Taiwan Salamander, Formosan Hynobiid
© 2016 Arnaud Jamin (1 of 2)
Hynobius formosanus is a relatively small salamander with a snout-vent length ranging between 47.0 – 62.7 mm in males and 46.4 – 56.7 mm in females. Its tail length ranged from 31.6 – 46.1mm in males and 30.8 – 38.1 mm in females. The head is longer than it is wide (Lue and Lai 2008) and is flattened and round with nostrils that are closer to the tip of the snout than the eye. The space in between each nasal opening has a greater distance than the space between the eyelids, and eyelid size is the same as the interorbital space. The eyes are large. Hynobius formosanus have a gular fold. This species of salamander have long vomerine teeth row that are equivalent to three-fourths the width of the tongue (Dunn 1923). Individuals of the species also have paratoid glands that are flat and smooth skin. The fore- and hind-limbs are relatively short compared to body proportions and do not touch when adpressed, separated by 0 - 2 costal groves. The salamander has a paddle-shaped tail. Both males and females have 11 – 12 costal grooves (Lue and Lai 2008).
Recently hatched larvae have an open mouth and short gills that branch and spread out (Vassilieva et al. 2015) with total body length measuring about 19 – 21 mm (Sparreboom 2014). They also have flat forelimbs and conical buds of hind limbs. At around 2 weeks, larvae have forelimbs that are slightly larger than their hindlimbs and have medium sized tails compared to the ratio of their size. Additionally, these 2-week old larvae have a gelatin-like underside on their tail, which they have retained to serve as a paddle-like tail. At about 20 - 50 days after hatching, the first endochondral bones form along with its frontal nasal capsule. The dental structure starts with only two fused teeth that are not attached to the bone with an asymmetrical coronoid, which is found only in early larvae. These fused teeth are later lost in the adult stage and they end up having 3 - 4 functional teeth with coronoid definition. Older larvae still have an abundant source of egg yolk in their guts. Young salamanders have pre-existing fin-like outgrowth on fore- and hind limbs without balancers (Vassilieva et al. 2015).
Hynobius formosanus differs from other hynobiids because of its specific skeletal ontogeny and larval development. Specifically, there is an absence of palatine bone in all developing stages (Vassilieva et al. 2015), instead a dentigerous bone is present as part of a palatopterygoid in all larvae studied to date (Rose 2003). They also possess heterochronic alteration of patterns in cranial bone development different than those of other hynobiid species and an absence of the separate lacrimal, which is abnormal for hynobiids (Vassilieva et al. 2015), and they also have five toes (Sparreboom 2004).
Hynobius formosanus is the only member of the Hynobiidae family that completes metamorphosis with endogenous feeding throughout entire larval period (Kakegawa et al. 1989, Vassilieva et al. 2015). The salamander also produces a larger egg than other species in the family (Kakegawa et al. 1989). The outer envelope in the egg sac is soft and smooth, unlike Hynobius sonani, and has randomly placed horizontal grooves with lightly tinted longitudinal stripes compared to those found in H. sonani (Kakegawa et al. 1989).
More specific differences include, H. formosanus being lighter in color than H. arisanensis (Dunn 1923). Hynobius formosanus is sympatric with H. sonani in part of their range and can be differentiated by H. formanus having a lower elevational range and by coloration. Hynobius formosanus is similar to H. fuca but can be differentiated by H. formosanus having yellowish-brown dorsal blotches (Lai and Lau 2008).
Adult H. formosanus have brown dorsal colored with golden yellow-brown blotches on skin (Lue and Lai 2008). Other salamanders of the same species have “tawny yellow” bodies covered in dark tan spots with some on the ventral side of the body. The eyes are black (Dunn 1923).
Hynobius formosanus larval bodies don’t have much color; they have only light hues of white on their ventral skin. Recently hatched larvae possess dark pigmented eyes. At around 2-week old larvae have a light brown spotted ventral side (Vassilieva et al. 2015).
During the breeding season, there is sexual dimorphism with males having broader heads with more well-developed temporal muscles and longer tails (Chang et al. 2009).
Distribution and Habitat
Hynobius formosanus is endemic to Taiwan. The salamander is restricted to small patches of habitat within the Central Mountain range and the Syueshan Mountain range. It is found mostly near creeks and does not roam more than 5 m away from small, slow-moving bodies of water (Lee et al. 2006).
The salamander prefers high elevations ranging from 2,300 to 2,900m. Its habitats include primary forests of woodlands, broadleaf forests, coniferous forests, and ecotones between coniferous forests and bamboo grasslands (Lue and Chou 2004, Lue and Lai 2008). These areas are characterized by low temperatures, high rainfall and humidity, and infrequent disturbances (Lee et al. 2006).
Life History, Abundance, Activity, and Special Behaviors
The species' population distribution is affected by humidity; they are near creeks during the dry months of November through April, and farther during heavy rainfall months of May through October. The home range of each Taiwanese salamander varies from 0.02 to 12.47 m² and often overlaps with the home ranges of other members of the species (Lue and Lai 2008). Because it is restricted to such small patches of habitat, the Taiwan salamander is relatively rare (Lee et al. 2006).
The salamanders are highly associated with water, inhabiting areas beneath logs and rocks near small, cool creeks and seepage areas. Though adults are terrestrial when they are not breeding, larvae require water and can be found in headwater streams and underground seepages. Adult salamanders are nocturnal (Sparreboom 2014).
The breeding season for these salamanders occurs between November and January, when precipitation levels are lowest. Though no specific courtship behavior has been documented, males have been known to demonstrate aggression towards other males and to inflict serious injuries on each other (Chang et al. 2009).
Fertilization occurs externally in water after the female lays her eggs. Once the eggs have been fertilized, males will often stay with the fertilized egg sacs for several days to protect them from other males (Chang et al. 2009). Eggs are laid in clutch sizes of fewer than 25, typically between 14 and 15 eggs (Lee et al. 2006, Sparreboom 2014). This clutch size is the lowest amongst other Hynobius species, but the salamander makes up for this by having the largest relative egg size. Eggs are laid in egg sacs that are attached under stones in slow-moving water. These egg sacs are unique to the Hynobiid family, though their morphology differs between species (Chang et al. 2009).
The Taiwan salamander has pale yellow-brown tinted egg sacs, but the brown fades as the embryos develop. The egg sacs also have irregular grooves and stripes and act to protect the eggs and aid in attachment of the eggs to a substrate. Eggs inside the egg sac are made up of jelly layers believed to prevent entry of competing sperm, to aid in the attachment of eggs to each other, and to protect the embryos from predators, pathogens, contaminants, and stressors like temperature and UV light (Sparreboom 2014).
As embryos develop into larvae inside the egg, the jelly layers and egg sacs break down. Three months after the eggs have been laid, the eggs hatch and larvae emerge, measuring about 19 – 21 mm in length (Sparreboom 2014). The larvae retain a large amount of yolk, which acts as a food source and may help to explain why larvae have been reported to require little food. Larvae have four pairs of gill slits and caudal fins. Complete metamorphosis occurs two months after the eggs have hatched. Adults do not exhibit paedomorphism and so do not retain any juvenile features (Chang et al. 2009).
Relative to other Hynobiids, the Taiwan salamander has a shortened larval period and rapid embryonization, features that suggest a transition towards direct development. Metamorphosis in H. formosanus lasts typically from 48 to 55 days at temperatures of 14 to 16° C and can take up to 55 more days to metamorphose completely when at 10° C (Vassilieva et al. 2015). Such a transition may be the result of adaptations to the salamander’s environment where the number of breeding sites is limited and the suitability of streams for longer larval periods is lacking (Chang et al. 2009).
Adults search for terrestrial invertebrates like earthworms or sow bugs on the forest floor. Predation from snakes poses a threat to adult salamanders, but no information could be found on predation threats to larvae. Though no mention of specific coloration to protect against predators was found, based off the salamander’s morphology it does not appear to have aposematic coloration (Sparreboom 2014).
Trends and Threats
Hynobius formosanus is listed as “Endangered” on the IUCN Red List (Lue and Chou 2004) due to its small range size, habitat fragmentation, and continued decline of habitat quality and extent. Most of its habitat loss is due to the spread of ecotourism and the urbanization in Taiwan (Lue and Chow 2004, Sparreboom 2014). The only suitable habitat left in its range is found mostly within and nearby three of the province’s national parks. While these areas could serve as potential refuges for the species, there still exists the issue of human disturbance (Lee et al. 2006).
Taiwan’s national parks are major tourist destinations, attracting large numbers of people to the area for sightseeing. Taroko National Park, located in the Hehuanshan region of Taiwan, is predicted to have the largest population of H. formosanus in and around it. However, this park also contains one of the biggest tourist attractions in Taiwan, the Taroko Gorge. This, undoubtedly, means that habitat degradation will continue in this area as more people visit the park and more infrastructure is built to accommodate its popularity. Yushan National Park is the only one of three parks with a population of the salamander contained entirely within its borders (Lee et al. 2006). Long-term population monitoring programs and further data collection are highly recommended for conservation purposes (Lee et al. 2006). Although many sources point to ecotourism as the major threat to the species, specificities are not known, so an in-depth analysis of current threats is also recommended.
A second, possible threat to the Taiwan salamander is the use of agrochemicals. This is a major threat to many amphibian species in Taiwan (Lin et al. 2008). The Taiwan salamander, like most amphibians have incredibly permeable skin, which is useful for respiration. However, this means that agrochemicals may be easily absorbed from polluted creeks or directly from the soil. Although the species is predicted to be found only in montane areas, agriculture makes up about 24% of Taiwan’s landmass (Lee et al. 2006). For this reason, it is possible that populations of the Taiwan salamander, like many amphibian species, may reside on farmland.
Awareness of the species’ threat-level has existed since 1986 when it was listed under the Cultural Heritage Preservation law as a precious and rare species. The Taiwan salamander was later listed by the Wildlife Conservation Law in 1989 and on the IUCN Red List as "Endangered" in 2004 (Lau and Chou 2004, Sparreboom 2014).
Possible reasons for amphibian decline
General habitat alteration and loss
The species authority is: Maki, M. (1922). “Notes on the salamanders found in the island of Formosa.” Zoological Magazine Tokyo 34:635–639.
The loss of specimens during World War II and insufficient information in the original descriptions of H. formosanus and other related species has caused the phylogenetic relationships of H. formosanus to remain unclear (Lee et al. 2006). In 1922, three species under the Hynobius genus (H. sonani, H. arisanensis, and H. formosanus) were recognized and classified based on morphological characteristics (Lee et al. 2006). However, whether these species should be considered three distinct species or whether they should all be under the name of H. formosanus has been debated numerous times (Dunn 1923). Mitochondrial sequence data has classified H. formosanus as having a Nenggao subtype II, which distinguishes it from the closely related Hynobius sonani with a Nenggao subtype I (Lue and Lai 2008). Hynobius formosanus is now accepted to form a monophyletic group with three other species: H. glacialis, H. arisanensis, and H. sonani. However, its placement within this monophyletic group remains unknown. The sister taxon to this group is H. fuca (Lue and Lai 2008).
Morphological variation between the Taiwan salamander and other closely related hynobiids in Taiwan show that there has been blockage of gene flow between different populations due to past and present barriers. This has resulted in the formation of new species, such as Hynobius glacialis and Hynobius fuca, because the differences in genetic makeup prevent the species from interbreeding (Lue and Lai 2008).
The Taiwan salamander’s scientific species name “formosanus” may originate from the historic name of Taiwan – Formosa.
The karyotype for Hynobius formosanus is 2n = 58 (Iizuka et al. 1988).
According to one study, oviposition has been induced in H. formosanus in the lab, but researchers have not been able to do so in the wild (Sparreboom 2014).
Chang, J. C.-W., Tang, H.-C., Chen, S.-L., Chen, P.-C. (2008). ''How to lose a habitat in 5 years: trial and error in the conservation of the farmland green tree frog Rhacophorus arvalis in Taiwan.'' International Zoo Yearbook, 42(1), 109-115.
Chen, S. H., and Lue K. Y (1986). ''The Study of Salamanders from Taiwan (II) The Population Study of Hynobius formosanus Maki in Alishan.'' Journal of Biology, 21, 47-72.
Dunn, E. R. (1923). ''The salamanders of the Family Hynobiidae.'' Proceeding of the American Academy of Arts and Sciences, 58, 479-480.
Iizuka, K., Kezer, J., and Seto T. (1988). ''Karyotypes of Two Rare Species of Hynoboiid Salamanders from Taiwan, Hynobius Sonani (Maki) and Hynobius Formosanus Maki (Urodela).'' Genetica, 78.2, 105-110.
Kakegawa, M., Iizuka K., and Kuzumi S. (1989). ''Morphology of egg sacs and larvae just after hatching in Hynobius sonani and H. formosanus from Taiwan, with an analysis of skeletal muscle protein compositions.'' ,
Lai, J.-S., and Lue, K.-Y. (2008). ''Two new Hynobius (Caudata: Hynobiidae) salamanders from Taiwan.'' Herpetologica, 64, 63-80.
Lee, P. F., Lue, K. Y., and Wu, S. H. (2006). ''Predictive Distribution of Hynobiid Salamanders in Taiwan.'' Zoological Studies, 45.2, 244-254.
Lin, H.-C. , Cheng, L.-Y., Chen, P.-C., and Chang, M.-H. (2008). ''Involving local communities in amphibian conservation: Taipei frog Rana taipehensis as an example.'' International Zoo Yearbook, 42(1), 90-98.
Lue K., Chou W. 2004. Hynobius formosanus. The IUCN Red List of Threatened Species 2004: e.T59093A11870421. http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T59093A11870421.en. Downloaded on 12 October 2017.
Rose, C.S. (2003). '' Rose, C. S. (2003). “The developmental morphology of salamander skulls.'' Amphibian Biology, 5, 1686-1783.
Sparreboom, M. (2014). Salamanders of the Old World: The Salamanders of Europe, Asia and Northern Africa. Zeist, Brill, The Netherlands.
Vassilieva, A. B., Lai, J. S., Yang, S. F., Chang, Y. H., and Poyarkov Jr., N. A. (2015). ''Development of the bony skeleton in the Taiwan salamander, Hynobius formosanus Maki, 1922 (Caudata: Hynobiidae): heterochronies and reductions.'' Vertebrate Zoology, 65, 117-130.
Written by Michelle Gin, Brenden Mitchum, Karen Zuniga (mmgin AT ucdavis.edu, bsmitchum AT ucdavis.edu, kfzuniga AT ucdavis.edu), University of California, Davis
First submitted 2017-10-05
Edited by Ann Chang, Maxine Weber (2017-10-24)
Species Account Citation: AmphibiaWeb 2017 Hynobius formosanus: Taiwan Salamander <http://amphibiaweb.org/species/3883> University of California, Berkeley, CA, USA. Accessed Feb 19, 2019.
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Citation: AmphibiaWeb. 2019. <http://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 19 Feb 2019.
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