Odorrana Graminea
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''Odorrana graminea'', the large odorous frog, inhabits fast-flowing streams in elevated mountainous regions of Southern China and Northern Indochina. 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. Studies on ''O. graminea'' courtship vocalizations suggest female preference for increased proportion of nonlinear vocal phenomena (NLP).


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 , whereas males attain a more modest length of . 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. ''Odorrana graminea'' can produce
ultrasonic Ultrasound is sound waves with frequencies higher than the upper audible limit of human hearing. Ultrasound is not different from "normal" (audible) sound in its physical properties, except that humans cannot hear it. This limit varies fr ...
calls. This is very rare among non-mammalian vertebrates, but has been shown for the related
concave-eared torrent frog ''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-flowi ...
''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.


Habitat and distribution

''Odorrana graminea'' is found in southern
China China, officially the People's Republic of China (PRC), is a country in East Asia. It is the world's most populous country, with a population exceeding 1.4 billion, slightly ahead of India. China spans the equivalent of five time zones and ...
(from southern
Anhui Anhui , (; formerly romanized as Anhwei) is a landlocked province of the People's Republic of China, part of the East China region. Its provincial capital and largest city is Hefei. The province is located across the basins of the Yangtze River ...
and northern
Zhejiang Zhejiang ( or , ; , also romanized as Chekiang) is an eastern, coastal province of the People's Republic of China. Its capital and largest city is Hangzhou, and other notable cities include Ningbo and Wenzhou. Zhejiang is bordered by Jiang ...
west to extreme southern
Gansu Gansu (, ; alternately romanized as Kansu) is a province in Northwest China. Its capital and largest city is Lanzhou, in the southeast part of the province. The seventh-largest administrative district by area at , Gansu lies between the Tibet ...
, southeastern
Sichuan Sichuan (; zh, c=, labels=no, ; zh, p=Sìchuān; alternatively romanized as Szechuan or Szechwan; formerly also referred to as "West China" or "Western China" by Protestant missions) is a province in Southwest China occupying most of the ...
, and southern
Yunnan Yunnan , () is a landlocked Provinces of China, province in Southwest China, the southwest of the People's Republic of China. The province spans approximately and has a population of 48.3 million (as of 2018). The capital of the province is ...
to the border of
Vietnam Vietnam or Viet Nam ( vi, Việt Nam, ), officially the Socialist Republic of Vietnam,., group="n" is a country in Southeast Asia, at the eastern edge of mainland Southeast Asia, with an area of and population of 96 million, making i ...
,
Laos Laos (, ''Lāo'' )), officially the Lao People's Democratic Republic ( Lao: ສາທາລະນະລັດ ປະຊາທິປະໄຕ ປະຊາຊົນລາວ, French: République démocratique populaire lao), is a socialist ...
and
Myanmar Myanmar, ; UK pronunciations: US pronunciations incl. . Note: Wikipedia's IPA conventions require indicating /r/ even in British English although only some British English speakers pronounce r at the end of syllables. As John C. Wells, Joh ...
, although it has not yet been recorded in the latter two countries. Its type locality is the
Wuzhi Mountain Wuzhi Mountain () is the highest mountain in Hainan, China, towering above the center of Hainan Island. The surrounding areas of Wuzhi Mountain are inhabited mainly by the Li ethnic group. It is located adjacent to Wuzhishan City but is not pa ...
in
Hainan Hainan (, ; ) is the smallest and southernmost province of the People's Republic of China (PRC), consisting of various islands in the South China Sea. , the largest and most populous island in China,The island of Taiwan, which is slightly l ...
. Until the revision of "'' Rana livida''" in 2003, this frog was considered a synonym of ''
Odorrana livida ''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 neot ...
''. The species occurs near fast-flowing rivers and streams in montane (sub-)tropical forests.


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.


Conservation

The conservation status of ''Odorrana graminea'' is Least concern according to the International Union for Conservation of Nature. 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.


Habitat loss

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


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.


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.


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.


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. A thin tympanic membrane shared by ''O. tormota'' and ''O. graminea'' may be involved in this feat. Interestingly, ultrasonic communication is limited to males, while females are unable to detect at this range. ''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.


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).


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. ''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.


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).


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. AMPs function as a crucial innate immunity defense against pathogenic microbes. 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. 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. 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. Unlike certain other amphibians, the ''Odorrana tiannanensis'' AMPs under study did not demonstrate any cytotoxic or tumor cell anti-proliferative properties.


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. 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. A 2022 study investigating gut microbiome determinants compared the compositions of ''O. graminea'' and closely related ''Odorrana tormota'' and ''Amolops wuyiensi'' . 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. Relative abundance of various microbiota depends on habitat - but does not severely impact core microbiome functionality.


Physiology


Size sexual dimorphism

As in 90% of frog species, female ''Odorrana graminea'' are significantly larger than males). 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.


Ear structure

''Odorrana graminea'' males have a non-recessed tympanic membrane. 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''). 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.


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 cataract is a cloudy area in the lens of the eye that leads to a decrease in vision. Cataracts often develop slowly and can affect one or both eyes. Symptoms may include faded colors, blurry or double vision, halos around light, trouble w ...
, 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.


References

{{Taxonbar, from=Q3010930 graminea Amphibians described in 1900 Amphibians of China Amphibians of Vietnam Taxonomy articles created by Polbot