AMPHIBIAWEB
Bufotes boulengeri
Sicilian Green Toad, Rospo smeraldino siciliano, Sizilianische Wechselkröte, crapaud vert de Sicile, Sapo verde siciliano
family: Bufonidae
Taxonomic Notes: The toads discovered on Sicily and a few additional Mediterranean islands and assigned to Bufotes siculus were reduced to a subspecies of the otherwise exclusively African Bufotes boulengeri by Dufresnes, Mazepa, Jablonski, Oliveira, Wenseleers, Shabanov, Auer, Ernst, Koch, Ramírez-Chaves, Mulder, Simonovo,Tiutenko, Kryvokhyzhar, Wennekes, Zinenko, Korshunov, Al-Johany, Peregontsev, Masroor, Betto-Colliard, Denoël, Borkin, Skorinov, Pasynkova, Mazanaeva, Rosanov, Dubey, Litvinchuk 2019 Molecular Phylogenetics and Evolution 141: 1–25.
 
Species Description: Lataste, F. (1879). ''La zoologie descriptive et la zoologie geographique.'' Revue Internationale des Sciences. 2e année. Paris, 4, 436–438.

© 2011 Martin Pickersgill (1 of 45)
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
Bufotes boulengeri is a medium- to large-sized green Palearctic green toad from the Bufotes viridis subgroup (Stöck et al. 2008). In general, specimens from Morocco, have male snout-vent lengths of 63 - 80 mm and female snout-vent lengths of 70 - 80 mm. However, unsexed specimens from Egypt have snout-vent lengths of 73 - 95 mm and a maximum snout-vent length of 107 mm was reported in Libya. In the dorsal view the snout is rounded, and in the lateral view, the head is obtuse. The dorsolaterally directed nostrils are located approximately halfway between the eyes and the snout-tip. The eyes are also directed dorsolaterally and have horizontal elliptical pupils. The parotoids are large, ovoid, and parallel to each other. The tympanum is distinct and about 45% the size of the eye. Males possess a single subgular vocal sac (Escoriza and Ben Hassine 2019).

Males have more robust forelimbs and fingers than females. In both sexes, the palms have two metacarpal tubercles, with the palmar tubercle being larger than the thenar tubercle. The fingers do not have discs or webbing and have relative lengths of IV < II < I < III. There is a single subarticular tubercle on each finger. In breeding males, there are nuptial pads on the first three fingers. On the foot, the inner and outer metatarsal tubercles are distinct. The rudimentarily webbed toes do not have discs and have relative toe lengths of I < II < V < III < IV. Like the fingers, the toes have a single subarticular tubercle on each toe, with the fourth toe occasionally having paired subarticular tubercles. The dorsal skin is rough with small to medium sized tubercles and spinules, while the skin on the ventral surfaces is granular (Escoriza and Ben Hassine 2019).

At stage 36, the total length is approximately 38.1 mm, the body length is 14.8 mm, and the tail length is approximately 1.6 times the body length. The body is depressed with a nearly rounded snout in the dorsal view and a rounded snout in the lateral view. The nostrils are located closer to the tip of the snout and directed anterolaterally. The small eyes are positioned dorsally. The emarginated oral disc is positioned anteroventrally with a labial tooth row formula of 2(2)/3 uniserial rows. The two anterior rows are similar in length, but the first two posterior rows are either equal in length or a quarter larger than the third posterior row. There are small, uniserial marginal papillae that have dorsal and ventral gaps. The jaw sheaths are medium in size, keratinized, and have blunt serrations. The spiracle is sinistral and the vent is medial. The dorsal fin starts at the tail body junction and is low. The height of the tail musculature is slightly less than half the maximum tail height. The tail tip is rounded (Escoriza and Ben Hassine 2019).

Bufotes boulengeri can be differentiated from other North African Bufonids by a combination of their size, iris color, and parotoid shape. Bufotes boulengeri is smaller than Bufo spinosus and Sclerophrys mauritanica. Bufotes boulengeri is larger than Barbarophryne brongersmai, Sclerophrys dodsoni, and Sclerophrys kassasii. It is generally larger than Sclerophrys pentoni and Sclerophrys regularis, but can over lap at the extreme sizes of the species, and it is of similar size to Sclerophrys xeros. However, B. boulengeri's green iris differentiates it from all of these species except B. brongersmai. Bufotes boulengeri's large, elongated parotoid differentiates it from B. brongersmai's small, oval paratoid and from the flat paratoids of S. dodsoni, S. kassasii, and S. pentoni (Escoriza and Ben Hassine 2019).

In the Mediterranean, B. boulengeri differs from all others, especially all circum-Mediterranean green toad species, by its distinct mitochondrial haplotype group, coloration, and patterning. Bufotes boulengeri exhibits brownish to olive (but barely bright greenish) spots that often form light dorsal stripes (not to be confused with a yellowish pigmented stripe), a character rarely found in the green toads of Italy. Bufotes boulengeri almost never shows a reddish-orange coloration, characteristic of many B. balearicus, the only member of the subgroup with which it may co-occur on Sicily. Bufotes boulengeri is further distinguishable from B. balearicus, by the latter exhibiting pinhead-sized red (female B. balearicus) or brownish (male B. balearicus) spots around tips of lateral glands, but are not seen in B. boulengeri. In Sicily, the ratio of the vertical diameter of the tympanum by the diameter of the eye is smaller in B. boulengeri [0.530 (max) ≥ 0.381 (mean) ≤ 0.247 (min) (N = 42)] than in allo- or parapatric B. balearicus [0.622 ≥ 0.478 ≤ 0.345 (N = 31)]. The two species also differ in breeding behavior. Bufotes boulengeri exhibits a much longer, potentially bimodal breeding period (January-June and September-November) versus a short reproductive period in spring (February-April) that is typical of B. balearicus (Stöck et al. 2008).

In life, B. boulengeri exhibits strong variability in coloration with adult males showing less contrast in marbled patterns than females. The basic dorsal coloration ranges from reddish brown, olive green, to creamy. Some specimens may have diffused orange on the head (Escoriza and Ben Hassine 2019). They have brownish to olive or bright greenish spots are often fused to form light dorsal stripes (not to be confused with a yellowish pigmented stripe). Some specimens have a green-yellow middorsal line. They do not have pinhead-sized spots around the tips of their lateral glands. The ventrum is a uniform yellowish-white, but some specimens have small green or dark spots. The iris is reported as dark yellowish-golden in populations from Sicily (Stöck et al. 2008), but lime green with black vermiculations and a gold pupil border in North Africa. Nuptial pads are dark brown (Escoriza and Ben Hassine 2019).

In life, larval coloration is affected by water conditions and larval developmental stage. In turbid water, the body is uniformly ivory white, but in clear water the body is dark-gray to dark olive. The body color becomes paler at later Gosner stages. The tail musculature is the same color as the tail, but the fins are transparent. The eyes range from yellow to dark brown, but are occasionally almost black (Escoriza and Ben Hassine 2019).

Based on genetics, there are two recognized subspecies: B. boulengeri boulengeri found only in North Africa and B. boulengeri siculus found only on Italian islands (see Distribution below; Stöck et al. 2008, Dufresnes et al. 2014, Nicolas et al. 2017, Dufresnes et al. 2019). Pygmy-sized populations have been reported in Egypt and Algeria at the edge of the Sahara, but these individuals have not been investigated further (Escoriza and Ben Hassine 2019).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Algeria, Egypt, Italy, Libyan Arab Jamahiriya, Morocco, Tunisia

 

View distribution map using BerkeleyMapper.
As a whole, B. boulengeri is found in North Africa and on several Italian Islands. More specifically, B. b. boulengeri can be found from Western Sahara and Morocco, in the West, through to Algeria, Tunisia, Libya, and Egypt with a southern limit in El Argoub, Western Sahara (Martínez-Solano et al. 2015, Escoriza and Ben Hassine 2019). Bufotes b. siculus is endemic to Sicily, as well as Favignana Island and Ustica Island, Italy (Stöck et al. 2008). The species can be found in a variety of environments ranging from humid to hyperarid at elevations of sea level to 2670 m. Their habitat ranges from mesic and xeric forests, scrubland, semideserts, alpine grasslands, cultivated fields, and desert oases, river valleys, and wadis (Escoriza and Ben Hassine 2019).

Populations in Arabia, southern Israel and Jordan were suspected of being B. boulengeri (Stöck et al. 2008, Escoriza and Ben Hassine 2019), however further investigation indicates that these populations are B. sitibundus (Dufresnes et al. 2019)

Life History, Abundance, Activity, and Special Behaviors

Bufotes boulengeri is crepuscular and nocturnal. In some locations, they are active all year round. The home range is reported to be about 142 m2 (Escoriza and Ben Hassine 2019).

Mating can occur on land or in water with the species exhibiting a longer, potentially bimodal breeding period (January-June and September-November), and high plasticity (Lo Valvo and Giacalone 2005, Sicilia et al. 2006, Stöck et al. 2008). However, breeding typically occurs in intermittent streams, temporary ponds, alpine lakes, water reservoirs, gueltas, and sabkhas. It is capable of tolerating high concentrations of sodium chloride to about 1221.9 g/L (Escoriza and Ben Hassine 2019).

Males frequently vocalize during the day at the edges of ponds or partially submerged in the water with a call described as “rrrou, rrrou” (Escoriza and Ben Hassine 2019) composed of individual notes that rise and fall symmetrically (Stöck et al. 2008). At temperatures of 21°C in North Africa, the call consists of trains of 90 - 136 short pulses with a dominant frequency between 1205 - 1240 Hz (Escoriza and Ben Hassine 2019). At temperatures of 16°C in Sicily, the call is similar to B. viridis, sounding like a canary trill. The call has up to 75 actively pulsed notes at a dominant frequency of 1600 Hz that are separated by consistent internote intervals. Note series are separated by at least 12 seconds (Stöck et al. 2008).

Amplexus is axillary (Escoriza and Ben Hassine 2019).

Females deposit eggs close to the surface of water at breeding sites. Larvae are ready to hatch after three to five days and are detritivores, but may also feed on animal matter. Metamorphose occurs after one to two months at sizes of 15 - 20 mm and can be found between March and July (Escoriza and Ben Hassine 2019). Larval B. boulengeri have been found in sympatry with D. pictus and H. meridionalis in northern Algeria and Tunisia and with S. mauritanica and B. brongersmai in southern Morocco (Escoriza and Ben Hassine 2019).

Bufotes boulengeri adults feed on Arthropoda, mainly Coleoptera, and are preyed on by ardeids (B. ibis) and owls (Bubo ascalaphus; Escoriza and Ben Hassine 2019).

When threatened B. boulengeri tries to escape and urinates (Escoriza and Ben Hassine 2019).

Trends and Threats
Although B. boulengeri appears to tolerate some habitat modification, as long as irrigation provides suitable breeding sites, the species is threatened by habitat loss, especially at coastal marshes. It is also threatened by introduced species, eutrophication or pollution of temporary ponds, desiccation, and road mortality (Martínez-Solano et al. 2015, Escoriza and Ben Hassine 2019). Additionally, the species is likely found in some protected areas given its wide range (Martínez-Solano et al. 2015).

Possible reasons for amphibian decline

General habitat alteration and loss
Habitat modification from deforestation, or logging related activities
Disturbance or death from vehicular traffic
Prolonged drought
Drainage of habitat
Subtle changes to necessary specialized habitat
Local pesticides, fertilizers, and pollutants
Predators (natural or introduced)
Introduced competitors
Climate change, increased UVB or increased sensitivity to it, etc.

Comments
The species authority is: Lataste, F. (1879). ''La zoologie descriptive et la zoologie geographique.'' Revue Internationale des Sciences. 2e année. Paris, 4, 436–438.

The subspecies, B. b. siculus was described by: Stöck, M., Sicilia, A., Belfiore, N., Buckley, D., Lo Brutto, S., Lo Valvo, M., Arculeo, M. (2008). ''Post-Messinian evolutionary relationships across the Sicilian channel: Mitochondrial and nuclear markers link a new green toad from Sicily to African relatives.'' BMC Evolutionary Biology, 8, 56-74.

Based on Bayesian Inference of the mitochondrial control region, an intron of alpha-tropomyosine, and a fragment of the RAG 1 gene, B. boulengeri is sister to the clade composed of B. balearicus and B. viridis (Stöck et al. 2008).

The genus, "Bufotes" is derived from the Latin "Bufo meaning "toad" (Escoriza and Ben Hassine 2019).

The species epithet, "boulengeri" is the Latinization of George Albert Boulenger, a Belgian herpetologist who helped Fernand Lataste describe the species (Lataste 1879, Escoriza and Ben Hassine 2019).

The subspecies name, "siculus" means, "native of Sicily" in Latin as a reference of where the subspecies is found (Stöck et al. 2008, Escoriza and Ben Hassine 2019).

Initially, B. b. siculus was described as a full species (Stöck et al. 2008). However, further analysis indicted that B. b. siculus did not meet the criteria of distinctiveness from B. boulengeri (Dufresnes et al. 2014, Nicolas et al. 2017, Dufresnes et al. 2019).

References

Dufresnes, C., Bonato, L., Novarini. N., Betto-Colliard, C., Perrin, N., Stöck, M. (2014). ''Inferring the degree of incipient speciation in secondary contact zones of closely related lineages of Palearctic green toads (Bufo viridis subgroup).'' Heredity, 113, 9–20. [link]

Dufresnes, C., Mazepa, G., Jablonski, D., Oliveira, R.C., Wenseleers, T., Shabanov, D.A., Auer, M., Ernst, R., Koch, C., Ramírez-Chaves, H.E., Mulder, K.P., Simonov, E., Tiutenko, A., Kryvokhyzha, D., Wennekes, P.L., Zineko, O.I., Korshunov, O.V., Al-Johany, A.M., Peregontsev, E.A., Masroor, R., Betto-Colliard, C., Denoël, M., Borkin, L.J., Skorinov, D.V., Rasynkova, R.A., Mazanaeva, L.F., Rosanov, J.M., Dubey, S., Litvinchuk, S. (2019). ''Fifteen shades of green: The evolution of Bufotes toads revisited.'' Molecular Phylogenetics and Evolution, 141(106615). [link]

Escoriza, D., Ben Hassine, J. (2019). ''14 Bufotes boulengeri (Lataste, 1879) African green toad.'' Amphibians of North Africa. Academic Press , San Diego, CA, 159 - 168. [link]

Lataste, F. (1879). ''La zoologie descriptive et la zoologie geographique.'' Revue Internationale des Sciences. 2e année. Paris, 4, 436–438. [link]

Lo Valvo, M., and Giacalone, G. (2005). ''Dati e considerazioni sulla biologia riproduttiva della popolazione di Rospo smeraldino, Bufo viridis Laurenti, 1768, della Riserva Naturale di Monte Pellegrino (Palermo).'' Annali Museo Civico Storia Naturale di Ferrara, 6(2003), 61-65.

Lo Valvo, M., and Giacalone, G. (2006). ''Morfometria e selezione sessuale di una popolazione di Bufo viridis in Sicilia.'' V Congresso della Societas Herpetologica Italica, 145-149.

Martínez-Solano, I., Sindaco, R., Romano, A. (2015). ''Bufotes boulengeri''. The IUCN Red List of Threatened Species 2015: e.T153568A74497730. http://dx.doi.org/10.2305/IUCN.UK.2015-1.RLTS.T153568A74497730.en. Downloaded on 06 November 2019.

Nicolas, V., Mataame, A., Crochet, P.-A., Geniez, P., Fahd, S., Ohler, A. (2018). ''Phylogeography and ecological niche modeling unravel the evolutionary history of the African green toad, Bufotes boulengeri boulengeri (Amphibia: Bufonidae), through the Quaternary.'' J Zool Syst Evol Res., 56, 102–116. [link]

Sicilia, A., Lillo, F., Zava, B., and Bernini, F. (2006). ''Breeding phenology of Bufo viridis Laurenti, 1768 in Sicily.'' Acta Herpetologica, 2, 107-117.

Stöck, M., Moritz, C., Hickerson, M., Frynta, D., Dujsebayeva, T., Eremchenko, V., Macey, J. R., Papenfuss, T. J., and Wake, D. B. (2006). ''Evolution of mitochondrial relationships and biogeography of Palearctic green toads (Bufo viridis subgroup) with insights in their genomic plasticity.'' Molecular Phylogenetics and Evolution, 41, 663-689.

Stöck, M., Sicilia, A., Belfiore, N., Buckley, D., Lo Brutto, S., Lo Valvo, M., and Arculeo, M. (2008). ''Post-Messinian evolutionary relationships across the Sicilian channel: Mitochondrial and nuclear markers link a new green toad from Sicily to African relatives.'' BMC Evolutionary Biology, 8, 56-74.



Written by M. Stöck, A. Sicilia, N. M. Belfiore, D. Buckley, S. Lo Brutto, M. Lo Valvo, and M. Arculeo; updated by Ann T. Chang (matthias.stoeck AT unil.ch), UC Berkeley
First submitted 2019-11-01
Edited by Ann T. Chang (2019-11-11)

Species Account Citation: AmphibiaWeb 2019 Bufotes boulengeri: Sicilian Green Toad <http://amphibiaweb.org/species/7081> University of California, Berkeley, CA, USA. Accessed Dec 12, 2019.



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Citation: AmphibiaWeb. 2019. <http://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 12 Dec 2019.

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