Research Article |
Corresponding author: Sonja Mudri-Stojnić ( sonja.mudri-stojnic@dbe.uns.ac.rs ) Academic editor: Thorleif Dörfel
© 2021 Sonja Mudri-Stojnić, Andrijana Andrić, Zlata Markov-Ristić, Aleksandar Đukić, Ante Vujić.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Mudri-Stojnić S, Andrić A, Markov-Ristić Z, Đukić A, Vujić A (2021) Contribution to the knowledge of the bee fauna (Hymenoptera, Apoidea, Anthophila) in Serbia. ZooKeys 1053: 43-105. https://doi.org/10.3897/zookeys.1053.67288
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The current work represents summarised data on the bee fauna in Serbia from previous publications, collections, and field data in the period from 1890 to 2020. A total of 706 species from all six of the globally widespread bee families is recorded; of the total number of recorded species, 314 have been confirmed by determination, while 392 species are from published data. Fourteen species, collected in the last three years, are the first published records of these taxa from Serbia: Andrena barbareae (Panzer, 1805), A. clarkella (Kirby, 1802), A. fulvicornis (Schenck, 1853), A. intermedia (Thomson, 1870), A. lapponica (Zetterstedt, 1838), A. pandellei (Pérez, 1895), A. paucisquama (Noskiewicz, 1924), A. simillima (Smith, 1851), Panurginus herzi (Morawitz, 1892), Epeoloides coecutiens (Fabricius, 1775), Nomada leucophthalma (Kirby, 1802), Chelostoma nasutum (Pérez, 1895), Hoplitis claviventris (Thomson, 1872), and Dasypoda pyrotrichia (Förster, 1855). Almost all the species recorded so far in Serbia belong to the West-Palaearctic biogeographical region, except Megachile sculpturalis (Smith, 1853), which is an alien invasive species native to East Asia. According to the European Red List of bees, 221 species listed in this paper were assessed as Data Deficient; threatened species mostly belong to the families Apidae with 13 species, Colletidae with eight species, and Halictidae with five species. This study contributes to the knowledge of the distribution of bee species in Europe. The present work provides a baseline for future research of wild bee diversity in Serbia and neighbouring regions at the local and regional levels, and a basis for their conservation.
diversity, fauna, Serbia, wild bees
The first available data on the faunistic research of Hymenoptera: Apoidea: Anthophila in the Balkan countries derives from the late 19th century, from the period of the Austro-Hungarian Empire. At that time, scientists were collecting data on the wild bee fauna while travelling through the area of today’s Balkan countries, or they researched parts of the countries where they lived. The borders and names of the Balkan countries have changed several times since then. Therefore, in the present paper, the localities are shown within the current borders of the Republic of Serbia.
The earliest publication, which provided the data on the bee fauna of Serbia is by
After World War II, many authors mainly focused their research on studying the ecology or life history and biology of some species, or the bee diversity of certain regions. Grozdanić studied the life history and ecology of Lasioglossum marginatum (Brullé, 1832) (as Halictus marginatus Brullé, 1832), L. interruptum (Panzer, 1798) (as H. interruptus (Panzer, 1798)), L. malachurum (Kirby, 1802) (as H. malachurus (Kirby, 1802)), H. sajoi (Blüthgen, 1923), H. maculatus (Smith, 1848), H. asperulus (Pérez, 1895), Seladonia kessleri (Bramson, 1879) (as H. kessleri Bramson, 1879), Osmia bicornis Linnaeus, 1758, O. bicolor (Schrank, 1781), O. rufohirta (Latreille, 1811), O. bidentata (Morawitz, 1876), Xylocopa violacea (Linnaeus, 1758), X. valga (Gerstäcker, 1872), X. iris Christ, 1791 (as X. cyanescens Brullé, 1832), Bombus pascuorum Scopoli, 1763 (as B. agrorum (Fabricius, 1787)), Apis mellifera (Linnaeus, 1758), Anthophora plumipes Pallas, 1772 (as A. acervorum (Linnaeus, 1758)), A. plagiata Illiger, 1806 (as A. parietina (Fabricius, 1793)), A. salviae (Panzer, 1804) (as A. crinipes Smith, 1854), A. pubescens (Fabricius, 1781), Eucera (Tetralonia) lyncea (as Tetralonia lyncea (Mocsáry, 1879)), Eucera (Tetralonia) nana (as T. nana (Morawitz, 1874)), Systropha planidens (Giraud, 1861), S. curvicornis (Scopoli, 1770), Eucera excisa (Mocsáry, 1879), Megachile ericetorum (Lepeletier, 1841), and Ceratina spp. (
The importance of bees in terrestrial ecosystems, as well as their ecosystem role in the process of pollination of agricultural crops and wild plants, is widely known. In many European countries, Red Data Books or Red Lists of bees have been produced at the national level. Some European countries have developed specific national actions in order to enhance bee populations and to arrest decline, introduced legislation with the aim of legally protecting all or some species of bees, and/or produced checklists of bees. For some Balkan countries, such as Serbia, data on the diversity of bees are scarce. Among the reasons for such a situation are an insufficient number of wild bee experts and the absence of proper collections. Up-to-date entomological research programmes of wild bees have not been spatially systematic, so certain areas of Serbia have been studied more, while others less. Although there is clear evidence of a decline in pollinators diversity and abundance across Europe (
The present study summarises for the first time all the available records of species of wild bees in Serbia. This paper is not intended as a national checklist of bees, since there are undoubtedly more species yet to be found. The aims of this study are: 1) to review the records on the bee fauna, according to bibliographic sources known to the authors, 2) to present some more recent observations, and finally 3) to provide an updated preliminary list of the species of bees occurring in Serbia. The major purpose of this article is to broaden the knowledge of bee diversity in Serbia and pave the way for future research of wild bee fauna at local and regional levels. Another important aim is to improve an understanding of the status and trends of European pollinators.
Serbia is situated in central and southeast Europe, mostly in the central Balkan peninsula, while its northern part spreads over the southern belt of the Pannonian Plain. The country’s total area is 88,361 km² (Spatial Plan RS 2021–2035, Official Gazette of RS No. 48/19). The main geographic units in Serbia are the Pannonian Region in the north, which covers a third of the country, the Peripannonian Region in the central part of the country, which chiefly consists of hills traversed by rivers, and the mountain and basin region which are dominant in the south. The Carpathian Mountains and the Balkan Mountains stretch in the north-south direction through east Serbia. The Dinaric Arc stretches in the west and southwest. The climate of Serbia is under the influences of the landmass of Eurasia, the Atlantic Ocean, and the Mediterranean Sea. It classifies as a warm-humid continental or humid subtropical climate. In the north of the country, the climate is more continental, whereas south and southeast Serbia are influenced by the Mediterranean climate (
Serbia is a country with a number of rich ecosystems, and species diversity of many groups of organisms is high and contributes to a significant part of Europe’s biodiversity. According to previous research, in the territory of the Republic of Serbia there are: 39% of the European vascular flora, 74% of the European bird fauna, 67% of the European mammal fauna, 51% of the European fish fauna, and 49% of the European reptile and amphibian fauna (
This paper represents a list of bee species in Serbia based on the compiled data known to the authors, gathered from available entomological collections and literature sources between 1890 and 2020, and our own faunistic studies in the decade 2010–2020. Therefore, it includes previously published and unpublished data, supplied by different specialists, as well as some recent records from the authors of this paper. In total, more than 100 publications were examined for relevant records. Additionally, the present list was based on reviewing a database from the online Checklist of Western Palaearctic Bees (Hymenoptera: Apoidea: Anthophila) by
The following abbreviations are used in the text:
AĐ coll. Aleksandar Đukić private collection (determined by Zsolt Józan, specialist in Aculeata research in Central Europe; bee specialist Dr Andrej Gogala from the Slovenian Museum of Natural History, Ljubljana, Slovenia; Prof. Denis Michez, Laboratory of Zoology, University of Mons, and PhD student Jelle Devalez, Department of Geography, University of the Aegean);
AZ coll. Aleksandra Zatezalo collection of the Institute for Nature Conservation of Serbia, Belgrade, Serbia (determined by Zsolt Józan);
SG coll. Simeun Grozdanić collection of the NHMB (Natural History Museum, Belgrade), Serbia;
ZM coll. Zoran Mučalica collection of the NHMB, Serbia.
The cited PhD thesis of
A map of Serbia (Fig.
The list of bees in Serbia presented consists of six families, 58 genera, and 706 species, recorded during the past 130 years. Of the total number of the recorded species, 314 have been confirmed by determination, while 392 species are from literature data. The reported families with the numbers of species (confirmed by determination/based only on literature data) are: Apidae 226 species (91/135), Megachilidae 148 species (62/86), Halictidae 138 species (73/65), Andrenidae 112 species (68/44), Colletidae 69 species (14/55), and Mellitidae 13 species (6/7). The present list includes 14 species with no previously published records for Serbia: Andrena barbareae (Panzer, 1805), A. clarkella (Kirby, 1802), A. fulvicornis (Schenck, 1853), A. intermedia (Thomson, 1870), A. lapponica (Zetterstedt, 1838), A. pandellei (Pérez, 1895), A. paucisquama (Noskiewicz, 1924), A. simillima (Smith, 1851), Panurginus herzi (Morawitz, 1892), Epeoloides coecutiens (Fabricius, 1775), Nomada leucophthalma (Kirby, 1802), Chelostoma nasutum (Pérez, 1895), Hoplitis claviventris (Thomson, 1872), and Dasypoda pyrotrichia (Förster, 1855).
The diversity and proportional representation of bee families are given in Table
Diversity and proportional representation of bee families in Serbia, Europe, and the West Palaearctic region (WP).
Family | Serbia | Europe ( |
WP* ( |
|||||
---|---|---|---|---|---|---|---|---|
No of genera | % of 58 genera | No of species | % of 706 species | No of species | % of 1,965+86 species | No of species | % of 3,408 species | |
Andrenidae | 6 | 10.3 | 112 | 15.9 | 465+24 | 23.8 | 716 | 21.0 |
Apidae | 18 | 31.0 | 226 | 32.0 | 561+16 | 28.1 | 926 | 27.2 |
Colletidae | 2 | 3.4 | 69 | 9.8 | 146 | 7.1 | 270 | 7.9 |
Halictidae | 12 | 20.7 | 138 | 19.5 | 314+30 | 16.8 | 585 | 17.2 |
Megachilidae | 17 | 29.3 | 148 | 21.0 | 442+14 | 22.2 | 852 | 25.0 |
Mellitidae | 3 | 5.2 | 13 | 1.8 | 37+2 | 1.9 | 59 | 1.7 |
Summary of numbers and proportion of bee species within each category of threat.
The European Red List | Europe ( |
Serbia | ||
---|---|---|---|---|
Category | No of species | % of 1,942 species* | No of species | % of 704 species** |
Critically Endangered | 7 | 0.4 | 1 | 0.1 |
Endangered | 46 | 2.4 | 18 | 2.6 |
Vulnerable | 24 | 1.2 | 10 | 1.4 |
Near Threatened | 101 | 5.2 | 64 | 9.1 |
Least Concern | 663 | 34.1 | 390 | 55.4 |
Data Deficient | 1,101 | 56.7 | 221 | 31.4 |
Andrena Fabricius, 1775 (104 species)
Camptopoeum Spinola, 1843 (2 species)
Clavipanurgus Warncke, 1972 (1 species)
Melitturga Latreille, 1809 (1 species)
Panurginus Nylander, 1848 (2 species)
Panurgus Panzer, 1806 (2 species)
Amegilla Friese, 1897 (5 species)
Ammobatoides Radoszkowski, 1867 (1 species)
Ammobates Latreille, 1809 (2 species)
Anthophora Latreille, 1803 (18 species)
Apis Linnaeus, 1768 (1 species)
Biastes Panzer, 1806 (3 species)
Bombus Latreille, 1802 (47 species)
Ceratina Latreille, 1802 (11 species)
Epeoloides Giraud, 1863 (1 species)
Epeolus Latreille, 1802 (5 species)
Eucera Scopoli, 1770 (33 species)
Note: According to
Habropoda Smith, 1854 (2 species)
Melecta Latreille, 1802 (7 species)
Nomada Scopoli, 1770 (77 species)
Pasites Jurine, 1807 (1 species)
Thyreus Panzer, 1806 (7 species)
Triepeolus Robertson, 1901 (1 species)
Xylocopa Latreille, 1802 (4 species)
Colletes Latreille, 1802 (27 species)
Hylaeus Fabricius, 1793 (42 species)
Ceylalictus Strand, 1913 (1 species)
Dufourea Lepeletier, 1841 (4 species)
Halictus Latreille, 1804 (18 species)
Lasioglossum Curtis, 1833 (72 species)
Nomiapis Cockerell, 1919 (3 species)
Nomioides Schenck, 1867 (1 species)
Rhophitoides Schenck, 1861 (1 species)
Rophites Spinola, 1808 (2 species)
Seladonia Robertson, 1918 (8 species)
Sphecodes Latreille, 1802 (25 species)
Systropha Illiger, 1805 (2 species)
Vestitohalictus Blüthgen, 1961 (2 species)
Aglaoapis Cameron, 1901 (1 species)
Anthidiellum Cockerell, 1904 (1 species)
Anthidium Fabricius, 1804 (12 species)
Chelostoma Latreille, 1809 (12 species)
Coelioxys Latreille, 1809 (17 species)
Heriades Spinola, 1808 (2 species)
Hofferia Tkalců, 1984 (1 species)
Hoplitis Klug, 1807 (17 species)
Icteranthidium Michener, 1948 (2 species)
Lithurgus Latreille, 1825 (2 species)
Megachile Latreille, 1802 (34 species)
Osmia Panzer, 1806 (26 species)
Protosmia Ducke, 1900 (1 species)
Pseudoanthidium Friese, 1898 (3 species)
Rhodanthidium Isensee, 1927 (2 species)
Stelis Panzer, 1806 (10 species)
Trachusa Panzer, 1804 (5 species)
Dasypoda Latreille, 1802 (4 species)
Macropis Panzer, 1809 (3 species)
Melitta Kirby, 1802 (6 species)
Of the 706 species from six families of bees presented here for Serbia, more than half (53%) belong to only two families of the group of long-tongued bees, i.e. Apidae (32%) and Megachilidae (21%). Apidae is also the family represented with most genera, 31% of the total number of 58. The genus most rich in species is Andrena (fam. Andrenidae) with 104 reported species, followed by Nomada (fam. Apidae) – 77 and Lasioglossum (fam. Halictidae) – 72 species. Among all genera, 26 (44.8%) are represented with only one or two species. Regarding families, the lowest number of species is recorded within Mellitidae, only 13 (1.8%).
According to the first Red List of European bees (
For most of the species listed here, newer records (starting with year 2000) have been found in various bibliographic sources and collections. However, for 97 species there are no publicly available records from the 21st century. Furthermore, for 15 of these species the only found data of presence in Serbia are from the 19th century, most of them reported only once, therefore the current presence of these species in the given localities is not certain. Our knowledge of bee fauna is still somewhat fragmentary and uneven among different parts of Serbia, since many localities remain understudied or were investigated a long time ago. A comprehensive future research is needed in order to confirm and update the data in this provisional list that is meant to represent a review of so far published records and a basis for further studies. Moreover, among 706 species, the presence in Serbia for 314 species was confirmed by determination and review of materials, while data are from literature for 392 species. A third of all the species (227) are included in our list according to only one literature source each, and for almost a quarter (153) of all the species, the only source for their occurrence in Serbia is the “Checklist of the Western Palaearctic Bees” (
According to the European Red List (
Two of the species presented in our list are without the category of threat, since they are not in the European Red List (
An up-to-date species list is the foundation of biodiversity and conservation work, and knowing which species make up the diverse ecosystems will be critically important in order to protect and restore them. Bees represent one of the key components of global biodiversity, providing vital ecosystem services, being the primary pollinators of most agricultural crops and wild plants. Climate change, land-use change and other anthropogenic pressures have been affecting the diversity of bees throughout the world (
We gratefully thank Aleksandar Stojanović for providing access to the collections of the Natural History Museum, Belgrade, Serbia and Aleksandra Zatezalo for providing material from collection of the Institute for Nature Conservation of Serbia, Belgrade, Serbia. Special thanks to Zsolt Józan (HU), Andrej Gogala (SI), Jelle Devalez (GR), and Denis Michez (BE) for the specimen identifications. We thank Laura Likov for translating literature from Hungarian. We thank Arijana Luburić – Cvijanović for English proofreading. We also thank the editor Thorleif Dörfel, the reviewer Petr Bogusch, and one anonymous reviewer who contributed with constructive suggestions that improved the final version of the paper. The authors acknowledge financial support of the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 451-03-9/2021-14/200358; 451-03-9/2021-14/200125). The authors declare that no competing interests exist.