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Bombina orientalis

Bombina orientalis (Source)

Superregnum: Eukaryota
Regnum: Animalia
Subregnum: Eumetazoa
Cladus: Bilateria
Cladus: Nephrozoa
Superphylum: Deuterostomia
Phylum: Chordata
Cladus: Craniata
Subphylum: Vertebrata
Infraphylum: Gnathostomata
Superclassis: Tetrapoda
Classis: Amphibia
Subclassis: Lissamphibia
Ordo: Anura

Familia: Bombinatoridae
Genus: Bombina
Species: Bombina orientalis
Name

Bombina orientalis (Boulenger, 1890)

Type locality: "Chefoo [= Yantai, Shandong]...N. China...S.E. coast of Corea...Chabarowka".

Syntypes: BM 1947.2.25.53-64, 1947.2.25.69, 1947.2.25.70-72 & 1947.2.25.73-76.
Synonyms

Bombinator orientalis Boulenger, 1890
Bombina orientalis — Stejneger, 1907
Bombina orientalis var. silvatica Korotkov, 1972
Bombina orientalis var. praticola Korotkov, 1972
Bombina (Bombina) orientalis — Tian & Hu, 1985

References

Boulenger, 1890, Ann. Mag. Nat. Hist., Ser. 6, 5: 143.
Tian and Hu, 1985, Acta Herpetol. Sinica, N.S., 4: 219–224.
Frost, D.R. 2021. Amphibian Species of the World: an Online Reference. Version 6.1. Electronic Database accessible at https://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA. DOI: 10.5531/db.vz.0001 Bombina orientalis . Accessed on 14 July 2008.
2007 IUCN Red List of Threatened Species IUCN: Bombina orientalis (Least Concern) Downloaded on 14 July 2008.

Vernacular names
English: Oriental Firebelly Toad
español: Sapillo de vientre de fuego oriental
日本語: チョウセンスズガエル
한국어: 무당개구리
polski: Kumak dalekowschodni

The Oriental fire-bellied toad (Bombina orientalis) is a small semiaquatic frog species found in northeastern Asia, where they primarily dwell in slow-moving bodies of water and temperate forests. Quite common throughout much of their range, these frogs have mild toxins that can be excreted through their skin, with their vibrant underbellies serving as a warning of this. While not a true toad, their green and black skin is covered in small tubercles, giving them a toadlike appearance. Their sounds, mainly produced by males during the mating season, are very unlike those of other frogs. While their population is in decline, their numbers are still high overall, with the International Union for Conservation of Nature (IUCN) rating them as a least-concern species.They are commonly kept as pets in land and water vivaria, as a relatively easy-to-care for species. They are also frequently used in scientific research, with their behavior, vocalizations, and learning skills all moderately studied.

Etymology

According to the American Museum of Natural History, the red-bellied toad, Chinese bell toad, Oriental bell toad, eastern fire-bellied toad, and Korean fire-bellied toad are all common names that have been used to describe the species at one point or another.[2]
Taxonomy

The Oriental fire-bellied toad was first described by George Albert Boulenger as Bombinator orientalis, who placed it within the same genus as the European fire-bellied toad and the Apennine yellow-bellied toad, noting their many similarities. He considered it an "intermediate" between the latter two species, although he thought it was closer to the Appenine yellow-bellied toad overall. His research was based on 19 specimens housed in the British Museum. The three species have been moved into the genus Bombina in 1907 by Leonhard Stejneger.[3][4]

The toad was later divided into two subspecies in 1972, B. o. practicola and B. o. silvatica, with the former being more aquatic and the latter more terrestrial, although newer research has found them to display few genetic differences, despite some physical ones. These findings support their classification as a monotypic species, albeit one with multiple morphs that may have diverged rather recently.[5] A population in Beijing, despite having existed for less than a hundred years, has shown signs of evolution at a molecular level, displaying genetic uniqueness from the original population. While genetic diversity is somewhat low, it is still high enough that the Beijing toads may continue to survive.[6]

In the late Quaternary, seismic activity at the Yilan–Yitong fault zone is believed to have split the toad into two subpopulations in its native range, with the much smaller western one having low genetic diversity. In more recent times, gene flow has begun to occur between the two.[7]
Description
A fire-bellied toad showing off the characteristic green and black back with orange toes

Oriental fire-bellied toads can be bright, grayish, or brownish green, with black mottling on their dorsal regions. Like other Bombina species, B. orientalis has a brightly colored ventral region, which can be yellow, red, or orange-red, mottled with dark spots.[8] The finger and toe tips are usually red.[3] The skin on its upper side is covered in small tubercles, the most pronounced of the genus Bombina.[9] Although it is typically referred to as a toad, the fire-bellied toad is not a true toad.[10] They can reach a length of about 3.8–5.1 centimetres (1.5–2.0 in), weighing about 28–57 grams (0.99–2.01 oz).[11] Males and females can be told apart by the males' nuptial pads on their first and second fingers.[12]

Besides having more noticeable tubercles on their skin, B. orientalis can also be distinguished from other members of Bombina by their lack of gular sacs (like B. pachypus and unlike B. bombina) and nuptial pads (like B. bombina and unlike B. pachypus, although later research has shown that males do in fact have a few, as previously mentioned[12]). Subtler differences include their belly coloration, which is typically more red than yellow (unlike B. pachypus) and bright finger tips (unlike B. bombina).[3]
Distribution and habitat

The toad can be found in Korea, northeastern Russia, (where they have become rather rare[12]) and northeastern China, and possibly southern Japan, specifically Tsushima Strait, although the latter is very likely erroneous, as a team of Japanese researchers in the later half of the 20th century was unable to locate any.[13] There is also a somewhat genetically distinct population in Beijing that was introduced from Yantai in Shandong in 1927 by Mr. Liu Cheng-chao. About 200 were released into wetland habitats, where they later bred.[6] There have been multiple reports of escaped specimens in Broward County, Florida, US, mostly in the immediate vicinity of an animal importer's facility.[14] There have been no other reports of such occurrences in the United States, and there are no well-established escaped populations.[15]

They are semiaquatic, generally dwelling in slow-moving streams or ponds. When out of the water, they can often be found in coniferous and broadleaved forests.[11] They can be found at elevations of up to 1,100 metres (3,600 ft).[1] They are very resilient to environmental disturbance, especially compared to other amphibians, and as such can be found living and even breeding in heavily polluted water.[16]
Ecology and behavior

B. orientalis are one of the most plentiful amphibians in their native lands, particularly the central part of their range. The toads are diurnal (active during the day), and studies have found that while they can acquire some from their diet, Oriental fire-bellied toads rely partly on sunlight to obtain adequate levels of vitamin D3.[17][18]
Diet

As larvae, Oriental fire-bellied toads consume algae, fungi, detritus, plants and protozoans. As adults, their diet consists of terrestrial invertebrates, including worms, molluscs and insects.[8] Their diet in the wild contributes to their toxicity, and for that reason, wild specimens have more potent toxins.[19] Oriental fire-bellied toads are incapable of extending their tongues to catch prey, but must instead leap at their target.[8]
Breeding
A mating pair of Oriental fire-bellied toads

Breeding takes place around mid-May, when temperatures become warmer. It is at this time that the toads emerge from hibernation.[12][11] Males call to the females with a light sound that is comparable to a musical triangle. They will jump onto the backs of any other fire-bellied toad that happens to pass by, which in some cases will cause them to accidentally attempt to mate with other species of amphibians, fish, plants, or even human fingers. Females lay 40 to 110 eggs in a large cluster near the surface of the water. The tadpoles begin to develop legs in 6–8 weeks, and are fully metamorphosed by August or September.[8]
Vocalizations

Unusually for a frog species, the Oriental fire-bellied toad does not have an eardrum or resonator, making their calls by inhaling.[8] The males' light mating calls are similar to those of B. bombina.[12] While vocalizing, males will attempt to space out their calls so as to avoid overlap between different individuals, a behavior also observed in European fire-bellied toads.[20] Females have been found to be quickly attracted to the advertisement call, but not the release call, displaying an ability to differentiate between them. Males typically ignore the advertisement calls, but will approach the source of release calls. In both cases, visual stimuli are also necessary to trigger a reaction.[21] In addition to their lighter sounds, they can also produce a croaking noise.[9]
Predation

Oriental fire-bellied toads can discourage most predators with their poisonous skin, with the bright colors of their undersides warning predators of their toxicity.[11] The toxin is secreted through the skin mostly from the hind legs, and sometimes the belly, in a milky substance when the frog is disturbed or frightened. When producing this substance, the frogs may also lie on their backs to show the color of their bellies, indicating their potential danger, holding up their limbs and arching their heads.[8][15] This does not always work, and in addition to predation by birds and mammals, grass snakes and other water dwelling snakes are known to the consume the toads without any ill effect.[12][8]
Research
Bombesin

The skin of Oriental fire-bellied toads contains bombesin, a peptide first isolated from their relatives, European fire-bellied toads (and later other types of frogs, in the genera Rana and Phyllomedusa). Among other effects, bombesin hinders gastric functions in mammals, including dogs, cats, rabbits, and rodents. Later studies on B. orientalis discovered that the peptide came in three separate forms.[22][23]
Intelligence

Oriental fire-bellied toads are rapid learners, especially compared to other frogs. In an experiment, slightly dehydrated toads were found able solve both simple and more complex mazes using water as a reinforcement, unlike other types of frogs (members of Rana, Bufo, and Hyla simply either did not try or leapt around aimlessly). In a simple T-maze, with their target on the right side, 80% had navigated their way successfully in only three days, with 100% having finished after four days. The left side proved more challenging, with 80% finished in three days, but the rest not done until day eight.[24]
As a model organism

As common amphibians, B. orientalis make excellent model organisms for studying the effects of pollution and toxic chemicals on local environments. Studies involving them having demonstrated the harmful effects of carbaryl (which include bent trunks, thicker-set bodies, bent tails, and ventral blistering) and nonylphenol (which significantly decreased overall survival rates) on amphibian embryonic development.[25][26]
In captivity
Oriental fire-bellied toads in a terrarium

B. orientalis are relatively easy to care for in captivity, requiring little in the way of specialized lighting or heating and readily consuming feeder insects or small feeder fish.[10] Handling can require caution, as although harmless to the skin, the mucus can cause discomfort to the mouth and eyes,[8] however captive individuals generally are less toxic.[19] The toxin does not pose a significant threat to human health.[10] In captivity, Oriental fire-bellied toads often live for around 12 years, but in some cases can live up to 30.[19]
Conservation status

The oriental fire-bellied toad was listed as least concern species by the International Union for Conservation of Nature with little threat of extinction, although the population is declining, but not at a significant rate.[1] They occur in many protected areas in China and the Koreas, as well as six Russian nature reserves. The population in the Russian part of their range may be more threatened than others. Dangers include pollution, urbanization, and use in traditional Chinese medicine.[8]
References

Sergius Kuzmin; Li Pipeng; Masafumi Matsui; Vladimir Ishchenko; Irina Maslova (January 2019). "Bombina orientalis". The IUCN Red List of Threatened Species. IUCN. 2004: e.T54449A11146991. doi:10.2305/IUCN.UK.2004.RLTS.T54449A11146991.en. Retrieved 15 January 2018. Database entry includes a range map and a brief justification of why this species is of least concern
"Bombina orientalis (Boulenger, 1890) | Amphibian Species of the World". amphibiansoftheworld.amnh.org. Retrieved 2022-01-09.
The Annals and magazine of natural history; zoology, botany, and geology. 5. London, England: Taylor and Francis, Ltd. 1890. pp. 143–144.
Stejneger, Leonhard Hess (1907). Herpetology of Japan and adjacent territory. Harvard University. Washington, Govt. print. off. p. 51.
Kuzmin, S. L.; Poyarkov, N. A.; Maslova, I. V. (2010-03-01). "On the variability of fire-bellied toads in the Far East". Moscow University Biological Sciences Bulletin. 65 (1): 34–39. doi:10.3103/S0096392510010074. ISSN 1934-791X.
Teng, Yang; Yang, Jing; Zhu, Guofen; Gao, Fuli; Han, Yingying; Bao, Weidong (17 May 2021). "Population Genetic Structure Analysis Reveals Decreased but Moderate Diversity for the Oriental Fire-Bellied Toad Introduced to Beijing after 90 Years of Independent Evolution". Animals. 11. Retrieved 2 January 2022 – via MDPI.
Yu, Liqun; Zhao, Shuai; Shi, Yanshuang; Meng, Fanbing; Xu, Chunzhu (2021). "Evolutionary history of the oriental fire-bellied toad (Bombina orientalis) in Northeast China". Ecology and Evolution. 11 (9): 4232–4242. doi:10.1002/ece3.7318. ISSN 2045-7758. PMC 8093726. PMID 33976806.
"Oriental fire-bellied toad". Smithsonian's National Zoo. 2016-04-25. Retrieved 2021-12-29.
Szcodronski, Todd. "Bombina orientalis". Animal Diversity Web. Retrieved 2022-01-08.
"Fire-Belly Toad | Zoo Med Laboratories, Inc". Retrieved 2021-12-29.
"Oriental Fire-Bellied Toad | National Geographic". Animals. 2010-03-12. Retrieved 2021-12-29.
"Bombina orientalis". AmphibiaWeb. University of California, Berkeley. Retrieved 2021-12-29.
Kawamura, Toshijiro; Nishioka, Midori; Ueda, Hiroaki (1972). "Reproduction of the Oriental Fire-bellied Toad, Bombina orientalis, with Special Reference to the Superiority of this Species as a Laboratory Animal" (PDF). Scientific report of the Laboratory for Amphibian Biology. 1: 303–317 – via CORE.
"Oriental Fire-bellied Toad - Collections". nas.er.usgs.gov. Retrieved 2021-12-29.
"Oriental Fire-bellied Toad (Bombina orientalis) - Species Profile". nas.er.usgs.gov. Retrieved 2021-12-29.
Maslova, Irina; Rodina, Elvira; Borzée, Amaël; Yikweon, Jang (June 2018). "Breeding populations of Bombina orientalis Boulenger, 1890 (Amphibia Anura Bombinatoridae) in degraded urban habitat in Vladivostok, Russia". Biodiversity Journal. 9 (2): 127–130. doi:10.31396/Biodiv.Jour.2018.9.2.127.130. Retrieved 6 January 2022 – via ResearchGate.
Michaels, C. J.; Antwis, R. E.; Preziosi, R. F. (2015). "Impacts of UVB provision and dietary calcium content on serum vitamin D3, growth rates, skeletal structure and coloration in captive oriental fire-bellied toads (Bombina orientalis)". Journal of Animal Physiology and Animal Nutrition. 99 (2): 391–403. doi:10.1111/jpn.12203. ISSN 1439-0396.
Langhout, Martine van Zijll; Struijk, Richard P. J. H.; Könning, Tessa; Zuilen, Dick van; Horvath, Katalin; Bolhuis, Hester van; Maarschalkerweerd, Roelof; Verstappen, Frank (September 2017). "EVALUATION OF BONE MINERALIZATION BY COMPUTED TOMOGRAPHY IN WILD AND CAPTIVE EUROPEAN COMMON SPADEFOOTS (PELOBATES FUSCUS), IN RELATION TO EXPOSURE TO ULTRAVIOLET B RADIATION AND DIETARY SUPPLEMENTS". Journal of Zoo and Wildlife Medicine. 48 (3): 748–756. doi:10.1638/2016-0238.1. ISSN 1042-7260.
"Fire-bellied Toad". Seneca Park Zoo. Retrieved 2021-12-29.
Walkowiak, Wolfgang (1992). "Acoustic communication in the fire-bellied toad: an integrative neurobiological approach". Ethology Ecology and Evolution. 4: 63–74 – via Taylor & Francis Online.
Zeyl, Jeffrey N.; Laberge, Frédéric (2011-12-01). "Multisensory signals trigger approach behaviour in the fire-bellied toad Bombina orientalis: sex differences and call specificity". Zoology. 114 (6): 369–377. doi:10.1016/j.zool.2011.08.001. ISSN 0944-2006.
"Bombesin - an overview | ScienceDirect Topics". www.sciencedirect.com. Retrieved 2022-01-07.
Nagalla, Srinivasa R.; Barry, Brenda J.; Falick, Arnold M.; Gibson, Bradford W.; Taylor, John E.; Dong, Jesse Z.; Spindel, Eliot R. (1996-03-29). "There Are Three Distinct Forms of Bombesin: IDENTIFICATION OF [Leu13]BOMBESIN, [Phe13]BOMBESIN, AND [Ser3,Arg10,Phe13]BOMBESIN IN THE FROG BOMBINA ORIENTALIS(∗)". Journal of Biological Chemistry. 271 (13): 7731–7737. doi:10.1074/jbc.271.13.7731. ISSN 0021-9258. PMID 8631814.
Brattstrom, Bayard H. (1990). "Maze Learning in the Fire-Bellied Toad, Bombina orientalis". Journal of Herpetology. 24 (1): 44–47. doi:10.2307/1564288. ISSN 0022-1511.
Kang, Han Seung; Park, Chan Jin; Gye, Myung Chan (2010-05-01). "Effect of Carbaryl on Survival and Development in Bombina orientalis (Boulenger) Embryos". Bulletin of Environmental Contamination and Toxicology. 84 (5): 550–553. doi:10.1007/s00128-010-9979-y. ISSN 1432-0800.
Park, Chan Jin; Kang, Han Seung; Gye, Myung Chan (2010-11-01). "Effects of nonylphenol on early embryonic development, pigmentation and 3,5,3′-triiodothyronine-induced metamorphosis in Bombina orientalis (Amphibia: Anura)". Chemosphere. 81 (10): 1292–1300. doi:10.1016/j.chemosphere.2010.08.039. ISSN 0045-6535.

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