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Phyllomedusa sauvagii
Waxy Monkey Tree Frog, Waxy Monkey Leaf Frog, Painted-bellied Tree Frog, Painted-belly Monkey Frog, Painted-belly Leaf Frog
family: Hylidae
subfamily: Phyllomedusinae

© 2018 Mauro Teixeira Jr (1 of 23)

  hear Fonozoo call

Conservation Status (definitions)
IUCN (Red List) Status Least Concern (LC)
CITES No CITES Listing
Other International Status None
National Status None
Regional Status None

 

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Description

The snout-vent length for Phyllomedusa sauvagii ranges from 69.0 - 89.2 mm for males and between 83.4 - 96.6 mm for females. The head of the frog is longer than it is wide, and shaped like a trapezoid from both the dorsal and lateral view. This makes a broad, angular head that is not as wide as the body. The snout itself is truncated (Ruiz-Monachesi et al. 2016). The teeth on the maxilla and premaxilla both have circular tips. Phyllomedusa sauvagii possesses vertically elliptical pupils in relatively protruding eyes (Kok and Kalamandeen 2008). This anuran has well-developed, protruding parotoid glands (De La Riva 1999). A singular, subgular, and non-distinct vocal sac, as well as vocal slits are present (Duellman 2010; Kok and Kalamandeen 2008). The tympanum is visible on the sides of the head (Ruiz-Monachesi et al. 2016). The skin of P. sauvagii exhibits distinct wrinkles (De La Riva 1999). Phyllomedusa sauvagii has long, thin limbs, reduced terminal discs in the phalanges, lacks toe webbing, and has opposable thumbs used to grip trees (Wells 2007; Sheil and Alamillo 2005).

Larvae measure around 6.7 mm at stage 24. At this stage gills are still present, but have an opercular fold covering the base. Gill ciliation is also still present. The tail is relatively long, measuring around 0.7 mm, with high fins and narrows to a thin flagellum. The defining features of the mouth are the presence of two marginal papillae and serrated jaw sheaths in the oral disc. Keratodonts and amedical spiracle aren’t seen in the larvae until stage 25 of development (Salica et al. 2011).

The skull of Phyllomedusa sauvagii resembles that of P. vaillantii and P. venusta, with less resemblance seen in P. atelopoides (Ruiz-Monachesi et al. 2016). Unlike the P. tarsius group, P. sauvagii does not have black reticulations in the iris (De La Riva 1999). The truncated snout is distinct from that of other related species, such as P. vaillanti, which have round snouts (Ruiz-Monachesi et al. 2016). The body of P. sauvagii is larger, more robust and round than P. boliviana and P. burmeisteri, which are especially slender and angular (Rodrigues et al. 2007).

In life, the body of P. sauvagii ranges from light-brownish to bright green with a very distinctive opaque overlayer from their natural waxy coating (De La Riva 1999). In preservative, its skin turns to a deep purple (Kok and Kalamandeen 2008). Most frogs have distinctive white ventral stripes, varying in continuity, distinctiveness and placement. Most frogs also have a variable white striped marking along the bottom mandible that extends down the length of the body. In addition, some individuals may have orange and black coloration on the bottom sides of their limbs that vary in continuity and placement. Their eyes are a pale gray color (De La Riva 1999).

Sexual dimorphism is present in P. sauvagii. The snouts of females are rounder than males (Rodrigues et al. 2007). Females are larger than males and the mass of the gonads make up a higher percentage of the female’s body mass (Rodrigues et al. 2007). In addition, the maxillae are bent in the females and straighter in males (Ruiz-Monachesi et al. 2016).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Argentina, Bolivia, Brazil, Paraguay

 

View distribution map using BerkeleyMapper.

Phyllomedusa sauvagii can be found in South American rainforests and humid montane forests, specifically in the Chacoan region of eastern Bolivia, northern Paraguay, Mato Grosso do Sul of central Brazil, and Northern Argentina (Duellman 2010; Aquino et al. 2004). The species can be found up to 1500 meters above sea level (Aquino et al. 2004).

Life History, Abundance, Activity, and Special Behaviors

Phyllomedusa sauvagii is an arboreal breeder that, during mating season, lives near temporary lagoons and flooded fields and has adapted to living in areas with dry seasons (Aquino et al. 2004, Rodrigues et al. 2007). During the dry period, individuals can be found “in small forest fragments near to ponds” (Rodrigues et al. 2007).

In accordance with its nocturnal lifestyle, the frog calls at night, usually around two hours after sunset (Rodrigues et al. 2007). During the rainy seasons, the male P. sauvagii will call nearly every night. This occurs when heavy rainfall over several days fills nearby ponds (Schaulk et al. 2016). In addition, Halloy and Espinoza (2000) found that all P. sauvagii males will fight over some calling sites, but did not determine if it is specifically for oviposition sites or calling sites (Wells 2007). Corresponding with calling, reproduction occurs in the rainy season, from October to May (Rodrigues et al. 2007). Phylomedusa sauvagii has characteristics of both an explosive breeder and a prolonged breeder in that there is a concentration of males calling after rain, but the reproductive period lasts longer than 6 months (Rodrigues et al. 2007). After vocalizing on shrubs during heavy rainy days (and up to 2 days after), a mating pair will go to a pond or a flooded field and into the vegetation (Wells 2007, Rodrigues et al. 2007). The males do not seem to actively search for females, and the females do not exhibit polyandry (Rodrigues et al. 2007).

Like many of the Phyllomedusa genus, P. sauvagii lays terrestrial clutches in nests made out of leaves (Wells 2007). In axillary amplexus, the parents use their body weight and movement of their legs to fold up one to three leaves of the Asteraceae family, into which they deposit their clutches. The pair places their nest above water (Rodrigues et al. 2007; Garcia et al. 2013). Amongst the eggs, there are gelatinous eggless capsules, which, along with the folded leaf nests, decrease chances of desiccation (Rodrigues et al. 2007; Wells 2007). Additionally, because of the non-aquatic egg phase, females choose microhabitats specifically to reduce desiccation (Garcia et al. 2013).

Eggs are relatively large (2.54 mm is the average) and highly yokey, with a range of 201 to 829 eggs per clutch (Rodrigues et al. 2007; Salica et al. 2011). Phyllomedusa sauvagii has indirect development and ontogeny. Complete embryonic development lasts around seven days (Salica et al. 2011). Larvae feed on the yolk in the egg until they hatch (Rodrigues et al. 2007). Once they hatch, tadpoles fall from their leaf nests down into the water (Garcia et al. 2013). Gill regression begins once the tadpoles enter the water, occasionally fully regressing within two hours (Salica et al. 2011).

Since P. sauvagii lives in a habitat that has a limited and unpredictable amount of water, the adults exhibit uricotelism. Additionally, P. sauvagii larvae exhibit ureotelism, despite the fact that they are aquatic. This means that they secrete urea, and only start excreting uric acid during metamorphosis (Hellman et al. 2009).

In females, there is a positive correlation between snout-vent length and ovary mass, as well as body and ovary mass. However, the number of mature eggs has no correlation with either body mass or snout-vent length. Females also have no correlation between snout-vent length and reproductive energy. However, there is a negative correlation between reproductive output and body mass. In males, there are no major correlations between snout-vent length and reproductive energy, and no correlation between body mass and reproductive energy (Rodrigues et al. 2007).

Generally, arboreal frogs have lower evaporative water loss than non-arboreal frogs. We see even lower evaporative water loss in Phyllomedusa (Shoemaker et al. 1975; Faivovich et al. 2010). Phyllomedusa sauvagii achieves these low rates through waxy skin secretions that are produced by skin lipid glands and spread over the body through movement of the hind limbs and rear in a motion referred to as “wiping behavior” of which there are four variations (Blaylock et al. 1976; Gomez et al. 2006). The waxy secretion is a mix of wax esters and triglycerides, with free fatty acids and hydrocarbons that block water evaporation up to 38 to 39 degrees Celsius (McClanahan et al. 1978; Hillman et al. 2009). This waxy secretion, along with the excretion of uric acid (up 80% of the nitrogen waste), and diurnal torpor, allows for impermeabilization of the skin (Castanho et al. 2001). Due to its waterproof skin, the frog can bask in the sunlight and raise its body temperature from 35 to 40 degrees Celsius. When dehydrated, P. sauvagii will increase their body temperature, supposedly for water conservation. To prevent overheating, they use a mucous gland discharge. Phyllomedusa in general can use their serous skin glands to modulate secretions, similar to sweating in other animals (Hillman et al. 2009).

When not sitting on small branches with its legs tucked in, P. sauvagii moves by walking instead of hopping (Wells 2007; Soliz and Ponssa 2016). Due to this walking gait and its opposable digits, the frog has a lemuroid manner of climbing (Duellman 2010). The genus Phyllomedusa is adapted to an arboreal lifestyle, specifically in the forelimb. The forelimb has an “elongation and increase in size of the muscles, the presence of strong and long tendons, … and the presence of elongated and naked bony areas” (Manzano et al. 2008). Muscles have accessory branches, and there is a greater abduction of the fifth digit, which all allow for a better grip. Interestingly, P. sauvagii can utilize a precision grip on narrow branches and in its wiping behavior; precision grip is only seen elsewhere in higher primates (Manzano et al. 2008).

The small, narrow leaves of Asteraceae can expose the eggs, so when egg predation is evident, it seems that the eggs are wrapped in more leaves. Adult anurans also see predation from birds and crocodiles (Rodrigues et al. 2007).

While the diet of P. sauvagii remains unclear, assumptions can be made based on closely related species. Most anurans eat terrestrial invertebrates. The frog’s sister taxon, the P. burmeisteri group, regularly eats arthropods (de Paula Lima et al. 2010). Pyllomedusa sauvagii practices dermatophagy, which means that they ingest stratum corneum after molting. This provides a supplementary source of vitamin D and proteins (Castanho et al. 2001). During rain, P. sauvagii drinks rain drops that drip from the leaves of its habitat by lifting its snout in the air to pump water down its throat, allowing the frog to obtain water without leaving its primary habitat (Wells 2007; Hillman et al. 2009).

Trends and Threats

This species currently has a stable population trend and has an IUCN Red Listing status of "Least Concern". However, P. sauvagii is threatened by the international pet trade, habitat destruction, pollution, and fires (Aquino et al. 2004). In the Córdoba, Argentina part of the Chacoan forest, forest degradation from logging and overgrazing has simplified diversity and structure. This changes the frog’s ability to find proper vegetation for reproduction (Garcia et al. 2013).

Larval development is also affected by arboreal habitat partially converted for agriculture or lost completely (Rodrigues et al. 2007). In addition, the rate of gametogenesis in the frog has been observed to decline in times of high heat and drought (Wells 2007). While there are no specific conservation efforts for P. sauvagii, the frog occurs in several protected areas (Aquino et al. 2004). Within the Chacoan forest specifically, there are many protected areas, including the Bolivian Chaco, with indigenous people co-managing a large area of land (Arambiza and Painter 2006).

Relation to Humans

These frogs are part of the international pet trade but are not protected under the CITES Treaty Act. Of the 33,000 amphibians recorded in the Hong Kong pet trade between 1 December 2005 and 30 November 2006, five were found to be P. sauvagii (Rowley et al. 2007).

In addition to the pet trade, P. sauvagii skin toxins are being researched for their antimicrobial properties. Important compounds include Phylloseptin-1, which is potent in eliminating Staphylococcus aureus biofilm (Zhang et al. 2010), Phylloseptins-S, which is an anti-parasitic against the promastigote of Leishmania infantum, Leishmania braziliensis, and Leishmania major (although toxic to mammalian cells)(Raja et al. 2013), and Sauvagine, which is used in the pharmacy industry for its linked similarity to urotensin I and as aid in diuresis, cardiovascular system, and endocrine system functions (Mantecucchi and Henschen 1980).

Possible reasons for amphibian decline

General habitat alteration and loss
Habitat modification from deforestation, or logging related activities
Prolonged drought
Drainage of habitat
Local pesticides, fertilizers, and pollutants
Disease
Intentional mortality (over-harvesting, pet trade or collecting)

Comments

The species authority is: Boulenger, G.A., (1882). Catalogue of the Batrachia Salientias. Ecaudata in the collection of the British Museum, 2nd Ed. Taylor and Francis.

Through the sequencing of 12 nuclear and mitochondrial genes, plus three intervening tRNA sequences, P. sauvagii is found to belong to the family Hylidae, the subfamily Phyllomedusinae, and the genus Phyllomedusa. Thirty species belong to this genus, which contains two main clades and four main groups. However, the four groups do not encompass all species within the genus (Salica et al. 2011). Phyllomedusa sauvagii does not belong to any of the four groups. The clade that P. sauvagii belongs to includes P. boliviana, P. camba, P. bicolor, P. vailantii, and the P. burmeisteri and P. tarsius groups. Phyllomedusa sauvagii is the sister taxon to the P. burmeisteri group, and P. boliviana is the sister taxon to P. sauvagii and the P. burmeisteri group. Phyllomedusa sauvagii is “one of the most highly specialized members of the evolutionary line,” due to its “reduced discs on the digits and the prominent parotoid glands” (Faivovich et al. 2010).

The genera name means leaf guardian where “phyllo” is Greek for leaf and “medousa” is Greek for guardian. The species epithet, "sauvagii", was named after Dr. Henri-Emile Sauvage, a French paleontologist, herpetologist, and ichthyologist who lived from 1844 to 1917 (Boelens et al. 2013).

References

Aquino, L., Colli, G., Reichle, S., Silvano, D., di Tada, I., Lavilla, E. (2004). Phyllomedusa sauvagii. The IUCN Red List of Threatened Species 2004: e.T55863A11382074. http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T55863A11382074.en. Downloaded on 31 October 2017.

Blaylock, L. A., Ruibal, R., and Platt-Aloia, K. (1976). ''Skin structure and wiping behavior of Phyllomedusine frogs.'' Copeia, 1976(2), 283-295.

Castanho, L. M. and de Luca I. M. S. (2001). ''Moulting behavior in leaf-frogs of the genus Phyllomedusa (Anura: hylidae).'' Zoologischer Anzeiger, 240(1), 3-6.

De La Riva, I. (1999). “A new Phyllomedusa from southwestern Amazonia.” Rev. Esp. Herp, 13, 123-131.

Duellman, W. (1968). ''The Genera of Phyllomedusine Frogs (Anura Hylidae).'' University of Kansas Publications Museum of Natural History, 18(1), 1-10.

Evelio, A. and Painter, M. (2006). ''Biodiversity conservation and the quality of life of indigenous people in the Bolivian Chaco.'' Human Organization, 65.

Faivovich, J., Haddad, C. F. B., Baêta, D., Jungfer, K.-H., Álvares, G. F. R., Brandão, R. A., Sheil, C. A., Barrientos, L. S., Barrio-Amorós, C. L., Cruz, C. A. G., and Wheeler, W. C. (2010). '' The phylogenetic relationships of the charismatic poster frogs, Phyllomedusinae (Anura, Hylidae).'' Cladistics, 26, 227-261.

García, C. G., Lescano J. N., and Leynaud G. C. (2013). ''Oviposition-site selection by Phyllomedusa sauvagii (Anura: Hylidae): An arboreal Nester inhabiting arid environments.'' Acta Oecologica , 51, 62-65.

Hillman, S. S. (2009). Ecological and Environmental Physiology of Amphibians. Oxford University Press, Oxford, England .

Kok, P.J., and Kalamandeen, M. (2008). Introduction to the taxonomy of the amphibians of Kaieteur National Park, Guyana. Koninklijk Belgisch Instituut voor Natuurwetenschappen , Brussels, Belgium .

Manzano, A., Abdala, V., and Herrel A. (2008). ''Morphology and function of the forelimb in arboreal frogs: specializations for grasping ability?'' Journal of Anatomy , 214(3), 296-307.

Mc Clanahan, L. L., Stinner, J. N., and Shoemaker V. H. (1978). ''Skin lipids, water loss, and energy metabolism in a South American tree frog (Phyllomedusa sauvagei).'' Physiological and Biochemical Zoology , 51(2).

Raja, Z., Andre, S., Piesse, C., Serona, D., Nicolas, P., Foulon, T., Oury, B., and Ladram, A. (2013). ''Structure, antimicrobial activities and mode of interaction with membranes of novel phylloseptins from the painted-belly leaf frog, Phyllomedusa sauvagii.'' PLoS One, 8(8).

Rodrigues, D., Uetanabaro, M., and Lopes, F. (2007). ''Breeding biology of Phyllomedusa azurea Cope, 1862 and P. sauvagii Boulenger, 1882 (Anura) fom the Cerrado, Central Brazil.'' Journal of Natural History, 41, 1841-1851.

Rowley, J. J. L., Chan, S. K. F., Tang, W. S., Speare, R., Skerratt, L. F., Alford, R. A., Cheung, K. S., Ho, C. Y., and Campbell, R. (2007). ''Survey for the amphibian chytrid Batrachochytrium dendrobatidis in Hong Kong in native amphibians and in the international amphibian trade.'' Diseases of Aquatic Organisms, 78, 87-95.

Ruiz-Monachesi, M.R., Lavilla E. O., and Montero R. (2016). ''The skull of Phyllomedusa sauvagii (Anura, Hylidae).'' The Anatomical Record, 299(5), 557-572.

Salica, M. J., Haad, M. B., Candioti, F. V., and Faivovich, J. (2011). ''Early development of two species of Phyllomedusa (Anura: Phyllomedusinae).'' Salamandra, 47(3), 144-154.

Shoemaker, V. H., and McClanahan L. L. (1975). ''Evaporative water loss, nitrogen excretion and osmoregulation in Phyllomedusine frogs.'' Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 100(4), 331-345.

Soliz, M., and Ponssa, M. L. (2016). ''Development and morphological variation of the axial and appendicular skeleton in Hylidae (Lissamphibia, Anura).'' Journal of Morphology , 277(6), 786-813.

Wells, K. D. (2007). The Ecology and Behavior of Amphibians. Chicago, The University of Chicago Press.

Wells, K. D. (2010). The ecology and behavior of Amphibians. University of Chicago Press, Chicago, USA.

Zhang, R., Zhou, M., Wang, L., McGrath, S., Chen, T., Chen, X., and Shaw, C. (2010). ''Phylloseptin-1 (PSN-1) from Phyllomedusa sauvagei skin secretion: a novel broad-spectrum antimicrobial peptide with antibiofilm activity.'' Molecular immunology, 47(11), 2030-2037.

de Paula Lima, J. E., Rödder, Dennis, and Solé, M (2010). ''Diet of two sympatric Phyllomedusa (Anura: Hylidae) species from a cacao plantation in southern Bahia, Brazil.'' North-West Journal of Zoology , 6(1), 13-24.



Written by Jessica Chen, Hallie Daly, Kennedy Gould (jsmchen AT ucdavis.edu, hpdaly AT ucdavis.edu, ktgould AT ucdavis.edu), University of California Davis
First submitted 2017-10-26
Edited by Darren Ayoub (2017-11-02)

Species Account Citation: AmphibiaWeb 2017 Phyllomedusa sauvagii: Waxy Monkey Tree Frog <http://amphibiaweb.org/species/661> University of California, Berkeley, CA, USA. Accessed Dec 14, 2018.



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Citation: AmphibiaWeb. 2018. <http://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 14 Dec 2018.

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