Tree-dwelling (pigmy) narrow-mouth frog; Nhai bau cay (Vietnamese)
Species Description: Poyarkov Jr NA, Vassilieva AB, Orlov NL, Galoyan EA, Dao TTA, Le DTT, Kretova VD, Geissler P 2014 Taxonomy and distribution of narrow-mouth frogs of the genus Microhyla Tschudi, 1838 (Anura: Microhylidae) from Vietnam with descriptions of five new species. Russian J Herpetol 21: 89-148.
Microhyla arboricola is a moderately slender frog with a snout vent length range of 13.2 - 15 mm for males and 15.9 - 17 mm for females. Their head is comparatively long and triangular with a snout that is pointed in dorsal and profile view, and protrudes slightly beyond the margin of the lower jaw. Laterally, the nostril is round and well below the canthus rostralis, closer to the tip of the snout than to the eye. The top of the head is flat with the canthus rostralis distinct and straight, however, in the dorsal view the canthus is curved and runs from the anterior corner of the eye to the nostril and then sharply curves ventrally anterior to the nostril. The loreal region is vertically concave. The eyes are large and protuberant in lateral view, while being slightly less pronounced in dorsal view, and shorter than the snout. The interorbital distance is narrow and is almost equal to the internarial distance. The upper eyelid is more than two times narrower than the interorbital distance. There is no pineal gland and the tympanum is hidden with no signs of a discernible supratympanic fold. The choanae is large with a transverse oval-shape, is also not widely spaced, and is largely concealed under the margin of the upper jaw. They have a toothless upper jaw along with missing vomerine teeth. The tongue does not have papillae and is missing a median notch, it is also narrow and spatulate. At the rear half of its length there are slit-like openings to a median vocal sac (Poyakov et al. 2014).
Microhyla arbicola has short and slender forelimbs. Their lower arms are comparatively long and massive with hands that are more than two times shorter than the forelimb length. There are two indistinct metacarpal tubercles. The inner metacarpal tubercle is oval-shaped. There is a single outer metacarpal tubercle that is rounded and flattened with unclear edges, it is indistinct and sub equal in diameter to the length of the inner metacarpal tubercle. The fingers are dorso-ventrally flattened with wide skin fringes on the fingers. The fringes are well developed and reach the finger disks for all fingers. The postaxial side of the first finger and preaxial side of the second finger are relatively developed with rudimentary webbing reaching the base of the disk at the first finger and the posterior edge of the proximal subarticular tubercle on the second finger. There is also rudimentary webbing between the second and third fingers that reaches the proximal subarticular tubercles. The first finger is greatly reduced and is shorter than one-third the length of the second finger. The second finger is slightly shorter than the fourth. They have a relative finger length of I < II < IV < III. The tip of the first finger is rounder with the tips of the outer fingers notably dilated, forming oval shaped truncated disks of the same width as the basal phalange on the third finger. The truncated disks are slightly wider than the basal phalanges on the second and fourth fingers with the first finger’s diameter sub equal to that of the third finger’s disk. Microhyla arboricola has clear peripheral grooves that are well developed on all finger disks; the narrow peripheral groove can be discernible on the first fingertip, however, dorsally the tips of the three outer fingers are short and poorly developed but have comparatively deeper median longitudinal furrows. They have relative finger disk widths of I < IV < II = III. The subarticular tubercles on fingers are rounded and greatly flattened with indistinct edges. The proximal subarticular tubercles are distinct and prominent with the distal subarticular tubercles on the two outer fingers not being very distinct. On the third finger the distal subarticular tubercle is discernible but no traces of the distal subarticular tubercle can be seen on the fourth finger. The subarticular tubercle formula is 1, 1, 2, 1. There is no nuptial pad (Poyakov et al. 2014).
Microhyla arboricola have hind limbs that are slender and long. They are a little less than three times the length of the forelimb. The tibia, in particular, is long and slender, around one-third that of the hind limb length. When the limbs are held at right angles to the body the heels are in contact. The tibiotarsal articulation of the hind limbs when adpressed to the body reach well beyond the snout. The foot is slightly shorter than the tibia length. The tarsus is smooth and there is no inner tarsal fold. They have relative toe lengths of I < II < V < III < IV. The tips of all five toes are distinctly dilated into wide truncated disks that wider than those of the fingers. The disks of all toes have well developed peripheral grooves. Dorsally, all toes disks with short median longitudinal grooves are similar to the finger disks but are more prominent and well developed. The relative toes disk width is I < V < II < III = IV. Dorso-ventrally the toes are distinctly flattened and have narrow fringes on the preaxial and postaxial sides of the outer four toes reaching to the disks. Well-developed webbing is between the toes and reaches the level of penultimate subarticular tubercles. The webbing becomes fringes as it reaches the toe disks. The webbing formula is I 1 ⅔ – 2¼ II 2 – 3 III 2½ – 3½ IV 3 – 1½ V. The subarticular tubercles on toes are round, flattened, very indistinct, and have a formula of 1, 1, 2, 3, 2. The proximal subarticular tubercles at all toes are distinct, however the distal tubercles have unclear edges and are less prominent. There is a single metatarsal tubercle. The inner metatarsal tubercle is prominent but small, short, and bean-shaped; it is slightly longer than half of the first toe. The outer metatarsal tubercle is absent (Poyakov et al. 2014).
They have a smooth dorsum that can be slightly tubercular at the lateral sides. Dorsally, the skin is feebly granular with a few small round low tubercles and granules scattered over the dorsum. There is a pair of notably larger elongated granules located on scapular region, which are surrounded by smaller tubercles. Two oblique rows of small glandiform granules run from the posterior corner of the eye toward larger granules in the scapular area. The length of the glandular rows is greater than the eye diameter. Small granules are also scattered over dorsal surfaces of the forelimbs and lower arm. The dorsal surface of the hind limbs is covered by irregularly scattered low tubercles and pustules. The granules on the hind limbs are larger than those on the forelimbs. The dorsolateral edges of the hind limbs are not clearly distinct even with the occasional granules on them and gradually flatting posteriorly. The eyelids do not have supraciliary spines or granules. The flanks of the body and lateral sides of the head are smooth with small granules present only in the tympanal area and axilla. The ventral side of the body and limbs are smooth, along with the vent. The cloacal opening is unmodified and directed posteriorly at the upper level of the thighs (Poyakov et al. 2014).
Larvae of M. arboricola have a morphology that is not similar to any other larvae from the Microhyla genus from Indochina or Eastern Asia. Their body is elliptical or pyriform with a depressed, bluntly rounded snout. The eyes are dorsal and not visible from below. The tail is more than three times longer than the body, there are also developed muscular parts and low fins. The slit-like spiracle is ventral and medial without dermal flaps. The oral disk is wide and oriented dorsally with the upper labium edges having two large rounded protuberances. The oral funnel and keratinized elements are absent (Poyakov et al. 2014). Larval M. arboricola lack any keratinized mouthparts representing toothless oophagous tadpoles (Vassilieva et al. 2017).
Adult M. arboricola have well-developed digital disks on three outer fingers and all toes that distinguishes them from other members of the genus, where digit tips are not expanded to disks or are restricted to only toes. The presence of one metatarsal tubercle differentiates M. arboricola from all other Indochinese and East Asian congeners, expect for M. nanapollexa. However, M. nanapollexa does not have as broad foot webbing that reaches the toe disk. Additionally, M. arboricola is smaller than Microhyla minuta. Microhyla picta has a stouter body and an enlarged outer metatarsal tubercle comparatively (Poyakov et al. 2014).
Larvae of M. arboricola more closely resemble the larvae of Rhacophorus vampyrus than other Microhyla species (Vassilieva et al. 2017).
In life, M. arboricola has a pinkish beige dorsal coloration and a light yellow-brown anterior part of the dorsum and head. They continue to get darker posteriorly but turn to light ochre on the posterior part of the dorsum. The sides of the head are slightly darker than the dorsum with the upper jaw being dark ochre to dark brown. The upper jaw had irregular whitish molting and larger cream-white spots along the edge of maxilla. There is a distinct brown-black stripe that curves from the snout tip towards the nostril and then runs posteriorly along the canthus rostrails toward the anterior edge of the eye. The stripe has irregular borders and distinctly widens closer to the eye. The upper eyelid may have tiny spots on the periphery. The posterior edge of the eye has an irregularly shaped black triangular blotch. The iris is a dark copper with dense black reticulation. The pupil is round and black, outlined with copper-orange circle. An indistinct light-brownish interorbital bar runs transversally across the head between the most medial parts of the upper eyelids covering the posterior fourth of the eyes. The interorbital bar forms a very indistinct broad V-shaped figure across the head, running posteriorly to the scapular area. The V-shaped figure is edged with two light-colored beige narrow lines; they mark characteristic glandular rows running from the posterior edge of the eyes toward the scapular area. The light colored glandular rows are easily discernible both in life and in preservative. The interorbital bar and the base of the head are covered with irregular darker marbling that does not form a clear distinct pattern. The supratympanic area does not have a dark line, but both sides of the head have a small black spot in the middle of the distance between the eye and axilla. A row of three narrow cream-yellow spots runs from the posterior corner of the eye ventrally and then posteriorly towards the mouth, a larger spot is located closer to the eye with two smaller spots at the angle of the mouth. The tympanic and axillar areas are covered by whitish mottling. The forehead and snout are lighter and have no spots or dark markings. The pineal area is without dark markings and has the same light coloration as the forehead (Poyakov et al. 2014).
The dorsal markings become darker and more distinct posterior from the head basis where it narrows and has a smaller width when compared to the upper eyelid at the scapular area. The markings run sharply posteriorly and then widens, forming an hourglass or X-shape. The dark dorsal marking is edged with a thin cream-beige line. Posterior from the scapular narrowing of the X-shaped dark dorsal marking, two distinct bands gently curve toward the groin area where they eventually become indistinct. On both sides of the dorsum in the scapular region, two small distinct brown-black oval-shaped spots are located laterally from the anterior part of X-shaped dark dorsal marking. Two prominent pinkish warts, along with similar pinkish tubercles and pustules can be seen on the posterior part of the dorsum. There is no medial round black spot or vertebral stripe present on the dorsomedial line. There are two small black ocelli that are accompanied by two black spots located on the sacrum along the coccyx . The flanks are slightly darker than the dorsum with a grey brownish coloration. From the area above the axilla there is an interrupted dark stripe that runs posteriorly along the dorsolateral edge, it reaches the groin and sharply ends about 1 mm anterior to the hind limb. On both sides of the body there is a large black triangular blotch that is above the limb insertion and a black stripe that runs from the area above the axilla to the groin where it slightly widens posteriorly. Both of the black marks are edged with a thin cream white line. The brown color of the body flanks turn somewhat lighter at the belly. There is a small rounded black spot edged with white located on the flanks posterior to axilla on each of the body sides (Poyakov et al. 2014).
Dorsally, the surfaces of the forelimbs are light orange-brownish with irregular brownish blotches. Normally, there are black spots on the posterior surface of the forearm, more proximal than the elbow. The dorsal surfaces of the hind limbs are slightly darker with a tan-brownish coloration. The thighs and shanks have distinct brown cross-bars edged with thin cream-white lines. There are three bars on each of the thighs and knees along with two bars on the shanks. The cross-bars have comparatively straight borders. When the frog is sitting, the dark stripes from the thighs and shanks line up, appearing continuous. Larger black spots are on the anterior surface of the thighs over the knee area. There are double black spots on the posterior edges of the shanks. Posterior to the hind limb insertion the body flanks have small bluish or whitish spots. Dorsally, the fingers and toes have indistinct brownish molting (Poyakov et al. 2014).
The ventral surfaces are greyish-beige on the belly to reddish-brown on the throat with numerous small cream-yellow or whitish posts. On the chest and central parts of the belly there is scattered mottling. The chin is notably darker. On the throat margin, dark brownish colors are more abundant, there is no medial line on the chin. The vent is pinkish-beige. Ventrally, the limbs are brownish and mottling. There is irregular dark mottling on the ventral surfaces of the hand and fingers. The ventral surfaces of the hind limbs have a distinct large black spot on the tibiotarsus and irregular brownish markings on the foot and toes that continues to the ventral surface of the fingers and toes (Poyakov et al. 2014).
In preservative, M. arboricola has the same pattern as in life but the colors are faded. More specifically, M. arboricola has a grey-brown interorbital bar along with the top of the snout. There is a short cream stripe from the posterior corner of the eye to the corner of the mouth, the mouth is bordered by dark grey underneath. The reddish coloration on the ventrum disappears and the belly appears cream-yellowish with irregular brown spots (Poyakov et al. 2014).
Tadpoles in life are uniformly dark brown or grey with the tail fin and belly being slightly paler (Poyakov et al. 2014).
Microhyla arboricola males are much smaller than females and have snout vent lengths under 15 mm while females had snout vent lengths over 15.9 mm. Males also have medial gular pouches and normally have a somewhat lighter coloration including the X-shaped dorsal pattern being less prominent and lighter. Female dorsal coloration is often darker, the forehead is lighter than the dorsum, interorbital bar is a brownish-red, and the X-shape is more of an hourglass shape along with having irregular boarders that are edged with white. Females also have a dark dorsolateral stripe that is wider and runs from the axilla to the groin along the dorsolateral edges. The lateral and ventral surfaces also have darker reddish-brown coloration with a white stripe from the eye to the mouth has a more distinct angle than the males (Poyakov et al. 2014).
Distribution and Habitat
Microhyla arboricola can be found in the Chu Yang Sin National Park and Hon Ba Natural Reserve in Vietnam. They were found in water-filled tree hollows in a high montane evergreen tropical forest on the slope of Chu Pan Phan Mountain at elevations of 1000 m a.s.l. Specimens were also collected in tree hollows on the limited grove of primary montane poly-dominant evergreen forest on the top of the mountain ridge at about 1500 m a.s.l. within the Hon Ba Nature Reserve (Poyakov et al. 2014).
Life History, Abundance, Activity, and Special Behaviors
Within the microhylid frogs, M. arboricola is unique in its reproductive biology and larval appearance. Microhyla arboricola have relatively smaller clutch sizes as well as larger eggs. Larvae also take part in oophagy and and have body morphologies consistent with this lifestyle (Vassilieva et al. 2017).
Reproduction in M. arboricola was observed in Chu Yang Sin National Park towards the end of March and into April after a series of heavy rains at a temperature around 15 - 16ºC at night and 20 - 23ºC during the day. However, in Hon Ba Nature Reserve breeding was recorded in mid-June during the rainy season at a slightly higher humidity and temperatures than those in Chu Yang Sin. Microhyla arboricola is an obligate phytotelm breeder and deposit their clutches in the water-filled tree hollows. The tree hollows they use for reproduction varied greatly in size, location, and capacity, however all hollows were located in broadleaved trees. Clutches comprise up to 30 large pigmented eggs that are suspended on the inner walls of the hollows above water level. All clutches were fixed in a dense transparent jelly layer. The hatching tadpoles drop to the water where they eventually develop until metamorphosis. Newly hatched tadpoles had endogenous yolk but switched to oophagy for nutrition after the yolk supplies run out. Morphology of the mouth and body is consistent with oophagy making M. arboricola the first of its genus to display tree-breeding oophagy (Poyakov et al. 2014, Vassilieva et al. 2017).
Larvae from Chu Yang Sin had an embryonic period of about five to six day in temperatures of about 18 - 20º C. The hatching larvae were at stages 25 or 26 and had nearly developed opercula folds and small remnant gill openings on both sides, with faintly pigmented cornea, developed adhesive organs, and a terminal mouth opening with a large amount of yolk. Once larvae hatched, the total length among clutches varied. Other Microhyla species larvae hatch around stages 20 - 21 and did not have an opercular fold or a spiracle but had pigmented cornea and a smaller total length. In M. arboricola yolk resorption in tadpoles occurred at stage 26, about 4 - 5 days after hatching when active feeding began (Vassilieva et al. 2017).
In Chu Yang Sin National Park, M. arboricola occurs syntopically with Theloderma chuyangsinense and Michrohyla annamensis. In Hon Ba Nature Reserve, M. arboricola occur syntopically with Kalophrymus honbaensis, Raorchestes gryllus, Hylarana montivaga, Leptobrachium leucops, and Ingerophrynus galeatus. Microhyla arboricola share breeding sites with other obligate hollow breeders like, Rhacophorus vampyrus and Theloderma truongsonense (Poyakov et al. 2014). In Chu Yang Chin, Theloderma palliatum also reproduces in water-filled tree holes. In Hon Ba, Theloderma truongsonense, have close breeding sites to M. arboricola, about the same elevation and only 10 - 50 meters separation between tree hollows (Vassilieva et al. 2017).
Trends and Threats
Microhyla arboricola has seen a decrease in population due to logging and wood harvesting as well as habitat shifting and severe climate change (IUCN 2017).
Possible reasons for amphibian decline
General habitat alteration and loss
The species authority is: Poyarkov Jr, N.A., Vassilieva, A.B., Orlov, N.L., Galoyan, E.A., Dao, T.T.A., Le, D.T.T., Kretova, V.D., Geissler, P. (2014) "Taxonomy and distribution of narrow-mouth frogs of the genus Microhyla Tschudi, 1838 (Anura: Microhylidae) from Vietnam with descriptions of five new species." Russian Journal of Herpetology 21: 89-148.
The phylogenetic position of M. arboricola is unknown and needs more molecular analyses. While M. arboricola shares some external morphology with all other species of Indochinese Microhyla as well as with M. nanapollexa, such as long hindlimbs, single metatarsal turbercle, developed digits that have median grooves dorsally, and relatively miniature flattened toes with dermal fringes, it is phylogenetically unclear if these traits hold any value. A broad study of phylogenetic relationships is needed to clarify the evolutionary relationship of this new species (Poyarkov et al. 2014).
The species epithet, “arboricola” is Latin for “inhabitant of trees” used as a noun in apposition. The species epithet references the site the new species uses for reproduction (Poyakov et al. 2014).
At the time of its description, M. arboricola was the smallest known frog of Vietnam (Poyakov et al. 2014).
IUCN SSC Amphibian Specialist Group (2017). ''Microhyla arboricola.'' The IUCN Red List of Threatened Species 2017: e.T73727593A73727604. http://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T73727593A73727604.en. Downloaded on 07 February 2019.
Poyarkov, Jr, N.A., Vassilieva, A.B., Orlov, N.L., Galoyan, E.A., Dao, T.T.A., Le, D.T.T., Kretova, V.D., Geissler, P. (2014). ''Taxonomy and distribution of narrow-mouth frogs of the genus Microhyla Tschudi, 1838 (Anura: Microhylidae) from Vietnam with descriptions of five new species.'' Russian Journal of Herpetology, 21(2), 89-148. [link]
Vassilieva, A.B., Vitaly, L., Trounov, Nikolay, A., Poyyarkov Jr., N.A., Eduard, A., Galoyan (2017). ''The phytotelm tadpoles of Microhyla arboricola (Anura: Microhylidae) from Vietnam, with comments on reproductive biology and development.'' Zootaxa, 4(4247), 413–428. [link]
Written by Maxine Weber (maxine349 AT berkeley.edu), UC Berkeley
First submitted 2019-03-14
Edited by Ann T. Chang (2019-04-04)
Species Account Citation: AmphibiaWeb 2019 Microhyla arboricola: Tree-dwelling (pigmy) narrow-mouth frog; Nhai bau cay (Vietnamese) <http://amphibiaweb.org/species/8223> University of California, Berkeley, CA, USA. Accessed Apr 21, 2019.
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Citation: AmphibiaWeb. 2019. <http://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 21 Apr 2019.
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