Odorrana graminea

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Odorrana graminea
Odorrana graminea.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Amphibia
Order: Anura
Family: Ranidae
Genus: Odorrana
Species:
O. graminea
Binomial name
Odorrana graminea
(Boulenger, 1900) [2]
Synonyms

Rana gramineaBoulenger, 1900

Odorrana graminea, the large odorous frog, inhabits fast-flowing streams in elevated mountainous regions of Southern China and Northern Indochina. [3] It is one of 56 species in the genus Odorrana. Male O. graminea are noted for their ultrasonic call characteristics and are one of three frog species able to detect ultrasonic frequencies (>20 kHz), likely evolved to facilitate communication amidst noisy streams and waterfalls. [4] Studies on O. graminea courtship vocalizations suggest female preference for increased proportion of nonlinear vocal phenomena (NLP). [5]

Contents

Description

Odorrana graminea have a dorsoventrally compressed body with large eyes. Dorsum is green with smooth skin; flanks are brown with yellow marbling and with slight granulations. They are relatively large frogs, particularly the females: females grow to a snout–vent length of 78–100 mm (3.1–3.9 in), whereas males attain a more modest length of 42–53 mm (1.7–2.1 in). Apart from size, males differ from females by their smaller digital disks, stronger forearms, larger tympanum, velvety nuptial pads on thumb, and paired gular pouches below jaw articulations. [6]

Odorrana graminea can produce ultrasonic calls. This is very rare among non-mammalian vertebrates, but has been shown for the related concave-eared torrent frog Odorrana tormota. However, O. graminea does not have recessed ears, a feature believed to be important for ultrasonic hearing in O. tormota. Exactly how O. graminea detects ultrasound remains yet to be determined. [4]

Habitat and distribution

Odorrana graminea is found in southern China (from southern Anhui and northern Zhejiang west to extreme southern Gansu, southeastern Sichuan, and southern Yunnan to the border of Vietnam, Laos and Myanmar, although it has not yet been recorded in the latter two countries. Its type locality is the Wuzhi Mountain in Hainan. [7] Until the revision of " Rana livida " in 2003, [6] this frog was considered a synonym of Odorrana livida . [7] The species occurs near fast-flowing rivers and streams in montane (sub-)tropical forests. [1]

Taxonomy

Odorrana graminea is one of 56 species in the genus Odorrana.  All Odorrana frogs live in tropical and subtropical mountainous regions in East and South Asia. The genus is rapidly growing, with over twenty new species documented since 2005. [8]

Conservation

The conservation status of Odorrana graminea is Least concern according to the International Union for Conservation of Nature. [1] Species in genus Odorrana ranges from “Least Concern” (e.g., Odorrana schmackeri) to “Endangered” (e.g., Odorrana splendida) - with many other species also documenting data deficiency. [1]

Habitat loss

Rampant deforestation has led to habitat loss and subsequent population decrease for many amphibians. [9] Residential and commercial development, agriculture, aquaculture, and biological resource use (e.g. logging and wood harvesting) are documented ecosystem stressors for Odoranna graminea. [6]

Research on closely related species Odorrana morafkai in the Viatnamese Langbian plateau suggests a decrease in population density in highly-disturbed sites. In both moderately-disturbed and non-disturbed sites, no such population density decrease was observed. There was no elucidated relationship between diet composition and habitat disturbance. Prey availability did not differ significantly in sites exhibiting various levels of habitat disturbance, suggesting that factors besides prey availability contribute to the gradient in population density. [10]

Conservation efforts

There has been no population monitoring or conservation effort specific to Odorranna graminea. Conservation efforts are in progress for certain endangered Odorrana species in order to preserve genetic diversity in a rapidly diminishing gene pool. A 2011 study on the highly-endangered Odorrana ishikawae presented a method of strategic artificial insemination of a parent generation, then natural mating in subsequent generations. Researchers struggled with yield, with less than 50% of inseminated eggs surviving to metamorphosis. However, it presents a promising strategy of manual intervention that could boost local diversity in other species of endangered Odorrana. [11]

Diet

Information on the O. graminea diet is lacking. However, studies of the related Odorraa morafkai in Southern Vietnam suggest a diverse diet of both aquatic and terrestrial prey. 90% of O. morafkai prey consists of insects, especially beetles. Distribution of prey type varied with season, likely due to increased range of access during the rainy versus dry season. [10]

Vocalizations

Odorrana graminea has a large repertoire of calls. They are highly variable both between and within individuals. Odorrana graminea has six basic types of calls with variation within each category: a. short tonal call (dominant type), b. long tonal call, c. multi-note calls, d. tonal calls with shallow or no frequency modulation, e. narrow-band call, and f. staccato call. All except for narrow-band and staccato contain ultrasonic frequencies (20 kHz or higher). Narrow-band and staccato calls are specifically used for short-range communication. [5]

Ultrasonic characteristics

Male Odorrana graminea exhibit a wide variety of ultrasonic harmonics (>20 kHz), and is one of few non-mammalian vertebrate species able to detect this frequency range. Huia cavitympanum, Odorrana graminea, and O. graminea’s close relative Odorrana tormota are the only known frog species able to detect ultrasonic waves. [4] A thin tympanic membrane shared by O. tormota and O. graminea may be involved in this feat. [12] Interestingly, ultrasonic communication is limited to males, while females are unable to detect at this range. [13]

O. graminea’s ability for ultrasonic communication may have evolved due to their natural proximity to noisy streams and waterfalls (a habitat niche shared by all three ultrasonic frog species). Both biotic and abiotic sounds tend to have a frequency far below ultrasonic range, so O. graminea is able to differentiate between intra-species communication and background noise in order to effectively locate other males of their species. [4]

Auditory sexual differences

Total and high-sensitivity hearing ranges vary greatly between O. graminea males and females. Males have a total range of 11-24 kHz, and a sensitive frequency range of 3-15 kHz. Females have a total range of 3-16 kHz, and a sensitive frequency range of 1-8 kHz (below the ultrasonic threshold of 20 kHz). [13]

Nonlinear vocal components

O. graminea males are known to exhibit nonlinear vocal phenomena “NLP”. NLPs are exhibited in many animal species, and are characterized by harsh and chaotic voice features intended to attract attention or convey arousal. [14] O. graminea can produce four types of NLP components: subharmonics, deterministic chaos, frequency jumps, or biphonations. Most vocalizations contain one or more of these components. Studies suggest that females prefer males with a higher proportion of nonlinear vocal components (P-NLP-C). Additionally, body size is positively correlated with P-NLP-C and amplectant mating behavior. It is possible that females use P-NLP-C as a long-distance indicator of fitness in potential mates. [5]

Phonotaxis

Female O.graminea vocalize as an indication of readiness to mate. In an experimental setup, female calls were played over a loudspeaker in the presence of O. graminea males. This prompted the male to orient his body and jump towards the loudspeaker with an impressive acuity of less than 1° (very precise compared to other amphibian species, which generally exhibit 16-23° acuity). [15]

Anti-microbial defense

Genus Odorrana exhibits notably abundant levels of anti-microbial peptides (AMPs) compared to other amphibians. Antimicrobial defense is considered a necessary tool to enable general amphibian colonization of damp or aquatic habitats, which tend to be pathogen-rich. [16] AMPs function as a crucial innate immunity defense against pathogenic microbes. [17] They are generally 10-50 residues long and vary in both sequence and structure for species across genus Odorrana. AMPs function by damaging the membranes of target organisms such as bacteria, fungi, parasites, and viruses. Different AMPs target unique ranges of microbes. Growing concern regarding increased antibiotic resistance has prompted further interest into the use of AMPs in medicinal applications. [18]

Research conducted on 22 AMPs derived from relative Odorrana tiannanensis demonstrated low potency against bacteria that are relevant to human health. Researchers hypothesize that either 1) these bacteria are not harmful to the frog, and friendly colonization helps to defend the frog against harmful environmental pathogens, or 2) these bacteria are eliminated by an immune system other than AMP. [18]

Four Odorrana tiannanensis AMPs were tested for antioxidant properties against free radicals, which can arise due to factors such as oxidative stress of UV exposure. Three of the four exhibited significant radical scavenging activity. Level of radical scavenging activity was correlated with the number of cysteine residues and disulfide bridges present in the AMP. [18]

Unlike certain other amphibians, the Odorrana tiannanensis AMPs under study did not demonstrate any cytotoxic or tumor cell anti-proliferative properties. [18]

Gut microbiome

Gut microbiota is affected by a large set of factors such as diet, habitat, health, and age. Temperature has been observed to induce direct changes in microbiome diversity and composition in terrestrial amphibians. [19] Habitat proximity agriculture is known to impact expression levels of bacterial genes associated with pesticide degradation. In this way, the microbiome was observed to adapt in a way that increased frog health and survival. [20]

A 2022 study investigating gut microbiome determinants compared the compositions of O. graminea and closely related Odorrana tormota and Amolops wuyiensi . [21] All three species are sympatric in Eastern China and tend to exist on rocks nearby running water. Researchers found significantly differing microbiota in all three species in terms of relative abundance of gut microbiota and predicted gene function. In all three species of this study, the present phyla include (in decreasing abundance): Proteobacteria, Bacteroidetes, Verrucomicrobia, and Firmicute. Proteobacteria is hypothesized to facilitate stress tolerance to cold streams. [21] Relative abundance of various microbiota depends on habitat - but does not severely impact core microbiome functionality. [20]

Physiology

Size sexual dimorphism

As in 90% of frog species, female Odorrana graminea are significantly larger than males). [3] Studies suggest that female frogs are under greater size-based selectional pressure due to an associated increase in fecundity. In certain frog species, larger males enjoy greater reproductive success due to victory in combat against smaller males; however, other traits such as forearm thickness and vocalization energy expenditure can be greater indicators of reproductive success in other species. [22]

Ear structure

Odorrana graminea males have a non-recessed tympanic membrane. [13] This is contrary to previous theories that recessed tympana specifically enable perception of high-frequency sounds (recessed tympanic membranes are exhibited in both other species of ultrasonic-communicating frogs: Odorrana tormota, Huia cavitympanum ). [23] Similarly to O. tormota, the tympanic membrane of O. graminea is relatively thin and transparent compared to other frog species, which could partially explain the ultrasonic hearing ability of both species. [4]

Growth defects and ocular abnormalities

Growth defects and malformations are an increasing phenomenon for amphibians worldwide, particularly in high-polluted areas (oil and gas sites, agricultural land with pesticide use or livestock). Odorrana graminea have also been observed with various limb malformations, for example stunted forelegs attributed to physical disruptions during the larval stage. Adult O. graminea have also been observed with cataracts, a clouding of the lens of the eye. This is rarely observed in adult frogs, as vision is essential for the individual's ability to find prey and avoid predation. [3]

Related Research Articles

Odorrana tormota, also known as the concave-eared torrent frog, is a species of frog native to China. Its distribution is restricted to Huangshan Mountains in Anhui and Jiande and Anji counties in northern Zhejiang. It occurs in fast-flowing streams and the surrounding habitats, and breeds in streams. The informally assigned common name for frogs in this genus is torrent frog.

<i>Odorrana aureola</i> Species of amphibian

Odorrana aureola, also known as the Phu Luang cliff frog or gold-flanked odorous frog, is a true frog species from northeastern Thailand. The specific name aureola is Latin and means ornamented with gold, in reference to the characteristic yellow markings on the limbs and flanks of this frog. It is notable for its ability to change color between green and brown, according to the surroundings.

<span class="mw-page-title-main">Túngara frog</span> Species of amphibian

The Túngara frog is a species of frog in the family Leptodactylidae. It is a small nocturnal terrestrial frog found in Mexico, Central America, and the northeastern regions of South America.

<i>Amolops torrentis</i> Species of frog

Amolops torrentis, commonly known as the torrent sucker frog or the little torrent frog is a species of frog in the family Ranidae and genus Amolops that is endemic to China, specifically only on the island of Hainan. They are most likely to be found in streams and surrounding wetland areas. Males have high-pitched mating calls, which are favored by females. Glands on this species' skin can secrete toxins. This species suffers from parasitism and habitat loss. Currently it is listed as vulnerable by the IUCN and is protected by law in China.

<span class="mw-page-title-main">Hole-in-the-head frog</span> Species of amphibian

The hole-in-the-head frog is a species of frog in the family Ranidae. It is the only member of the genus Huia. It is found on the island of Borneo. Its natural habitats are subtropical or tropical moist lowland forests, subtropical or tropical moist montane forests, and torrential rivers. It is threatened by habitat loss. The genus name honors Chinese herpetologist Shuchin Hu.

<span class="mw-page-title-main">Javan torrent frog</span> Species of amphibian

The Javan torrent frog is a species of frog in the family Ranidae. It is endemic to Java, Indonesia. It is found in Mount Halimun Salak National Park, Ujung Kulon National Park, and Gunung Gede Pangrango National Park in West Java, as well as in Dieng Nature Reserve in Central Java.

Odorrana andersonii is a species of frog in the family Ranidae.

The Tonkin frog is a species of frogs in the family Ranidae. It is found in northern Vietnam and in adjacent southern China. The specific name is derived from Bac Bo, the Vietnamese name for northern Vietnam, as the species was first described from there.

Odorrana exiliversabilis is a species of frogs in the family Ranidae that is endemic to southeastern China where it is found in Fujian, western Zhejiang, and southern Anhui provinces. These frogs can be found in mountain forest streams and are common in suitable habitat. The species is not considered threatened by the IUCN.

<i>Odorrana grahami</i> Species of frog

Graham's frog – also known as the diskless-fingered odorous frog – is a species of frog in the family Ranidae. It is found in China and Vietnam. Presumably it is also found in Myanmar in areas adjacent to its Chinese distribution area.

Odorrana hejiangensis is a species of frog in the family Ranidae that is endemic to China. It is found in the Yangtze River Valley of southern Chongqing and northern Guizhou, with an isolated record in western Guangxi. Its name refers to the type locality, Hejiang County in northern Sichuan. Its natural habitats are shaded hill streams and the surrounding riparian forests. Its status is insufficiently known.

Odorrana junlianensis, also known as the Junlian odorous frog, is a species of frogs in the family Ranidae. It is found in southern China and in the northernmost Laos and Vietnam. Its type locality is the eponymous Junlian County in Sichuan.

Odorrana kuangwuensis is a species of frog in the family Ranidae that is endemic to China. It is found in northeastern Sichuan and northwestern Hubei. Its name refers to the type locality, Mount Guangwu in Nanjiang County, northern Sichuan.

<i>Odorrana livida</i> Species of frog

Odorrana livida, also known as the green mountain frog, green cascade frog, Tenasserim frog, bright frog, large odorous frog, or large-eared rock frog, is a species of frog in the family Ranidae. It is known with certainty only from its neotype locality at the Dawna Range in Myanmar, near the border to Thailand, but molecular data suggest that it is present in northeastern India and in peninsular Thailand too, while records from China refer to other species. In much of the literature, this species has been confused with other species, including Odorrana graminea.

Odorrana lungshengensis is a species of frogs in the family Ranidae that is endemic to China. It is found in northeastern Guangxi, southwestern Hunan, and eastern Guizhou. Its natural habitats are hill streams in broad-leaf forests. It is becoming rare due to habitat loss.

Odorrana morafkai is a species of frogs in the family Ranidae. It is found in eastern Cambodia, southern Laos, and central Vietnam. This frog is highly unusual because it turns from its daytime green color to brown at night.

<i>Odorrana schmackeri</i> Species of amphibian

Odorrana schmackeri is a species of frog in the family Ranidae. It is endemic to China and distributed in southern and south-central China. Reports from Thailand and Vietnam require confirmation.

<i>Odorrana swinhoana</i> Species of frog

Odorrana swinhoana is a species of frog in the family Ranidae. It is endemic to Taiwan and widely distributed in hilly areas below 2,000 m (6,600 ft). It is named for Robert Swinhoe, a British naturalist and diplomat. Its common names include Swinhoe's brown frog, Bangkimtsing frog, brown-backed odorous frog, Taiwan odorous frog, and Taiwan sucker frog.

A mating call is the auditory signal used by animals to attract mates. It can occur in males or females, but literature is abundantly favored toward researching mating calls in females. In addition, mating calls are often the subject of mate choice, in which the preferences of one gender for a certain type of mating call can drive sexual selection in a species. This can result in sympatric speciation of some animals, where two species diverge from each other while living in the same environment.

<i>Odorrana</i> Genus of amphibians

Odorrana, commonly known as odorous frogs, is a genus of true frogs (Ranidae) from East Asia and surrounding regions. Many of these frogs inhabit fast-flowing mountain streams, and they typically have a remarkably pointed snout, as evidenced by common names like tip-nosed frog and scientific names like nasica or nasutus.

References

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  2. ↑ "Odorrana graminea (Boulenger, 1900)". Integrated Taxonomic Information System . Retrieved 25 May 2014.
  3. 1 2 3 Yeung, Ho Yuen; Yang, Jian-Huan (2022-02-13). "Limb malformation and ocular abnormalities in a Large Odorous Frog, Odorrana graminea (Boulenger, 1899) (Anura: Ranidae)". Reptiles & Amphibians. 29 (1): 101–102. doi: 10.17161/randa.v29i1.16274 . ISSN   2332-4961. S2CID   246840860.
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  5. 1 2 3 Chen, Pan; Wang, Jinmei; Miao, Junqi; Dong, Hao; Bao, Jiahui; Wu, Yatao; Zhang, Fang (January 10, 2022). "Female large odorous frogs ( Odorrana graminea ) prefer males with higher nonlinear vocal components". Ecology and Evolution. 12 (2): e8573. Bibcode:2022EcoEv..12E8573C. doi:10.1002/ece3.8573. ISSN   2045-7758. PMC   8831212 . PMID   35169452.
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  8. ↑ Wang, Ying-Yong; Lau, Michael Wai-Neng; Yang, Jian-Huan; Chen, Guo-Ling; Liu, Zu-Yao; Pang, Hong; Liu, Yang (2015-08-10). "A new species of the genus Odorrana (Amphibia: Ranidae) and the first record of Odorrana bacboensis from China". Zootaxa. 3999 (2): 235–254. doi: 10.11646/zootaxa.3999.2.4 . ISSN   1175-5334. PMID   26623573.
  9. ↑ Rowley, Jodi J. L.; Tran, Dao T. A.; Frankham, Greta J.; Dekker, Anthony H.; Le, Duong T. T.; Nguyen, Truong Q.; Dau, Vinh Q.; Hoang, Huy D. (2015-05-28). Guralnick, Robert (ed.). "Undiagnosed Cryptic Diversity in Small, Microendemic Frogs (Leptolalax) from the Central Highlands of Vietnam". PLOS ONE. 10 (5): e0128382. Bibcode:2015PLoSO..1028382R. doi: 10.1371/journal.pone.0128382 . ISSN   1932-6203. PMC   4447284 . PMID   26020250.
  10. 1 2 Le, Duong Thi Thuy; Rowley, Jodi J.L.; Tran, Dao Thi Anh; Hoang, Huy Duc (2020-06-12). "The diet of a forest-dependent frog species, Odorrana morafkai (Anura: Ranidae), in relation to habitat disturbance". Amphibia-Reptilia. 41 (1): 29–41. doi:10.1163/15685381-20191171. ISSN   0173-5373. S2CID   202852589.
  11. ↑ Sumida, Masayuki; Satou, Naoki; Yoshikawa, Natsuhiko; Kurabayashi, Atsushi; Islam, Mohammed Mafizul; Igawa, Takeshi; Oumi, Shohei; Katsuren, Seiki; Ota, Hidetoshi; Shintani, Nozomi; Fukuniwa, Hiroko; Sano, Naomi; Fujii, Tamotsu (November 1, 2011). "Artificial Production and Natural Breeding of the Endangered Frog Species Odorrana ishikawae , with Special Reference to Fauna Conservation in the Laboratory". Zoological Science. 28 (11): 834–839. doi:10.2108/zsj.28.834. ISSN   0289-0003. PMID   22035306. S2CID   32718977.
  12. ↑ Shen, Jun-Xian; Xu, Zhi-Min; Yu, Zu-Lin; Wang, Shuai; Zheng, De-Zhi; Fan, Shang-Chun (September 2011). "Ultrasonic frogs show extraordinary sex differences in auditory frequency sensitivity". Nature Communications. 2 (1): 342. Bibcode:2011NatCo...2..342S. doi: 10.1038/ncomms1339 . ISSN   2041-1723. PMID   21673663.
  13. 1 2 3 Liu, Wei-Rong; Shen, Jun-Xian; Zhang, Yu-Jiao; Xu, Zhi-Min; Qi, Zhi; Xue, Mao-Qiang (November 1, 2011). "Auditory sexual difference in the large odorous frog Odorrana graminea". Journal of Comparative Physiology A. 200 (4): 311–316. doi:10.1007/s00359-014-0885-3. ISSN   0340-7594. PMID   24510208. S2CID   17971793.
  14. ↑ Anikin, Andrey; Pisanski, Katarzyna; Reby, David (December 2020). "Do nonlinear vocal phenomena signal negative valence or high emotion intensity?". Royal Society Open Science. 7 (12): 201306. Bibcode:2020RSOS....701306A. doi:10.1098/rsos.201306. ISSN   2054-5703. PMC   7813245 . PMID   33489278.
  15. ↑ Shen, Jun-Xian; Xu, Zhi-Min; Narins, Peter M. (2022-08-08). "Male antiphonal calls and phonotaxis evoked by female courtship calls in the large odorous frog (Odorrana graminea)". Journal of Comparative Physiology A. 209 (1): 69–77. doi:10.1007/s00359-022-01561-2. ISSN   0340-7594. PMID   35939131. S2CID   251399937.
  16. ↑ Clarke, B. T. (2007-01-11). "The Natural History of Amphibian Skin Secretions, Their Normal Functioning and Potential Medical Applications". Biological Reviews. 72 (3): 365–379. doi:10.1111/j.1469-185X.1997.tb00018.x. PMID   9336100. S2CID   21041052.
  17. ↑ He, Weiyu; Feng, Feifei; Huang, Yong; Guo, Huanhuan; Zhang, Songyan; Li, Zheng; Liu, Jingze; Wang, Yipeng; Yu, Haining (September 16, 2011). "Host defense peptides in skin secretions of Odorrana tiannanensis: Proof for other survival strategy of the frog than merely anti-microbial". Biochimie. 94 (3): 649–655. doi:10.1016/j.biochi.2011.09.017. PMID   21963433.
  18. 1 2 3 4 Huan, Yuchen; Kong, Qing; Mou, Haijin; Yi, Huaxi (2020-10-16). "Antimicrobial Peptides: Classification, Design, Application and Research Progress in Multiple Fields". Frontiers in Microbiology. 11: 582779. doi: 10.3389/fmicb.2020.582779 . ISSN   1664-302X. PMC   7596191 . PMID   33178164.
  19. ↑ Fontaine, Samantha S.; Novarro, Alexander J.; Kohl, Kevin D. (2018-01-01). "Environmental temperature alters the digestive performance and gut microbiota of a terrestrial amphibian". Journal of Experimental Biology. 221 (Pt 20): jeb.187559. doi: 10.1242/jeb.187559 . ISSN   1477-9145. PMID   30171093. S2CID   52142122.
  20. 1 2 Huang, Bing-Hong; Chang, Chun-Wen; Huang, Chih-Wei; Gao, Jian; Liao, Pei-Chun (2018-01-11). "Composition and Functional Specialists of the Gut Microbiota of Frogs Reflect Habitat Differences and Agricultural Activity". Frontiers in Microbiology. 8: 2670. doi: 10.3389/fmicb.2017.02670 . ISSN   1664-302X. PMC   5768659 . PMID   29375532.
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  22. ↑ Nali, Renato C.; Zamudio, Kelly R.; Haddad, Célio F. B.; Prado, Cynthia P. A. (2014), Data from: Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs, Dryad, doi:10.5061/dryad.270sf , retrieved 2022-10-13
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