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Arctic
Environmental Research
Arctic Environmental Research 19(2): 49-55
UDC 595.799 DOI 10.3897/issn2541-8416.2019.19.2.49
Local fauna of bumblebees (Hymenoptera, Apidae) in the lower reaches of the Northern Dvina River
GS Potapov1, YuS Kolosova1
1 N. Laverov Federal Center for Integrated Arctic Research of Russian Academy of Sciences (Arkhangelsk, Russian Federation) Corresponding author: Grigory Potapov ([email protected])
Academic editor: Yuliya V. Bespalaya ♦ Received 30 April 2019 ♦ Accepted 3 June 2019 ♦ Published 20 June 2019
Citation: Potapov GS, Kolosova YuS (2019) Local fauna of bumblebees (Hymenoptera, Apidae) in the lower reaches of the Northern Dvina River. Arctic Environmental Research 19(2): 49-55. https://doi.org/10.3897/issn2541-8416.2019.19.2.49
This article is devoted to an investigation of the local fauna of bumblebees in the lower reaches of the Northern Dvina River in northern Russia where 27 species of bumblebees were found during the present study. The basis of the local fauna of bumblebees in the lower reaches of the Northern Dvina River is related to species with a wide range. The majority of the species are Transpalaearctic. Holarctic, Sub-Transpalaearctic, whereas West-Central Palaearctic are less represented. According to the latitudinal aspect the majority of the species are temperate, and the rest are boreal and arcto-temperate. One of species found in the local fauna is subbo-real. The number of species in the studied local fauna is the largest among the local faunae of the northern part of the Arkhangelsk Region. It is comparable to the local faunae of the southern part of this region. Here is recorded species such as Bombus soroeensis, B. distinguedus, B. ruderarius, B. veteranus, B. humilis, and others, which are not typical of native taiga habitats but are the meadow species in the European North of Russia. Due to the wide development of meadows and ruderal communities in the lower reaches of the Northern Dvina River, these species are widely represented here. The rare species in the studied local fauna are B. patagiatus, B. humilis, B. consobrinus, and B. schrencki.
Keywords
Bumblebees, local fauna, biodiversity, European North, Arkhangelsk Region
Abstract
Copyright Potapov GS, Kolosova YuS. 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.
Introduction
The study of the bumblebee fauna in the Arkhangelsk Region (north of European Russia) has a long history. A small amount of data is known from the end of the 19th century to the end of the 20th century (Potapov and Kolosova 2016a). An intensive study of the local faunae of this region began from the beginning of the 21st century. The localities include the Solovetsky Island, the taiga landscapes of the Russian Plain, the Mezen River, and a number of localities situated in the southern and central part of the Arkhangelsk Region (main publications: Bolotov and Kolosova 2006, Kolosova 2010, Kolosova and Podbolotska-ya 2010, Kolosova and Potapov 2011, Bolotov et al. 2013, Potapov and Kolosova 2016b, 2017). Available materials are presented in the general summary of a previous study regarding the bumblebee fauna of the Arkhangelsk Region (Potapov and Kolosova 2016a).
Concerning the lower reaches of the Northern Dvina River, there are currently a few publications that are mainly related to bumblebee ecology (Po-
tapov 2010, Kolosova et al. 2011, 2012). However, for a long period of time since the 1990s the large bulk of material on this territory was collected but not analysed.
These local data are important in connection with the forecasts of changes in the range of bumblebee species under conditions of global warming (Ras-mont et al. 2015, Potapov et al. 2018). The territories of the European North of Russia are especially interesting, because they are not well studied compared with Europe, and here we can observe the northwards expansion of a number of species which can affect the future scenario (Potapov et al. 2018).
The purpose of this paper is to analyse the local fauna of bumblebees in the lower reaches of the Northern Dvina River.
Materials and methods
Bumblebees were collected in the lower reaches of the Northern Dvina River (Fig. 1) during the period 1994-
Fig. 2. Typical foraging habitats for bumblebees in the lower reaches of the Northern Dvina River. (A) Ruderal communities with Epilobium angustifolium. (B) Meadow with Trifolium repens. (C) Meadow with Cirsium arvense. (D) Roadsides alongside the forest. Photos: G.S. Potapov
2016 by the researchers M.V. Podbolotskaya, I.N. Bo-lotov, B.Yu. Filippov, Yu.S. Kolosova and G.S. Potapov.
The studied territory is located in the northern part of the Arkhangelsk Region. Various types of meadow habitats are widely represented here, both on small islands of the delta and on the mainland (Parinova et al. 2014). The meadow habitats have an anthropogenic origin and they are formed on the areas of native taiga. The age of most of these ecosystems is estimated at several centuries, since their appearance is associated with the development of economic management in the lower reaches of the Northern Dvina River (Shvartsman and Bolotov 2008). However, on this territory large areas of native taiga are preserved.
During this study, bumblebees were collected in various types of habitats. The typical sites of concentration of bumblebee individuals in the lower reaches of the Northern Dvina River are meadows and ruderal communities (Fig. 2). In native taiga forests, bumblebees are rarely encountered, but they are quite abundant on roadsides alongside the forest areas.
A total of 6793 individuals of bumblebees were studied. The specimens of bumblebees are deposited in the Russian Museum of the Biodiversity Hotspots (RMBH) of the Federal Center for Integrated Arctic Research (FCIARctic) of the Russian Academy of Sciences (RAS), and in the Northern (Arctic) Federal
University named after M.V. Lomonosov (NArFU), Arkhangelsk, Russia.
The nomenclature of species follows Williams (2018). The species of bumblebees were identified according to L0ken (1973, 1984) and Panfilov (1978). Identification of species of the Bombus lucorum-com-plex is according to Rasmont (1984), Rasmont et al. (1986), and Rasmont and Terzo (2010). However, according to Bossert (2015), the identification of these cryptic species solely in accordance with morphological characters and without using the DNA-barcod-ing is not always reliable, especially for workers and males. We identified most of the specimens of this complex from the lower reaches of the Northern Dvina River as B. cf. cryptarum (Fabricius, 1775). A small number of specimens are B. cf. lucorum (Linnaeus, 1761). In the European North, B. cryptarum dominates in the bumblebee communities, but B. lucorum is also present (Pamilo et al. 1997).
Types of distributions of bumblebees are given according the classification of Gorodkov (1984). We used the materials of Russian and European entomologists (Pekkarinen and Teras 1993, Byvaltsev 2009, Levchenko and Tomkovich 2014, Rasmont and Iserbyt 2018, and Williams 2018).
The plant species are given according to The Plant List (2013). The source of the map is the Open Street Map.
Results
According to the results of our study, 27 species of bumblebees were found in the lower reaches of the Northern Dvina River (Table 1). Most of the species in the studied local fauna are Transpalaearctic (17 species), 4 species are each of Holarctic and Sub-Transpalaearctic origin, and two species are West-Central Palaearctic. Concerning the zonal distribution, 15 species are temperate, 7 are boreal and 4 are arcto-temperate. One of the species found in the local fauna is subboreal.
The rarest species in the studied territory is B. pata-giatus Nylander, 1848. Only one specimen was collected near Severodvinsk (the pine forest on Yagry Island) by Yulia Kolosova on 15th July 2013. This species is rare in the Arkhangelsk Region and is typical for the meadow habitats (Potapov 2015, Potapov and Kolosova 2016a).
Table 1. Local fauna of bumblebees in the lower reaches of the Northern Dvina River
№ Species Type of distribution
1 Bombus (Kallobombus) soroeensis (Fabricius, 1777) Tp Te
2 B. (Subterraneobombus) distinguendus Morawitz, 1869 Hol Te
3 B. (Megabombus) hortorum (Linnaeus, 1761) Tp Te
4 B. (Mg.) consobrinus Dahlbom, 1832 STp Bo
5 B. (Thoracobombus) muscorum (Linnaeus, 1758) Tp Te
6 B. (Th.) ruderarius (Müller, 1776) Tp Te
7 B. (Th.) veteranus (Fabricius, 1793) Tp Te
8 B. (Th.) humilis Illeger, 1806 Tp Sb
9 B. (Th.) pascuorum (Scopoli, 1763) Tp Te
10 B. (Th.) schrencki Morawitz, 1881 STp Bo
11 B. (Psithyrus) rupestris (Fabricius, 1793) Tp Te
12 B. (Ps.) bohemicus Seidl, 1837 Tp At
13 B. (Ps.) barbutellus (Kirby, 1802) Tp Te
14 B. (Ps.) flavidus Eversmann, 1852 Hol Bo
15 B. (Ps.) norvegicus (Sparre-Schneider, 1918) Tp Te
16 B. (Ps.) quadricolor (Lepeletier, 1832) W-Cp Te
17 B. (Ps.) sylvestris (Lepeletier, 1832) Tp Te
18 B. (Pyrobombus) hypnorum (Linnaeus, 1758) Tp Te
19 B. (Pr.) pratorum (Linnaeus, 1761) W-Cp At
20 B. (Pr.) jonellus (Kirby, 1802) Hol At
21 B. (Pr.) cingulatus Wahlberg, 1854 Tp Bo
22 B. (Bombus) sporadicus Nylander, 1848 Tp Bo
23 B. (Bo.) lucorum (Linnaeus, 1761) Tp Te
24 B. (Bo.) patagiatus Nylander, 1848 STp Bo
25 B. (Bo.) cryptarum (Fabricius, 1775) Hol At
26 B. (Melanobombus) sichelii Radoszkowski, 1860 Tp Te
27 B. (Cullumanobombus) semenoviellus Skorikov, 1910 STp Bo
Note: Hol - Holarctic, Tp - Transpalaearctic, W-Cp - West-Cen-tral-Palaearctic, STp - Sub-Transpalaearctic, At - arcto-temperate, Bo -boreal, Te - temperate, Sb - subboreal.
B. humilis Illeger, 1806 is limited to the lower reaches of the Northern Dvina River but only in the areas near Kholmogory (the southern part of the studied territory). This species was not found in the delta of the Northern Dvina River. However, B. humilis is quite widely distributed on the meadow habitats in the southern and central parts of the Arkhangelsk Region (Potapov 2015, Potapov and Kolosova 2016a).
Also there are quite rare findings in the lower reaches of the Northern Dvina River of B. conso-brinus Dahlbom, 1832 and B. schrencki Morawitz, 1881. These species are recorded here mainly on roadsides alongside the forest areas. B. consobrinus and B. schrencki are belonging to the forest species and they are common in the region, for example, in the northern taiga karst ecosystems (Bolotov and Kolosova 2006).
Discussion
Local fauna of bumblebees in the lower reaches of the Northern Dvina River include 27 species that are close to the number of bumblebees species in the regional fauna (34 species) (Potapov and Kolosova 2016a). As well as throughout the Arkhangelsk Region, in the local fauna of the lower reaches of the Northern Dvina River there are presented species that are widely distributed in the Palaearctic. The reason for this is that the recent distribution of bumblebee species in the study region is a result of post-glacial immigration (Potapov and Kolosova 2016a).
Some of the species in the regional fauna are not represented in the lower reaches of the Northern Dvina River. The first group is B. lapponicus (Fabricius, 1793), which is the tundra species that is typical of many of the Arctic and Subarctic territories (Loken 1973, Chernov 1978, Proshchalykin and Kupianskaya 2005). The most southern locality with a record of B. lapponicus in the Arkhangelsk Region is the lower reaches of the Mezen River (Potapov and Kolosova 2016b).
The second group consists of the species that do not reach the northern part of the Arkhangelsk Region. These are B. laesus Morawitz, 1875, B. deuter-onymus Schulz, 1906, B. campestris (Panzer, 1801), and B. lapidarius (Linnaeus, 1758). They are restricted mainly to the southern part of the Arkhangelsk Region, but B. lapidarius reaches the central part of the region (the Mirniy Town, 62°45'N, 40°20'E) (Potapov and Kolosova 2016a).
These species, as well as B. soroeensis, B. disting-uedus, B. muscorum, B. ruderarius, B. veteranus, B. humilis, B. rupestris, B. barbutellus, B. quadricolor, B. sichelii, and B. semenoviellus are the meadow species in the European North of Russia (Bolotov and Kolosova 2006, Shvartsman and Bolotov 2008, Potapov 2015). They are the typical species for anthropogenic and meadow habitats and they are usually absent in the native taiga (Potapov and Kolosova 2016a). Due to the widespread development of these types of habitats in the lower reaches of the Northern Dvina River, these species are widely represented here. Similar patterns were analysed in detail for bumblebee communities in the European North of Russia, where meadow species quite often have a significant pres-
ence (Shvartsman and Bolotov 2008, Potapov and Kolosova 2016a, 2016b, 2017, 2018).
Concerning B. consobrinus in the lower reaches of the Northern Dvina River, it is noteworthy that, according to Scandinavian authors, this species is nearly monolectic and is closely related with its main food plant Aconitum septentrionale (Loken 1973, Pekka-rinen et al. 1981, Pekkarinen 1988, Pekkarinen and Teras 1993). For this reason, it can be stated that their ranges are quite identical in Fennoscandia. However, Bolotov and Kolosova (2006) note that the close relation of B. consobrinus with A. septentrionale is not so distinct in other regions. In the lower reaches of the Northern Dvina River, we recorded B. consobrinus mainly on A. septentrionale. Nevertheless, this species of bumblebee was found in the areas of the delta without any Aconitum. We assume that B. consobri-nus could be visiting the other entomophilous plants.
According to the models of changes in the species range of bumblebees under conditions of global warming, it is expected that the northwards expansion of a number of species will be apparent between the years 2050 and 2100 (Rasmont et al. 2015). However, it is quite difficult to predict how this process will affect the bumblebee communities in the studied region. Since the 1990s, there has been a decline in agricultural production and the development of natural succession processes on agricultural territories (Shvartsman and Bolotov 2008). This process leads to a reduction in the areas of meadow communities, which in turn will affect the meadow species of bumblebees. At the present time, it is rather difficult to assess the potential contribution of landscape and climatic processes to the predicted change in the local fauna of bumblebees in the lower reaches of the Northern Dvina River.
Conclusion
The local fauna of bumblebees in the lower reaches of the Northern Dvina River has 27 species, and in general it is quite typical for areas of the Arkhangelsk Region, characterised by a wide development of secondary meadows. Similar local faunae are enriched with species that are not typical for the native habitats of taiga. Future studies of bumblebees in the lower
reaches of the Northern Dvina River should be directed towards the research of long-term trends in the bumblebee communities.
Acknowledgements
We are especially grateful to Dr Marina V. Podbolotskaya (NArFU) (1956-2014), who established the research of bumblebees in Arkhangelsk Region and in the lower
reaches of the Northern Dvina River in particular. We are indebted to Dr Ivan N. Bolotov (FCIARctic), and Dr Boris Yu. Filippov (NArFU), who generously supplied us with material from some areas in the studied territory. The bumblebee ecology was studied according to the federal programme of the FCIARctic (no. AAAA-A18-118011690221-0). This study of bee fauna was supported by the project of the Young Scientists of Pomorye (no. 14-2019-02a). Special thanks are due to Dr. M. Copley for improving the language of the paper.
References
■ Bolotov IN, Kolosova YuS (2006) Trends in the formation of biotopic complexes of bumblebees (Hymenoptera, Apidae: Bombini) in the northern taiga karst landscapes of the Western Russian Plain. Russian Journal of Ecology 37(3): 156-166. https://doi.org/10.1134/S1067413606030039
■ Bolotov IN, Kolosova YuS, Podbolotskaya MV, Potapov GS, Grishchenko IV (2013) Mechanism of density compensation in island bumblebee assemblages (Hymenoptera, Apidae, Bombus) and the notion of reserve compensatory species. Biology Bulletin 40(3): 318-328. https://doi.org/10.1134/S1062359013030035
■ Bossert S (2015) Recognition and identification of bumblebee species in the Bombus lucorum-complex (Hymenoptera, Apidae) - a review and outlook. Deutsche Entomologische Zeitschrift 62 (1): 19-28. https://doi.org/10.3897/dez.62.9000
■ Byvaltsev AM (2009) Bumblebees (Hymenoptera: Apidae, Bombini) of the forest steppe and steppe in south of the West Siberian Plain: fauna and communities. PhD Thesis, Institute of Systematics and Animal Ecology of Siberian Branch of RAS, Novosibirsk.
■ Chernov YuI (1978) Structure of the animal population in the Subarctic. Nauka, Moscow, 167 pp.
■ Gorodkov KB (1984) Types of areas of tundra and forests zones insects of the European Part of USSR. Areas of insects in the European part of the USSR: Atlas, Maps 179-221. Nauka, Leningrad, 3-20.
■ Kolosova YuS (2010) Local fauna of bumblebees (Hyme-noptera, Apidae: Bombini) of the European North of Russia: Konosha District of Arkhangelsk Region. Vestnik Pomorsko-go universiteta. Ser.: Estestvennye nauki 3: 57-68.
■ Kolosova YuS, Podbolotskaya MV (2010) Population dynamics of bumblebees (Hymenoptera: Apidae, Bombus Latr.) on
Solovetskiy Archipelago: results of 10-year monitoring. Proceedings of the Russian Entomological Society 81(2): 135-141.
■ Kolosova YuS, Potapov GS (2011) Local faunas of bumblebees (Hymenoptera: Apidae, Bombini) in the European North of Russia: neighbourhood of spacedrom «Plesetsk» of Arkhangelsk Region. Vestnik Pomorskogo universiteta. Ser.: Estestvennye nauki 1: 45-54.
■ Kolosova YuS, Potapov GS, Podbolotskaya MV (2011) Local faunas of bumblebees (Hymenoptera: Apidae, Bombini) of the European North of Russia: the lower reaches of the Northern Dvina River. Vestnik Pomorskogo universiteta. Ser.: Estest-vennye nauki 3: 43-48.
■ Kolosova YuS, Potapov GS, Podbolotskaya MV (2012) Seasonal dynamics in populations of bumblebees (Hymenoptera, Apidae: Bombus) in the northern taiga. Vestnik Severnogo (Arkticheskogo) federalnogo universiteta. Ser.: Estestvennye nauki 1: 71-76.
■ Levchenko TV, Tomkovich KP (2014) Contribution to the bee fauna (Hymenoptera: Apiformes) of the Khanty-Mansi Autonomous Region, Western Siberia, Russia. Entomofauna: Zeitschrift für Entomologie 35(5): 85-100.
■ L0ken A (1973) Studies of Scandinavian bumblebees (Hymenoptera, Apidae). Norsk Entomologisk Tidsskrift 20(1): 1-218.
■ L0ken A (1984) Scandinavian species of the genus Psithyrus Lepeletier (Hymenoptera, Apidae). Entomologica Scandina-vica 23: 1-45.
■ Pamilo P, Tengö J, Rasmont P, Pirhonen K, Pekkarinen A, Kaarnama E (1997) Pheromonal and enzyme genetic characteristics of the Bombus lucorum species complex in Northern Europe. Entomologica Fennica 7: 187-194.
■ Panfilov DV (1978) Key to species of the Family Apidae -Bees. Key to insects of the European Part of the USSR. Nauka, Leningrad 3(1): 508-519.
■ Parinova TA, Nakvasina EN, Sidorova OV (2014) Meadows of the island floodplain in the delta of the North Dvina River. Northern (Arctic) Federal University, Arkhangelsk, 146 pp.
■ Pekkarinen A, Teräs I, Viramo J, Paatela J (1981) Distribution of bumblebees (Hymenoptera, Apidae: Bombus and Psithyrus) in eastern Fennoscandia. Notulae Entomologicae 61: 71-89.
■ Pekkarinen A (1988) Euro-Siberian element in the Fennoscan-dian bumblebee fauna (Hymenoptera, Apidae: Bombus and Psithyrus). Svyazi entomofaun Severnoy Evropy i Sibiri. Publishing Office of the Zoological Institute, Leningrad, 115-122.
■ Pekkarinen A, Teräs I (1993) Zoogeography of Bombus and Psithyrus in Northwestern Europe (Hymenoptera, Apidae). Annales Zoologici Fennici 30 (3): 187-208.
■ Potapov GS (2010) Bumblebees (Hymenoptera: Apidae, Bombus Latr.) on a gradient of the anthropogenic transformation of landscapes in the delta of Northern Dvina. Proceedings of the Russian Entomological Society 81(2): 153-159.
■ Potapov GS (2015) Structure of bumblebee communities (Hymenoptera: Apidae, Bombus Latr.) in the European North of Russia. PhD thesis. Tomsk: Tomsk State University. https:// doi.org/10.17238/issn2227-6572.2015.3.51
■ Potapov GS, Kolosova YuS (2016a) Fauna of bumblebees (Hymenoptera: Apidae: Bombus Latr.) in the mainland part of Arkhangelsk Region, NW Russia. Annales de la Société ento-mologique de France (N.S.) 52(3): 150-160. https://doi.org/10 .1080/00379271.2016.1217167
■ Potapov GS, Kolosova YuS (2016b) Local faunae of bumblebees (Hymenoptera: Apidae, Bombus Latr.) in the European North of Russia: the lower reaches of the Mezen River. Vestnik Severnogo (Arkticheskogo) federalnogo universiteta. Ser.: Es-testvennye nauki 2: 74-81. https://doi.org/10.17238/issn2227-6572.2016.2.74
■ Potapov GS, Kolosova YuS (2017) Local faunae of bumblebees (Hymenoptera: Apidae, Bombus Latr.) in the European North of Russia: vicinity of the town of Shenkursk. Arctic Environmental Research 17(1): 41-49. https://doi.org/10.17238/ issn2541-8416.2017.17.1.41
■ Potapov GS, Kolosova YuS (2018) Distribution and habitat preference of Bombus (Kallobombus) soroeensis (Fabricius, 1777) on the territory of Arkhangelsk Region. Arctic Environmental Research 18(2): 66-70. https://doi.org/10.3897/ issn2541-8416.2018.18.2.66
■ Potapov GS, Kolosova YuS, Vlasova AA (2018) Local fauna of bumblebees (Hymenoptera: Apidae: Bombus Latr.) in the outskirts of the town of Kandalaksha, southwest Kola Peninsula. Arctic Environmental Research 18(2): 62-65. https://doi. org/10.3897/issn2541-8416.2018.18.2.62
■ Proshchalykin MY, Kupianskaya AN (2005) The bees (Hymenoptera, Apoidea) of the northern part of the Russian Far East. Far Eastern Entomologist 153: 1-39.
■ Rasmont P (1984) Les bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et central. Spixiana 7: 135-160.
■ Rasmont P, Scholl A, de Jonghe R, Obrecht E, Adamski A (1986) Identité et variabilité des mâles de bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale (Hymenoptera, Apidae, Bombinae). Revue suisse de Zoologie 93: 661-682. https://doi.org/10.5962/bhl.part.79505
■ Rasmont P, Terzo M (2010) Catalogue et clé des sous-genres et espèces du genre Bombus de Belgique et du nord de la France (Hymenoptera, Apoidea). Mons University, Mons, 28 pp.
■ Rasmont P, Franzén M, Lecocq T, Harpke A, Roberts SPM, Biesmeijer JC, Castro L, Cederberg B, Dvorak L, Fitzpatrick U, Gonseth Y, Haubruge E, Mahé G, Manino A, Michez D, Neumayer J, 0degaard F, Paukkunen J, Pawlikowski T, Potts SG, Reemer M, Settele J, Straka J, Schweiger O (2015) Climatic risk and distribution atlas of European bumblebees. Biorisk 10 (Special issue). https://doi.org/10.3897/biorisk.10.4749
■ Rasmont P, Iserbyt S (2018) Atlas of the European Bees: genus Bombus. Mons University, Mons. http://www.zoologie.umh. ac.be//hymenoptera/page.asp?ID=169
■ Shvartsman YuG, Bolotov IN (2008) Spatio-temporal heterogeneity of the taiga biome in the Pleistocene continental glaciations. The Ural Branch of the RAS, Ekaterinburg, 302 pp.
■ The Plant List (2013) Version 1.1. http://www.theplantlist.org/
■ Williams PH (2018) Bumblebees of the World. The Natural History Museum, London. http://www.nhm.ac.uk/re-search-curation/projects/bombus/index.html
