AmphibiaWeb - Proceratophrys cristiceps
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Proceratophrys cristiceps (Müller, 1883)
Muller's smooth horned frog
family: Odontophrynidae
genus: Proceratophrys
Species Description: Müller, F. 1883. Dritter Nachtrag. Katalog der herpetologischen Sammlung des Basler Museums. Basel: J. G. Bauer.
 
Taxonomic Notes: Synonymized Protoceraphrys caramaschii and P. aridus with Protoceraphrys cristiceps after Mangia et al 2019 Revising the taxonomy of Proceratophrys Miranda-Ribeiro, 1920 (Anura: Odontophyrnidae)from the Brazilian semiarid Caatinga: morphology, calls and molecules support a single species. J Zool. Sys. Evol. Res. 2020;00:1-22 DOI:10.1111/jzs.12365

© 2023 Lindembergue R. França Junior (1 of 5)
Conservation Status (definitions)
IUCN Red List Status Account Least Concern (LC)
CITES No CITES Listing
National Status None
Regional Status None

   

 

View distribution map in BerkeleyMapper.

Description

Proceratophrys cristiceps is an aestivating frog with an adult male snout-vent length ranging from 32.5 - 56.3 mm. Six female specimens had snout-vent lengths ranging from 43.3 - 65.0 mm (Cruz et al. 2012). Proceratophrys aridus and P. caramaschii were recognized as junior synonyms of P. cristiceps in 2020 (Mangia et al. 2020). The head is wider than it is long with a rounded or nearly-triangular snout in dorsal view and an obtuse shape in lateral view. The nostrils are elliptical and slightly prominent, while the canthal crests are poorly defined. The loreal region is concave and there are preocular vestigial crests as well as long tubercles at the jaw angle. The frontoparietal crest is not developed. The eyes point anterolaterally and the tympanum is indistinct. Two transverse crests of tubercles on the head join at the inner edge of the upper eyelid. Two distinct rows of warts run longitudinally and symmetrically on the dorsum, from the upper eyelid to the sacrum. The vocal sac is not externally expanded (Cruz et al. 2012). Proceratophrys cristiceps appears rough on both the dorsal and ventral sides because of the presence of keratinized spicules on the epidermis. There are mucous and poison glands in the dermis, as well as a very thin and discontinuous calcified layer (Jared et al. 2019).

The arms and legs are somewhat robust, with a patagium present on the upper arm. There may be a row of warts extending from the external margin of the ventral forearm surface to the external margin of finger IV. The relative finger lengths are IV = II < I < III and there is no interdigital webbing. The inner metacarpal tubercle is oval-shaped and large. The outer metacarpal tubercle is divided into two parts: a small internal part and a larger external part, both being oval-shaped. Numerous round supernumerary tubercles are present and the large subarticular tubercles range from being round to spatulated. The legs are also robust, with thighs somewhat longer than the tibia. The relative toe lengths are I < II < V < III < IV. A row of warts may extend from the external edge of toe V to the ventral surface of the tarsus. The inner metatarsal tubercle is large, round, and spade-shaped, while the subarticular tubercle is small and rounded. Numerous supernumerary tubercles are present and they are also small and rounded. The subarticular tubercles are large and conical. Warts and small granules of varying sizes are scattered on the dorsum. Circular granules uniformly cover the ventral side except for hands and feet (Cruz et al. 2012).

Proceratophrys cristiceps can be distinguished from P. concavitypanum, P. cururu, P. strussmannae, and P. vielliardi by the presence of two interocular and transverse tubercle crests, which are absent in the other species. Proceratophrys cristiceps also has an outer metacarpal tubercle divided into two oval-shaped parts, with the outer part larger than the inner part. Meanwhile, the outer metacarpal tubercle of P. concavitypanum is obliquely and evenly divided into two parts; P. cururu has a round, elongated inner metacarpal tubercle; P. strussmannae has an outer part that is smaller than the elliptical inner part; and P. vielliardi has a rounded inner metacarpal tubercle. The snout of P. cristiceps appears round in dorsal view and obtuse in lateral view, and is more obtuse than the snout of P. cururu but less obtuse than the snout of P. strussmannae. Additionally, P. cristiceps lacks a skin depression at the tympanum, which is distinct in P. concavitypanum and P. strussmannae (Cruz et al. 2012).

Compared to P. concavitypanum, P. cristiceps does not have well-defined canthal crests, which are distinct in P. concavitypanum. Proceratophyrys cristiceps can be further diagnosed from P. cururu by its more uniform dorsal tubercles, which are larger and more variable in P. cururu. Compared to P. goyana, which has triangular eyelids and undefined canthal crests, P. cristiceps has rounded eyelids and well-defined canthal crests. Proceratophrys cristiceps is larger than P. moratoi, with an adult male snout-vent length ranging from 39.5 - 50.2 mm compared to 26.4 - 30.0 mm, and also does not have the X-shaped dorsal stripe that P. moratoi has (Cruz et al. 2012)

Compared to non-aestivating species, the cutaneous layer of P. cristiceps is not particularly different. The skin is thin and delicate, which is likely an adaptation to maintain water balance rather than prevent desiccation. Though the skin is thin, the skin on the dorsum is somewhat thicker than that of Physalaemus sp. and Pleurodema diplolister, which occupy the same habitat (Jared et al. 2019).

The dorsal side has a cream base color with brown marbling in life and preservative (Cruz et al. 2012). An arrowhead or spear-shaped ornamentation is formed on the dorsal side between the darker stripes running from the eyelid through the dorsum (Vieira et al. 2022). However, there are six color variations that have been observed in this species (see below) (Vieira et al. 2022).

In aestivation, the marmoreal pattern and color of the dorsal skin distinctly contrasts with the unpigmented ventral skin. The pelvic patch becomes bright reddish in color due to high vascularization (Jared et al. 2019).

There is variation in sagittal crest morphology and coloration. Though the presence or absence of a sagittal crest is what defines some species in Proceratophrys, some P. cristiceps specimens had a sagittal crest, while others did not. This has been acknowledged as an inconsistency in the description of the genus (Cruz et al. 2012).

Six main color or chromatic variations have been observed in the coloration of P. cristiceps. Chromotype 1 often occurs in leaf litter and is defined by its tawny olive-brown color on a brown background. The diverse range of hues, spots, and/or stripes make the arrowhead design on the dorsum less distinct. Brown suborbital bands are present, along with two or more interorbital stripes. Chromotype 2 is similar to chromotype 1, having brown coloration and both suborbital and interorbital bands. Dark maroon bands extending from the eyelids toward the cloaca better define the design on the middle of the dorsum. The flanks, limbs, stomach, and snout also have lighter salmon-white tones. This chromotype usually occurs in leaf litter or gravel. Chromotype 3 inhabits earthy soil areas with sparse leaf litter, having a slightly variegated brown-gray coloration. The arrowhead shape on the dorsum is distinct and light yellow-brown in color, limited by two darker brown bands. There is one interocular stripe and two suborbital stripes. Chromotype 4 is clearly trichromatic, with a rusty red making up most of the coloration. Dark brown bands limit the arrowhead figure on the dorsum, which is pale yellow. Suborbital stripes are not evident and only one interocular stripe is present, while a pineal spot is present. Similar to chromotype 2, whiter colors occur on the side of the body and limbs. Chromotype 4 usually occurs in sandy soils or gravel. Chromotype 5 is relatively monochromatic compared to the others, having a rusty red or yellow-brown coloration, and occurs in grit or gravel areas. Any spots and streaks are barely distinct. Chromotype 6 has an overall brown-gray coloration with yellow-brown or lighter spots on the snout and suprascapular areas. The figure on the dorsum is poorly defined by spots in an arch shape. Chromotype 6 generally occurs in sandy soils and may inhabit leaf litter. These chromotypes are almost identically distributed between males and females, except for chromotype 5, which was slightly more common in males than females (Vieira et al. 2022). In preservative, the dorsums of the populations formerly known as P. aridus and P. caramaschii have a brown marbled pattern on a cream background. There is also a spear-shaped ornamentation on the back (Cruz et al. 2012).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Brazil

 

View distribution map in BerkeleyMapper.
Proceratophrys cristiceps only inhabits Caatinga, Brazil, a semi-arid region located in the interior northeast of the country. Proceratophrys cristiceps is limited to the lowlands region along the Atlantic coast, with the northern boundary being Rio Grande do Norte and a southern boundary at Todos os Santos Bay (Cruz et al. 2012). After the synonymization of P. aridus and P. caramaschii (Mangia et al. 2020) with P. cristiceps, the range of P. cristiceps was expanded to also include the municipalities of Fortaleza and Milagres in state of Ceará of north eastern Brazil. The average temperature is around 30°C (ranging from 20 to 35°C) and the climate is dry, with irregular rainfall for the first three or four months of the year. Humidity ranges from 66% to 75% from January to July and stays below 60% for the rest of the year. Dry years have an average of 200 mm in rain while rainfall can reach 1,100 mm in wet years. Periods of drought may last for two years or longer. Most of the rivers are temporary and are completely dried out during drought periods. The volume of water in perennial rivers varies greatly, depending on the rain. The sandy soil in the Caatinga retains little water so all of the vegetation is xerophytic, mainly consisting of shrubs and trees with waxy cuticles, cacti, and succulents (Jared et al. 2019).

Moisture accumulates at temporary riverbeds. During the rainy season, water is retained at the deepest layers of the sand, where it may stay for months or years. The local people have used this water resource for generations through wells known as cacimbas (Jared et al. 2019).

Life History, Abundance, Activity, and Special Behaviors
Having a moisture-dependent permeable integument in the xeric conditions of the Caatinga limits P. cristiceps to remaining in aestivation for most of its life, waiting underground for rain for months or years at a time. In the dry season, P. cristiceps burrows in temporary river beds at typical depths of 10 - 15 cm, but may be more than 1.50 m. Using keratinized spades on their feet, individuals descend through the sand vertically and backwards until they are submerged. As moisture evaporates from the upper layer of sand, P. cristiceps moves downwards toward the increased humidity, otherwise remaining inert. Burrowing individuals stay in fetal position, keeping their eyes closed with limbs juxtaposed to the body, and are often close to one another. The skin on the pelvic patch becomes bright red because of high vascularization during aestivation, indicating that this is important for absorbing water. Unlike other anurans that aestivate, P. cristiceps does not burrow in cocoons and maintains the ability to move horizontally and vertically underground. When disturbed, either by being touched or exposed to light, they exhibit the escape reflex of jumping away and oftentimes expelling water through the cloaca. Of aestivating species in the Caatinga, P. cristiceps expels the largest volume of stored water through the cloaca when perturbed (Jared et al. 2019).

Proceratophrys cristiceps has been observed to emerge from aestivation in the evening after a heavy rain (often in the first few months of the year), even while the rain may not have been heavy enough for water to flow on the surface. Individuals and amplectant pairs then move towards river banks in search of food and water. Males vocalize alone in shrub vegetation in the evening, distant from bodies of water. Individuals take turns vocalizing with long intervals between them (Jared et al. 2019).

Male calls were recorded at night from two specimens near a temporary stream. Calls consist of one multipulsed note (average 57 pulses) with a dominant frequency between 0.90 and 0.99 Hz, lasting for an average of 0.66 seconds (ranging from 0.52 to 0.79 s). The pulse rate is 89.54 pulses/s on average (Nunes and Junca 2006).

Amplexus is inguinal (Jared et al. 2019).

The eggs are then laid in temporary streams (Cruz et al. 2012). The eggs are often deposited at a site that is far from the original vocalization site because the female leads the amplectant pair to a body of water (Jared et al. 2019). Surface activity usually only lasts for three to five months. Reproductive activity is still triggered after smaller rains that do not bring enough water to sustain offspring, and the tadpoles will die while surface water evaporates (Jared et al. 2019).

Larva
Stage 39 tadpoles have a spherical body shape that appears slightly depressed in lateral view and ovoid in the dorsal and ventral view. The body is wider than it is high and the average body length (12.45 mm) is approximately 41.1% of the total length (30.31 mm on average). In both the lateral and dorsal view, the snout is short and rounded. The eyes are large, with diameters being 15.2% of the total body length. The inter-nasal distance is 15.2% of the body width and the nostrils are small and rounded, located dorsally midway between the eyes and the snout. The inter-orbital distance is 26.7% of the body length, the eye-snout distance is 15.5% of the body length, and the eye-nostril distance is 7.9% of the body length. The emarginate oral disk has a width of 36.1% of the body width and is surrounded by a row of marginal papillae, which are interrupted on the anterior side. Submarginal papillae are present and located toward the interior, having a long, conical, and rounded shape. Both the upper and lower jaw sheaths are heavily pigmented and slightly serrated, and the upper sheath is U-shaped while the lower is only slightly convex. The short spiracle is transparent and located on the lateral side of the middle third of the body, opening dorsally. The vent tube is short and fused to the tail, opening dextrally. The tail has a wide base, a rounded edge, and is 64.1% of the total length. The dorsal fin is located at the latter third of the body and is higher than the ventral fin, which is somewhat arched (Vieira et al. 2007).

The characteristics of P. cristiceps tadpoles are shared by tadpoles of species in Proceratophrys, except for the presence of submarginal papillae on both the superior and inferior lips (Vieira et al. 2007).

The dorsum of live tadpoles is olive with dark brown blotches scattered. The anterior third of the ventrum is whitened while the posterior third is pigmented, and internal organs are visible. Both fins are somewhat pigmented, having blotches like those on the dorsum. The muscular area of the tail is more pigmented than the ventral side of the tail, also having blotches like on the dorsal side. The jaw sheaths are heavily pigmented. In preservative, the dorsum becomes dark brown with black blotches and the ventrum is transparent (Vieira et al. 2007).

Trends and Threats
Using riverbed sand for construction poses a threat to aestivating anurans (Jared et al. 2019).

Relation to Humans
For generations, locals have used the presence of aestivating anurans such as P. cristiceps at certain sites as an indicator of a good location to set up a cacimba (Jared et al. 2019).

Possible reasons for amphibian decline

Intensified agriculture or grazing
Urbanization

Comments

Based on Maximum Likelihood analysis of the nuclear genes CRYBA, POMC, and RHO, and mtDNA 16S, P. cristiceps is in the same clade as P. aridus and P. caramaschii, with little genetic difference (19%) among the three species’ mtDNA. Additionally, Bayesian analysis grouped P. aridus, P. caramaschii, and P. cristiceps as one genetically indistinguishable lineage, so P. aridus and P. caramaschi are considered junior synonyms of P. cristiceps. The next most closely related clade is composed of P. minuta and P. redacta (Mangia et al. 2020).

References

Cruz, C.A., Nunes I., and Juncá F.A. (2012). "Redescription of Proceratophrys cristiceps (Müller, 1883) (Amphibia, Anura, Odontophrynidae), with description of two new species without eyelid appendages from Northeastern Brazil." South American Journal of Herpetology, 7(2), 110-122. [link]

Jared, C., Mailho-Fontana, P.L., Mendelson, J., and Antoniazzi, M.M. (2019). "Life history of frogs of the Brazilian semi‐arid (Caatinga), with emphasis in aestivation." Acta Zoologica, 101, 302-310. [link]

Mângia, S., Oliveira, E.F., Santana, D.J., Koroiva, R., Paiva, F., and Garda, A.A. (2020). "Revising the taxonomy of Proceratophrys Miranda‐Ribeiro, 1920 (Anura: Odontophrynidae) from the Brazilian semiarid Caatinga: morphology, calls and molecules support a single widespread species." Journal of Zoological Systematics and Evolutionary Research, 58, 1151-1172. [link]

Nunes, I., and Junca, F.A. (2006). "Advertisement calls of three leptodactylid frogs in the state of Bahia, Northeastern Brazil (Amphibia, Anura, Leptodactylidae), with considerations on their taxonomic status." Arquivos Do Museu Nacional, 64(2), 151-157. [link]

Vieira K.S., Santos Oliveira E.K., Vieira W.L.S., and Alves R.R.N. (2022). "Polymorphism in a neotropical toad species: ontogenetic, populational and geographic approaches to chromatic variation in Proceratophrys cristiceps (Müller, 1883) (Amphibia, Anura, Odontophrynidae)." PeerJ, 10, e12879. [link]

Vieira, W.L., Vieira, S., and Santana, G. (2007). "Description of the tadpoles of Proceratophrys cristiceps (Anura: Cycloramphidae, Odontophrynini)." Zootaxa, 1397(1), 17-24. [link]



Originally submitted by: Madeline Ahn (2022-10-25)
Description by: Madeline Ahn (updated 2022-10-25)
Distribution by: Madeline Ahn (updated 2022-10-25)
Life history by: Madeline Ahn (updated 2022-10-25)
Larva by: Madeline Ahn (updated 2022-10-25)
Trends and threats by: Madeline Ahn (updated 2022-10-25)
Relation to humans by: Madeline Ahn (updated 2022-10-25)
Comments by: Madeline Ahn (updated 2022-10-25)

Edited by: Ann T. Chang (2022-10-25)

Species Account Citation: AmphibiaWeb 2022 Proceratophrys cristiceps: Muller's smooth horned frog <https://amphibiaweb.org/species/5622> University of California, Berkeley, CA, USA. Accessed Feb 28, 2024.



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Citation: AmphibiaWeb. 2024. <https://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 28 Feb 2024.

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