Research Article |
Corresponding author: Cory S. Sheffield ( cory.sheffield@gov.sk.ca ) Academic editor: Michael S. Engel
© 2020 Cory S. Sheffield, Ryan Oram, Jennifer M. Heron.
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:
Sheffield CS, Oram R, Heron JM (2020) Bombus (Pyrobombus) johanseni Sladen, 1919, a valid North American bumble bee species, with a new synonymy and comparisons to other “red-banded” bumble bee species in North America (Hymenoptera, Apidae, Bombini). ZooKeys 984: 59-81. https://doi.org/10.3897/zookeys.984.55816
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The bumble bee (Hymenoptera, Apidae, Bombini, Bombus Latreille) fauna of the Nearctic and Palearctic regions are considered well known, with a few species occurring in both regions (i.e., with a Holarctic distribution), but much of the Arctic, especially in North America, remains undersampled or unsurveyed. Several bumble bee taxa have been described from northern North America, these considered either valid species or placed into synonymy with other taxa. However, some of these synonymies were made under the assumption of variable hair colour only, without detailed examination of other morphological characters (e.g., male genitalia, hidden sterna), and without the aid of molecular data. Recently, Bombus interacti Martinet, Brasero & Rasmont, 2019 was described from Alaska where it is considered endemic; based on both morphological and molecular data, it was considered a taxon distinct from B. lapponicus (Fabricius, 1793). Bombus interacti was also considered distinct from B. gelidus Cresson, 1878, a taxon from Alaska surmised to be a melanistic form of B. lapponicus sylvicola Kirby, 1837, the North American subspecies (
Bombus johanseni is here recognized as a distinct taxon from B. lapponicus sylvicola Kirby, 1837 (sensu
Arctic, bumble bee, DNA barcode, Holarctic species, melanism, morphology, synonymy
The bumble bees, Bombus Latreille, 1802 (Hymenoptera: Apoidea, Apidae) are one of the most thoroughly studied groups of bees, and extensive taxonomic coverage has existed for the North American fauna since
One common trend exists for most of these recently treated bumble bee species in North America – they are taxa with ranges that extend into, or are restricted to, northern regions of the globe. In North America and elsewhere, northern latitudes have been one of the most poorly studied and sampled regions for bumble bees (
Recent research contributing to the overall creation of a DNA barcode library for bees in Canada (
Bumble bee specimens from northern Canada contained the Royal Saskatchewan Museum (RSKM) were subject to DNA barcoding (
Species and specimens of bumble bees with COI sequences in BOLD used for genetic analyses in this study, including BOLD Process IDs (when available) for each specimen, the Barcode Index Number (BIN) to which the specimens have been assigned, and the genetic distance observed within each species.
To document the geographic range of the taxon of interest, localities from literature (i.e.,
List of Bombus species for which sequences were obtained from GenBank, with GenBank accession numbers, Barcode Index Number (BIN) and the genetic distance observed within each species. Published source of the data are
Species | GenBank Acc. No. | BIN | Genetic distance (%) |
---|---|---|---|
B. glacialis | KY202838, KY202839, KY202840, KY202841, KY202842, KY202843 | BOLD:ADU5113 | 0 |
B. interacti | MG280603 | BOLD:ABA8452 | * |
B. monticola | GU705913, KJ838349, KJ838456, KJ837131, KF434337, KF434338, KF434339 | BOLD:AAD8242 | 0.0011 |
B. lapponicus | KF434329, KF434330, KF434331, KF434332 | BOLD:AAA8078 | 0.0011 |
Photomicrography was undertaken with a Canon EOS 5D Mark II digital camera with an MP-E 65 mm 1:2.8 1–5× macro lens. Measurements were made with an ocular micrometer on a Nikon SMZ1000 stereomicroscope.
Diagnostic nucleotides and their position within the COI mitochondrial gene (i.e., DNA barcode) for Bombus glacialis (ADU5113), B. johanseni (ABA8452, includes B. interacti), B. lapponicus (ssp. lapponicus – AAA8078), B. monticola (AAD8242) and B. lapponicus (ssp. sylvicola – AAA8078).
Species | Nucleotide position | ||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
48 | 105 | 195 | 207 | 241 | 259 | 270 | 318 | 333 | 334 | 349 | 387 | 402 | 411 | 433 | 447 | 504 | 537 | 540 | 555 | 603 | 607 | 648 | |
B. glacialis | C | C | A | C | C | ||||||||||||||||||
B. johanseni | A | C | C | C | C | C | G | ||||||||||||||||
B. lapponicus | C | C | |||||||||||||||||||||
B. monticola | A | C | A | G | C | C | C | ||||||||||||||||
B. sylvicola | G | G | C |
Phylogenetic analysis and genetic distance of COI sequences support the close affinity of B. johanseni to B. glacialis (1.98% genetic distance) and B. monticola (2.74% genetic distance), both Old World taxa (Fig.
Bombus sylvicola var. johanseni
Sladen, 1919: 30g [♀].
Holoytpe ♀. CANADA, Northwest Territories
Bombus (Pyrobombus) interacti
Martinet, Brasero, & Rasmont, 2019: 611 [♀, ♂]. syn. nov.
Holotype ♂. USA, Alaska, Toolik field station, 68°37'32.9"N 149°35'48.8"W, 725m, 28 July 2015, by Martinet and Rasmont, on Epilobium angustifolium [Royal Belgian Institute of Natural Sciences]. Photographs of holotype (as per
Among the members of the Bombus lapponicus – complex, and other Pyrobombus considered here, B. johanseni is genetically most similar to the northern Palearctic B. glacialis (and see
Bombus johanseni female from Sachs Harbour, Banks Island, Northwest Territories, Canada. A Left arrow shows the characteristic black pubescence of the face, right arrow shows the solid area of darker pubescence on the anterior part of thorax B left arrow shows the solid area of darker pubescence on the anterior part of thorax, right arrow shows the typical “red-banding” of the abdomen. Photographs by JMH.
The “red-banded” pattern (Fig.
A A typical “red-banded” bumble bee, Bombus huntii, showing the two red bands (terga 2 and 3) with yellow bands on either side (arrows, terga 1 and 4), and “red-tailed” bumble bees B B. centralis, with red band (terga 3 and 4) preceded by a yellow band (terga 1 and 2) with black apically (arrow) C B. mixtus, with a black band (arrow) separating the basal yellow and apical red bands. Photographs by CSS.
Examples of “red-banded” bumble bees. A Bombus huntii female. Top arrow shows the complete yellow hair patch on the rear of the thorax (scutellum), bottom arrow shows the completely black tegum 5 B B. ternarius female. Top arrow shows the face with both yellow and black hairs, middle arrow shows the entirely yellow anterior area of the thorax, bottom arrow shows the yellow hair patch on the rear of the thorax (scutellum) divided in two by a wedge of black hairs. Photographs by CSS C, D B. ternarius female, from Newfoundland. Arrow in C shows the atypical intermixed black hair on the anterior area of the thorax. Top arrow in D shows the yellow hair patch on the rear of the thorax (scutellum) divided in two by a wedge of black hairs, bottom arrow shows all black tergum 5. Photographs by Carolyn Parsons E B. vancouverensis female (red form). Left arrow shows the pale hair patch on the rear of the thorax (scutellum) divided in two by a wedge of black hairs, right arrow shows the incomplete red band of tergum 2, with black hairs in basal half F B. rufocinctus female (red form). Arrow shows the incomplete red band of tergum 2, being yellow medially in the basal half. Photographs by CSS.
In North America, the males of B. johanseni resemble B. lapponicus sylvicola, B. ternarius, B. huntii, some B. vancouverensis, and pale individuals of B. melanopygus. The males of B. johanseni and B. lapponicus sylvicola can be distinguished from all other Pyrobombus in North America by the bulbous tip of the penis valve (
The Bombus lapponicus – complex (
Unfortunately, Sladen’s taxon B. sylvicola var. johanseni has received little attention, and until this time it was still considered conspecific with B. lapponicus sylvicola (
Future phylogenetic analysis that includes all New and Old World Pyrobombus may clarify the relationships between B. johanseni and B. glacialis, though it would be very useful to obtain additional material, including males, from the Aleutian Islands for additional molecular and morphological analyses. This island chain has proven an interesting link to the Old World bumble bee fauna (
Thanks to Andy Bennett and Sophie Cardinal (Canadian National Collection of Insects (CNC), Ottawa) and Joel Kits (Joel Kits, Ottawa Research and Development Centre, Ottawa) for providing photographs of the holotype of B. sylvicola var. johanseni, and Jason Weintraub and Jon Gelhaus (Department of Entomology, Academy of Natural Sciences, Philadelphia) for photographs of the holotype of B. gelidus during a difficult time of museum closure due to COVID-19. We thank the Government of the Northwest Territories, Wildlife Division, Environment and Natural Resources who provided some of the funding for inventory in that territory, with sincere thanks to Suzanne Carriere (Government of the Northwest Territories, Yellowknife) and Allison Thompson (Wildlife Management Advisory Council [Northwest Territories], Inuvik) for advice, facilitation, local knowledge and genuine support for work in that territory. We received kind help from Rosemin Nathoo (Wildife Management Advisory Council), John and Samantha Lucas, Kyle Wolki, the Hunters and Trappers Committee, staff at the Sachs Harbour Parks Canada office and many others in the community of Sachs Harbour, Northwest Territories. Funding from NatureServe Canada contributed to the processing of specimens collected in Northwest Territories and Yukon. Additional thanks to Paul Williams (Natural History Museum, London) for encouraging continued research on bumble bee taxonomy, and to Paul and Pierre Rasmont (Université de Mons, Mons, Belgium) for constructive comments and critique of the manuscript. Thanks also to Doug Yanega (University of California, Riverside, Riverside) for continued discussions of the ICZN code – it is always much appreciated.
This work is dedicated to Dr. Ken W. Richards (1946–2019) for his work on Canadian bees, including arctic bumble bees.