Bombus pyrrhopygus Friese, 1902

Williams, Paul H., Berezin, Mikhail V., Cannings, Sydney G., Cederberg, Björn, Ødegaard, Frode, Rasmussen, Claus, Richardson, Leif L., Rykken, Jessica, Sheffield, Cory S., Thanoosing, Chawatat & Byvaltsev, Alexandr M., 2019, The arctic and alpine bumblebees of the subgenus Alpinobombus revised from integrative assessment of species’ gene coalescents and morphology (Hymenoptera, Apidae, Bombus), Zootaxa 4625 (1), pp. 1-68 : 23-28

2. Bombus pyrrhopygus Friese

( Figs. 2 , 22‒38 , 130 )

< Bombus kirbyellus subsp.> pyrrhopygus Friese 1902:495 , type-locality citation ‘Nowaja Semlja’ ( Russia). Lectotype female (#4707), MNHU examined PW, (Cyrillic) ‘[Novaya Zemlya]’ ( Russia). Notes 1, 2. Status revised to Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

[B.<ombus> kirbyellus var. pyropygus Friese ; Friese 1905: 509, incorrect subsequent spelling. Note 3.]

[ Bombus kirbyellus var. friesei Skorikov 1908:111 , infrasubspecific. Note 4.]

Bombus kirbyellus var. cinctus Friese 1911a:456 , type-locality citation ‘Kola und Nowaja Semlja’ (Murmanskaya and Novaya Zemlya, Russia). Lectotype male (#4711), MNHU examined PW, (Cyrillic) ‘[Novaya Zemlya]’ ( Russia). Note 5. Synonymisation with Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

Bombus kirbyellus var. cinctellus Friese 1911a:456 , type-locality citation ‘Nowaja Semlja’ (Novaya Zemlya, Russia). Lectotype male (#4712), MNHU examined PW, (Cyrillic) ‘[Novaya Zemlya]’ ( Russia). Note 6. Synonymisation with Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

Bombus alpinus var. diabolicus Friese 1911b:571 , type-locality citation ‘Kola’ (Murmanskaya, Russia). Holotype queen (#4709) by monotypy, MNHU examined PW, ‘Kola’ ( Russia). Synonymisation with Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

Bombus alpinus var. pretiosus Friese 1911b:571 , type-locality citation ‘Nordkap’ ( Norway). Holotype male (#4710) by monotypy, MNHU examined PW, ‘Tromsoe’ ( Norway). Synonymisation with Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

< Bombus> k.<irbyellus> var. semljaënsis Friese [1924] :4, type-locality citation ‘Maschigin-Bucht Pomorskaja-Bucht Serebryanka-Bucht’ (Novaya Zemlya, Russia). Lectotype male (#4713), MNHU examined PW, ‘Novaj Semlja’ ( Russia). Note 7. Republished by Friese 1924:438. Synonymisation with Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

< Bombus arcticus> var. alpiniformis Richards 1931:13 , type-locality citation ‘Dovre, Esmark’ (Oppland, Norway). Holotype male (#5009) by monotypy, ZMO examined FØ, photo examined PW, ‘Dovre’ (Oppland, Norway). Synonymisation with Bombus pyrrhopygus Friese suggested by Williams et al. (2016:2), confirmed here.

[< Alpinibombus tristis > mod. lineatus Skorikov 1937:56, infrasubspecific.]

Note 1 ( pyrrhopygus ). Friese (1902) described the taxon B. kirbyellus ssp. pyrrhopygus giving characters of colour pattern, and the type locality as ‘Nowaja Semlja’ (= Novaya Zemlya) from material collected by G. Jacobson ( Friese 1905). We now understand that this island has just two species: B. hyperboreus and the Old World sister-species to B. polaris , and does not have the true B. kirbiellus (the correct original spelling of B. kirbyellus ).

Friese (1905) on page 509 lists males and females of his ‘ B. kirbyellus - pyropygus ’ collected from Novaya Zemlya on August 2 and 4 of 1896. On page 515 he lists a further female collected by G. Jacobson from Novaya Zemlya on July 23 1896. Therefore it is likely that multiple syntypes existed. Unfortunately at no point did he state an intention to change the spelling of the name, and neither did he include both spellings of his pyrrhopygus and pyropygus in the same publication, so that the latter form has to be treated as an incorrect subsequent spelling ( ICZN 1999: Article 33.3).

Friese (1905) also includes the taxon pleuralis Nylander (a misidentification of a North American species of the subgenus Pyrobombus , = B. flavifrons Cresson , type examined by PW, but interpreted by Friese as a taxon of the subgenus Alpinobombus ) from Novaya Zemlya as a subspecies of B. kirbiellus . Friese’s interpretation of pleuralis presumably also represents the Old World sister-species to B. polaris . This is not the same species as the true B. kirbiellus , which we believe is absent from the island.

Skorikov (1914) distinguished his interpretation of B. pleuralis Nylander (as a species of the subgenus Alpinobombus ) from B. kirbiellus by the shape of the head. On page 124 he refers pyrrhopygus Friese to his interpretation of the species B. pleuralis rather than to B. kirbiellus , from which he reiterates that pyrrhopygus Friese differs in characters signifying a different species.

Richards (1931) places B. kirbyellus ssp. pyrrhopygus Friese in synonymy with his interpretation of B. arcticus Kirby.

Taking this information together, we consider that the oldest available name for the Old World sister-species to the New World B. polaris is likely to be B. pyrrhopygus Friese. An examination of the type material is needed.

Note 2 ( pyrrhopygus ). It is likely that multiple syntypes existed (note 1). The MNHU collection contains a small queen (#4707) that agrees with the original description (with red hair on T4‒6 and with some yellow hair) and carries the labels: (1) white, printed (Cryrillic) ‘[Mal. Karmakul, / Novaya Zemlya. / Yakobson] 23.VII.96 ’; (2) white, handwritten in pen ‘ B. kirbyellus / pyropygus / [female] 1900 Friese det. / Fr.’; (3) white, printed label ‘Zool. Mus. / Berlin’; (4) white, printed ‘ Alpinobombus / AL# 4707. det. PHW’; (5) red, printed ‘ LECTOTYPE [female] / Bombus / kirbyellus ssp. / pyrrhopygus / Friese, 1902 / det. PH Williams 2015 ’; (6) white, printed ‘[female] Bombus / ( Alpinobombus ) / pyrrhopygus / det. PH Williams 2015 ’. This specimen agrees with the collection data for 23 July 1896 referred to by Friese (1905:515) in connection with the description of this taxon. The specimen lacks most of the right antennal flagellum and has some Anthrenus damage to the left cheek. It is designated here as lectotype in order to reduce uncertainty in the identity and application of the name.

Note 3 (pyropygus). Friese’s (1902) original spelling of this name was ‘ pyrrhopygus ’. This is a compound, combining pyrros (meaning ‘flame-red’) with pygos (meaning ‘bottomed’), presumably relating to the red tail of this bee, but with a common incorrect Latinization that includes an ‘h’ (M.A. Alonso-Zarazaga, in litt.). Friese (1905) may then have sought to emend the spelling to ‘ pyropygus ’. However, Friese (1905) did not show the clear evidence for a demonstrably intentional change in the spelling from pyrrhopygus to pyropygus that is required for an emendation ( ICZN 1999: Article 33.2.1), so the spelling pyropygus remains an incorrect subsequent spelling and an unavailable name (Article 33.3). In the last fifty years, both names occur only in lists of synonyms or in notes on colour variation.

Note 4 (friesei). The name friesei was published by Skorikov (1908) for a taxon as a variety alongside other taxa given subspecific rank, so that infrasubspecific rank is clearly intended for the taxon friesei ( ICZN 1999: Article 45.6.1). Subsequent references to this taxon before 1985 (e.g. Richards 1931; Skorikov 1937; Løken 1973) make no change to this status ( ICZN 1999: Article 45.6.4.1), although they do refer the taxon friesei to the species now named here as B. pyrrhopygus .

Note 5 (cinctus). Friese specified that three syntype males existed. The MNHU collection contains a male (#4711) that agrees with the original description (like pyrrhopygus [hair of T4‒6 red] but hair of the face with yel- low, T3 posterior margin yellow, T4 anterior black) and carries the labels: (1) white, printed (Cryrillic) ‘[Mal. Karmakul, / Novaya Zemlya. / Yakobson] 23.VII.96 ’; (2) white, handwritten in pen ‘ B. kirbyellus / v. cinctus / [male] 1910 Friese det. / Fr.’; (3) dark red, printed label ‘Type’; (4) white, printed label ‘Zool. Mus. / Berlin’; (5) white, printed ‘ Alpinobombus / AL# 4711. det. PHW’; (6) red, printed ‘ LECTOTYPE [male] / Bombus / kirbyellus var. / cinctus / Friese, 1911 / det. PH Williams 2015 ’; (7) white, printed ‘[male] Bombus / ( Alpinobombus ) / pyrrhopygus / det. PH Williams 2015 ’. The specimen lacks part of the right antennal flagellum. It is designated here as lectotype in order to reduce uncertainty in the identity and application of the name.

Note 6 (cinctellus). Friese specified that two syntype males existed. The MNHU collection contains a male (#4712) that agrees with the original description (like pleuralis [hair of T4‒6 black] but hair of T3 posterior mar- gin yellow) and carries the labels: (1) white, printed (Cryrillic) ‘[Mal. Karmakul, / Novaya Zemlya. / Yakobson] 23.VII.96 ’; (2) white, handwritten in pen ‘ B. kirbyellus / v. cinctellus / [male] 1910 Friese det. / Fr.’; (3) white, printed label ‘Zool. Mus. / Berlin’; (4) white, printed ‘ Alpinobombus / AL# 4712. det. PHW’; (5) red, printed ‘LEC- TOTYPE [male] / Bombus / kirbyellus var. / cinctellus / Friese, 1911 / det. PH Williams 2015 ’; (6) white, printed ‘[male] Bombus / ( Alpinobombus ) / pyrrhopygus / det. PH Williams 2015 ’. The specimen lacks the left mid leg. It is designated here as lectotype in order to reduce uncertainty in the identity and application of the name.

Note 7 (semljaensis). Friese specified that five syntypes existed, although he lists them as workers. The MNHU collection contains a male (#4713) that agrees with the original description (hair of T1‒2 yellow, T3‒4 black, T5‒6 red) and carries the labels: (1) white, part handwritten in pen ‘Novaj Semlja Ökland / Pomorskye bügt / 27 aug. No. 286’; (2) white, handwritten in pen ‘ B. kirbyellus / v. semljaënsis / [male] 1922 Friese det. / Fr.’; (3) dark red, printed label ‘Type’; (4) white, printed label ‘Zool. Mus. / Berlin’; (5) white, printed ‘ Alpinobombus / AL# 4713. det. PHW’; (6) red, printed ‘ LECTOTYPE [male] / Bombus / kirbyellus var. / semljaensis / Friese, 1923 / det. PH Williams 2015 ’; (7) white, printed ‘[male] Bombus / ( Alpinobombus ) / pyrrhopygus / det. PH Williams 2015 ’. Although this is a male rather than a worker, it matches the specimen number (‘Nr. 286’) as well as the date and site data in the original description. It also carries the Friese type and ‘ semljaënsis’ determination labels. Misprinting of its sex in the paper is likely, so that this is believed to be a syntype. The specimen lacks most of the right antennal flagellum has substantial Anthrenus damage, especially to the head. It is designated here as lectotype in order to reduce uncertainty in the identity and application of the name.

Taxonomy and variation. Bombus pyrrhopygus has long been considered part of B. polaris but has recently been recognized as separate from evidence of a species coalescent in the COI gene ( Williams et al. 2015; Fig. 9 ). Morphometric distinction between B. pyrrhopygus (under the name B. polaris ) and B. alpinus has been demonstrated graphically by Løken (1973) and Pekkarinen (1979). Bombus pyrrhopygus is vicariant with B. polaris across the Bering Strait ( Figs. 22 , 39 ).

Variation in the colour pattern has been analysed previously ( Williams et al. 2015). Variation in the colour pattern is most obvious between the ‘unbanded’ pattern without yellow bands on the thorax or on T1‒2 (the taxon diabolicus ) in Scandinavia and Murmansk ( Figs. 27‒31, 37‒38 ) and the yellow-banded pattern further east in Rus- sia, beyond Beloye More (the White Sea) ( Figs. 23‒24, 32‒34 ). For the weakly banded or unbanded individuals, the hair of T2‒4 shows variation in the replacement of orange with black progressively from T2‒4 ( Figs. 25‒31, 35‒38 ). Otherwise the principal variation in this species is in whether the hair of T4‒5 is predominantly orange (the taxon pyrrhopygus Figs. 23, 32 ) or predominantly black (the taxon cinctellus Figs. 24, 33 ). There may be some variation in the relative frequency of the two patterns with latitude ( Williams et al. 2015).

Despite the apparent strong difference in the colour patterns, individuals with both the banded and the unbanded colour patterns share some of the same alleles ( Fig. 14 ). Nonetheless, more detailed study of variation in the COI gene within B. pyrrhopygus across Russia is needed.

Material examined. 61 queens 39 workers 102 males (plus 289 females with caste undetermined), from Norway, Sweden, Finland, and Russia ( Fig. 22 : AB FO MB MNHU NHMUK PW SC ZISP), with 37 specimens barcoded.

Habitat and distribution. Flower-rich arctic/alpine tundra in the Old World from the far north of Scandinavia, Taymyr, Novaya Zemlya and Wrangel Island, extending southwards into the subarctic region in the alpine zone of the Scandinavian, Kamchatkan, and Magadan mountains. One record for a Russian female in the ZISP collection from the Stanovoy range (#1332) needs confirmation because the habitat appears climatically unsuitable (cf. the Maxent climatic suitability model in Fig. 7 ). Regional distribution maps ( Løken 1973; Pekkarinen et al. 1981; Rasmont & Iserbyt 2012; Ødegaard et al. 2015; Rasmont et al. 2015).

Food plants. ( Mossberg & Cederberg 2012)

Behaviour. ( Løken 1973; Svensson & Lundberg 1977)

Conservation status. This species has been assessed in part for Red List threat status using IUCN criteria (2001). Rasmont et al. (2014) assessed the Red List status of this species (under the name B. polaris ) as ‘Vulnerable’ in Europe because its known area of occupancy (AOO) for Europe is small (<700 km ²) and because it has experienced a strong and continuing decline due to climate warming. Subsequently, Rasmont et al. (2015) have assessed the risk from climate change to this species (under the name B. polaris ) in Europe as ‘extremely high climate change risk’ (HHHR), projecting that it will have no chance of persistence in Europe to survive the expected warming.

Figures

FIGURE 7. Sample sites and climatic suitability for all Alpinobombus species combined estimated using Maxent from climate variables for the year 2000. Bright yellow and brown areas show where the logistic prediction of occurrence is p> 0.5 (the outlier records with exceptionally low probabilities of suitability were excluded in step-wise iterations); brown spots show all consistent Alpinobombus site records; ‘?’ shows the five records that are in climatically outlying sites. Polar projection, North Pole (starred) at the centre of the map, international boundaries and the Arctic Circle shown as narrow grey lines.

FIGURE 9. Estimate of the metric gene tree for the 54 longest unique COI-barcode alleles of the subgenus Alpinobombus from MrBayes combined with the Bayesian Poisson-tree-process (PTP) solution with the highest support with spots showing the nodes with the strongest support as coalescents for candidate species (outgroup B. ignitus not shown). Values above the nodes are Bayesian posterior probabilities showing branch support for groups; values below the nodes are PTP Bayesian support values that all daughter alleles are parts of a single species (probabilities within candidate species are all ≤ 0.44). The scale bar is calibrated in substitutions per nucleotide site. Each unique allele is represented by one of the longest available sample sequences, labelled with: the sequence length in number of nucleotides, a taxon name or name describing an unpublished colour pattern, and then a code that consists of a specimen identifier (AL#n) from the project database and (after the hyphen) a sample identifier from BOLD or GenBank, followed with its geographic origin (for simplicity Greenland is included without Denmark).

FIGURE 14. Assigning names to candidate species in a COI gene tree for the 235 specimens of the subgenus Alpinobombus with sequences. Based on the MrBayes analysis of all of the 54 longest unique alleles in Fig. 9, with the remaining sequences interpolated back into the tree with 0 branch lengths from their matching samples (where a sequence matches more than one longer sequence within a species in the Collapse results, it is arbitrarily added after the first matching sequence). The sequence labels follow the format used in Fig. 9. Lineages with high probabilities of representing candidate species in the Poisson-tree-process (PTP) results (Fig. 9) are shown as thick branches with the most recent common ancestors (coalescents) of each candidate species shown with a black spot, the branches within candidate species shown as thin branches. Asterisks mark samples used as informal proxies for the type specimens of each of the taxon names in Table 2. The proxy sample for the type specimen for the oldest available name (the valid name) for each candidate species (from Fig. 9) is marked in bold.

FIGURES 1‒6. Lateral views of foraging females (queens) of species of the subgenus Alpinobombus (with photo credits): 1, B. alpinus, Norway (A. Staverløkk); 2, B. pyrrhopygus, Sweden (G. Holmström); 3, B. polaris, Canada (B. Heinrich); 4, B. balteatus, Sweden (G. Holmström); 5, B. kirbiellus, USA (D. Wilson); 6, B. hyperboreus, Sweden (L.-I. Larsson). Some images reversed.

FIGURES 22‒38. 22: Bombus pyrrhopygus global distribution (as for Fig. 15). 23‒38 colour patterns (as for Figs. 16‒21): 23 (#4707) Russia-Arkhangelsk; 24 (#337) Russia-Arkhangelsk; 25 (#273) Sweden; 26 (#272) Sweden; 27 (#250) Sweden; 28 (#249) Sweden; 29 (#258) Sweden; 30 (#4709) Russia-Murmansk; 31 (#257) Sweden; 32 (#4711) Russia-Arkhangelsk; 33 (#4712) Russia-Arkhangelsk; 34 (#4713) Russia-Arkhangelsk; 35 (#242) Norway; 36 (#139) Sweden; 37 (#4710) Norway; 38 (#1375) Russia-Murmansk.

FIGURES 129‒137. Morphology of the male genitalia for species of the subgenus Alpinobombus from the dorsal aspect, anterior to the left of the image, posterior to the right: 129 B. alpinus (#3824); 130 B pyrrhopygus (#3833); 131 B. polaris (#73); 132 B. balteatus (#3843); 133 B. kirbiellus (#3768); 134 B. neoboreus (#4387); 135 B. kluanensis (#4876); 136 B. natvigi (#81); 137 B. hyperboreus (#3821).

FIGURES 39‒58. 39: Bombus polaris global distribution (as for Fig. 15). 40‒58 colour patterns (as for Figs. 16‒21): 40 (#4380) Canada-Labrador; 41 (#4396) USA-Alaska; 42 (#3856) Canada-Nunavut; 43 (#59) USA-Alaska; 44 (#43) Denmark- Greenland; 45 (#4740) Denmark-Greenland; 46 (#4407) USA-Alaska; 47 (#334) USA-Alaska; 48 (#285) Canada-Nunavut; 49 (#4383) USA-Alaska; 50 (#44) Denmark-Greenland; 51 (#19) Canada-Northwest Territories; 52 (#4401) USA-Alaska; 53 (#4403) USA-Alaska; 54 (#4884) Canada-Yukon; 55 (#4405) USA-Alaska; 56 (#4384) USA-Alaska; 57 (#4951) USA-Alaska; 58 (#29) Canada-Manitoba.