Research Article |
Corresponding author: Grigory S. Potapov ( grigorij-potapov@yandex.ru ) Academic editor: Michael S. Engel
© 2019 Grigory S. Potapov, Alexander V. Kondakov, Boris Yu. Filippov, Mikhail Yu. Gofarov, Yulia S. Kolosova, Vitaly M. Spitsyn, Alena A. Tomilova, Natalia A. Zubrii, Ivan N. Bolotov.
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:
Potapov GS, Kondakov AV, Filippov BYu, Gofarov MYu, Kolosova YS, Spitsyn VM, Tomilova AA, Zubrii NA, Bolotov IN (2019) Pollinators on the polar edge of the Ecumene: taxonomy, phylogeography, and ecology of bumble bees from Novaya Zemlya. ZooKeys 866: 85-115. https://doi.org/10.3897/zookeys.866.35084
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The High Arctic bumble bee fauna is rather poorly known, while a growing body of recent molecular research indicates that several Arctic species may represent endemic lineages with restricted ranges. Such local endemics are in need of special conservation efforts because of the increasing anthropogenic pressure and climate changes. Here, we re-examine the taxonomic and biogeographic affinities of bumble bees from Novaya Zemlya using historical samples and recently collected materials (1895–1925 vs. 2015–2017). Three bumble bee species inhabit the Yuzhny (Southern) Island and the southern edge of Severny (Northern) Island of this archipelago: Bombus glacialis Friese, 1902, B. hyperboreus Schönherr, 1809, and B. pyrrhopygus Friese, 1902. Bombus glacialis shares three unique COI haplotypes that may indicate its long-term (pre-glacial) persistence on Novaya Zemlya. In contrast, Bombus hyperboreus and B. pyrrhopygus share a rather low molecular divergence from mainland populations, with the same or closely related haplotypes as those from Arctic Siberia and Norway. A brief re-description of Bombus pyrrhopygus based on the newly collected topotypes is presented. Habitats, foraging plants and life cycles of bumble bees on Novaya Zemlya are characterized, and possible causes of extremely low bumble bee abundance on the archipelago are discussed. The species-poor bumble bee fauna of Novaya Zemlya is compared with those in other areas throughout the Arctic. The mean bumble bee species richness on the Arctic Ocean islands is three times lower than that in the mainland Arctic areas (3.1 vs. 8.6 species per local fauna, respectively). General linear models (GLMs) indicate that this difference can be explained by specific environmental conditions of insular areas. Our findings highlight that the insularity is a significant factor sharply decreasing species richness in bumble bee assemblages on the Arctic Ocean archipelagoes through colder climate (lower summer temperatures), prevalence of harsh Arctic tundra landscapes with poor foraging resources, and in isolation from the mainland.
Hymenoptera, Apidae, Bombus, Arctic Ocean archipelagoes, Pleistocene glaciations, mitochondrial DNA
Novaya Zemlya is an Arctic archipelago comprising two large islands, i.e., the Yuzhny (Southern) and Severny (Northern) islands, and numerous small islets. This huge insular area has a harsh Arctic climate (
The terrestrial invertebrate fauna of the Novaya Zemlya Archipelago is relatively poorly known, because there were few researchers compared with other areas of the Arctic (
This paper aims to re-examine the taxonomic and biogeographic affinities of bumble bees from Novaya Zemlya using newly collected samples from two sites on the Yuzhny Island. Based on our novel phylogeographic data, we suggest putative historical biogeographic scenarios explaining the origin of bumble bee fauna on Novaya Zemlya and other Arctic Ocean islands. We compare the species richness of bumble bees on the Arctic Ocean islands with that in the mainland Arctic areas and estimate a possible influence of polar climate and harsh landscapes on the low species richness of bumble bee faunas in the High Arctic using general linear modeling approach. Finally, issues concerning the current taxonomy of Bombus glacialis, B. hyperboreus, B. pyrrhopygus, and the entire subgenus Alpinobombus are critically discussed with a special focus to the newly obtained molecular sequence data from Novaya Zemlya and adjacent areas.
A bumble bee sample from Novaya Zemlya typically represents a daily sampling effort of a single collector in most cases, while only a few samples represent a bumble bee collection during several days (Table
Locality | N | E | Date | Collector | Number of specimens | Number of species | Depository |
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Recent samples | |||||||
Malye Karmakuly (YI) | 72.3992, 52.8671 | 27.vii.2015 | Spitsyn | 5 | 3 | RMBH | |
Malye Karmakuly (YI) | 72.3742, 52.7806 | 28.vii.2015 | Spitsyn | 4 | 2 | RMBH | |
Malye Karmakuly (YI) | 72.3754, 52.7241 | 30.vii.2015 | Spitsyn | 1 | 1 | RMBH | |
Malye Karmakuly (YI) | 72.3739, 52.7167 | 5.viii.2015 | Spitsyn | 1 | 1 | RMBH | |
Malye Karmakuly (YI) | 72.4229, 52.8143 | 6.viii.2015 | Spitsyn | 1 | 1 | RMBH | |
Malye Karmakuly (YI) | 72.3905, 52.7167 | 9.viii.2015 | Spitsyn | 1 | 1 | RMBH | |
Bezymyannaya Bay (YI) | 72.8169, 53.7843 | 21.vii.2017 | Spitsyn | 1 | 1 | RMBH | |
Bezymyannaya Bay (YI) | 72.8338, 53.3781 | 23.vii.2017 | Spitsyn | 6 | 2 | RMBH | |
Bezymyannaya Bay (YI) | 72.8120, 53.8411 | 23.vii.2017 | Spitsyn | 1 | 1 | RMBH | |
Bezymyannaya Bay (YI) | 72.8781, 53.6303 | 23.vii.2017 | Spitsyn | 1 | 1 | RMBH | |
Bezymyannaya Bay (YI) | 72.8667, 53.6335 | 19-21.vii.2017 | Spitsyn | 2 | 2 | RMBH | |
Bezymyannaya Bay (YI) | 72.8528, 53.7134 | 19-26.vii.2017 | Spitsyn | 8 | 2 | RMBH | |
Bezymyannaya Bay (YI) | 72.8335, 53.7339 | 19-26.vii.2017 | Spitsyn | 4 | 3 | RMBH | |
Mean ± s.e.m. | 2.77±0.66 | 1.62±0.22 | |||||
Historical samples | |||||||
n/a | n/a | n/a | n/a | n/a | 6 | 2 |
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Matochkin Shar Strait (YI)* | 73.2, 56.4 | 12.vii.1925 | Vakulenko | 1 | 1 | HNMUK | |
n/a | n/a | n/a | n/a | n/a | 1 | 1 | TMU |
Kostin Shar Strait (YI)* | 71.1, 53.7 | 19.vii.1895 | n/a | 1 | 1 | TMU | |
Krestovaya Bay (NI) | 74.0, 55.5 | 10-12.viii.1909 | Rusanov | 1 | 1 |
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Matochkin Shar Strait, broadcast station (YI) | 73.2, 56.4 | 3.vii.1924 | Tolmachev | 1 | 1 |
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Matochkin Shar Strait, Nochuev Stream (YI) | 73.2, 56.3 | 31.vii.1925 | Vakulenko | 1 | 1 |
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Kostin Shar Strait, Propashchaya Bay (YI)* | 71.1, 53.7 | 16.viii.1925 | Pokrovskiy | 1 | 1 |
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Matochkin Shar Strait (YI)* | 73.2, 56.4 | 11.viii.1925 | Pokrovskiy | 1 | 1 |
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Malye Karmakuly (YI) | 72.3, 52.7 | 23.vii.1896 | Jacobson | 10 | 2 |
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Verkhnyaya Tyulenya Bay (NI)* | 73.3, 56.0 | 9.vii.1901 | Timofeev | 9 | 1 |
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Chekin Bay (NI) | 73.5, 57.0 | 27.vii.1901 | Timofeev | 2 | 2 |
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Novosiltsev Lake (NI)* | 73.6, 56.3 | 2.viii.1901 | Timofeev | 1 | 1 |
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Peschanka River (YI) | 73.2, 53.6 | 22.viii.1902 | n/a | 1 | 1 |
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Bychkov River (NI)* | 73.5, 55.0 | 5.viii.1907 | n/a | 1 | 1 |
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Krestovaya Bay (NI) | 74.0, 55.5 | 10-12.viii.1909 | Rusanov | 5 | 1 |
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Krestovaya Bay (NI) | 74.0, 55.5 | 22.vii.1910 | Sosnovskiy | 7 | 1 |
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Kostin Shar Strait, Propashchaya Bay (YI)* | 71.1, 53.7 | 1-9.viii.1913 | Skribov | 2 | 2 |
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Matochkin Shar Strait, broadcast station (YI) | 73.2, 56.4 | 21.vi.-11.viii.1924 | Tolmachev | 6 | 2 |
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Matochkin Shar Strait (YI)* | 73.2, 56.4 | 13-15.vii.1924 | Tolmachev | 4 | 3 |
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Matochkin Shar Strait, Nochuev Stream (YI) | 73.2, 56.3 | 23.vii.1924 | Tolmachev | 2 | 2 |
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Matochkin Shar Strait, Poperechniy Cape (YI) | 73.2, 56.1 | 5.viii.1924 | Tolmachev | 5 | 2 |
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Matochkin Shar Strait (YI)* | 73.2, 56.4 | 2.vii.1925 | Tolmachev | 14 | 1 |
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Matochkin Shar Strait, Nochuev Stream (YI) | 73.2, 56.3 | 18.vii.1925 | Tolmachev | 2 | 1 |
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Matochkin Shar Strait, Nochuev Stream (YI) | 73.2, 56.3 | 1.viii.1925 | Tolmachev | 1 | 1 |
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Plateau (YI)* | 73.2, 56.3 | 1.viii.1925 | Tolmachev | 1 | 1 |
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Matochkin Shar Strait, coast (YI)* | 73.2, 56.4 | 9.vi.1925 | Vakulenko | 1 | 1 |
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Matochkin Shar Strait, Blizhnyaya Mountain (YI)* | 73.2, 56.5 | 21.vi.1925 | Vakulenko | 3 | 1 |
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Matochkin Shar Strait, observatory (YI) | 73.2, 56.4 | 29.vi.1925 | Vakulenko | 1 | 1 |
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Matochkin Shar Strait (YI)* | 73.2, 56.4 | 6.-15.vii.1925 | Vakulenko | 7 | 3 |
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Belushya Bay (NI) | 73.3, 56.0 | 5.-7.vii.1925 | Vakulenko | 2 | 1 |
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Mean ± s.e.m. | 3.26±0.59 | 1.35±0.11 |
The recent samples of bumble bees were collected by Vitaly M. Spitsyn from two sites on the Yuzhny Island of Novaya Zemlya: Malye Karmakuly Station, 27.vii-9.viii.2015 (N = 13 specimens); and Bezymyannaya Bay, 19–26.vii.2017 (N = 23 specimens) (Figs
Map of bumble bee collecting localities on Novaya Zemlya (YI – Yuzhny Island, NI – Severny Island). Recent samples (red circles): 1 – Malye Karmakuly (YI); 2 – Bezymyannaya Bay (YI). Historical samples (blue circles): 3 – Matochkin Shar Strait (YI); 4 – Kostin Shar Strait (YI); 5 – Matochkin Shar Strait, broadcast station (YI); 6 – Matochkin Shar Strait, Nochuev Stream (YI); 7 – Krestovaya Bay (NI); 8 - Kostin Shar Strait, Propashchaya Bay (YI); 9 – Malye Karmakuly (YI); 10 – Verkhnyaya Tyulenya Bay (NI); 11 – Chekin Bay (NI); 12 – Novosiltsev Lake (NI); 13 – Peschanka River (YI); 14 – Bychkov River (NI), 15 – Matochkin Shar Strait, Poperechniy Cape (YI); 16 – Matochkin Shar Strait, coast (YI); 17 – Matochkin Shar Strait, Blizhnyaya Mountain (YI); 18 – Matochkin Shar Strait, observatory (YI).
Habitats of bumble bees on Novaya Zemlya (Yuzhny Island). (A) Herb tundra patch with Alpine milkvetch (Astragalus alpinus), Bezymyannaya Bay, 20.vii.2017. (B) Herb tundra patch with Arctic sweetvetch (Hedysarum arcticum), Bezymyannaya Bay, 29.vii.2017. (C) Meadow-like association with dwarf fireweed (Chamaenerion latifolium) along a stream valley, Bezymyannaya Bay, 26.vii.2017. (D) Meadow-like association on a mountain terrace, Malye Karmakuly, 28.vii.2015. Photographs by Vitaly M. Spitsyn (A, C–D), Elena Y. Churakova (B).
Primary foraging resources of bumble bees on Novaya Zemlya (Yuzhny Island, Bezymyannaya Bay). (A) Alpine milkvetch (Astragalus alpinus), 26.vii.2017. (B) Arctic sweetvetch (Hedysarum arcticum), 27.vii.2017. (C) Tundra milkvetch (Astragalus umbellatus), 20.vii.2017. (D) Dwarf fireweed (Chamaenerion latifolium), 26.vii.2017. Photographs by Vitaly M. Spitsyn.
Bumble bee assemblages (total number of specimens) in historical and recent collections from Novaya Zemlya.
Locality | Year | Bombus glacialis | Bombus pyrrhopygus | Bombus hyperboreus | |||
N | Caste composite | N | Caste composite | N | Caste composite | ||
Recent samples | |||||||
Malye Karmakuly (YI) | 2015 | 7 | 4♀, 1♂, 2☿ | 5 | 4♀, 1☿ | 1 | 1♀ |
Bezymyannaya Bay (YI) | 2017 | 16 | 1♀, 15☿ | 5 | 4♀, 1☿ | 2 | 2♀ |
Total | 23 | 5♀, 1♂, 17☿ | 10 | 8♀, 2☿ | 3 | 3♀ | |
Historical samples | |||||||
Kostin Shar Strait (YI) | 1895 | 1 | 1♀ | – | – | – | – |
Malye Karmakuly (YI) | 1896 | – | – | 8 | 7♂,1☿ | 2 | 2♀ |
Verkhnyaya Tyulenya Bay (NI) | 1901 | 9 | 9☿ | – | – | – | – |
Chekin Bay (NI) | 1901 | 1 | 1♀ | – | – | 1 | 1♀ |
Novosiltsev Lake (NI) | 1901 | – | – | – | – | 1 | 1♀ |
Peschanka River (YI) | 1902 | 1 | 1♂ | – | – | – | – |
Bychkov River (NI) | 1907 | – | – | 1 | 1♂ | – | – |
Krestovaya Bay (NI) | 1909 | 5 | 1♀, 4♂, | – | – | 1 | 1♂ |
Krestovaya Bay (NI) | 1910 | 7 | 1♀, 4♂, 2☿, | – | – | – | |
Kostin Shar Strait, Propashchaya Bay (YI) | 1913 | – | – | 1 | 1♂ | 1 | 1♀ |
Matochkin Shar Strait (YI) | 1924 | 2 | 2♀ | 1 | 1♀ | 1 | 1♀ |
Matochkin Shar Strait, broadcast station (YI) | 1924 | 6 | 6♀ | 1 | 1♀ | ||
Matochkin Shar Strait, Nochuev Stream (YI) | 1924 | 1 | 1♀ | – | – | 1 | 1♀ |
Matochkin Shar Strait, Poperechniy Cape (YI) | 1924 | 4 | 1♀, 2♂, 1☿ | 1 | 1☿ | – | – |
Matochkin Shar Strait | 1925 | 21 | 11♀, 10☿ | 1 | 1♀ | 2 | 2♀ |
Matochkin Shar Strait, Nochuev Stream (YI) | 1925 | 4 | 1♀, 1♂, 2☿ | – | – | – | – |
Matochkin Shar Strait, Blizhnyaya Mountain (YI) | 1925 | 3 | 3♀ | – | – | – | – |
Matochkin Shar Strait, observatory (YI) | 1925 | – | – | – | – | 1 | 1♀ |
Kostin Shar Strait, Propastshaya Bay (YI) | 1925 | – | – | – | – | 1 | 1♀ |
Belushya Bay (NI) | 1925 | 2 | 2♀ | – | – | – | – |
Total | 67 | 31♀, 12♂, 24☿ | 14 | 3♀, 9♂, 2☿ | 12 | 11♀, 1♂ |
The bumble bee specimens were studied using a stereomicroscope Solo 2070 (Carton Optical (Siam) Co., Ltd., Thailand). For the morphological study of samples, we applied a standard approach and terminology described by
We obtained new sequences of the cytochrome c oxidase subunit I (COI) gene from 27 bumble bee specimens, including the topotypes of Bombus pyrrhopygus (Table
List of COI sequences for bumble bee specimens from Novaya Zemlya (Yuzhny Island). The list of additional sequences of bumble bees from other regions used in this study is presented in Suppl. material
Species | COI haplotype code | GenBank accession number | Specimen voucher [RMBH] | Locality |
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B. glacialis | GL1 | KY202838 | BMB78 | Malye Karmakuly |
B. glacialis | GL1 | KY202839 | BMB79 | Malye Karmakuly |
B. glacialis | GL1 | KY202840 | BMB80 | Malye Karmakuly |
B. glacialis | GL1 | KY202841 | BMB82 | Malye Karmakuly |
B. glacialis | GL1 | KY202842 | BMB83 | Malye Karmakuly |
B. glacialis | GL1 | KY202843 | BMB84 | Malye Karmakuly |
B. glacialis | GL1 | MK530672 | BMB158 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530674 | BMB162 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530669 | BMB153 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530670 | BMB154 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530675 | BMB164 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530676 | BMB165 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530677 | BMB166 | Bezymyannaya Bay |
B. glacialis | GL1 | MK530678 | BMB167 | Bezymyannaya Bay |
B. glacialis | GL2 | MK530671 | BMB157 | Bezymyannaya Bay |
B. glacialis | GL2 | MK530673 | BMB161 | Bezymyannaya Bay |
B. glacialis | GL3 | MK530683 | BMB172 | Bezymyannaya Bay |
B. pyrrhopygus [Topotype] | PY1 | MK530667 | BMB88 | Malye Karmakuly |
B. pyrrhopygus [Topotype] | PY1 | MK530668 | BMB90 | Malye Karmakuly |
B. pyrrhopygus | PY1 | MK530679 | BMB168 | Bezymyannaya Bay |
B. pyrrhopygus | PY1 | MK530680 | BMB169 | Bezymyannaya Bay |
B. pyrrhopygus | PY1 | MK530681 | BMB170 | Bezymyannaya Bay |
B. pyrrhopygus | PY1 | MK530682 | BMB171 | Bezymyannaya Bay |
B. pyrrhopygus | PY1 | MK530684 | BMB173 | Bezymyannaya Bay |
B. hyperboreus | HY1 | MK530666 | BMB87 | Malye Karmakuly |
B. hyperboreus | HY2 | MK530685 | BMB174 | Bezymyannaya Bay |
B. hyperboreus | HY2 | MK530686 | BMB175 | Bezymyannaya Bay |
We used a median-joining network approach using Network v. 4.6.1.3 with default settings (
For phylogenetic analyses, we used the dataset with unique COI haplotypes of Alpinobombus taxa from Novaya Zemlya (Table
Molecular Operational Taxonomic Units (MOTUs) for the subgenus Alpinobombus were obtained using the multi-rate Poisson tree processes (mPTP) model of
To estimate the possible role of climatic parameters and insular environment for the bumble bee species richness throughout the Arctic, we applied the general linear models (GLMs; Statistica v. 13.3, Stat Soft Inc., USA). We used species richness plotted against mean air temperature as a covariate and geographic position as a factor with two levels (island vs. mainland) (
Bumble bees are not abundant on Novaya Zemlya, with the mean value of 2.77 and 3.26 specimens per recent and historical sample, respectively (no significant differences, Mann-Whitney test: U = 189, Nrecent = 13, Nhistorical = 31, P = 0.74) (Table
The recent samples of bumble bees were collected in three habitat types, representing rather small patches within a continuous mountain tundra landscape: (1) meadow-like associations (17 specimens, 47.2% of a total sample), (2) herb tundra patches with Astragalus alpinus (16 specimens, 44.4% of a total sample), and (3) herb tundra patches with Hedysarum arcticum (3 specimens, 8.3% of a total sample) (Fig.
The maximum likelihood phylogeny reveals that two COI haplotypes of Bombus hyperboreus from Novaya Zemlya cluster together with those from Norway (Fig.
Maximum likelihood (IQ-TREE) phylogeny of the subgenus Alpinobombus based on the COI gene haplotypes. The red asterisks indicate the putative species-level clades supported by mPTP species-delimitation model. The black numbers near nodes are ultrafast bootstrap support values. The haplotypes from Novaya Zemlya are colored red. The Bombus hyperboreus species complex with two valid species is colored light blue. Outgroup is not shown.
Bombus hyperboreus and B. pyrrhopygus from Novaya Zemlya share a low molecular divergence from mainland populations, with the same or closely related haplotypes as those from Arctic Siberia and Norway (Fig.
Median-joining haplotype networks of the available COI sequences of bumble bees from Novaya Zemlya and other Arctic areas. (A) Bombus hyperboreus. (B) B. pyrrhopygus. (C) B. glacialis. The circle size is proportional to the number of available sequences belonging to a certain haplotype (smallest circle = one sequence). The small black dots indicate hypothetical ancestral haplotypes. Red numbers near branches indicate the number of nucleotide substitutions between haplotypes.
Morphological patterns of Bombus pyrrhopygus from Malye Karmakuly, Yuzhny Island, Novaya Zemlya: (A) Thorax (prospective topotype RMBH BMB90, queen). (B) Metasoma (same topotype queen). (C) Hind tibia (same topotype queen). (D) Surface of malar space (same topotype queen). (E) Flagellum (same topotype queen). (F) Metasoma (RMBH BMB88, worker). (G) Metasoma (RMBH BMB86, worker). Scale bars 2 mm (A-D, F-G); 1 mm (E). Photographs by Grigory S. Potapov.
The number of bumble bee species on islands of the Arctic Ocean varies from one (Devon Island, Canadian Arctic Archipelago) to seven (Iceland) species, while local faunas in the mainland Arctic areas contains from three (Taymyr Peninsula, Arctic Siberia) to 15 (Pechora River Delta in Arctic European Russia) species (Table
Species richness of bumble bees on the Arctic Ocean islands and the mainland.
Region | Latitude | Longitude | Biome type** | JMT, °C* | AMT, °C* | Number of species | References |
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Islands | |||||||
Novaya Zemlya | 72.3N, 52.8E | Arctic tundra | 10.42 | -7.48 | 3 | This study | |
Vaigach Island | 70.2N, 59.0E | Tundra | 11.38 | -7.00 | 5 |
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Kolguev Island | 68.8N, 49.2E | Tundra | 13.45 | -3.42 | 5 |
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Wrangel Island | 71.0N, 178.5W | Arctic tundra | 2.29 | -12.18 | 3 |
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Banks Island | 71.5N, 123.8W | Arctic tundra | 4.45 | -14.21 | 2 |
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Victoria Island | 69.1N, 105.0W | Tundra | 7.46 | -14.99 | 4 |
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Prince Patrick Island | 76.1N, 121.7W | Arctic tundra | 3.52 | -17.54 | 3 |
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Melville Island | 75.2N, 109.0W | Arctic tundra | 4.03 | -17.33 | 1 |
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Devon Island | 74.6N, 82.4W | Arctic tundra | 3.29 | -17.69 | 1 |
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Baffin Island | 72.6N, 77.9W | Arctic tundra | 4.41 | -15.98 | 5 |
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Southampton Island | 64.2N, 83.2W | Arctic tundra | 8.55 | -11.66 | 4 |
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Ellesmere Island | 80.0N, 85.9W | Arctic tundra | 4.41 | -20.38 | 4 |
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Greenland | 69.2N, 50.0W | Arctic tundra | 5.44 | -8.05 | 2 |
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Iceland | 64.0N, 21.6W | Tundra | 10.45 | 3.69 | 1[+6]*** |
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Mean ± s.e.m. | 6.7±1.0 | -11.7±1.8 | 3.1±0.4 | ||||
Mainland | |||||||
Finnmark, Norway | 70.8N, 29.0E | Tundra | 11.66 | -0.85 | 8 |
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Kola Peninsula (north) | 69.0N, 33.1E | Tundra | 12.34 | -0.19 | 7 |
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Kanin Peninsula (north) | 67.8N, 44.1E | Tundra | 14.25 | -1.57 | 5 |
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Kanin Peninsula (south) | 66.6N, 44.6E | Forest tundra | 14.65 | -1.27 | 14 |
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Pechora River Delta | 67.6N, 53.0E | Forest tundra | 13.09 | -3.72 | 15 |
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Pymvashor Hot Springs | 67.0N, 60.5E | Tundra | 12.82 | -5.55 | 12 |
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Yugorsky Peninsula | 69.7N, 61.6E | Tundra | 11.60 | -7.08 | 11 |
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Polar Ural | 66.9N, 65.7E | Tundra | 12.71 | -6.48 | 5 |
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Taymyr Peninsula (south) | 73.2N, 90.5E | Tundra | 10.49 | -12.49 | 3 |
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Tiksi, Yakutia | 71.6N, 128.8E | Tundra | 13.88 | -16.54 | 6 |
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Indigirka River Delta | 71.0N, 149.0E | Tundra | 10.67 | -14.45 | 8 |
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Chukotka Peninsula | 64.7N, 177.4E | Tundra | 10.70 | -7.54 | 7 |
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Alaska (north) | 69.4N, 152.1W | Tundra | 10.66 | -9.17 | 13 |
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Mackenzie River Delta | 67.5N, 134.1W | Tundra | 13.92 | -8.98 | 14 |
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Coppermine River Delta | 67.7N, 115.1W | Tundra | 9.75 | -11.45 | 4 |
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Bathurst Inlet | 66.5N, 108.0W | Tundra | 9.59 | -12.87 | 5 |
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Mean ± s.e.m. | 12.0±0.4 | -7.5±1.3 | 8.6±1.0 |
The bumble bee species richness is correlated with latitude (Spearman R = -0.39, N = 30, P = 0.0325), annual mean air temperature (Spearman R = 0.4219, N = 30, P = 0.0202), and July mean air temperature (Spearman R = 0.7537, N = 30, P < 0.0001). As the mean temperature of July was found to be the most influential factor based on the nonparametric correlation analyses, we have used this parameter in the general linear models (GLMs) (Table
Results of general linear models (GLMs) of bumble bee species richness on the Arctic Ocean islands and the mainland. Regression models were simplified to the minimal adequate models (
Response variable | Source | SS | d.f. | F | P |
Species richness (R2 = 0.72) | Intercept | – | – | – | n.s. |
July mean temperature | 734.75 | 1 | 87.02 | <0.0001 | |
Geographic position (island vs mainland) | – | – | – | n.s. | |
July mean temperature × Geographic position | 60.11 | 1 | 7.12 | 0.0125 | |
Error | 236.42 | 28 | |||
Species richness (R2 = 0.72) | Intercept | 888.43 | 1 | 102.25 | <0.0001 |
July mean temperature | – | – | – | n.s. | |
Type of biome | 259.40 | 2 | 14.93 | <0.0001 | |
July mean temperature × Type of biome | – | – | – | n.s. | |
Error | 234.60 | 27 |
Apis alpina Linnaeus (by subsequent designation)
Bombus kirbyellus subsp. pyrrhopygus
Bombus kirbyellus var. pleuralis
sensu Friese, 1902 non Nylander, 1848:
Bombus kirbyellus var. cinctus
Bombus kirbyellus var. cinctellus
Bombus alpinus var. diabolicus
Bombus alpinus var. pretiosus
Bombus kirbyellus var. semljaensis
Bombus arcticus var. alpiniformis
Nowaja Semlja [Novaya Zemlya] (
Whereabouts unknown.
(pinned specimens). Topotypes: NOVAYA ZEMLYA, YUZHNY ISLAND: Malye Karmakuly, 72.3992°N, 52.8671°E, meadow-like association in tundra, 2♀, Spitsyn leg. [RMBH: voucher nos. BMB88 and BMB90]; Malye Karmakuly, 72.3742°N, 52.7806°E, meadow-like association in tundra, 28.vii.2015, 1☿, Spitsyn leg. [RMBH]; Malye Karmakuly, 72.3754°N, 52.7241°E, meadow-like association in tundra, 30.vii.2015, 1♀, Spitsyn leg. [RMBH]; Malye Karmakuly, 72.3905°N, 52.7167°E, meadow-like association in tundra, 9.viii.2015, 1♀, Spitsyn leg. [RMBH]. Other recent material examined: NOVAYA ZEMLYA, YUZHNY ISLAND: Bezymyannaya Bay, 72.8169°N, 53.7843°E, tundra with Astragalus alpinus, 21.vii.2017, 1♀, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8338°N, 53.3781°E, tundra with Astragalus alpinus, 23.vii.2017, 1♀, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8781°N, 53.6303°E, tundra with Hedysarum arcticum, 23.vii.2017, 1☿, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8667°N, 53.6335°E, tundra with Hedysarum arcticum, 19–21.vii.2017, 1♀, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8335°N, 53.7339°E, meadow-like association with Artemisia tilesii and Salix lanata, 19–26.vii.2017, 1♀, Spitsyn leg. [RMBH]. Historical material examined: NOVAYA ZEMLYA, YUZHNY ISLAND: Matochkin Shar Strait, 11.viii.1925, 1♀, Pokrovskiy leg. [
Queen morphology: Malar space slightly longer than the distal width. Central part of clypeus with rather sparse puncturing, while puncturing becomes gradually denser laterally and in the lower part of clypeus. Supra-orbital line transecting ocelli. A3 distinctly longer than A4, A4 shorter than A5. Outer surface of the hind tibia distinctly alutaceous, dull. T4 and T5 chagrinated and punctured. Queen color pattern: Head and face black, vertex with slight admixture of yellow hairs. Collar, scutellum, T1 and T2 ochreous-yellow. T3 – T6 black. T6 with slight admixture of ferruginous hairs, which is more distinct in the specimen BMB88.
Other specimens collected on Novaya Zemlya (Table
This species differs from the other Novaya Zemlya bumble bees by the shortest flight period from mid-July to mid-August, with workers and males emerging in late July (Fig.
Arctic Eurasia from Scandinavia to Chukotka Peninsula (
Bombus hyperboreus
Lapponia [Lapland], Sweden
Holotype NHRS-HEVA000004559, Swedish Royal Museum of Natural History (Naturhistoriska riksmuseet), Stockholm, Sweden.
(pinned specimens). Recent material examined: NOVAYA ZEMLYA, YUZHNY ISLAND: Malye Karmakuly, 72.3992°N, 52.8671°E, meadow-like association in tundra, 27.vii.2015, 1♀, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8528°N, 53.7134°E, tundra with Astragalus alpinus, 19–26.vii.2017, 1♀, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8335°N, 53.7339°E, meadow-like association with Artemisia tilesii and Salix lanata, 19–26.vii.2017, 1♀, Spitsyn leg. [RMBH]. Historical material examined: NOVAYA ZEMLYA, YUZHNY ISLAND: exact locality and date unknown, 1♀, Pittioni det. [
This species flights from late June to late August, with male appearance in mid-August (Fig.
The nominative subspecies inhabits Arctic Eurasia, including the Yuzhny Island and the southern edge of Severny Island of the Novaya Zemlya Archipelago, while Bombus hyperboreus natvigi is known from Arctic North America, and Greenland (
Taxonomic comments on the Bombus hyperboreus species complex. Three taxa belong to the Bombus hyperboreus species complex: B. hyperboreus from Arctic Eurasia (including Novaya Zemlya), B. natvigi from Arctic North America and Greenland, and B. kluanensis from Alaska and Yukon (
Apis hypnorum Linnaeus (by monotypy)
Bombus lapponicus subsp. glacialis
Bombus lapponicus
sensu Friese, 1923 non Fabricius, 1793. –
Bombus lapponicus var. errans Friese, 1923: 4.
Bombus lapponicus var. errans var. aberrans Friese, 1923: 4 [intrasubspecific name (Art. 45.6.1 of ICZN), unavailable (Art. 45.5 of ICZN)].
Pratibombus glacialis
Sparre-Schneider, 1902. –
Bombus glacialis
Sparre-Schneider, 1902. –
Bombus glacialis
Friese, 1902. –
Nowaja Semlja [Novaya Zemlya] (
Syntype ♀ No. TSZX 7288 labelled “Nova Semlja. v. glacialis Sp. Schn.”, Sparre-Schneider’s type collection, Tromsø University Museum, Norway [examined and re-described by us (
Recent material examined: NOVAYA ZEMLYA, YUZHNY ISLAND: Malye Karmakuly, 72.3992°N, 52.8671°E, meadow-like association in tundra, 27.vii.2015, 1♀, 1♂, Spitsyn leg. [RMBH]; Malye Karmakuly, 72.3742°N, 52.7806°E, meadow-like association in tundra, 28.vii.2015, 2♀, 1☿, Spitsyn leg. [RMBH]; Malye Karmakuly, 72.3739°N, 52.7167°E, meadow-like association in tundra, 5.viii.2015, 1♀, Spitsyn leg. [RMBH]; Malye Karmakuly, 72.4229°N, 52.8143°E, meadow-like association in tundra, 6.viii.2015, 1☿, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8338°N, 53.3781°E, tundra with Astragalus alpinus, 23.vii.2017, 5☿, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8120°N, 53.8411°E, tundra with Astragalus alpinus, 23.vii.2017, 1☿, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8667°N, 53.6335°E, tundra with Hedysarum arcticum, 19–21.vii.2017, 1☿, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8528°N, 53.7134°E, tundra with Astragalus alpinus, 19–26.vii.2017, 1♀, 6☿, Spitsyn leg. [RMBH]; Bezymyannaya Bay, 72.8335°N, 53.7339°E, meadow-like association with Artemisia tilesii and Salix lanata, 19–26.vii.2017, 2☿, Spitsyn leg. [RMBH]. Historical material examined: NOVAYA ZEMLYA, YUZHNY ISLAND: Matochkin Shar Strait, 12.vii.1925, 1♀, Vakulenko leg. [
Phenology. This species has the longest flight period among Novaya Zemlya bumble bees that lasts from early June or mid-June to late August (Fig.
Distribution. Yuzhny Island and the southern edge of Severny Island of the Novaya Zemlya Archipelago, probably also Wrangel Island (
Taxonomic comments. The results of our previous integrative study indicate that Bombus glacialis is a separate bumble bee species that is phylogenetically and morphologically distinct from the other taxa in the B. lapponicus complex (
Three species of bumble bees were recorded from Novaya Zemlya based on recent and historical samples: Bombus pyrrhopygus, B. hyperboreus, and B. glacialis (Table
It is known that old European entomologists often confused Bombus pyrrhopygus with B. balteatus (= B. kirbyellus s. lato) due to the high levels of variability in external coloration patterns (fide
Specimens of Bombus lapponicus are also lacking in recent and historical samples from Novaya Zemlya (Tables
Based on newly obtained results, we suggest that this subgenus includes eight valid species as follows:
(1) B. alpinus (Linnaeus, 1758) [supported by the COI (
=B. alpinus helleri von Dalla Torre, 1882 [
(2)B. balteatus Dahlbom, 1832 [supported by the COI (
(3) B. hyperboreus Schönherr, 1809 [supported by the COI (
ssp. hyperboreus Schönherr, 1809 [Arctic Eurasia]
ssp. natvigi Richards, 1931 [Arctic North America and Greenland]
(4) B. kluanensis Williams & Cannings, 2016 [supported by the high level of the COI divergence (
(5) B. kirbiellus Curtis, 1835 [supported by the COI (
(6) B. neoboreus Sladen, 1919 [supported by the COI (
(7) B. polaris Curtis, 1835 [supported by the COI (
(8) B. pyrrhopygus
Based on our assessment (Table
As for the mainland, sites with the highest number of bumble bee species are situated in river and mountain valleys having species-rich flowering plant associations that allows environment-induced local expansions of boreal bumble bees (e.g., Bombus distinguendus, B. hortorum, and B. consobrinus) to the Arctic (
We found that the mean species richness of bumble bees on the Arctic Ocean islands is three times lower than that in the mainland Arctic areas (3.1 vs. 8.6 species per local fauna, respectively). Our GLMs revealed that this difference could be explained by specific environmental conditions of insular areas, i.e., the colder climate (lower mean summer temperature) and the prevalence of harsh Arctic tundra landscapes with extremely poor foraging resources. These results support the conclusion of
Bombus pyrrhopygus was described from Novaya Zemlya, and we have sequenced the prospective topotypes of this species from Malye Karmakuly. The topotypes share the same COI haplotype as samples from Norway and Kamchatka, indicating a broad range of this species across the Arctic Eurasia in the Late Pleistocene or Early Holocene. The phylogeographic pattern discovered in Bombus hyperboreus is similar to that in B. pyrrhopygus, with similar haplotypes in Novaya Zemlya and the mainland areas (Fig.
The populations of Bombus glacialis from Novaya Zemlya share three COI haplotypes, indicating its long-term persistence on the archipelago that agrees with the hypothesis of
At first glance, we could assume that Bombus pyrrhopygus and B. hyperboreus spread across the emerged Eurasian shelf margin in the Late Pleistocene, with subsequent fragmentation of their continuous ranges in the Holocene. Bombus glacialis shares another phylogeographic pattern, with at least three unique COI haplotypes in Novaya Zemlya’s population, while this species was not found from the mainland areas (
Bumble bees are extremely scarce on Novaya Zemlya, with only a few specimens being collected per sampling effort (Table
The collection of bumble bees from Novaya Zemlya was performed during the ‘Floating University’ Scientific Expedition of the Northern Arctic Federal University in the years 2015 and 2017. This study was carried out using facilities of the Russian Museum of Biodiversity Hotspots, Federal Center for Integrated Arctic Research of the Russian Academy of Sciences (Arkhangelsk, Russia). The molecular analyses of bumble bees were supported by the Russian Foundation for Basic Research, RFBR (Projects Nos. 18-44-292001 and 19-34-50016). The phylogenetic investigation was partly funded by the Russian Ministry of Education and Science (Project No. 6.2343.2017/4.6) and Northern Arctic Federal University. The study of bumble bee ecology was supported by the federal program of the Federal Center for Integrated Arctic Research of the Russian Academy of Sciences (АААА-А18-118011690221-0). We are grateful to Dr. Elena Y. Churakova (Federal Center for Integrated Arctic Research of the Russian Academy of Sciences, Arkhangelsk, Russia) for providing the photograph of the habitat (herb tundra patch with Arctic sweetvetch) and for assistance in identification of flowering plant species. Special thanks go to Dr. J. Paukkunen (Finnish Museum of Natural History, University of Helsinki, Finland) and M. V. Berezin (Moscow Zoo, Russia) for their help with literature and valuable discussions on the Arctic bumble bees. Additionally, we are grateful to the staff of the Natural History Museum (London, United Kingdom), the Tromsø University Museum (Tromsø, Norway), the Zoological Museum of Moscow University and the Zoological Institute of Russian Academy of Sciences (Saint Petersburg, Russia) for the opportunity to examine their collections. We are grateful to Dr. Denis Michez (University of Mons, Belgium) and the anonymous reviewer for their helpful comments on earlier versions of this paper.
Tables S1–S2. Lists of the COI gene sequences
Data type: molecular sequence data
Table S3. Samples of bumble bees from Novaya Zemlya examined in this study
Data type: specimen data