RESEARCH ARTICLE
A fossil bumblebee (Hymenoptera, Apidae, Bombini) from the Middle Pleistocene Shiobara Group in Nasushiobara, Tochigi, Japan
2025 年 29 巻 p. 246-252
詳細
2025 年 29 巻 p. 246-252
Fossils of bumblebees and their kin (Bombini) are extremely rare, with only 15 occurrences from the Upper Eocene to Upper Miocene representing 14 species reported to date, all of which are extinct. Here, we report a new bumblebee (Bombus) fossil, a queen bee from the Middle Pleistocene of the Shiobara Group in Nasushiobara, Tochigi, Japan. The fossil was identified as Bombus (Megabombus) cf. diversus Smith, 1869, a species distributed throughout Japan. The fossil is large, with an estimated total body length of 24 mm. The new specimen is the first bumblebee fossil from the Middle Pleistocene, the most geologically recent occurrence of a bumblebee fossil, and the first fossil of an extant bumblebee species. This discovery suggests that modern bumblebee species originated between the Pliocene and Middle Pleistocene. This new fossil is a valuable resource for studying bumblebee speciation.
Bumblebees are medium-sized to very large (9–22 mm long) hairy bees of the tribe Bombini, which includes only one extant genus, Bombus (Michener, 2007). They are essential pollinators of many wild plants and major crops and are primarily found in temperate and upland areas of the Northern Hemisphere (Brown, 2011; Ghisbain et al., 2025). Approximately 260 species have been identified and classified into 15 subgenera (Williams et al., 2008). Their robust morphology, relatively small colonies, and distinctive color pattern make them favorites among entomologists and the general public (Wappler et al., 2012). Therefore, many studies have been conducted on bumblebees, including taxonomic surveys (e.g. Williams, 1998, 2007; Kawakita et al., 2004; Cameron et al., 2007; Kozmus et al., 2011; Williams et al., 2011, 2012, 2019). In Japan, there are 15 species and six subspecies of extant bumblebees belonging to five subgenera (Kinota et al., 2013).
In contrast, bumblebee fossils are scarce, and only 14 species of Bombus or closely related genera have been described from fossils to date (Table 1). Of these, all but Calyptapis florissantensis (Cockerell, 1906) are known only from a single specimen. The oldest known bumblebee fossil is Oligobombus cuspidatus Antropov et al. 2014 from the Upper Eocene of the Isle of Wight, UK. The second oldest, Calyptapis florissantensis, is known from two specimens from the Eocene–Oligocene boundary in the Florissant Formation of Colorado, USA (Cockerell, 1906). Neither species fits within the shape space of any contemporary Bombus subgenus, suggesting that they likely belong to the stem group Bombini. Two fossils date to the Oligocene–Miocene boundary: B. (Paraelectrobombus) patriciae (Nel and Petrulevičius, 2003), which belongs to an extinct subgenus, and B. (Mendacibombus) beskonakensis (Nel and Petrulevičius, 2003), which is placed in an extant subgenus. The remaining 10 species are from the Miocene and fall within the contemporary shape space of Bombus, with some assigned to contemporary subgenera such as Cullumanobombus, Melanobombus, and Mendacibombus. The fossil record of bumblebees is therefore limited to the Upper Eocene to Upper Miocene, with no fossils from the Pliocene to the Recent (Wappler et al., 2012). All these fossils represent extinct species, and no fossils of extant species have been identified. Therefore, fossils from the Pliocene and Pleistocene are potentially important sources of information on this gap in our understanding of the evolution of extant bumblebee species.
| Taxon | Age (Ma) | Epoch | Locality | Country |
|---|---|---|---|---|
| Bombus (Megabombus) cf. diversus (Smith, 1869) | 0.3 | middle Pleistocene | Shiobara | Japan |
| B. (Melanobombus) cerdanyensis Dehon et al., 2014 | 10.0 | Late Miocene | La Cerdanya | Spain |
| B. (Cullumanobombus) pristinus Unger, 1867 | 11.2–7.1 | Late Miocene | Euboea | Greece |
| B. vetustus Rasnitsyn and Michener, 1991* | 11.2–7.1 | Late Miocene | Botchi River | Russia |
| B. anacolus Zhang et al., 1994* | 17.0–15.2 | Middle Miocene | Shandong | China |
| B. dilectus Zhang et al., 1994* | 17.0–15.2 | Middle Miocene | Shandong | China |
| B. luianus Zhang, 1990* | 17.0–15.2 | Middle Miocene | Shandong | China |
| B. (Cullumanobombus) randeckensis Wappler et al., 2012 | 18.0–16.0 | Early Miocene | Randeck Maar | Germany |
| B. crassipes Novak, 1877 | 18.0–17.0 | Early Miocene | Krottensee | Czech Republic |
| B. (Cullumanobombus) trophonius Prokop et al., 2017 | 20.0 | Early Miocene | Bilina Mine | Czech Republic |
| B. proavus Cockerell, 1931 | 21.3–12.1 | Early–Middle Miocene | Latah | USA |
| B. (Mendacibombus) beskonakensis (Nel and Petrulevičius, 2003) | 22.5 | Oligocene–Miocene | Bes-Konak | Turkey |
| B. (Paraelectrobombus) patriciae (Nel and Petrulevičius, 2003) | 22.5 | Oligocene–Miocene | Bes-Konak | Turkey |
| Calyptapis florissantensis Cockerell, 1906 | 37.0–33.9 | Eocene–Oligocene | Florissant | USA |
| Oligobombus cuspidatus Antropov et al., 2014 | 36.0 | Late Eocene | Isle of Wight | UK |
Over 100 Middle Pleistocene (~ 0.3 Ma) fossil insect species have been described from the Shiobara Group, a lacustrine deposit that is widely distributed in Nasushiobara, Tochigi, Japan (Aiba, 2015; Aiba and Hayashi, 2024). In 1997, one of the authors (HA) introduced a hands-on science activity for classrooms in which students break rocks from the Shiobara Group and search for fossils, which has since been adopted by many Japanese schools (Aiba, 1997; Aiba, 2016). Here, we describe a new bumblebee fossil discovered by a high school student during one of these activities.
The bumblebee fossil was discovered during a high school science lesson by student Rimo Ichikawa (Keio Shonan Fujisawa Junior and Senior High School, 5322 Endo, Fujisawa, Kanagawa, Japan) in October 2024. The fossil was discovered within a slab of siltstone from the Middle Pleistocene Miyajima Formation (Shiobara Group) collected at the fossil quarry of the Konoha Fossil Museum in Nasushiobara, Tochigi, Japan. For geological and paleontological background, refer to Onoe (1989), Tuzino et al. (2009), and Aiba (2015).
Specimens were examined under a Leica M205 C stereo microscope (Leica Corporation, Wetzlar, Germany). Photographs and measurements were obtained using a Leica MC170 HD microscope camera with Leica Application Suite Version 4.1.3. Images were sharpened and adjusted for contrast and tonality using Adobe Photoshop version CS6 (Adobe Systems Incorporated, San Jose, CA, USA). The morphological terminology used to describe bees follows that of Engel (2001) and Michener (2007). Abbreviations: 1cc = 1st cubital cell; 1mc = 1st medial cell; 1sc = 1st submarginal cell; 2cc = 2nd cubital cell; 2mc = 2nd medial cell; 2sc = 2nd submarginal cell; 3sc = 3rd submarginal cell; mc = marginal cell; rc = radial cell; S5 = sternite 5, S6 = sternite 6; TI–VI = tergite I–VI.
Order Hymenoptera Linnaeus, 1758
Family Apidae Latreille, 1802
Subfamily Apinae Latreille, 1802
Tribe Bombini Latreille, 1802
Genus Bombus Latreille, 1802
Bombus (Megabombus) cf. diversus Smith, 1869
[Japanese name: Toramaruhanabachi]
Specimen.—KYFSI243, female (queen) preserved in two pieces: a concave impression exposing dorsal side (KYFSI243a: Figure 1A) and a convex counterpart exposing ventral side (KYFSI243b: Figure 1B). Mesosoma, metasoma, left fore wing, part of right mid and hind legs, part of left fore, mid, and hind legs are preserved without the head.
Locality and horizon.—The specimen was collected from a laminated siltstone bed of the Middle Pleistocene Miyajima Formation (Shiobara Group) at the fossil quarry of the Konoha Fossil Museum (36°58′52″N, 139°48′23″E) in Nasushiobara, Tochigi, Japan.
Description.—Body large. Combined length of mesosoma and metasoma 20.21 mm; estimated total body length 24 mm.
Mesosoma: Sclerotized black, almost circular, slightly transverse, 8.33 mm long, widest at middle, 9.21 mm wide. Partially preserved reddish-brown hairs (Figure 1C). However, detailed structure not visible.
Fore wing (Figures 1A, 2A): Length 18.25 mm, maximum width 6.54 mm; membrane infumate with alar papillae beyond apical cross veins; boundary between pterostigma and prestigma obscured; marginal cell elongate, 4 times as long as wide with dense setae on upper half, length 5.23 mm, width 1.31 mm; basal vein almost straight; cu-a slightly arched posteriorly; 1st cubital cell elongated, rectangular, brown in color, length 5.49 mm, width 0.65 mm; radial cell elongate, half-length of fore wing, length 8.50 mm, width 1.18 mm; 1st medial cell transparent and same length as marginal cell, length 5.23 mm, width 1.64 mm; 2nd medial cell same length as 2nd cubital cell, length 3.99 mm, width 1.37 mm; first submarginal cell length 2.62 mm (as measured from origin of M+Rs to juncture of r-rs and Rs), width 0.98 mm (as measured from M+Rs to pterostigma); second and third submarginal cells not distinct, as vein 1rs-m not clearly preserved; 1st abscissa of Rs almost straight; 2nd abscissa of Rs slightly bent; r-rs almost straight; M+Rs straight and longer than r-rs; posterior half of 2rs-m not preserved; 1m-cu almost straight; 2m-cu slightly curved.
Legs: Left fore leg femur with dense black setae, length 4.31 mm (Figure 1B). Right mid leg preserved (Figures 1B, E; 2B); femur with relatively sparse long black setae, length 5.46 mm; tibia with dense black setae, length 4.82 mm; basitarsus with posterior apical angle acutely spinosely produced at apex and coarsely bristled (Figures 1E, 2B), length 4.53 mm. Left hind leg (Figures 1F, 2C) relatively completely preserved; femur covered with sparse black setae, length 5.04 mm; tibia with black corbicular fringe, with rastellum posterior corner (Figure 2D), length 5.57 mm; basitarsus with dense black setae, length 3.25 mm. Hind tibial spurs not preserved.
Metasoma (Figures 1A, B, D, G; 2E): Sclerotized black, almost circular, 11.86 mm long, widest at posterior third, 11.54 mm wide. Tergites I and II have no hair preserved. Tergites III and IV preserved groomed light-colored long dense hairs (Figure 1D); however, boundary between tergites III and IV unclear. Tergite V with black hairs. Tergite VI protruding, observed on ventral side (Figure 1G).
KYFSI243 was identified as female based on its pointed abdominal tip and as a queen based on its large size (>20 mm) (Michener, 2007; Kinota et al., 2013). The fossil preserves some reddish-brown hairs on the mesosoma and some lighter hairs on the metasoma, which we infer were yellow. Based on these observations, we infer that the mesosoma was covered with reddish-brown hairs, tergites III and IV were covered with uniform yellow hairs, and tergites V and VI were covered with black hairs in life (Figure 2E).
KYFSI243 can be referred to the tribe Bombini of the family Apidae based on the following characteristics: hairy, large size (combined length of the mesosoma and metasoma is 20.21 mm), rounded body shape, a hind tibia with a corbicula, and a fore wing with strong venation (e.g. small stigma and long marginal cell) (Michener, 2007).
The genus Bombus is the only extant genus within the tribe Bombini, which is further divided into 14 subgenera (Williams et al., 2008). Among these subgenera, KYFSI243 exhibits characteristics consistent with those of the subgenus Megabombus, including a tibia with a black corbicular fringe and a rastellum and a middle basitarsus with posterior apical angle acutely spinosely produced at apex and coarsely bristled (Williams, 1991).
Twenty-two extant species of the subgenus Megabombus have been previously described (Cameron et al., 2007). In Japan, four species have been reported: Bombus (Megabombus) consobrinus Dahlbom, 1832; Bombus (Megabombus) diversus Smith, 1869; Bombus (Megabombus) ussurensis Radoszkowski, 1877; and Bombus (Megabombus) yezoensis Matsumura, 1932 (Kinota et al., 2013). The characteristics of a mesosoma covered with reddish-brown hairs, a metasoma covered with yellow hairs, and black hairs at the tip of the metasoma are like those of B. (M.) diversus (Figure 2G). Furthermore, a comparison of the entire fore wing venations of KYFSI243 and a modern B. (M.) diversus queen revealed strong similarities (Figure 2A, F). Wing venation can be analyzed based on shape (with geometry morphometry) (Dehon et al., 2014). However, this fossil may be taphonomically deformed, so this method was not used here. Based on these characteristics, KYFSI243 most closely resembles B. (M.) diversus.
Bombus (M.) diversus is widely distributed in present-day Japan and is known for its large size, with queens ranging from 18.9 to 24.6 mm (Kinota et al., 2013). Most insect fossils from the Shiohara Group are extant species (Aiba and Hayashi, 2024). Therefore, it is likely that it can be referred to this species. Unfortunately, the fossil is not completely preserved and is missing its head. Therefore, it cannot be unambiguously identified as B. (M.) diversus, and we here refer it to B. (M.) cf. diversus Smith, 1869 pending the discovery of better-preserved fossil specimens.
Bombus (M.) diversus comprises two subspecies in Japan: B. (M.) diversus tersatus, which is found in Hokkaido (the northern island of Japan), and B. (M.) diversus diversus, which is distributed throughout the rest of the country. Of these subspecies, KYFSI243 more closely resembles B. (M.) diversus tersatus in the absence of black hair on tergite IV. However, the separation of bumblebees based on colored hair patterns is unreliable (Terzo et al., 2007; Williams, 2007; Valterová et al., 2019), and interspecific variation further complicates identification. Thus, subspecies level identification is not possible. The discovery of fossil species comparable to B. (M.) diversus suggests that the climate of Japan in the Middle Pleistocene was not significantly different from the current climate.
Bumblebees are thought to have undergone rapid diversification during the Miocene, as suggested by molecular phylogenetic analysis and fossil occurrences (e.g. Hines, 2008; Dehon et al., 2019). Until now, no fossils have been identified as belonging to an extant species. The discovery of a fossil of B. (M.) cf. diversus from the Middle Pleistocene of Japan suggests that modern bumblebee species originated between the Pliocene and Middle Pleistocene.
We would like to thank Rimo Ichikawa for discovering this specimen and Hiroki Takeda of Keio Shonan Fujisawa Junior and Senior High School for giving us the opportunity to study it. We express our gratitude to Reiji Kukihara, Tatsumi Suguro and Yui Takahashi (Keio Yochisha Elementary School) for supporting this study. Finally, we would like to express our gratitude to the editors of Paleontological Research, Dr. Denis Michez (University of Mons), and the anonymous reviewers for their valuable comments on our manuscript.
H. A. initiated the study, drafted the manuscript, and compiled all the figures. M. O. revised the manuscript and provided taxonomic input. All authors contributed to the writing of the manuscript.
