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Публикации 2017 года

Контактная информация:
Ключевые слова:
падевый мед, растительные тли, лесные деревья, Турция
Страницы:
101–110

Реферат

УДК 638.165.81:595.75:582.475.4

Ünal S., Ayan S., Karadeniz M., Yer E. N. Some forest trees for honeydew honey production in Turkey (Унал С., Аян С., Карадениз М., Йер Е. Н. Использование некоторых лесных деревьев для производства падевого меда в Турции) // Сибирский лесной журнал. 2017. № 4. С. 101–110 (на английском языке, реферат на русском).

DOI: 10.15372/SJFS20170409

© Унал С., Аян С., Карадениз М., Йер Е. Н., 2017

Приводятся материалы исследования насекомых и лесных видов древесных растений, имеющих важное значение для производства падевого меда в Турции. Мед в основном используется в качестве источника питательных веществ и энергии, а также при лечении различных заболеваний. Мед классифицируют на цветочный и падевый. Цветочный мед получают из нектара цветущих растений, тогда как падевый – из медвяной росы, выделяемой насекомыми и собираемой пчелами. Медвяная роса представляет собой сахара, содержащиеся в экскрециях насекомых, питающихся соками растений (из флоэмы деревьев), таких как тли, белокрылки, мучнистые и мягкие червецы. Медвяная роса играет важную роль при производстве падевого меда, который очень востребован как на внутреннем, так и на международном рынке. Ведущими поставщиками падевого соснового меда в мире являются Турция и Греция. Основной производитель медвяной росы в Турции – насекомое Marchalina hellenica Gennadius, обитающее в основном на деревьях сосны турецкой Pinus brutia Ten. и сосны алеппской Pinus halepensis Miller, реже на деревьях сосны кедровой скальной Pinus pinea L., сосны черной Pinus nigra J. F. Arnold и сосны обыкновенной Pinus sylvestris L. В Турции имеются и другие производители медвяной росы, но их доля в продукции падевого меда незначительна, биология не изучена, и до настоящего времени о них ничего не было известно. Всего в результате нашего исследования обнаружено 12 производителей медвяной росы, обитающих на деревьях хвойных пород, и восемь – на деревьях лиственных пород.

Текст статьи


INTRODUCTION

One of the sources of honey in Turkey is so-called honeydew honey, which is produced by bees collecting sugar-contained matters on tree twigs. Honeydew is a sugar-rich sticky liquid, secreted by insect, mainly by aphids and scale insect, as they feed on plant sap. Aphids excrete the rest of the sugar substances after digesting the necessary nutrients. Bees convert this intense sugary substance into honey called honeydew honey (Schmutterer, 1953, 1956; Pechhacker, 1977; Zander and Koch, 1994). Honeydew honeys are known and appreciated by their particular characteristics of strong colors and flavors. The composition criteria for honeydew honeys in respect of fructose and glucose content, as well as with regard to electrical conductivity are different than the composition criteria for floral honeys (Sancho et al., 2008). Scientifically and philosophically precise definitions of honeydew are elusive and references can vary widely. Manna, honeydew and nectar are the words used throughout the Ancient World to describe sweet desirable liquid or crystalline substance sometimes referred to as «food of the gods» (Jones, 2008).

Honeydew honey refers to honey produced by the bees from the secretions of aphides and other bugs, feeding on plant sap. This honey is considered to be a delight in some areas of the world because of its taste and because its rarity. Honey is produced mainly in Turkey, Greece, Germany, Austria, and Spain. In Turkey the dominant tree species for production of the honeydew are pines, mainly Pinus brutia, and then firs, cedars, oaks, junipers and olives (Ermin, 1950; Crane and Walker, 1985; Gürkan, 1988; Morales et al., 1988; Kunkel, 1997; OGM, 2009; Rybak-Chmielewskahszczesna, 2013; Ülgentürk et al., 2013a). Overall, the season of honey production is longer in comparison to flower honey production season because the former begins in the second half of August and lasts till the end of October. This prolonged honey production season is essential for income of beekeepers living in marginal areas and thus important for the intensive agriculture (MAYBİR, 2008; OGM, 2009). Anatolia's geographical location, land formation, climate varieties, variety of plant and insect species, provide different agricultural forestry systems and various insect-plant combinations.

This study reviewers the diversity of insects producing honeydew and their host tree species involved in honeydew production in Turkey.


Honeydew Honey Production in Turkey

Honey is one economically important production. Turkey is one of the 10 largest producers of honey and particularly the largest producer of pine honey, with approximately 15 000 tons of production each year (Sunay, 2008). Pine honey constitutes one fourth of all the honey produced in Turkey. Pine honey is a honeydew honey based on honeydew production by a scale insect Marchalina hellenica living mainly on Turkish pine Pinus brutia and stone pine P. pinea (OGM, 2009; Ayan et al., 2014) (Fig. 1, 2).


Fig. 1.jpg

Fig. 1. The scale insect Marchalina hellenica (Hemiptera: Margarodidae) on pine trees – a main honeydew producer in Turkey. Photo: Y. Yanmadık, Muğla province in Aegean region, autumn period.


Fig. 2.jpg

Fig. 2. Domestic honeydew production in forest region of Turkey.


Droplets of honeydew are collected by honeybees and used to make honeydew honey. There are 35 species from Hemiptera order as well as Marchalina hellenica which produce sugar contained secretion from phloem sap of various plants (Tables 1, 2) (Ülgentürk et al., 2013a).


Table 1. Honey producing insects from the family Hemiptera colonizing conifers in Turkey*

Insect species

Insect Family

Tree species

Tree species E/N**

Cinara cedri Mimeur

Aphididae

Cedrus libani A. Rich,

Pinus brutia Ten.

N

N

C. palaestinensis Hille Ris Lambers

Aphididae

P. brutia Ten.

N

C. (Cedrobium) laportei Remaudiere

Aphididae

C. libani A. Rich

N

C. pilicornis Hartig

Aphididae

P. brutia Ten.

N

Eulachnus rileyi Williams

Aphididae

P. brutia Ten.

N

Schizolachnus pineti Fabricius

Aphididae

P. brutia Ten.

N

Coccus hesperidum Linnaeus

Coccidae

Abies nordmanniana subsp.

bornmuelleriana Mattf.,

C. libani A. Rich.,

P. pinaster Aiton,

P. pinea L.,

Taxus baccata L.

N

N

E

N

N

Ceroplastes floridensis Comstock

Coccidae

C. libani A. Rich.

N

Marchalina hellenica Gennadius

Margarodidae

C. libani,A. Rich

P. brutia Ten.,

P. halepensis Miller,

P. nigra J.F. Arnold.

N

N

N

N

Palaeococcus fuscipennis Burmeister

Margarodidae

A. cilicica (Ant. et Kotschy) Carr.

N

Phenacoccus arambourgi

Balachowsky

Pseudococcidae

C. libani A. Rich.

N

P. yerushalmi Ben-Dov

Pseudococcidae

P. halepensis Miller,

P. pinaster Aiton,

P. sylvestris L.

N

E

N

Planococcus vovae Nasonov

Pseudococcidae

Juniperus oxycedrus L.,

J. horizontalis Moench,

J. excelsa M. Bieb.

N

N

N

Note: *According to Yeşil et al., 2005; Aytar, 2006; Ülgentürk et al., 2012b; Ülgentürk, 2013a; 

**E  ̶  exotic species; N  ̶  native species.


Table 2. Honeydew producing insects from the family Hemiptera colonizing broadleaf trees Turkey

Insect species

Insect family

Tree species

Tree species E/N**

Lachnus roboris (Linnaeus)

Aphididae

Quercus suber L.

E

Filippia follicularis

(Targioni Tozzetti)

Coccidae

Olea europaea L.

N

Lichtensia viburni Signoret

Coccidae

O. europaea L.

N

Saissetia oleae (Olivier)

Coccidae

O. europaea L.,

Ceratonia siliqua L.

N

N

Parthenolecanium rufulum (Cockerell)

Coccidae

Q. cerris L.,

Quercus sp.

N

N

Acanthococcus roboris Goux

Eriococcidae

Q. cerris L

N

Icerya purchasi Maskell

Monophlebidae

Acacia sp.

E

Puto israelensis

Ben-Dov

Pseudococcidae

Quercus sp.

N

Kermes vermilio Planchon

Kermesidae

Quercus sp.

N

Kermes palestiniensis

Balachowsky

Kermesidae

Quercus sp.

N

Kermes greeni Bodenheimer

Kermesidae

Quercus sp.

N

Note: *According to Bodenheimer, 1953; Kaydan, 2004; Ülgentürk et al., 2013a, b; Akça et al., 2016; 

Kaplan and Turanlı, 2016; **E  ̶  exotic species; N  ̶  native species.


The most important characteristic of pine honey is its consistency and durability for many years. The forest land of 1000 m2 produces approximately 20–25 kg pine honey (Mere, 2010). The pine honey from forests forms about 25 % of all the honey produced in Turkey (OGM, 2013). The major pine honey areas for the pine honey productions are in the provinces of İzmir, Aydın, Kuşadası, Dilek Peninsula, Milas, Bodrum, Mugla, Marmaris, Datca, Fethiye, Kas, Balıkesir, Manisa and Canakkale in Mediterranean and Eagean regions in Turkey. About 80 % of all pine honey in Turkey comes from the province of Muğla (Mere, 2010) where nearly ten thousand beekeepers derive their livelihood from pine honey production. M. hellenica is the most common and abundant species there. According to the data from years 1991–2011, yield of pine honey varied from 7 970 to 15 000 tons of the total honey production per year (Firatli et al., 2010; TUİK, 2013; Ülgentürk, 2013a). In Greece annual honey production amounts approximately to 15 000 tons of which about 65 % is derived from honeydew (Bacandritsos, 2004). In general, the majority of Turkish honey production is exported to the EU countries providing in average $ 9–12 million of income. Due to its impact on the economy and employment, beekeeping is an important part of agricultural sector in Turkey, especially in the Muğla province (Ülgentürk et al., 2013a).

Thirteen conifer and eleven broadleaf species were determined as the hosts of the insects producing honeydew (Table 1, 2). Among them, twenty plant species are native and three are exotic: Pinus pinaster, Quercus suber and Acacia sp. (Table 1, 2).

Regarding to the producers of honeydew, Marchalina hellenica seems to be the most significant species for pine honey production. Its stable population is a basic condition for honeydew collection by honeybees (Gürkan, 1988; Gounari, 2006; Ülgentürk et al., 2012a, b, c). Apart from Turkey, M. hellenica has been recorded in Greece and Italy (Bacandritsos, 2004; Kandemir, 2009). The cedar of Lebanon, Cedrus libani, has been recorded as a new host plant of M. hellenica. The infested cedars are found exceptionally in urban areas (Ülgentürk, 2013a). The relation between cedar and M. hellenica should be studied more deeply because the infested cedar trees could become an important alternative for honeybees at higher altitudes (Ülgentürk, 2013a).

Other sap sucking insects such as the aphids Cinara cedri, C. palaestinensis, C. pilicornis, Eulachnus rileyi, Schizolachnus pineti and the scales Palaeococcus fuscipennis and Phenacoccus yerushalmi were recorded on pine trees (Table 1).

Aphids generally live on pine needles and twigs producing honeydew from early spring to late autumn. Contribution of the scales P. fuscipennis and P. yerushalmi to honeydew production is rather insignificant but P. fuscipennis is common in pine forests of eastern Mediterranean and Marmara regions, especially in areas where M. hellenica is very rare. In addition, the fir, Abies cilicica is determined as a new host plant of P. fuscipennis (Ülgentürk, 2013a).

In the Mediterranean region, Cinara cedri on Cedrus libani is the second important honeydew producer. It excretes large quantities of honeydew from April to late June and from September to late October. The honey made from this honeydew could be an appropriate alternative for pine honey production (Ülgentürk et al., 2012c).

Only the scale insect, Puto israelensis, is known to produce sufficient amount of honeydew on broadleaf trees. P. israelensis usually reaches high population density and produces honeydew during the whole spring. Additionally, Parthenolecanium rufulum was recorded on oaks (Ülgentürk et al., 2013b). The distribution of honeydew producing insect species in the different regions of Turkey is given in Fig. 3.


Fig. 3.jpg

Fig. 3. Distribution of the honeydew producing insect species in Turkey.


Despite their economic importance, honeydew producing insects can be treated as serious pests of conifer and broadleaf trees. They suck sap piercing stems, leaves, root and other tender plant partsand. It can cause growth-stunting, deformation on leaves, stems or roots. The insect species Ceroplastes floridensis, Cinara cedri, C. laportei, Eulachnus rileyi, Icerya purchase, Kermes vermilio, Lichtensia viburni and Saissetia oleae are reported as pests in many European, Asian and African countries (Table 3) (Aytar, 2006; Grafton-Cardwell, 2003; Haber and Mifsud, 2007; FAO, 2009; Catalogue of life, 2011; Byron et al., 2015; ).


Table 3. Pest status of insects producing honeydew in Turkey

Insect species

Pest status in countries

References

Acanthococcus roboris

TNB: Hungary, Turkey

Kozár et al., 2013

Ceroplastes floridensis

TNPC: Egypt, Kenya, America, Turkey, China, Cyprus, India, Israel, Australia, France, Greece, Italy, Spain, Brazil

Sharma and Buss, 2011

Cinara cedri

TNPC: Algeria Argentina, Belgium, France, Hungary, Cyprus, 

DNPC: Lebanon, Turkey

Aytar, 2006

Cinara (Cedrobium) laportei

TNC: Algeria, France, India, Israel, Italy, Morocco, Spain, South Africa, Lebanon, Turkey

Aytar, 2006

Cinara palaestinensis

TNC: Greece, Turkey

Tsitsipis et al., 2007

Cinara pilicornis

TPC: Argentina, Turkey

FAO, 2008

Coccus hesperidum

TNPC: Iraq, Iran, Turkey

Aliakbarpour et al., 2010; 

Ülgentürk et al. 2012b

Abdul-Rassoul, 2016

Eulachnus rileyi

TPC: Argentina, Chile, Kenya, Malawi, Turkey

TNPC: Colombia

FAO, 2009.

Filippia follicularis

TNB: Greece, Turkey

Pellizzari et al., 2011

Icerya purchasi

TNB: Slovakia, USA, Hungary, Czech Republic, Turkey

Grafton-Cardwell, 2003; 

Kollár et al., 2016.

Kermes vermilio

TNB: Algeria, Corsica, Crete, France, Greece, Italy, Morocco, Portugal, Sardinia, Sicily, Spain, Turkey

Catalogue of life, 2011

Kermes palestiniensis

TNB: Turkey, Greece, Israel

Catalogue of life, 2011

Kermes greeni

TNB: Turkey, Israel, Syria

Catalogue of life, 2011

Lachnus roboris

TPB: Slovakia

TNB: Poland, Turkey

Kollár et al., 2009; 

Lubiarz and Cichocka, 2014; 

Akça et al., 2016

Lichtensia viburni

TNB: Czech Republic, France, Germany, Russia, Italy, Yugoslavia, England, Wales, Spain, Portugal and USA, Turkey

Haber and Mifsud , 2007

Marchalina hellenica

TNPC: Australia, Italy

DNPC: Greece, Turkey

Ülgentürk et al., 2012b

Palaeococcus fuscipennis

TNPC: America, Turkish Republic of Northern Cyprus, Israel, Turkey

Mendel et al., 1991; 

Fagan et al., 2002; 

Şişman and Ülgentürk, 2010; 

Ülgentürk et al., 2013a

Parthenolecanium rufulum

TNB: Bulgaria, Italy, Turkey

TNPB: Poland

Rainato and Pellizzari, 2009; 

Goliszek et al., 2011; 

Trencheva and Tomov, 2014; 

Kaplan and Turanlı, 2016

Phenacoccus arambourgi

TNC: Lebanon, Turkey

Ülgentürk et al., 2012c

Phenacoccus yerushalmi

TNC: Greece, Turkey

Ben-Dov, 2006

Planococcus vovae

TNC: Iran, Cyprus, Turkey

Kaydan, 2004; Talebi et al., 2008; 

Şişman and Ülgentürk, 2010

Puto israelensis

TNB: Israel, Cyprus, Turkey

Catalogue of life, 2011

Saissetia oleae

TNB: USA, Europe, Asia, Africa, Australia

Byron et al., 2015

Schizolachnus pineti

TPC: Slovakia, Turkey

Kollár et al., 2009

Note: T  ̶  introduced pest; D  ̶  indigenous pest; N  ̶  naturally regenerated forest; P  ̶  planted forest; 

C  ̶  coniferous trees; B  ̶  broadleaf trees.


CONCLUSION

In Turkey, the pine honey is mostly produced from honeydew of M. hellenica and 85 % of this yield has been exported to the EU countries (Fıratlı et al., 2005). In spite of the existence of other honeydew producing insects in Turkey, the data about their participation in honeydew production are rather limited.

During the half-century, the number of bee colonies increased by 3 million, while the forest areas used by bees decreased by 5 million ha, and pastureland areas by 16 million ha (Fıratlı et al., 2010). For this reason, the Ministry of Forest and Water Affairs and the General Directorate of Forestry has prepared an action plan on so-called bee forest. This plan is focused to honey production, which will subsequently assure not only enhancement of income for local residents but also certain protection of forest lands. Importantly, the main part of the plan is based on honeydew production made by the scale insect, M. hellenica. Other honeydew producing insect species and their potential contribution to honeydew honey produce in Turkey need deeper research.


ACKNOWLEDGEMENT

The authors would like to thank to Yüksel YANMADIK, Director of Non-wood Products in Muğla Forestry Regional Directorate (Turkey) for sharing the photographic archive.


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