DERLEME MAKALESİ / REVIEW ARTICLE BEEKEEPING AND RECENT COLONY LOSSES IN TURKEY TÜRKİYE’DE ARICILIK VE GÜNCEL KOLONİ KAYIPLARI (Genişletilmiş Türkçe Özet Makalenin Sonunda Verilmiştir) İbrahim ÇAKMAK1and Selvinar SEVENÇAKMAK2 1 Beekeeping Development Application and Research Center, Uludag University, Gorukle Campus, Nilüfer, Bursa, Turkey, icakmak@uludag.edu.tr 2 Department of Biology, Faculty of Science, Ankara University, 06100 Tandogan-Ankara, Turkey Geliş Tarihi: 07.04.2016 Kabul Tarihi: 02.09.2016 ABSTRACT Beekeeping has a long history in Anatolia going back to Hittite civilization, B.C. 1300 about 9000 years. Also Turkey having at least five subspecies of Apis mellifera is a bridging country connecting Europe, Asia and Africa by Middle East and gene center of western Honey bee Apis mellifera. Anatolia also has three out of 37 phytogeography rich areas in the world and there are about 10.000 plant species and 3506 of them are endemic to this country. Turkey is representing one of the highest potential in world beekeeping with about 7,709,636 colonies, more than 150.000 families in beekeeping business, 79 Beekeeping Unions in each province as parts of Central Beekeeping Union of Turkey representing 56,000 professional beekeepers and 107,665 tons of honey production annually in Turkey. There are a number of factors affecting colony losses up to 80% high in some areas in Turkey including such as Varroosis, Nosemiosis, Foulbrood diseases, new generation of pesticides as neonicotinoids, queen failure, colony management and large scale long distance migratory beekeeping. Finally, Turkey still has great potential of genetic reservoir of western honey bee, Apis mellifera and may provide vital solutions for a number of beekeeping problems in the world facing today. Keywords: Honey bees, Apis mellifera, Beekeeping, Colony losses, Turkey, Anatolia ÖZ Bu çalışmanın amacı ülkemizde genel olarak arıcılığın durumu ve son yıllardaki arı kayıplarının nedenlerinin açıklanmasıdır. Anadolu’da arıcılık milattan önce 1300 yılından, yaklaşık 9000 yıl öncesine kadar uzanmaktadır. Türkiye en az 5 arı ırkı ile Avrupa, Orta Doğu ve Asya kıtalarını birbirine bağlayan bir köprü durumunda olup batı bal arısının gen merkezi durumundadır. Anadolu dünyadaki 37 fitocoğrafya bölgelerinden üçüne yaklaşık 10,000 bitki türüne sahip olup bunlardan 3506’sı endemik olarak bulunmaktadır. Türkiye 7,709,636 koloni, 150,000 den fazla aile arıcılık ile geçimini sağladığı, 79 arı yetiştirici birlikleri, 56,000 profesyonel arıcı ve 107,665 ton yıllık bal üretimi ile arıcılıkta dünyanın en yüksek potansiyeline sahip ülkelerinden biridir. Türkiye’de bazı bölgelerde % 80’lere kadar varabilen koloni kayıplarını etkileyen faktörler oarak; varroa, nosema, yavru çürüklüğü, yeni nesil tarım ilaçları olan nikotin türevi neonikotinoidler, ana arı yetersizliği, koloni yönetimi ve uzun mesafeli gezginci arıcılık sıralanabilir. Sonuç olarak Türkiye batı bal arısının genetik merkezi olarak büyük bir potansiyele sahip olup bugün dünyada karşılaşan birçok arıcılık sorunlarının çözümünde hayati çözümler sunabilecek durumdadır. Anahtar Kelimeler: Bal arısı, Apis mellifera, Arıcılık, Koloni kayıpları, Türkiye, Anadolu Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 31 DERLEME MAKALESİ / REVIEW ARTICLE BEEKEEPING IN GENERAL to this, In the Middle East, the oldest known apiary has been found recently in archeology research Beekeeping has long history in Anatolia about dated 3000 years ago in the ancient city of Tel 9,000 years and it is known one of the oldest Rehov in Jordan (10th–early 9th centuries B.C.E) agricultural activities. The first beekeeping laws of and identifiedas Apis mellifera anatoliaca, (Picture 202 clauses in the world about B.C. 1300 belong to 1) a subspecies found only in what is now Turkey Hittite civilization that has been found in Anatolia (Bloch et al. 2010).This finding suggests the long (Sarıöz, 2006, Akkaya and Alkan, 2007). In addition time relations between humans and honey bees. Picture 1. Anatolian worker honeybee Turkey is geographically bridging country of Asia approximately 3,5 million colonies and average Europe, and Africa by Middle East. Potential of this 2,000 km in the country (Güler and Demir, 2005; country with at least five Apis mellifera subspecies Yılmaz and Canlı, 2012). Anatolia with different has not been emphasized sufficiently in the world climatic zones and habitats can also be provide beekeeping literature. great diversity of honeybees, Apis mellifera in Turkey. Therefore at least five different races of Anatolia has three out of 37 phytogeography rich Apis mellifera; A.m. anatoliaca, caucasica, meda, areas in the world and there are about 10,000 plant syriaca and carnica exist in this country (Kandemir species and 3506 of them are endemic to this et al., 2000; 2006). Recently another honey bee country. About five hundred of them provide large subspecies “A .m macedonica” in Greek border amount of nectar and pollen for bees (Sorkun, area is suggested to exit (Pers. Comm.). 2008). Migratory beekeepers move with 32 U. Arı Drg. Mayıs 2016, 16 (1): 31-48 / U. Bee J. May 2016, 16 (1): 31-48 DERLEME MAKALESİ / REVIEW ARTICLE These different races adapted to different habitats country”. Honey bees are well respected because and have differences in many characters such as there are two Surahs or chapters with the name of size, over-wintering ability, honey production, Al Nahl (16:68-69) in “Holly Kur’an” explaining defensiveness, resistance to parasites and about honey bees, honey and the healing effects of diseases, flower fidelity and all can be evaluated bee products. There are also words mentioning and selected for different purposes (Ruttner 1988; about bees and honey in the Bible and Torah Çakmak 1998; Kandemir et al., 2000; Çakmak, (Sarıöz, 2006). Honey and bee products are 2001; Akyol et al., 2003). The great diversity of consumed not for only food but also for health honeybees has not been used efficiently for concerns as natural medicine. However, there is a breeding purposes in Turkey so far but some serious concern of consumers for adulterated studies such as resistance to parasites and honey, pollution in most regions, residues, and also diseases are on the way to explore these traits non-hygienic process and packaging and handling. (Çakmak, 2010; Öztürk and Akyol, 2010; Çakmak Beekeepers are concerned with bee products and Fuchs, 2013). recently such as pollen, propolis, royal jelly, apilarnil, bee venom. Also api-therapy or api-cure is There are recently about 7,709,636 million colonies, catching great interest not only beekeepers but also more than 150,000 families in beekeeping many others including hive air. business, about 56.000 professional beekeepers, 79 Beekeeping Unions in each province as parts of Beekeeping in Turkey is a great growing industry Central Beekeeping Union of Turkey and 107,665 with new types of hives, wood, plastic, and tons of honey production annually in Turkey Styrofoam materials including smart hives recently. (Yılmaz, 2013, Haygem, 2016). Also the Turkish Ministry of Forestry and Water Resources supports some areas as honey forest There is considerable progress in beekeeping area or designates some areas to beekeeping in industry in Turkey in recent years and almost all order to use for honey production. provinces have established beekeeping union and all united as Central Turkish Beekeeping Union Turkey as a gene center of western honeybee and (TAB). The number of beekeepers and colonies are may hold the solution of major beekeeping mostly registered and supported financially by the problems particularly recent colony losses. Turkish Ministry of Food, Agriculture, Husbandry Because genetic variation of honey bees may and each beekeeper has an identification number provide natural protection against predators and in that can be tracked down for the products. This pathogens such as Varroa destructor that has been brings better control of production when consider thought the major factor of colony losses. Of course consumers’ concern about health and residue there are a number of problems waiting for solution problems and artificial feeding of colonies during such as chemical residues, agricultural pesticides nectar flow. There was only one beekeeping journal beside varroa mite. However, such problems are in 1980’s but now there are three scientific journals usually linked to each other. Preserving endemic and half a dozen beekeeping magazines published honeybee subspecies and ecotypes are essential mostly by beekeeping unions. When it comes to for future beekeeping industry not only for Turkey different types of honey, Turkey with different but also for the world. geographical regions and climate, about 10,000 First, we all have to find ways to preserve and plant species offer a great diversity of honey with protect our native honeybee subspecies and different taste, color and aroma (Sorkun, 2008). ecotypes in their natural habitats in preserved areas Pine honeydew in the world is mostly (about 85%) or isolated areas such as islands. Turkey has also produced in Turkey (Yılmaz, 2008). some islands in Marmara and Aegean Sea that has There are also growing interest of research on good flora for bees such as Marmara Island in honey bees and hive products. Culturally and in Marmara Sea and Gokceada in Aegean Sea religious perspective, Turkey is called “honey (Picture 2). Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 33 DERLEME MAKALESİ / REVIEW ARTICLE Picture 2. Honey bee colonies in Marmara island. Caucasian or mountain bee Apis caucasica is also Using chemicals for parasites and diseases may preserved in northeast Anatolia, border region with slow down the process of natural selection and Georgia in military zone. The rest of four artificially selecting more honey producing colonies, subspecies are not preserved and large scale beekeepers end up with sensitive and weak migratory beekeeping in Turkey threatens this great colonies against different ecological factors such as diversity of honey bees. climate, parasites, diseases, chemicals, stress etc. Breeding work is in very small scale and queen breeders and queen production are very low BEE PRODUCTS, API-THERAPY and compared to USA. If not done properly with many POLLINATION lines of breeder queens, large scale queen production with a few breeder lines may cause to Interest to other hive products such as propolis, lose genetic variation and may lead to small gene royal jelly, pollen, apilarnil and bee venom have pool in a country. Swarm catching is still wide been increasing. Honey is produced in all areas in spread way of increasing colony number and this Turkey and pollen in most areas and royal jelly and keep genetic variation in high level of natural way of propolis is mostly produced in Marmara and Bursa selection of highly reproducing colonies in the province and bee venom and apilarnil are only for country. curiosity by interested beekeepers since no market 34 U. Arı Drg. Mayıs 2016, 16 (1): 31-48 / U. Bee J. May 2016, 16 (1): 31-48 DERLEME MAKALESİ / REVIEW ARTICLE is available for these at this moment. Apitherapy (or in Turkey. Also package bee production stimulates Api-cure) has growing area of interest and api- production of honey in some countries and this line therapy association of Turkey has been established of bee production is not practiced sufficiently in recently. Apitherapy studies are just starting to take Turkey. place as a new section in meetings, congress and Pollination has been considered the most important symposiums. part of beekeeping on economic perspective in Bee products such as honey has always been USA and also in EU. Honey bee colony use for major part of beekeeping production, and recently pollination has been limited in small areas for a few pollen, royal jelly, bee wax, particularly propolis and crops such as cherries, almonds and sunflowers bee venom are produced. Pollen, propolis, and areas. The great potential of beekeeping has not royal jelly production have been increased recently. been used for pollination purposes in Turkey. There is more emphasis about trials and research However, pollination research is still mostly lacking in propolis use. Also organic-ecological-biological sufficient interest and only a few scientists working beekeeping gets more supports from universities in this field. Turkey has a huge density of honey and Ministries because of increased health concern bee colonies and also great number of wild bees recently and chemical residue problems in bee including many solitary species. Pollination products (Picture 3). deficiencies might be compensated in most years with great density of bees (Özbek, 2003; Çakmak, Total colony number in Turkey is determined as 2004; Öz et al., 2008, 2009, Gonzales et al., 2014). 7,709,636, out of this number primitive hive number Recently bumble bees are produced and used in 223,015 and modern hive number 7,486,621 in the greenhouses extensively in small boxes. (Gösterit year of 2015. Honey production has increased from and Gürel, 2005; Gürel et al., 2011; Gösterit and 81,115 in 2010 to 107,665 tons in 2015 and honey Gürel, 2014). is the most produced bee product in Turkey and yearly production of honey is reported as 14 kg per The Turkish Ministry of Food, Agriculture and colony in the years of 2012-2015 but this level is Husbandry has started to provide more support for actually lower in the field when all colonies pollination particularly for bumble bees in green considered. Bee wax production is 4750 tons in houses. This should be extended to use of honey 2015 (Haygem, 2016). bees colonies for a number of crops. More progress is expected in pollination of crops by honey bee Pollen production varies year to year and there is colonies in the near future. no sufficient data to calculate yearly production. The same is true for royal jelly, propolis, and bee The economic value of insect pollination has been venom yearly. estimated about 22 billion euros in EU (Gallai et al., 2009). About 84% cultivated plants in Europe Bee wax production is not sufficient to meet the depend on insect pollination (Williams, 1994) and demand in recent years and some wax has been wild and honeybees are the main pollinators of imported in recent years. Organic bee wax is also these crops (Garibaldi et al., 2013; Rader et al., highly demanded when some beekeepers need for 2012). Honey bees are mostly responsible for production. It seems that bee wax production cultivated crops. The economic value of pollination should be supported to make progress in Turkish has been estimated more than 18 billion dollars in beekeeping because bee wax quality and safety is USA (Mader et al., 2011). Recent study suggests also important to avoid chemical residues disturbing that economic value of pollination comes from effects in beekeeping. pollinators 266 billion euros for 60 crops per year Queen production is an important part of productive worldwide (Lautenbach et al., 2012). Economic beekeeping. However selected queens are not value of pollination by honey bees is under sufficient and queen production is about 100,000. investigation recently in Turkey. This number is far from meeting the queen demand Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 35 DERLEME MAKALESİ / REVIEW ARTICLE Picture 3. Bee products Pollination is a huge industry and increase quality and quantity of crop production. A few studies have also been performed in Uludag University and crop production had been increased significantly such as sunflower and canola. Even though Turkey has big honeybee industry and GAP is a huge agricultural project, honeybee pollination has not been used effectively. Reduced crop production is significant in some years and honey bees pollination is not considered as one of the main reasons for reduced crop production. On the other hand, there are some good improvements to use honey bee colonies for pollination. Recently some fruit producing companies and some farmers rent colonies for pollination of some crops such as cherry, almond, canola, sunflower (Oz et al., 2008; 2009; Pers. Comm.). 36 U. Arı Drg. Mayıs 2016, 16 (1): 31-48 / U. Bee J. May 2016, 16 (1): 31-48 DERLEME MAKALESİ / REVIEW ARTICLE HONEY BEE RESEARCH established in Easter Anatolia, Malatya Province in 2013. There are already ten honey bee research centers in four different universities and there is one Honey Muğla Sıtkı Koçman University “Beekeeping and bee Institute that belongs the Turkish Ministry of Pine Honey Application and Research Center and Food, Agriculture, Husbandry. These research Beekeeping and Silkworm Research and centers are aiming mostly to increase production, Application Research Center was established in breeding best honey bee races or ecotypes, better 2013 in Wetern Anatolia, Mugla province. Mugla treatment for parasites and diseases, to conserve has been known for having the highest number of local or regional races and ecotypes to support beekeepers in Turkey and and well known for pine organic-ecological beekeeping, to educate honey production in the World. beekeepers, to determine local honey and other Bayburt University Beekeeping Research and hive products, to investigate pollination problems Application Center was established in 2015 and suggest solutions and etc. between Blacksea and Eastern Anatolia, Bayburt The Beekeeping Institute belongs to Turkish Province. Ministry of Food, Agriculture, Husbandry was Van Yüzüncü Yıl University Beekeeping Research established on the date of 22 December 1994 in and Application Center in East Anatolia, close the Blacksea region, Ordu province and publish Iranian border, Ardahan University Caucasian Bee “The Beekeeping Research Journal” in Turkish. Research and Application Center in East Anatolia, Ordu province has the second highest number of close to Armenian border, Bingöl University beekeepers in Turkey. and it is also well known for Beekeeping Research and Application Center. migratory beekeeping and comb honey production in Turkey. Among these research centers AGAM is unique and has become a pioneer in leading the Turkish These ten research centers in different Universities beekeeping integrating with the world beekeeping are; by collaborating with the Uludag Beekeeping AGAM, (Beekeeping Development-Research and Association first, then start publishing the Uludag Application Center) was established in Uludag Bee Journal, organizing International Beekeeping University, in 2004 in Marmara region, Bursa meetings and becoming the first emphasizing the province, and has published “Uludag Beekeeping Apimondia membership and applying for Journal” since 2001 in Turkish with extended membership to Apimondia in Turkey. Uludag Bee abstract in English mainly but articles in English are Journal has been used as the link to beekeepers in also published. Turkey and other countries. AGAM has also researchers from different background or HARUM (Hacettepe University Beekeeping disciplines work together. Researchers from Research and Application Center) was established Biology, Veterinary Medicine, Agricultural Sciences, in Hacettepe University in the same year 2004, in Food, Economy work together to investigate or find Central Anatolia, Ankara province and has solutions for different problems. published “Mellifera” since 2001 journal in English. The main research focus areas in AGAM; There are also some beekeeping magazines honeybee pathology (varroa and other parasites published by various beekeeping unions in Turkey. and diseases), behavioral ecology, pollination, bee DAGEM, (Düzce University Beekeeping Research products, beekeeping equipments. and Application Center) was established in Duzce A new team of scientists has started to collaborate University in 2009, in western Blacksea region, in different research projects in AGAM and Duzce Province. progress and important developments are expected ARIUM, (Mustafakemalpaşa University Beekeeping in the near future. Graduate program in Honey bee and Silkworm Application and Research Center) science or apiculture is not present in Turkey but a was established in 2010 in Southeast Anatolia, new graduate program as inter disiplinary area as Antakya Province, in Syrian border. Beekeeping or Apiculture in preparation and expected to offer a MSc degree in Uludag INAGAM, (İnönü University Beekeeping University. Development-Research and Application) was Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 37 DERLEME MAKALESİ / REVIEW ARTICLE COLONY LOSSES and Honey Bee Parasites and the second the most serious problem in some years Diseases (Aydın et al., 2003, Çakmak et al., 2003b). Varroa mite was not known to occur in Turkey before 1977, Honey bee parasites and diseases cause and then only in the far western area of the country. significant colony losses and since it was called Soon after however, varroa had reached all regions winter losses by the beekeepers. The most of Turkey due to the large migratory beekeeping important of these parasites and diseases are; industry, with 600,000 colonies reported lost each varroosis, brood diseases and nosemiosis (Bailey year to this disease alone in the country by 1984 and Ball, 1991; Aydın et al., 2003; Çakmak, 2012). (Anonymous). Varroa destructor is the main focus Previous survey results in Marmara region research area since this parasite is responsible for suggested that colony losses mostly occurred in the most colony losses, low honey production and fall and winter by varroa, brood diseases, nosema residue problems. Actually V destructor opens the and chalkbrood (Aydın et al., 2003; Çakmak et al., door for other parasites and diseases by weakening 2003b; Doğaroğlu and Sıralı, 2005).However the bees particularly transferring viruses. Since V recently unpredictable high colony losses have destructor is the most serious problem not only in been reported by beekeepers up to 80% in some Turkey (Picture 4) but also in the world recently areas of Marmara region and other regions of more researchers are interested in varroa research. Turkey (Giray et al., 2007, Pers. Comm.). The goal is to select varroa resistant/tolerant bee Varroa destructor is the most serious problem in colonies (Fries et al. 2006, Fries and Bommarco, Turkey. It was reported that in Marmara region 2007). varroosis has been found the first and chalkbrood Picture 4. Varroa on bees The most popular method of selection is hygienic hygienic colonies that remove dead pupae in behavior by pin or liquid nitrogen to select the most usually 24 hours. A number of papers published on 38 U. Arı Drg. Mayıs 2016, 16 (1): 31-48 / U. Bee J. May 2016, 16 (1): 31-48 DERLEME MAKALESİ / REVIEW ARTICLE hygienic behavior (Spivak, 1998; İbrahim et al., colonies with high level of mites very effectively and 2007; Harris, 2007; Wilson-Rich et al., 2009; leave low mite colonies untreated. All three Çakmak, 2010). However, varroa problem still methods bad, ugly and good strategy were applied continues with almost same speed and even worse in Uludag University Beekeeping Development- and more chemicals have been developed for this Application and Research Center (AGAM) and the parasite. Other researchers select the colonies with last one proved to be more applicable to continue “live or die” method. These methods are more exact this line of selection research. Also varroa selection but not so practical since all colonies or most of research includes island study on beekeeping level them die in two years and it is almost impossible to as an isolated area and artificially insemination to continue selection process (Kefuss et al., 2004; control mating on professional level in AGAM Fries et al., 2006; Fries and Bommarco, 2007; (Kefuss et al., 2004; Fries et al., 2006, Çakmak and Seeley, 2007; Bühler et al., 2010). Therefore more Fuchs, 2013; Unpublished data). applicable method (good strategy) is to treat Picture 5. Powder sugar method and varroa mites Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 39 DERLEME MAKALESİ / REVIEW ARTICLE Çakmak et. al (2003a) reported the incidence of taken and these bees were killed (Sammataro and varroa (Varroa destructor) and tracheal mites Avitabile, 2011). Powder sugar method provide (Acarapis woodi) in Turkish honey bees (Apis better way to estimate varroa level with 94% mellifera). Acarapis woodior otherAcarapisspp were accuracy compared to detergent method with 300 not found in any of the 10,200 bees examined. The bees from brood area and these bees are returned data suggest that for unknown reasons tracheal alive to their colonies (Çakmak et al., 2011). mites appear to be very rare or do not exist in Powder sugar method (Picture 5) has recently been Turkey. Even though there has been one study improved to be more exact to determine varroa suggested that tracheal mite presence in small level and also the efficay of treatment methods quantities in Turkey (Özkırım and Keskin 2005) this used to control varroa mite (Çakmak and Çakmak report has not been verified by later research and it in Preparation). seems that tracheal mites are not present in This method also provides better estimate of mites Turkey. The question why there is no tracheal when considering the ants carrying out mites mitesin Turkey needs to be explained. (Picture 6) from the pollen traps or drawers. Different materials and chemicals (ether, alcohol, Fackimzadeh used powder sugar to control varroa detergent and etc.) had been used to determine mites but not for determining varroa level of each varroa level in the past and about 200 bees were colony (Fakimzadeh, 2001; 2010). Picture 6. Ants carrying varroa mites Pollen traps had been reported to reduce varroa reported to about ineffectiveness of varroa load up to 35-50% (Çakmak et al, 2002; 2006). treatment and varroa resistance The sufficient Amitraz, (smoke, plastic strips). Coumaphos results had not been obtained due to wrong (pouring), Flumethrin (wood, plastic stipt), Tau- treatment time, migratory beekeeping to control Fluvalinat, Tyhmol (jel, pastry) Formic acid (stript, varroa mite problem (Temiz, 1983; Girişgin and House-made) oxalic acid (Syrup, Smoke) Aydın, 2010;Sammataro and Aviatible, 2011). A treatments are used for varroa control in our promising result has been obtained by selection country. Unfortunately no studies has been studies with artificial insemination and natural 40 U. Arı Drg. Mayıs 2016, 16 (1): 31-48 / U. Bee J. May 2016, 16 (1): 31-48 DERLEME MAKALESİ / REVIEW ARTICLE mating of selected colonies (Çakmak et al., 2011; Molecular identification between N apis and N Cakmak and Fuchs, 2013; Çakmak et al., In cerenae has been performed by PCR-RFLP and by preparation). PCR method (Ütük et al. 2010, Muz et al. 2010, Muz and Muz 2010, Özkan-Koca et al. 2016). It has Viruses carried by varroa mites actually kill the been reported that there was a positive relation with honey bee colonies (Yang and Cox-Foster, 2005; rain and nosemiosis if the nosema spore level is 2007). Viral diseases of honey bees were studied over one million per bee clinical symptoms get very and deformed wing virus, acute bee paralysis, bee clear and there are more risk of nosemiosis in North paralysis, black queen cell virus and Isareli acute and Northwest of Turkey (Bailey and Ball 1991, paralysis virus were determined by RT-PCR Traver and Fell 2014). The fumagillin has been method, in bee larva and this is the first molecular used for nosema treatment and since EU has put study of reporting honey bee viruses in Turkey. limits for usage of Fumagillin and menthol, tymol Chronic bee paralysis was not identified in any and mixture of these have also been used recently samples analyzed (Gülmez et al., 2009; Muz and (Doğaroğlu 2008). Muz, 2009; Okursoy et al., 2010; Beyazit et al., 2012; Özkırım and Schiessen, 2013). Brood diseases have been not investigated sufficiently and might be one of the major factors Nosemiosis are reported in most regions to be affecting colony losses in Turkey. Generally brood present except in desert and poles and more in diseases cause by non-hygienic beekeeping beekeeping developing and humid areas than applications and dirty water sources Özakın et al. others and reported differently depending on (2003). New and old foundations were analyzed geography and beekeepers’ breeding conditions in and 54,5% from old foundations were found to Turkey (Ellis and Munn, 2005). Nosemiosis had include more than one type of bacteria (total 14) been removed in category of WORLD Animal that had been isolated and neither American Health (WAHID-OIE) diseases list in 2004, Paris 72 foulbrood (AFB) nor European foulbrood had been and also it has been removed in 2012 honey bee diagnosed. Some similar hygienic problems were disease emergency diseases list in General determined as a result of unhygienic packaging Assembly“. from honey samples from markets and beekeepers Nosema has been an important one in Marmara (Özakın et al. 2007). Beyazit et al. (2012) and Black Sea regions in some seasons particularly determined 5 (1,27%) AFB (Paenobacillus larvae) in wet season, spring. This new species in Europe from 394 apiaries, 4 (1,01%) EFB (Melissococus and US, Nosema cerenae in recent years has pluton) and 5 (1,27%) chalkbrood (Ascosphera become an important part of CCD (Colony Collapse apis) isolated and AFB had not been identified from Disorder) or colony losses in reports and research 73 wax foundation from companies. results had been linked N ceranae for colony losses Foulbrood diseases as European (EFB) and (Higes et al., 2006). This new nosema species N American foulbrood (AFB) has been diagnosed in cerenae has ben also reported in Turkey recently regions of Turkey. A few cases from apiaries comb (Muz and Muz, 2010; Muz et al., 2010; Özkan-Koca with honey bee larva and in honey and bee wax et al., 2016). Recently the new Nosema species were analyzed and in different regions around the Nosema cerena has been identified in Turkey and country has been reported (Şimşek and Özcan, suspected or causes more colony losses than 2001; Şimşek, 2007; Dümen et al., 2007; expected (Muz and Doğaroğlu, 2011). N ceranae Yalçınkaya and Keskin, 2010). Some researchers has some symptoms such as diarrhea in bees and even reported 16,6% AFB (Özkırım ve Keskin, dead colonies without seeing dead bees around 2005; Yalçınkaya ve Keskin, 2010). However other colonies were called “silent death” by beekeepers. bacterial agents other than European or American Also it seems that N apis is replaced by N cerenae foulbrood also cause some damages if not treated (Higes et al., 2006). properly or without requeening process. Some of Nosemiosis has been found in different rates in these brood diseases caused by unknown reasons different regions and provinces in Turkey in such as queen failure that produces not resistant different ratios (Topcu and Aslan, 2004;Aydın et al. workers to soil bacteria (vanEngelsdorp et al., 2005; Sıralı and Doğaroğlu, 2005; Simsek, 2005; 2013; Çakmak In Preparation). In Turkey, AFB has 2007). Molecular identification of nosemiosis has been declared mandatory notification by the Turkish been done in 2004 (Webster et al., 2004). Ministry of Food, Agriculture, Husbandry. Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 41 DERLEME MAKALESİ / REVIEW ARTICLE Mandatory notification and general quarantine been used extensively in most of the world applies and these bees must be destroyed. including Turkey and new reports about the effects According to EU laws and in Turkey antibiotic use of neonicotinoids have been emphasized on recent to control bacterial brood diseases in honey bees colon losses (Blacquere et al., 2007; Alioune et al., has been prohibited. 2009; Bryden et al., 2013; Lui, 2014; Fisher et al., 2014; Report in Turkish Ministry of Food, Chalkbrood and stonebrood are sometimes seen Agriculture and Husbandry 2014). and wax moth might be a serious pest in summer and fall in mostly western part of Turkey. Fungal The neonicotinoids have been major concern in EU diseases in honey bees the most common are and some neonicotinoid use has been suspended chalkbrood (Ascosphera apis) and stone diseases for some years such as in France (Cressey, 2013). (Aspergillus) in Turkey. Borum (2006) analyzed old In recent years some studies have begun on foundations and found Ascosphera apis %100 and neonicotinoids including Imidocloprid, Thiometoxan 20% Penicillium spp. Even though some and others in Turkey. Neonicotinoids do not kill the medications used for chalbrood diseases (Zeybek, bees in sub-lethal doses but affect the foraging 1991) in recent years instead some practical behavior and consequently the food deposited by beekeeping methods have been used with great foraging bees decrease for winter. Also colonies die success such as strong colonies, changing queens during the winter by consuming more dosages of from healthier colonies with no chalkbrood history, neonicotiniods in the hives (Lu et al., 2014; reducing humidity and stress factors for colonies Karahan et al., 2015). Up to 80% colony losses (Çakmak unpublished data). were reported in European part of Turkey in 2007 an also some reports from Egean and Eastern Wax moth (Galeria mellonella) has been reported in Anatolia (Ünal et al., 2010) apiaries in Egean region (Beyazıt et al., 2012). However, this may reach to 100% in storage rooms Neonicotinoids have been investigated recently by with suitable conditions for wax moth. Recently cold universities and research Institutes and new data storage rooms have been started to be used to are expected to be seen in the near future. prevent wax moth damage for foundations. Also some plant extracts (walnut, thyme, leaves and etc.) and/or formic acid are used to prevent wax COLONY LOSSES and Queen Failure and damage to foundation in most areas. Colony Management There are some species such as bee eater, wasps Queen failure (old queen, non-productive or (hornets), bee wolves that must be considered disease sensitive queen) is also one of the major serious threat to bee colonies particularly in late factors affecting colony losses particularly in early summer and fall to decrease the number of bees or spring and late summer. In early spring it is very entirely decimate the colonies (Çakmak, difficult to requeen colonies due to insufficient 1997;Özbek ,2014). drones or low temperature for mating flights. Colony management as adjusting frames of bees inside the Finally, the future threats as the other mite from hive or adding insulation for temperature security South Asia, Tropilaleps clarea and Small hive and feeding the colonies are crucial in early spring beetle (Aethina tumida) have not been reported yet time. Some colonies die due to a lot of brood in Turkey and also as a major threat, Asian hornet, frames and insufficient food stores inside the hives Vespa velutina has not been notified yet in Turkey. (unpublished data). COLONY LOSSES and Pesticides COLONY LOSSES and Large Scale Migratory Pesticides have been known to affect honey bees Beekeeping in the agricultural fields (Johansen and Mayer Beekeepers, about over 75% of them, move their 1990). However, the new generation of pesticides, colonies three times in a year in Turkey (Güler and the neonicotinoids have been major concern in Demir, 2005; Yılmaz, 2013). Large scale migratory recent years. 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Türkiye’de Arıcılık. TSE Topçu B. and Arslan MÖ. 2004. The Prevalence of Standart Ekonomik ve Teknik Dergi 51(601) 40- Nosemosis in Honey Bee in The Province of 45. Kars. Uludağ Arıcılık Dergisi, 164-170. Yılmaz, B. 2013. Türkiye’de Arıcılık. V. Marmara Ünal , HH., Oruç, HH., Sezgin, A., Kabil, E. Arıcılık Kongresi, 4-6 Nisan, Uludağ 2010.Türkiye’de, 2006-2010 yılları arasında, bal Üniversitesi, Prof.Dr. Mete Cengiz Kültür arılarında Görülen ölümler sonrasında tespit Merkezi, Bursa. edilen pestisitler “Determined pesticides after Zeybek, H.1991. Arı Hastalıkları ve Zararlıları. honey bee deaths between 2006 and 2010 in Tarım ve Köy İşleri Bakanlığı Hayvan Hast. Turkey. U. Arı Derg./ U. Bee J. 10: 118,126. Araş. Enst. Müd. Etlik - Ankara. Ütük AE., Pişkin, FÇ., Kurt M. 2010. Türkiye’de Nosema ceranae’nın ilk moleküler tanısı. Ankara GENİŞLETİLMİŞ ÖZET Üniv Vet Fak Derg, 57, 275-278. vanEngelsdorp, D., Tarpy, DR., Lengerich, EJ., Amaç: Dünyada ve ülkemizde son yıllarda arıcılık Pettis, J., 2013. Idiopathic brood disease konusunda güncel bir konu olan koloni kayıpları ve syndrome and queen events as precursors of olabilecek nedenleri konusunda tartışmalı konular colony mortality in migratory beekeeping bulunmaktadır. Bu konu ülkemizin genel arıcılık operations in the eastern United States. durumu ile yakından ilgili bir konu olduğundan Preventive Veterinary Medicine, 108: 225-233. ülkemizin genel arıcılık konusu ile birlikte ele alınmıştır. Bu çalışmanın amacı ülkemizde genel Webster TC., Pomper KW., Hunt G., Thacker EM., olarak arıcılığın durumu ve son yıllardaki arı Jones SC. 2004. Nosema apis infection in kayıplarının nedenlerinin açıklanmasıdır. worker and queen Apis mellifera, Apidologie 35, 49–54. Tartışma ve Sonuç: Bu derlemede ülkemizde Wilson-Rich, N., Spivak, M., Fefferman, N.H., arıcılığın tarihsel kökleri, ülkemizin doğal kaynakları Starks, P.T. 2009. Genetic, individual and group ve arıcılık açısından özellikle ballı bitkilerin çok facilitiation of diseases resistance in insect olması, ülkemizin coğrafik konumu ile farklı socieities. Ann. Rev. Entomol. 54: 405-23. topoğrafyası ile en az beş farklı arı ırkına Apis mellifera; A.m. anatoliaca, caucasica, meda, Williams, IH. 1994. Bees for pollination-conclusion syriaca and carnicave çok sayıda bal arısı ekotipine and recommendations of the EC workshop on ev sahipiliği yapmasının önemli bir potansiyel bees for pollination held in Brussels, 2-3 March olduğu vurgulanmaktadır. Bal ne bal arısı 1992. Bee World 75(1):46-48. konusunda Kuranda Nahl suresinin 68-69. Yalçınkaya, A., Keskin, N., 2010. The Investigation ayetlerinde bal ve bal arısından bahsedildiği İncil ve of Honey Bee Diseases After Colony Losses in Tevrat’da da arı ve baldan bahsedildiği Hatay and Adana Provinces of Turkey, Mellifera, görülmektedir. Dolayısı ile balın çok önemli bir gıda 10:20 (24-31). olmasının yanında şifa kaynağı olarak tıbbi yönününde bulunduğu belirtilmektedir. Uludağ Arıcılık Dergisi Mayıs 2016, 16 (1): 31-48 / Uludag Bee Journal May 2016, 16 (1): 31-48 47 DERLEME MAKALESİ / REVIEW ARTICLE Koloni sayısı ve son yılardaki Gıda, Tarım ve Bunun yanında son yılarda oldukça gündemde olan Hayvancılık Bakanlığının da desteği ile tüm illerde koloni veya arı kayıpları ve bunların olabilecek Arı yetiştirici birliklerinin kurulması ve tüm nedenleri olarak başta varroa ve diğer parazit ve kolonilerin kayıt altına alınarak üretilen ürüne kadar hastalık etkenleri (Yavru çürüklüğü, nosema yeni geri gidebilme imkanı sağlanması gibi yenilikler türü Nosema ceranae, Marmara Bölgesi’nde bazı sıralanabilir. Ülkemizde üretilen arı ürünlerinin hem yıllar yaygın görülen kireç v.b.) ana arı üretimi ve miktar ve hem de çeşitliliğinin artması ve bu arada kolonilerde kullanımı, pestisitler ve özellikle son oldukça çelişkili olan koloni başına verimin hala yıllarda güncel olan yeni nesil neonikotinoid adı oldukça düşük olması gibi konular irdelenmektedir. verilen insektisitler, koloni yönetimi ve uzun mesafeli gezginci arıcılık gibi nedenler üzerinde Ülkemizde 7,709,636 sayı ile koloni sayısının durulmaktadır. dünyada ilk sıralarda, 56,00 profesyonel arıcı ve 150,000 fazla ailenin arıcılık ile geçinmesi, 107,665 Sonuç olarak ülkemizde bir taraftan bal arısı koloni ton bal üretimi ile ülkemizin 10,000 fazla bitki türü sayısı artarken diğer taraftan bazı bölgelerde ve bunları 3506 sının ülkemize has bitkiler olması önemli koloni kayıpları rapor edilmektedir. Bu bir ve bunları 500 civarının arıcılık açısından ballı çelişkidir ve bunun nedeni olarak Gıda, Tarım ve bitkiler grubuna giren ve nektar ve polen açısından Hayvancılık Bakanlığının giderek artan destekleri zengin bitkiler olduğu görülmektedir. ve arıcıların her yıl doğal oğul ve suni oğullarla koloni sayısını artırmaya çalışmasıdır. Bunun Bunun yanında ülkemizde arıcılık konusunda hem yanında ülkemizde koloni başına bal üretimi doğal yaygın olarak bilimsel arıcılık dergiler ve Arı olarak 18 kg dan 14’e kadar düşmüştür. yetiştirici birliklerinin çıkardığı arıcılık dergileri, son yıllarda kurulan arıcılıkta araştırma merkezleri gibi Ülkemizde arıcılık konusunda çok önemli bir bir çok ilerleme ve yenilikler görülmektedir. potansiyel sahip olduğu, batı bal arısının gen merkezi olması ve farklı topoğrafyası ile çok çeşitli Son yıllarda ülkemizde arıcılık konusunda ballı floraya sahip olması nedeni ile ve bugün ve gelişmelerden biri de arı ürünlerinde çeşitliliğin gelecekte dünya arıcılığında daha çok önemli artması ve yeni ürünlerin artmasıdır. Bunlardan olacağı ve bir sorunun çözümünde rol birisi özellikle Apiterapi konusunun giderek daha oynayabileceği önerilmektedir. çok gündeme gelmesi ve uygulama olanakları tartışılmaktadır. 48 U. Arı Drg. Mayıs 2016, 16 (1): 31-48 / U. Bee J. May 2016, 16 (1): 31-48