pollinate c Osmia ti to ed the current status o ollinator in Ja y p green Osmia mason bee as an orchard pollinator arc bee use as pollinators of fruit tree in 2007 to 2009. l l o HlH ti world cornifrons e . pollinator (Batra, 1998) and has also been tested on blueberries, orchard th the severa 1992 and is now established as an apple pollinator. Osmia (Maeta et al., 2006). The genus The species is now becoming established as an orchard O Osmia cornifrons Several We surve

Osmia , GSEE e; t u tit

ns

Ititt I

reage (ha) reage c c a Apple ogy l 31000 30000 29000 28000 27000 26000 25000 omo t n EtE l on h ec Yh Y , YEI GSEES Apple acreage on: ti a i Years rev Abb i ti spp. produced at two local organizations in . YEI Total 2009 2005 2006 2007 2008 2009 Osmia to 0 00000 50000 5 450000 400000 350000 300000 250000 200000 150000 100000 2005

mason bee as an orchard pollinator ia spp. ia Osm duced o o pr of mber u u N from Gyeongsangbukdo Sericulture & Entomology Experiment Station. Osmia Fig. 23. NumberKorea of

es (%) es e e b mason f f o Use the 80 60 40 20 100 0 for used Acreage Use rate bees mason in 2009. of 0.0% 0.0% 0.0% 0.0% 0.0% 0.0% Crops 5 1.4% rate 46 0.4% use 52 1.1% and 86 0% . 10 major fruit trees 70% 7 1,961 0 mason bee as an orchard pollinator Acreage 000 , .

8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000 9 000

10,000

s (ha) s p cro of ge a a Acre p 24 . Fig pollination of

Osmia the for used 000 bees Mason bee 0 0 mason in 2009. 14 of Crops 78 64 colonies of 139 10 major fruit trees 2,369 0 mason bee as an orchard pollinator 500 500 Numbers ,

5,000 4,500 4,000 3 3,000 2,500 2,000 1,500 1,000

.

y) o o umber/col n n (500 used y y colon of er b b Num 25 . Fig pollination of

Osmia Conclusion

We describes bumblebee rearing technology as well as the current status and agricultural utilization of insect pollinators in Korea.

We transferred more than 10 patents and 20 bumblebee rearing techniques to farmers for commercial rearing of bumblebees from 2004 There are over 10 producers in Korea today.

The total number of bumblebee colonies produced in 2009 was over ６00,000, of which 70% were produced by Korean bumblebee.

In 1994, the value of a bumblebee colony was $ 167. Now, 15 years later, is $ 67, which is more than 60% cheaper than in 1994. Conclusion

The use rates of bumblebees for 10 major horticultural crops and fruit trees were approximately 7.9% and 2.8% in 2009, respectively. The use numbers of bumblebees as pollinators was more than 51,400 colonies and 12,945 colonies, resppyectively.

The use rates of honeybees for 10 major horticultural crops and fruit trees were approximately 48.0% and 7.7% in 2009, respectively. The use numbers of honeybees as pollinators was more than 305,216 hives and 32,386 hives, respectively.

The number of Osmia mason bees used as orchard pollinators was approximately 1,331,499 individuals in 2009.

The value of commercial insect pollinators in 2009 was estimated at more than $45 million.