Description
Brachycephalus pitanga is a diminutive species of frog, as are all other members of the genus Brachycephalus. Snout-vent length of adult males ranges from 10.8 to 12.1 mm. Females are larger, with snout-vent length ranges from 12.6 to 14 mm. The skin on the head and back is co-ossified to the skull and axial skeleton. The head is as wide as it is long. It is slightly narrower than the stocky body but composes 39% of total snout-vent length. The inter-nostral distance is approximately a third of the head width. The snout is rounded in shape when viewed laterally or dorsally. It is short: its length is about the diameter of the eye. The nostrils project noticeably from the head and point backwards and outwards. There is weak concavity of the loreal region and the canthal ridge is weakly defined. The mouth is approximately C-shaped. The eye protrudes slightly from the orbit and is 25% of head length (as measured from the tip of the snout to the corner of the jaw). The eye diameter is two-thirds the interorbital diameter. The eye-nostril distance is equal to the interorbital diameter. There are no clearly extended vocal sacs and no tympanum (Alves et al. 2009).

Like other members of the genus, B. pitanga lack one or more phalanges in the hands and feet and have a reduced number of digits. Brachycephalus pitanga has slender forearms, which are roughly the same length as each humerus. The hand is unwebbed. The middle two fingers (digits II and III on the manus) are well developed, but digit II is comparatively more rounded and shorter. Digits I and IV are extremely reduced and appear as bumps on the side of the hand rather than projecting fingers. The digits and hands lack tubercles. The hind limbs are short; the femur region is significantly thicker than any other limb portion. Thigh length is roughly one third of snout-vent length, and the tibia is about 10% shorter than the thigh. There is one pronounced metatarsal tubercle on the foot and There is little to no webbing. Toes I and V are not visible externally. Toes II, III and IV are successively longer; Toe II is the shortest and has a more rounded tip than the others (Alves et al. 2009).

Skin texture is an important and distinctive characteristic of B. pitanga. The head, dorsum, and lateral and ventrolateral surfaces are all coarse and superficially bumpy, as is the area immediately surrounding the cloaca. The ventral surfaces of the body and legs lack this granular texture and instead are smooth (Alves et al. 2009).

Brachycephalus pitanga is distinguished from several congeneric species by the presence of co-ossified skin on the head and dorsum. Brachycephalus brunneus, B. ferruginus, B. izecksohni, B. pernix, and B. pombali all have smooth skin without calcification. The presence of irregular red splotches and mottling on the dorsum distinguishes B. pitanga from B. alipioi, B. ephippium, B. nodoterga and B. vertebralis, all of which lack red coloration. Brachycephalus pitanga (and all other aforementioned species) differs from B. didactylus and B. hermogenesi in having a snout with a rounded profile when viewed dorsally. Brachycephalus didactylus and B. hermogenesi instead have pointed snouts and are further identified by their brown coloration (versus orange and red color of B. pitanga) (Alves et al. 2009). Brachycephalus pitanga and numerous congeneric species have hyperossified skulls. Brachycephalus ephippium has a shield of bone extending down the back, though B. pitanga does not (Clemente-Carvalho et al. 2009). The advertisement call of males of B. pitanga can has longer call durations and lower dominant frequency compared to those of B. hermogenesi and B. ephippium (Oliveira and Haddad 2017).

In life, this species is typically orange, with irregular red splotches and mottling on the dorsum that are distinctive and can cover a significant portion of the back. It also possesses dorsal, lateral and ventral dark brown dots and speckles. In some adults, coloration ranges from almost entirely orange to almost entirely red; juveniles are typically darker than adults (Alves et al. 2009).

In preservative, the coloration fades to off-white in color, with amber or orange markings replacing the contrasting red patterning and dark spots that were present in life (Alves et al. 2009).

There is relatively little variation in adult size or morphology among adult B. pitanga—roughly a couple millimeters in snout-vent length, but with consistent proportions and head anatomy, which are diagnostically useful. The coloration is variable, ranging from almost entirely orange to almost entirely red, and coloration is darker in juveniles (Alves et al. 2009).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Brazil

View distribution map in BerkeleyMapper.

Brachycephalus pitanga occurs in the Serra do Mar of south/southeastern Brazil. The original species description referenced specimens from Núcleo Santa Vírginia in the Parque Estadual da Serra do Mar reserve in the region of São Luís do Pairatinga and in montane forests in Fazenda Capricórnio in the Ubatuba region, in the state of São Paulo, southeastern Brazil (S 23°21'58'', W 44°50'89' ). Frogs are found in and atop leaf litter. The species occurs between 600 and 1800 meters elevation, and its range is not believed to overlap with that of other members of its genus (Alves et al. 2009; Araújo et al. 2012).

Life History, Abundance, Activity, and Special Behaviors

Brachycephalus pitanga is active during the day and has terrestrial habits. It primarily inhabits leaf litter, but it has been found up to 1 m above the ground (Oliveira and Haddad 2017).

Activity is reduced during the dry season, when males call primarily in the morning during misty conditions or precipitation. Males have also been observed to call throughout the rest of the year. In its restricted range, B. pitanga can occur at very high densities of up to 208 frogs per 100 m² (Alves et al. 2009). When relative humidity is high (> 80%), males will call from atop the leaf litter; when the humidity is less than 80%, they instead call from within the litter (Oliveira and Haddad 2017).

The advertisement call of B. pitanga consists of approximately 11 low-intensity pulsed notes emitted at a rate of roughly 60 Hz, with a frequency of about 4.9 kHz. Territorial calls, by contrast, have a slightly higher frequency (~ 5.3 kHz) and a similar pulsing pattern. Three other types of calls have been documented (Oliveira and Haddad 2017). However, B. pitanga (and the closely related B. ephippium) are thought to be unable to hear their own calls, due to incompletely developed inner ears. Both are thought to instead rely upon visual communication. Though calling would be expected to be selected against if it doesn’t serve a purpose, it may have been retained because these frogs are toxic (only B. ephippium has been directly studied for toxicity) and likely have few predators (Pires et al. 2005; Goutte et al. 2017).

Brachycephalus pitanga utilizes aposematic coloration. Similarly to many other Brachycephalus species, they are toxic; their skin contains tetrodotoxins (Rebouças et al. 2019; Pires et al. 2005; Goutte et al. 2017).

In response to being captured, some B. pitanga open their mouth, which may be a defensive behavior (2009). In territorial displays, B. pitanga males wave their hands in front of their face, similar to the motion which they use to clean themselves of soil particles (Oliveira and Haddad 2017).

Mating is hypothesized to occur in the rainy season. Males are territorial and will engage in physical combat with encroaching males (Oliveira and Haddad 2015; Oliveira and Haddad 2017).

Brachycephalus pitanga is a direct-developing species (i.e., it has no free-living larval stage and no post-hatching metamorphosis). This is broadly true of all members of the family Brachycephalidae. Species in this family lay eggs on the ground or in trees (B. pitanga is not arboreal, so presumably the former is true of this species) and have axillary or sometimes inguinal amplexus (Hedges et al. 2008).

Brachycephalus pitanga actively forages for a wide range of prey including mites (Acari), springtails (Collembola), true bugs (Hemiptera), flies (Diptera), ants (Formicidae), beetles (Coleoptera), and larvae belonging to various taxonomic groups. The diversity of prey items is greater in the wet season, and prey size is, on average, larger during this part of the year as well. Generally, mites and springtails are favored, while ants appear to be avoided. The diet of B. pitanga is quite similar to those of its congeners. Males feed less during breeding season (Oliveira and Haddad 2015).

Brachycephalus pitanga and B. ephippium possess highly fluorescent dermal bones on the dorsum and the head, which are covered by a very thin layer of skin. Peak fluorescence occurs when exposed to light of 365 - 385 nm wavelength (invisible to naked human eye). The fluorescent tissue occurs in dorsal patches and is present in both males and females. However, juveniles whose skin has not yet co-ossified do not fluoresce. Fluorescence may function in intra- or interspecific signaling (possibly aposematically) though this hasn’t been tested (Goutte et al. 2019).

Trends and Threats

As of 2020, there is no data available from the IUCN for B. pitanga. Although, B. pitanga's current population health may belie vulnerability, the species has been deemed to be of little conservation concern given its documented distribution and abundance. While locally dense, they have a small and restricted range and are susceptible to habitat loss and disturbance. Populations are also altitudinally and climactically restricted, so climate change may pose a threat. These same attributes have led to high vulnerability of close relatives (Bornschein et al. 2019).

There is conflicting evidence for the risk posed to B. pitanga by chytrid fungus. One study has found that the symptoms of infection from the fungus Batrachochytrium dendrobatidis (Bd) are minimal and sublethal (Bovo et al. 2016). However, a second, more recent study found that spillover of Bd from aquatic-breeding frogs was in fact highly lethal and could pose a major threat to B. pitanga populations (Becker et al. 2019). Thus, it is reasonable to act under the conservative assumption that Bd poses a real threat to this species of frog with regard to conservation efforts.

Brachycephalus pitanga occurs in areas protected as part of Parque Estadual Serra do Mar (Sobre n.d.; Alves et al. 2009).

Possible reasons for amphibian decline

General habitat alteration and loss
Disease
Climate change, increased UVB or increased sensitivity to it, etc.

Comments
The species authority is: Alves, A. C. R., Sawaya, R. J., Reis, S. F., Haddad, C. F. B. (2009). "New species of Brachycephalus (Anura: Brachycephalidae) from the Atlantic rain forest in São Paulo State, southeastern Brazil." Journal of Herpetology, 43, 212–219. doi: 10.1670/0022-1511-43.2.212

Within Brachycephalus, B. pitanga is most closely related to B. vertebralis, B. nodoterga, and B. toby, according to a molecular study that evaluated three mitochondrial genes, Cytb, 12SrRNA, and 16S rRN, and two nuclear loci, Rag-1 and Tyr. Bayesian Inference was used to create a phylogeny, however gene 16S was excluded because they did not have the S16 sequence for B. hermogenesi. The results indicate that B. alipioi and B. hermogenesi belong in a clade sister to the clade consisting of B. pitanga, B. vertebralis, B. nodoterga, and B. toby (Clemente-Carvalho et al. 2011). However, the structure of the clade formed by these four species is not well-resolved.

The genus Brachycephalus is most closely related to the genus Ischnocnema. Together, these two genera comprise the family Brachycephalidae. This family is sister to the diverse clade consisting of Craugastoridae and Strabomantidae (Hedges et al. 2008). At least 17 species of Brachycephalus are known (Araújo et al. 2012).

Brachycephalus comes from the Greek words: “brachys” meaning “short” and “kephale” meaning “head” (Hedges et al. 2008).

The specific name “pitanga” comes from the language of the indigenous Tupi-Guarani people and means “reddish”, in reference to the dorsal coloration of the frog. Pitanga is also a name used for a widespread native species of plant, Eugenia uniflora, that produces a red fruit (Alves et al. 2009).

The family Brachycephalidae occurs widely in southern and southeastern Brazil and northern Argentina in forests along the Atlantic coast (Hedges et al. 2008).

The holotype is stored at Universidade Estadual de Campinas (Alves et al. 2009).

This species was featured as News of the Week on 2 December 2019:

In diverse wildlife communities, exchange of pathogens and symbiotic bacteria among host species influences disease dynamics. The aquatic fungal pathogen Batrachochytrium dendrobatidis (Bd) has wiped out tropical frog communities, with unresolved declines even in terrestrial-dwelling frogs. Becker et al (2019) studied communities of tropical Brazilian frogs to explore spread of pathogenic and potentially beneficial microbes to the disease-susceptible terrestrial-dwelling pumpkin toadlet Brachycephalus pitanga. Toadlets acquired lethal fungal infections, but rarely acquired protective bacteria, from naturally infected aquatic frogs, with disease causing imbalances in host symbiotic bacteria. Our results suggest that pathogen transmission from mildly infected aquatic frogs may lead to death and disruption of symbiotic bacteria in vulnerable terrestrial species (Written by Gui Becker).

References

Brachycephalus Search (IUCN). (2020, May 5). Retrieved May 6, 2020, from https://www.iucnredlist.org/search?query=brachycephalus&searchType=species

Alves, A. C. R., Sawaya, R. J., Reis, S. F., Haddad, C. F. B. (2009). “New species of Brachycephalus (Anura: Brachycephalidae) from the Atlantic rain forest in São Paulo State, southeastern Brazil.” Journal of Herpetology, 43(2), 212–219. doi: 10.1670/0022-1511-43.2.212

Araújo, C. B. D., Guerra, T. J., Amatuzzi, M. C. O., Campos, L. A. (2012). “Advertisement and territorial calls of Brachycephalus pitanga (Anura: Brachycephalidae).” Zootaxa, 3302(1), 66-67. doi: 10.11646/zootaxa.3302.1.5

Becker, C. G., Bletz, M. C., Greenspan, S. E., Rodriguez, D., Lambertini, C., Jenkinson, T. S., Guimarães, P., Assis, A., Geffers, R., Jarkek, M., Toledo, L., Vences, M., Haddad, C. F. B. (2019). “Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian.” Proceedings of the Royal Society B: Biological Sciences, 286(1908). doi: 10.1098/rspb.2019.1114

Bornschein, M. R., Pie, M. R., Teixeira, L. (2019). Conservation status of Brachycephalus toadlets (Anura: Brachycephalidae) from the Brazilian Atlantic rainforest.” Diversity, 11(150), 1-29. doi: 10.3390/d11090150

Bovo, R., Andrade, D., Toledo, L., Longo, A., Rodriguez, D., Haddad, C., Zamudio, K., Becker, C. (2016). “Physiological responses of Brazilian amphibians to an enzootic infection of the chytrid fungus Batrachochytrium dendrobatidis.” Diseases of Aquatic Organisms, 117(3), 245–252. doi: 10.3354/dao02940

Clemente-Carvalho, R.B.G., Klaczko, J., Perez, S.I., Alves, Ana C.R., Haddad, C.F.B., and dos Reis, S.F. (2011). ''Molecular phylogenetic relationships and phenotypic diversity in miniaturized toadlets, genus Brachycephalus (Amphibia: Anura: Brachycephalidae).'' Molecular Phylogenetics and Evolution, 61(1), 79-89.

Goutte, S., Mason, M. J., Antoniazzi, M. M., Jared, C., Merle, D., Cazes, L., Toledo, L., El-Hafci, H., Pallu, S., Portier, H., Schramm, S., Gueriau, P., Thoury, M. (2019). “Intense bone fluorescence reveals hidden patterns in pumpkin toadlets.” Scientific Reports, 9(1), 5388-5395. doi: 10.1038/s41598-019-41959-8

Goutte, S., Mason, M. J., Christensen-Dalsgaard, J., Montealegre-Z, F., Chivers, B. D., Sarria-S, F. A., Antoniazzi, M., Jared, C., Sato, L., Toledo, L. F. (2017). “Evidence of auditory insensitivity to vocalization frequencies in two frogs.” Scientific Reports, 7(1), 1-8. doi: 10.1038/s41598-017-12145-5

Hedges, S. B., Duellman, W. E., Heinicke, M. P. (2008). ''New World direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation.'' Zootaxa, 1737, 1-182.

Oliveira, E. G. D., Haddad, C. F. B. (2015). “Diet seasonality and feeding preferences of Brachycephalus pitanga (Anura: Brachycephalidae).” Journal of Herpetology, 49(2), 252–256. doi: 10.1670/13-211

Oliveira, E. G. D., Haddad, C. F. B. (2017). “Activity, acoustic repertoire and social interactions of the Red Toadlet, Brachycephalus pitanga (Anura: Brachycephalidae).” Salamandra, 53(4), 501–506.

Pires, Jr., O.R., Sebben, A., Schwartz, E.F., Morales, R.A.V., Bloch, Jr., C., Schwartz, C.A. (2005). “Further report of the occurrence of tetrodotoxin and new analogues in the anuran family Brachycephalidae.” Toxicon. 45(1), 73–79. doi:10.1016/j.toxicon.2004.09.016

Rebouças, R., Carollo, A. B., de Oliveira Freitas, M., Lambertini, C., Mateus Nogueira dos Santos, R., Felipe Toledo, L. (2019). “Is the conspicuous dorsal coloration of the Atlantic forest pumpkin toadlets aposematic?” Salamandra, 55(1), 39–47.

Sobre: Parque Estadual Serra do Mar – PESM. (n.d.). Retrieved May 6, 2020, from https://www.infraestruturameioambiente.sp.gov.br/pesm/sobre/

UNICAMP ZUEC-AMP 16746 Brachycephalus pitanga. (n.d.). Retrieved from http://portal.vertnet.org/o/zuec/zuec-amp?id=bra-unicamp-zuec-amp-0000016746

Species Account Citation: AmphibiaWeb 2020 Brachycephalus pitanga: Red Pumpkin Toadlet <http://amphibiaweb.org/species/7334> University of California, Berkeley, CA, USA. Accessed Nov 25, 2020.

Citation: AmphibiaWeb. 2020. <http://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 25 Nov 2020.

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