Bulletin of Insectology 66 (2): 315-318, 2013 ISSN 1721-8861

Opportunities for collaborative research with honey bees in and China

1 2 3 4 Charles I. ABRAMSON , Tugrul GIRAY , Zachary Y. HUANG , Xianbing XIE 1Department of Psychology, Oklahoma State University, Stillwater, OK, USA 2Department of Biology, University of Puerto Rico, San Juan, Puerto Rico 3Department of Entomology, Michigan State University, East Lansing, MI, USA 4Department of Laboratory Animal Science, Nanchang University, Jiangxi, China

Abstract

The study of honey bees represents one of the outstanding examples of the benefits of collaboration in science. What is not gener- ally known are the opportunities for collaborative research offered by laboratories in Turkey and China. We report the results of a short survey identifying laboratories in these two countries that wish to form collaborations and highlighting unique characteris- tics that these countries offer for honey bee research.

Key words: China, Turkey, collaboration, honey bee.

Introduction tember 7-9, 2010 (Abramson and Giray, 2011). One of the unique aspects of the symposium-workshop was a Collaboration enables the scientific community to ad- tour of several Turkish honey bee research centers. In dress projects that require large effort and to more effec- conducting the tour it became obvious to us that many tively distribute human and biological resources (Loan- researchers were unaware of the opportunities offered by Clark and Preston, 2002). One of the best examples of Turkey to study honey bees. These opportunities include scientific collaboration is found within the study of ho- the presence of at least five subspecies including Apis ney bees and include the honey bee genome sequencing mellifera syriaca, A. m. anatoliaca, A. m. meda, A. m. project, international efforts directed toward colony col- caucasica, and an ecotype from the carnica subspecies lapse disorder, and the open access COLOSS Beebook group. There is also easy access to the Cyprus honey that contains contributions from 243 authors representing bee, A. m. cyrica. For the A. m. caucasica and carnica 34 different countries (Robinson and Weaver, 2006; subspecies, there are government protected honey bee Whitfield et al., 2006; Navajas et al., 2008; Dietmann et population sites, and research facilities that maintain al., 2013). Not generally known to honey bee researchers pure lines. Further discussion led to the realization that are the opportunities available for collaboration in Tur- China is another country with great potential for collabo- key and China. Here we present the results of a survey rative efforts. In fact, China and Turkey top the list of identifying honey bee laboratories in Turkey and China countries with the greatest number of domestic honey seeking collaborations. Our results provide contact in- bee hives (FAO, 2013). formation of the laboratory directors and more general Like Turkey, China provides unique opportunities for information about housing, language, and research needs. honey bee researchers (Kuang and Kuang, 2009). China Partnerships among laboratories allow scientists to: has a honey bee germplasm bank in Jilin that maintains 1) acquire new skills, 2) more effectively use expertise, 5 subspecies of A. mellifera and a local subspecies of A. 3) serve as a source of stimulation and creativity, 4) de- cerana. Maintained A. cerana colonies amount to over 2 velop and extend networks, and 5) enhance dissemina- million and provides materials for comparative studies tion of information (Loan-Clark and Preston, 2002). In between it and A. mellifera (Quin et al., 2012). In addi- addition, collaboration at the international level helps tion, China has endemic A. dorsata, A. laboriosa, A. flo- build relationships between countries and serve as a rea and A. andreniformis subspecies. With nearly the conduit to provide international experiences for under- same land area as the U.S., China offers a high diversity graduate students. One popular program in the United of geographical areas and climate for studying adapta- States is the National Science Foundation Research Ex- tion of honey bee species (Lin et al., 2012). periences for Undergraduates program (Page et al., In a website listing the number of honey bee laborato- 2004) and in Europe the Erasmus program. ries around the world, no laboratories were mentioned The purpose of this note is to encourage those inter- from Turkey and only 4 from China (Cyberbee, 2013). ested in honey bee behavior to forge collaborations with In a Web of Science search starting from 1983, there fellow researchers in Turkey and China. The impetus for were only 139 publications where at least one author seeking such collaborations was stimulated by discus- affiliation was to a Turkish institution. The number of sions with attendees of the first symposium-workshop publications for Chinese institutions was 207. The low designed to explore honey bee behavioral plasticity from numbers of publications probably relates to publication nervous system to ecosystem. The symposium-workshop language and practices of the country and not to the le- was held as part of the IV Biennial European Conference vel and extent of honey bee research in either Turkey or of Apidology (Eurbee) in , Turkey during Sep- China. Two journals in Turkey publish English transla-

tions of their articles (Uludag Bee Journal and Mel- types of scholarships for graduate students outside China. lifera, respectively). No Chinese journals publish Eng- Beijing has the Institute of Apicultural Research which lish translations, although two provide translations of has more than 10 principle investigators specializing on abstracts (Apiculture of China and Journal of the Honey honey bee biology and pollination biology. Jiangxi Prov- Bees, respectively). ince also has four scientists specializing on honey bees. The Ministry of Agriculture of China has invested large amounts of money into honey bee research - over Materials and methods 20 individual honey bee researchers have each received 6 million yuan (¥) (~1 million $) for a 10 year period To assist honey bee researchers in forging collabora- (year 6 now). In addition, another 30 scientists from tions with Turkish and Chinese colleagues, we con- “Experimental Stations” which focus on more applied ducted a brief survey. The survey was designed to de- research (breeding, maintaining bee stock etc.), each re- velop a database of facilities in Turkey and China that ceived 4 million ¥ total for a 10 year period (also year 6). can be used as the basis for contact information. The One chief scientist focusing on pollination received 15 questions were divided into 6 sections related to: million ¥ (~2.5 million $) in the hopes of solving the 1) general contact information, 2) type of honey bees, problem of hand pollination for pear trees. Most Chinese 3) support, 4) facilities, 5) housing, and 6) collabora- respondents expressed difficulty in accessing primary tions. Sample questions within each category were de- literature in English and producing the right questions signed to provide: 1) contact information of the labora- for cutting edge research. With regards to equipment re- tory director, 2) type of subspecies, and number of lated to honey bee research, China is making great strides colonies associated with each, 3) type of support includ- due to the large investment by the central government to ing equipment, staff, and faculty, 4) range of facilities honey bee research. Living costs are relative low, with associated with the laboratory including shared facili- about $15.00 a day including food and lodging. ties, library information available on honey bees, access The surveys returned from both Turkey and China all to undergraduate and graduate research associates, and expressed an interest in collaborative research, had ap- language issues, 5) type of housing, dining facilities, propriate housing, dining, and laboratory facilities for and approximate cost, and 6) interest in collaboration, both students and faculty, and represent a wide variety existing collaborations, and type of collaborations the of research topics from behavioral to taxonomic investi- laboratory is interested in. gation. Most expressed a need for molecular studies. In Turkey, most researchers identified the chief limitation as having access to cutting edge molecular techniques Results such as expression profiling, next generation sequencing technologies, including high density genomic markers, Thirteen Turkish surveys were returned out of 30 (43%) and transcriptomic analyses for bee research. The key and 25 Chinese surveys were returned out of 45 (56%). areas of research in China are honey bee behavior and The completed Turkish surveys represent 5 geographic molecular biology. Assuming that potential collabora- areas: 1) Northern Turkey (Düzce, , ), tors have some familiarity with English, language does 2) Marmara Region (, Tekirdag), 3) Northeast not appear to be an issue since all of the laboratories Turkey (Trabzon), 4) Central Anatolia (Ankara) and have some access to English speakers. 5) Southern Turkey (Antalya). Of the 13 completed sur- veys, seven were concentrated in Northern and Central Anatolia. Northern Turkey is famous for the large num- Conclusions bers of domestic honey bee colonies, and specialty ho- ney types (such as the Anzer honey, chestnut honey, and To facilitate collaboration, we have identified laborato- the “mad” honey from Rhododendron nectar). There are ries in Turkey and China seeking new colleagues. We several different institutions in Northern Turkey distrib- have listed the name of the laboratories along with the uted over several provinces. The Central Anatolia sur- e-mail addresses of the laboratory directors. General in- veys are all from institutions located in the capital city formation is also provided on the needs and interests of where some of the largest research universities in Tur- Turkish and Chinese bee laboratories and the advan- key are located. In addition, Central Anatolia is the tages that these countries offer for research. home of many of the commercial queen breeders. Liv- We made a decision not to provide specific informa- ing costs are extremely low, with about $20.00 (USD) a tion about individual laboratories and their interests. day including food and lodging. To obtain the most re- Our rationale for this decision is that each survey is sev- cent information on cost of living in various cities in eral pages long and to report the results of individual Turkey and China we suggest that the reader access the questions would vastly increase the page length of this website www.numbeo.com. article without necessarily increasing the usefulness of The Chinese surveys were concentrated in the Prov- our findings. For example, laboratory priorities change, inces near the Southeast (e.g. Fujian, Zhejiang, Jiangxi) cost of living fluctuates, facilities may improve or dete- and Northeast (Beijing and Jilin) areas of China. Fujian riorate, and the variety of subspecies may change. As a Province harbors perhaps the world’s only college spe- compromise, however unsatisfactory it may be, we cializing on honey bees, with 485 undergraduate students summarized what we believed to be the most important and 50 graduate students. The college provides many data and provided contact information. Since our sample

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is relatively small, those interested in seeking collabora- nese laboratory in a specific geographical area. We an- tions in Turkey and/or China can easily send out a gen- ticipate that our survey will stimulate similar research to eral e-mail to the respondents identified in tables 1 and 2. uncover other honey bee laboratories in non-western Alternatively, an e-mail can be sent to a Turkish or Chi- countries seeking collaborations.

Table 1. Contact information to initiate collaboration with Turkish bee researchers.

Institution Location Director Contact Email Ahi Evran University Kirşehir Province Rashan Tunca [email protected] Akdeniz University Kemal Karabag [email protected] Ankara University H. Vasfi Gençer [email protected] Düzce Üniversitesi Province Meral Kekecoglu [email protected] Hacettepe University Ankara Province Çiğdem Özenirler [email protected] Hacettepe University Ankara Province Kadriye Sorkun [email protected] Hacettepe University Ankara Province Ömür Gençay [email protected] Karadeniz Technical University Sevgi Kolayli [email protected] Middle East Technical University Ankara Province Aykut Kence [email protected] Mustafa Kemal University Mustafa Muz [email protected] Namik Kemal University Tekirdag Province Devrim Oskay [email protected] Ondokuz Mayis University Ahmet Güler [email protected] Uludag University Levent Aydin [email protected]

Table 2. Contact information to initiate collaboration with Chinese bee researchers.

Institution Location Director Contact Email Honey Bee Research Institute, Nanchang, Zhijiang Zeng [email protected] Jiangxi Agricultural University Jiangxi Province Laboratory Animal Research Center, Nanchang, Xianbing Xie [email protected] Nanchang University Jiangxi Province The Medical Experimental Animal Center, Nanchang, Zhiyong Liu [email protected] Jiangxi Institute of Occupational Disease Prevention Jiangxi Province State Key Laboratory of Food Science and Technology, Nanchang, Liping Luo [email protected] Nanchang University Jiangxi Province Key Laboratory for Honey Bee Genetics and Queen Breeding, Jilin, Yunbo Xue [email protected] Jilin Provincial Institute of Apicultural Science Jilin Province College of Bee Science, Fuzhou, Xiaoqing Miao [email protected] Fujian Agriculture and Forestry University Fujiang Province Honey Bee Ecology Laboratory, Fuzhou, Bingfeng Zhou [email protected] Fujian Agriculture and Forestry University Fujiang Province Laboratory of Honeybee Physiology and Pathology, Fuzhou, Shaokang Huang [email protected] Fujian Agriculture and Forestry University Fujiang Province The Higher Educational Key Laboratory for Molecular Biology and Quanzhou, Liangxian Sun [email protected] Pharmacology of Fujian Province, Quanzhou Normal University Fujian Province Laboratory of Honey Bee Physiology and Behavior, Fuzhou, Songkun Su [email protected] Fujian Agriculture and Forestry University Fujiang Province Honey Bee Science Laboratory, College of Animal Sciences, Hangzhou, Fuliang Hu [email protected] Zhejiang University Zhejiang Province Hefei, Institute of Technical Biology and Agriculture Engineering Fanglin Liu [email protected] Anhui Province Institute of Bee Research, Chongqing, Jun Guo; [email protected] Chongqing Academy of Animal Sciences Sichuan Province Honey Bee Section, Miyun County, Qihua Luo [email protected] Bureau of Parks and Woods Beijing Xinxiang, Honey Bee Research Institute of Henan Institute of Science and Technology Zhongying Zhang [email protected] Henan Province Hefei, Apiculture Research Institute of Anhui Agricultural University Linsheng Yu [email protected] Anhui Province Bee Laboratory, Horticulture Research Institute, Taiyuan, Youquan Shao [email protected] Academy of Agricultural Sciences of Shanxi Province Shanxi Province National Key Laboratory of State Forestry Administration Resource Insect Kunming, Ying Feng [email protected] Cultivation and Utilization Yunnan Province Institute of Apicultural Research, Haidian District, Jie Wu [email protected] Chinese Academy of Agricultural Sciences Beijing The Ministry of Agriculture Key Laboratory of Pollinating Insect Biology Beijing Ting Zhou [email protected] Department of Beekeeping and Biotechnology, Beijing Jianke Li [email protected] Institute of Apicultural Research, Chinese Academy of Agricultural Science The Ministry of Agriculture Key Laboratory of Pollinating Insect Biology Beijing Shufa Xu [email protected] Guangzhou, Guangdong Entomological Institute Yuexiong Luo [email protected] Guangdong Province Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Tai’an, Baohua Xu [email protected] Control and Prevention Shandong Province Jinhua, Jinhua Institute of Apicultural Research Xujiang He [email protected] Zhejiang Province

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Acknowledgements NAVAJAS M., MIGEON A., ALAUX C., MARTIN-MAGNIETTE M. L., ROBINSON G. E., EVANS J. D., CROS-ARTEIL S., CRAUSER We would like to thank the many researchers in Turkey D. L., CONTE Y. 2008.- Differential gene expression of the and China who took the time to complete the survey and honey bee Apis mellifera associated with Varroa destructor infection.- BMC Genomics, 9: 301. to Shujin Zhou for help in translating the survey an- PAGE M., ABRAMSON C. I., JACOBS-LAWSON J. 2004.- The na- swers from Chinese to English. This research was sup- tional science foundation research experience for undergra- ported in part by National Science Foundation grant duates program: experiences and recommendations.- Tea- OISE-1043057. Our surveys are available upon request. ching of Psychology, 31: 241-247. QIN Q. H., HE X. J., TIAN L. Q., ZHANG S. W., ZENG Z. J., 2012.- Comparison of learning memory of Apis cerana and References Apis mellifera.- Journal of Comparative Physiology. A, Neu- roethology, Sensory, Neural and Behavioral Physiololgy, ABRAMSON C. I., GIRAY T., 2011.- Highlights of the first inter- 198: 777-786. national symposium and workshop on honey bee behavioral ROBINSON G., WEAVER D., 2006.- The honey bee genome pro- plasticity.- Bulletin of Insectology, 64: 151-152. ject: a model cooperation between academia, government, CYBERBEE 2013.- Honey bee research. [online] URL: and industry.- American Bee Journal, 146: 870-872. http://www.cyberbee.net/research.htm (accessed on 06 June WHITFIELD C. W., BEHURA S. K., BERLOCHER S. H., CLARK A. 2013). G., JOHNSTON J. S., SHEPPARD W. S., SMITH D. R., SUAREZ A. DIETEMANN V., NEUMANN P., ELLIS J. D., 2013.- The Coloss V., WEAVER D., TSUTSUI N. D., 2006.- Thrice out of Africa: Beebook volume 1: Standard methods for Apis mellifera re- ancient and recent expansions of the honey bee, Apis melli- search.- Journal of Apicultural Research, 52. fera.- Science, 314: 642-645. FAO, 2013.- Food and Agriculture Organization Corporate Statistical Database (FAOSTAT).- Food and Agricultural Organization of the United Nations [online] URL: Authors’ addresses: Charles I. ABRAMSON (corresponding http://faostat.fao.org/site/573/DesktopDefault.aspx?PageID= author: [email protected]), Laboratory of Com- 573#ancor (accessed on 06 June 2013). parative Psychology and Behavioral Biology, Departments of KUANG B. Y., KUANG H. O., 2009.- Biology of the honey bee.- Psychology and Zoology, 116 N. Murray, Stillwater, OK Yunan Science and Technology Press, China. 74078, USA; Tugrul GIRAY, Department of Biology, Univer- LIN Z. Y., WANG Z. L., YAN W. Y., WU X. B., ZENG Z. J., sity of Puerto Rico, San Juan, PR 00931, Puerto Rico; Zachary HUANG Z. Y., 2012.- The sex determination gene shows no Y. HUANG, Department of Entomology, Michigan State Uni- founder effect in the giant honey bee, Apis dorsata.- PLoS versity, East Lansing, MI 48824, USA; Xianbing XIE, Depart- ONE, 7 (4): e34436. ment of Laboratory Animal Science, 71 East Yangming Road, LOAN-CLARK J., PRESTON D., 2002.- Tensions and benefits in Nanchang University, Nanchang, Jiangxi 330006, China. collaborative research involving a university and another or- ganization.- Studies in Higher Education, 27: 169-185. Received July 5, 2013. Accepted September 26, 2013.

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