AmphibiaWeb - Barbarophryne brongersmai
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Barbarophryne brongersmai (Hoogmoed, 1972)
Tiznit Toad, Brongersma’s Toad, Moroccan Green Toad, Anti-Atlas Toad
family: Bufonidae
genus: Barbarophryne
Species Description: Hoogmoed, M. S. (1972). “On a new species of toad from southern Morocco.” Zoologische Mededelingen. Leiden 47: 49–64.
Barbarophryne brongersmai
© 2011 Stefano Doglio (1 of 11)
Conservation Status (definitions)
IUCN Red List Status Account Near Threatened (NT)
CITES No CITES Listing
National Status Near threatened (Morocco)
Regional Status None

   

 
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Description

Barbarophryne brongersmai is a small-bodied, monotypic toad described from a female holotype with a snout-vent length of 48 mm and two male paratypes with a maximum snout-vent length 51 mm (Hoogmoed 1972; Beukema et al. 2013). The head is roughly 25% of the snout-vent length and is longer than it is deep. From above, the snout is rounded, but from its profile, the snout is truncated, projecting slightly beyond the lower jaw. Oval, nearly rounded nostrils are located below the canthus rostralis in a slightly swollen area near tip of the snout and roughly half the distance to the anterior corner of the eye. The canthus rostralis is rounded and not distinct, and the loreal is distinct, concave and steeply sloping to the mouth. The interorbital space is wider than its upper eyelid. The horizontal diameter of the eye is slightly less than the distance of the tip of the snout to the anterior corner of the eye and 2.5 times greater than the horizontal diameter of the tympanum. The interorbital space is flat and slightly wider than an upper eyelid. Small ventral indentations are observable on the toad’s horizontally oval pupils. There are no maxillary or vomerine teeth, and the oblong tongue is wider posteriorly than anteriorly, attached at the foremost part. A distinct tympanum is taller than it is wide, featuring a bony ring and a margin slightly hidden by skin, and located one-fourth the diameter of the eye away from the eye itself. The parotoid glands are distinct and small, distinctly pitted on their surface, more narrow anteriorly than posteriorly, and longer than it is wide. These glands just extend behind the eyes to above the forelimb insertion (Hoogmoed 1972).

The hands, with no webbing between their fingers, have a large central and small inner metacarpal tubercle. Distinct, singular subarticular tubercles are also observable, with the distal ones tending to divide in two. Many rounded tubercles are on the palm and smaller than the subarticular tubercles. The first finger is slightly smaller than the second, and the tips of all fingers do not expand. When the hind limb is pressed forward along the body, the tibio-tarsal articulation reaches the forelimb insertion. When the hind limbs are at a right angle to the body, the ankles touch. Furthermore, the tibia do not have glands. Meanwhile, the feet have a protruding inner and small, round outer metatarsal tubercle, and an indistinct metatarsal fold is present. Distinct, singular subarticular tubercles are observable, except on the distal joint of the third toe and the two distal joints of the fourth, which are doubled. Many small supernumerary tubercles are on the soles and underside of toes and between the subarticular tubercles. Rudimentary webbing, between distinctly depressed toes, follows the formula: 1(1), 2i (2), 2e (1.5), 3i (3), 3e (2), 4i (4), 4e (3.75), 5 (1.75), with 1 - 5 reflecting the toe, i reflecting the inner side of the toe, and e reflecting the outer side of the toe. The toes do not expand into discs (Hoogmoed 1972).

Smooth skin covers the lateral and dorsal surfaces of the toad’s head, while the skin behind the corners of the head features a cluster of large warts. The body is covered in irregularly scattered warts, which have horny tips, dorsally and laterally. Except for the throat, the ventral skin is coarsely granular. Both the forelimbs, except for the lower arm’s dorsal surface, and the hindlimbs feature scatter warts (Hoogmoed 1972).

García-Muñoz et al. (2009) determined mean snout-vent length juveniles to be 19.52 mm.

Barbarophyrne brongersmai are monotypic, the only species in their genus. They are distinguishable from other Bufonidae through their size, warts, glands, tympanum, and tubercles. Specifically, in their adult stages, B. brongersmai is generally smaller than other bufonides. In addition, they lack warts on the dorsal surface of their heads and a gland in the tibia, while featuring nearly circular parotoid glands, nearly round tympanum, and paired distal subarticular tubercles on the fourth toe, which all distinguishes B. brongersmai from Bufotes viridis (Hoogmoed 1972; Beukema et al. 2013). Additionally, their is distinctly different from the call of Bufotes viridis and Bufo calamita (Doglio et al. 2009). Bogaerts (2001) describes the call to be similar to Hyla arborea, only a little quieter and with lower frequency.

In life, the female holotype is dorsally pale grayish-brown with small dark green spots dotted black. The upper eyelids, dorsal warts, and parotoid glands are reddish in shade, while the irises are green. Ventrally, the toad is white with green spots; furthermore, the posterior part of the belly and the underside of the thighs are flesh-colored. Meanwhile, in preservative, the dorsal surfaces are gray with dark blue-green spots. On the head, the spots form a “Y” with the arms on the upper eyelids, while the rest of the spots irregularly disperse across the back. From the anterior of the eye, through the canthus rostralis, and to the tip of the snout, a spot extends. On the upper lips, there are two spots, one smaller below the nostrils and one larger below the eyes. These spots are blue-green with a rim of black dots and some black dots dispersing into the blue-green. The parotoid glands and the upper eyelids’ outer rims are pale reddish. Ventrally, the toad is dirty white with small dark blue-green spots and no black dots (Hoogmoed 1972).

Unclear in life or in preservation, regardless of sex, the pattern on the head is not variable, with a transverse spot distinct on each upper eyelid; these spots can sometimes create a transverse bat. Under the eye and on the canthus rostralis, a large spot is present. In addition, irregularly dispersed spots are on the body and limbs and do not form a light stripe over the vertebral area (Hoogmoed 1972).

Variation, across sexes and life stage include the head encompasses 25 - 30% of snout-vent length, with the head 1.7 - 2.6 times longer than it is deep. The tympanum’s vertical diameter is 0.9 - 1.2 times longer than it is wide. In addition, in life, the red on the parotoid glands and upper eyelids vary in the intensity and extent of color, and the dorsal surface’s spots range from light to dark green. Between sexes, there exists variation regarding body size, mass, toe webbing, nuptial callosities, warts, and calling behavior. Fattah et al. (2014) determined that males are generally smaller than females in body size and weight, but this pattern of sexual dimorphism was not statistically significant. However, sexual dimorphism exists in the amount of toe webbing, as male webbing extends to the tips of their toes as fringes (Hoogmoed 1972). Males also feature nuptial callosities on the first three fingers of their hands. Small, dark brown horny warts also cover the inner side of such three fingers and the dorsal surface of the first finger. The warts on the dorsal surface of the body differ between sexes too, as females have opaque, rounded, and horny tips, while males have conical, sharply pointed, and brown tips. An internal subgular vocal sac, which allows calling behavior, is present in males as well (Hoogmoed 1972; Fattah et al. 2014).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Algeria, Morocco, Western Sahara

 
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Barbarophryne brongersmai is endemic to mainly southwestern regions of Morocco, the entire sub-Atlas region of Morocco, north onto Marrakech’s arid plain, Algeria, and the Western Sahara, which range from 5 - 1000 m in elevation (Hoogmoed 1972; Delfino et al. 2009; Beukema et al. 2013; Reques et al. 2013; IUCN 2021). In the southwestern Morocco regions, precipitation as rain is short, and highly intensive, causing water discharges into temporary rivers from the end of February to mid-April; annual precipitation itself seldom reaches 300 mm (Fattah et al. 2014). The area Fattah et al. (2014) studied features short grasses due to the heavy grazing and permanent movement of big herds of sheeps and goats. Fattah et al. (2022) determined B. brongersmai may also live in Azilal, a semi- to sub-arid region in Morocco’s central High Atlas Mountains. Azilal’s elevation ranges from 900 - 1,500 m, containing forests, non-wooded terrain, agricultural land, and brushwood. Cold and snowy winters, summer droughts, and annual precipitation averaging 578.5 mm also characterize Azilal. Overall, B. brongersmai exists in semi-arid and rocky environments that mostly lack vegetation, such as shrublands, inland wetlands, inland cliffs, mountain peaks, an deserts, and they live close to temporary bodies of water (Delfino et al. 2009; IUCN 2021).

Life History, Abundance, Activity, and Special Behaviors

In regards to reproductive behavior, B. brongersmai explosively breed from mid-March to early April, reproducing in ephemeral pools and brooks that form after periods of spring rain. On occasion, man-made water reservoirs can be breeding sites (Delfino et al. 2009; Beukema et al. 2013). Small clutches of eggs are attached to underwater vegetation or stones, whose larvae develop relatively quickly into juveniles, as compared to other Moroccan toads (Delfino et al. 2009; Beukema et al. 2013).

Male toads produce multiple short squeaks, around 3 - 8 pulses that last 0.53 - 3.11 seconds, as an advertisement call. Fundamental frequency ranges from 1217 - 1890 Hz, with a pulse length of 0.03 - 3.11 seconds, interpulse length of 0.09 - 0. 14 seconds, and pulse rate of 6.39 - 6.73 seconds; call length and number of pulses are variable (Doglio et al. 2009; Beukema et al. 2013). Bogaerts (2001) notes the advertisement calls to resemble a 'kèèk-kèk-kèk-kèk-kèk-kèk-kèk', with the first 'kèk' being slightly longer, and the others rapidly following. In addition, females produce release calls as well (Bogaerts 2001).

Delfino et al. (2009) observed that a low ossification degree is present in metamorphosing larvae, juveniles, and adults, noting that the skulls of metamorphosed juveniles are small and completely chondrified. The hypo-ossification of the skeleton is theorized to be an adaptation to its hostile semiarid environment and exploitation of small crevices for protection. Reduced energy investment in skeletal elements allows more economical metabolic costs in larval development and shortens such development, which subsequently reduces a dependence on water. In addition, the reduced ossification may aid in the toad’s use of crevices for protection against overheating and desiccation, a trade-off to its small size (Delfino et al. 2009).

The small size of the B. brongersmai is theorized by Fattah et al. (2014) to be a result of slow growth as juveniles, restricted by a scarcity of food and short activity period. A lack of sexual dimorphism was also observed by Fattah et al. (2014), which correlates to a low annual fecundity. Both of these characteristics are hypothesized to support greater longevity in B. brongersmai, but such findings were determined through a small sample size (Fattah et al. 2014).

Larva

The larvae of B. brongersmai are characterized by fast larval development, saving at least 3 - 8 weeks of development when compared to other Moroccan toads, as a critical adaptation to their arid environments with ephemeral bodies of water (Delfino et al. 2009).

Larvae hatch with a total length of 5.3 - 5.8 mm and with an adhesive organ and the anlagen of an oral disk is visible. When they reach a total length of 7.2 mm, a horny beak and the ridges of all five tooth rows form. At a total length of 9 mm, the marginal rim of the nostril appears and the cornea becomes transparent. Also at a total length of 9 mm, the marginal papillae, horny teeth, and the beak’s dark marginal pigmentation appear. While growing from 7.5 - 9 mm, the external gills with three pairs of ramified gills are covered by growing opercular folds. From at least a total length of 9 - 10 mm, the final tube shaped spiracular opening forms (Grillitsch et al. 1989).

At Stage 28, the larvae have a body length of 8.4 mm and a tail length of 12.5 mm, at Stage 30, the body length is 10.5 mm and tail length is 16 mm, and at Stage 33, the body length is 15 - 15.2 mm and the tail length is 20.1 - 23 mm (Hoogmoed 1972). Around Stage 36 - 37, the body length is 16 - 17.2 mm and the tail length is 21 - 30 mm (Hoogmoed 1972; Grillitsch et al. 1989). The bodies of B. brongersmai larvae are flattened dorsoventrally and ovoid, 1¼ times wider than they are deep and 1⅔ times longer than they are wide. The nostrils are kidney-shaped or oval, featuring an elevated rim, and are farther from the tip of the snout than the eyes. The large eyes are dorsally positioned on the head with a small interorbital space, 1 - 1½ times the internarial space. The eyes are not visible ventrally. A ventral, mostly kidney-shaped oral disc with a lateral indentation is observable in the larvae (Hoogmoed 1972). Its width is roughly 1½ times the interorbital space (Beukema et al. 2013). There are two upper (anterior) labial tooth rows and three lower (posterior) labial tooth rows, with the second anterior tooth row featuring a median gap. This median interruption is more narrow than the length of each labial tooth row part. The first anterior tooth row may also vary with some individuals having no gap, a narrow gap, or wide gap (Hoogmoed 1972). Lastly, clusters of papillae can be found at the lateral corners of the mouth, but are absent from the upper and lower lip (Hoogmoed 1972; Grillitsch et al. 1989).

The spiracle is sinistral and lateral, its opening roughly in the middle of the trunk, pointing slightly upwards or straight backwards. A median anus, with its tube opening right at the ventral caudal crest’s outer margin, is observable. Originating behind the spiracular opening, there is a slightly convex, narrow dorsal crest. The tail is roughly 1 ½ times longer than the body and three times longer than deep. The tail’s tip is rounded and the dorsal tail fin, which ends posteriorly of the tail’s muscular base, may be higher than the ventral tail fin (Hoogmoed 1972; Grillitsch et al. 1989; Beukema et al. 2013).

There is a dorsal seam of skin that is slightly wider than the ventral seam, which ends on the tail’s muscular base and is well in front of the anus (Hoogmoed 1972).

In life, hatchlings have a dark brown uniform pigmentation all over its body, which is stable throughout development. The ventral sides pale slightly over their development (Grillitsch et al. 1989; Beukema 2013). The caudal crests are transparent and gray, and the tail fins are unspotted (Beukema et al. 2013).

General morphology and coloration are fairly similar in Moroccan bufonid tadpoles around Stages 36 or 37, so diagnosis relies on a variety of characteristics (Beukema et al. 2013). Hoogmoed (1972) observed that the interorbital space and internarial space are equal in B. brongersmai, making it an important characteristic to differentiate the B. brongersmai larvae from B. boulengeri larvae. But, Grillitsch et al. (1989) later determined that these distances vary and are similar to those of B. boulengeri. Thus, Beukema et al. (2013) concluded that the presence or absence of tail spots can diagnose B. brongersmai larvae, which lack spots, from B. boulengeri larvae, which have brown tail fins spots. Tail fin patterning of brown polygonal meshes on the tail fins in D. scovazzi and large dark spots on the tail fins in A. maurus also differentiate them. A dark background color with golden specks on Amietophrynus mauritanicus differentiates the species from B. brongersmai. Eye position and coloration differentiate B. brongersmai from Pelobates varaldii and Hyla meridionalis, which both have laterally positioned eyes and light, uniform color. Discoglossus pictus, Discoglossus scovazzi, and Alytes maurus all feature midventral spiracles. A tail length more than twice the body length separates Pelophylax saharicus from B. brongersmai. Finally, the dorsal tail fin ending at the tail’s base separates Bufo bufo larvae from B. brongersmai larvae (Beukema et al. 2013).

Trends and Threats

Barbarophryne brongersmai is overall threatened by habitat loss and degradation, as a result of water management and droughts, which affect the creation of ephemeral bodies of water (Pleguezuelos et al. 2010; IUCN 2021). Man-made constructions for water retention, such as cisterns to water cattle, are described by García-Muñoz et al. (2009) to accidentally function like pit-fall traps for the toads seeking bodies of water, thus starving the toads, but not drowning them due to the dense vegetation in the waters (Reques et al. 2013). García-Muñoz et al. (2009) suggest providing natural escape measures, such as a pile of stones in the corner, for B. brongersmai.

Barbarophyrne brongersmai can be located in Parc National de Souss-Massa, a protected area, albeit not by national legislation (IUCN 2021).

Relation to Humans

The toads are found in the international pet trade and have been found in numerous private collections and bred in captivity (IUCN 2021). Bogaerts (2001) states that B. brongersmai is one of the few true toad species that can be bred repeatedly and successfully, given proper hygiene care.

Possible reasons for amphibian decline

General habitat alteration and loss
Prolonged drought
Dams changing river flow and/or covering habitat

Comments

Barbarophryne brongersmai is a monotypic species with a complicated taxonomic history (Beukema et al. 2013). Originally, Hoogmoed (1972) tentatively placed Barbarophryne brongersmai in the Bufo genus due to some morphological similarities to Bufotes viridis and Bufotes calamita. But, Frost et al. (2006) placed the toad in the Pseudepidalea genus, which was later synonymized with Bufotes, using 2,400 base pairs of mitochondrial fragments (12S, 16S, tRNAVal) and 2,300 base pairs of nuclear fragments (H3, 28S). Van Bocxlaer et al. (2009) supported such a position using 4,339 base pairs of mitochondrial fragments and 1,970 base pairs of nuclear fragments. However, while Speybroeck and Crochet (2007) determined B. brongersmai should be in a unique genus, they proposed Epidalea instead of Pseudepidalea. Later, Delfino et al. (2009) utilized osteological data to determine the toad should be in Bufo, but is different from all other western Palearctic Bufo species and is likely related to B. viridis (Doglio et al. 2010). Finally, through a Bayesian analysis of three mitochondrial fragments (16S, ND2, tRNAval) and two nuclear fragments (NCX1 and CXCR4), in addition to the works of Grillitsch et al. (1989), Delfino et al. (2009), and more, Beukema et al. (2013) determined B. brongersmai is sister to the clade of Eurasian toads (Epidalea), diverging from Epidalea during the Oligocene. However, there is low support for this position. Thus, Beukema et al. (2013) concluded that the Brongersma’s toad should be placed in the newly formed, Barbarophryne genus. Such action reduced the polyphyly of the “green toad group” (Reques et al. 2013).

Hoogmoed (1972) originally named Bufo brongersmai in honor of the director of the Rijksmuseum van Natuurlijke Historie, Professor Doctor Leo Daniel Brongersma (Hoogmoed 1995).

Beukema et al. (2013) derived the genus Barbarophryne from “Barbaro”, in relation to Barbary, a Northwestern African region that is northern to the Sahara, and “-phryne”, which is "toad" in Greek.

References

Beukema, W., De Pous, P., Donaire-Barroso, D., Bogaerts, S., Garcia-Porta, J., Escoriza, D., Arribas, O.J., El Mouden, E. H., & Carranza, S. (2013). Review of the systematics, distribution, biogeography and natural history of Moroccan amphibians. Zootaxa, 3661(1), 1-60. [link]

Bogaerts, S. (2001). Breeding Brongersma’s toad, Bufo brongersma. Pod@ rcis, 2, 81-88. [link]

Delfino, M., Doglio, S., Roček, Z., Seglie, D., & Kabiri, L. (2009). Osteological peculiarities of Bufo brongersma (Anura: Bufonidae) and their possible relation to life in an arid environment. Zoological Studies, 48(1), 108-119. [link]

Doglio, S., Seglie, D., & Kabiri, L. (2008). First skeletochronology results of Bufo (Epidalea) brongersmai from the Moroccan Anti Atlas (Anura, Bufonidae). In Herpetologia Sardiniae (pp. 226-230). Societas Herpetologica Italica/Edizioni Belvedere. [link]

Doglio, S., Seglie, D., Kabiri, L., & Delfino, M. (2009, September). Description of the advertisement call and release calls of Bufo (Epidalea) brongersmai Hoogmoed 1972, new distribution records and an attempt to a “total” bibliography. In Abstract book XV European Congress of Herpetology, Kusadasi (Turkey) (p. 166). [link]

Doglio, S., Seglie, D., Slimani, T., El Hassan Elmouden, L. K., & Delfino, M. (2010). The Brongersma’s toad (Bufo brongersma, Hoogmoed 1972): a summary of the new data on morphology, ecology, distribution and population dynamics. In Atti VIII Congresso Nazionale Societas Herpetologica Italica (Chieti, 22-26 Settembre 2010) (pp. 183-188). Ianieri Edizioni. [link]

Fattah, A., Atif, K., & El Alami, A. (2022). First record of Brongersma's toad Barbarophryne brongersmai (Anura, Bufonidae) in the central High Atlas Mountains, Morocco. Miscel· lània Zoològica, 20, 33-39. [link]

Fattah, A., Slimani, T., Grolet, O., & Joly, P. (2014). Age structure of a population of Barbarophryne brongersmai (Hoogmoed 1972)(Anura, Bufonidae) inhabiting an arid environment in the Central Jbilets (West-Morocco). Acta Herpetologica, 9(2), 237-242. [link]

Frank, N., & Ramus, E. (1995). A complete guide to scientific and common names of reptiles and amphibians of the world. NG Publishing, Inc.

Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F., De Sa, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P. E., Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C. (2006). The amphibian tree of life. Bulletin of the American Museum of natural History, 2006(297), 1-291. [link]

García-Muñoz, E., Ceacero, F., & Pedrajas, L. (2009). Notes on the reproductive biology and conservation of Pseudoepidalea brongersmai. Herpetology Notes, 2, 231-233. [link]

Grillitsch, H., Splechtna, H., & Grillitsch, B. (1989). The tadpole of Bufo brongersmai Hoogmoed 1972. Amphibia-reptilia, 10(3), 215-229. [link]

Hoogmoed, M. S. (1972). On a new species of toad from southern Morocco. Zoologische Mededelingen, 47(5), 49-64. [link]

Hoogmoed, M. S. (1995). LD Brongersma, 1907-1994. Copeia, 1995(2), 513-516. [link]

IUCN SSC Amphibian Specialist Group. 2021. Barbarophryne brongersmai. The IUCN Red List of Threatened Species 2021: e.T54594A179954755. https://dx.doi.org/10.2305/IUCN.UK.2021-3.RLTS.T54594A179954755.en. Accessed on 23 March 2023.

Pleguezuelos, J. M., Brito, J. C., Fahd, S., Feriche, M., Mateo, J. A., Moreno-Rueda, G., Reques, R., & Santos, X. (2010). Setting conservation priorities for the Moroccan herpetofauna: the utility of regional red lists. Oryx, 44(4), 501-508. [link]

Speybroeck, J., & Crochet, P. A. (2007). Species list of the European herpetofauna–a tentative update. Podarcis, 8(1/2), 8-34. [link]

Van Bocxlaer, I., Biju, S. D., Loader, S. P., & Bossuyt, F. (2009). Toad radiation reveals into-India dispersal as a source of endemism in the Western Ghats-Sri Lanka biodiversity hotspot. BMC evolutionary Biology, 9(131), 1-10. [link]



Originally submitted by: Hong Nguyen (first posted )
Description by: Hong Nguyen (updated 2023-04-19)
Distribution by: Hong Nguyen (updated 2023-04-19)
Life history by: Hong Nguyen (updated 2023-04-19)
Larva by: Hong Nguyen (updated 2023-04-19)
Trends and threats by: Hong Nguyen (updated 2023-04-19)
Relation to humans by: Hong Nguyen (updated 2023-04-19)
Comments by: Hong Nguyen (updated 2023-04-19)

Edited by: Ann T. Chang (2023-04-27)

Species Account Citation: AmphibiaWeb 2023 Barbarophryne brongersmai: Tiznit Toad <https://amphibiaweb.org/species/125> University of California, Berkeley, CA, USA. Accessed Jun 15, 2024.



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