The world is full of frogs, and while I’ve made reasonable efforts over Tet Zoo’s nearly nine years of operation to cover some of this diversity (see the links at the bottom of this article), there are many groups that I’ve never even mentioned. Today I want to talk about the Cycloramphus ‘button frogs’, the core members of the group Cycloramphidae (the spelling Cyclorhamphidae has also often been used). These are South American frogs, universally considered part of the same major group as treefrogs, glassfrogs and horned frogs, all of which are typically grouped together in a clade termed Hyloides, Hyloidea or Bufonoidea, depending on which author you follow.

Simplified hyloid phylogeny, based on Frost et al. (2006) but mostly consistent with the topology also recovered by Pyron & Wiens (2011). Bufonidae: image by Froggydarb, CC BY-SA 3.0. Dendrobatidae: image by Cliff, CC BY-SA 2.0. Cycloramphid: image by Felipe Gomes, CC BY-SA 2.5. Ceratophryidae: image by Grosscha, CC BY-SA 3.0. Centrolenidae: image by Mauricio Rivera Correa, CC BY-SA 2.5. Leptodactylidae: image in public domain. Hylidae: image by Kropsoq, CC BY-SA 3.0.

Even if you know your frogs, the name Cycloramphidae might not be all that familiar. It isn’t a new name: it was first published in 1850 but was later absorbed into Leptodactylidae, long used as an enormous ‘wastebasket group' imagined to contain all those American (and mostly South and Central American) hyloids that couldn’t be convincingly placed elsewhere.

The long-suspected non-monophyly of Leptodactylidae sensu lato was acted on by Frost et al. (2006) who broke the group up into numerous chunks, some newly named and others corresponding to groups named in previous decades but later sunk into synonomy. Frost et al. (2006) recognised a version of Cycloramphidae that – in addition to Cycloramphus – included the alsodines (the spiny-chested Alsodes frogs of Chile and Argentina and their kin), Proceratophrys (the smooth horned frogs), Rhinoderma (the Darwin’s or mouth-brooding frogs), and others. However, this assemblage hasn’t been recovered as a clade in other analyses (Pyron & Wiens 2011) and a reduced Cycloramphidae that contains only Cycloramphus, Thoropa, and perhaps Zachaenus is presently recognised (Pyron & Wiens 2011, Frost 2014).

The ‘core’ cycloramphids are the approximately 30 Cycloramphus species (four of which have been named since 2000, 16 of which have been named since 1983). All are restricted to the Atlantic Forest of south-eastern Brazil. They’re sometimes termed button frogs (I don’t know why). Snout profile, skin texture, the amount and presence of digital webbing, and patterning and pigmentation all vary within this group. Some species are notably flat-bodied; most have rough skin, with black-tipped or white-tipped tubercles covering their dorsal surfaces (Heyer 1983). None of these are large frogs, their SVLs usually being less than 30 mm. Females are bigger than males. [Photo below (c) Felipe Gomes.]

Cycloramphus eleutherodactylus, a litter-dwelling species that lacks digital webbing; photo (c), by Felipe Gomes, CC BY-SA 2.5.

Cycloramphus species mostly group into two ‘ecotypes’: stream-adapted species, closely associated with rocky, fast-flowing streams (a preference sometimes termed rheophilic) in evergreen forests that lay their eggs on rocks in splash zones and have tadpoles that feed on wet rocks, and litter-adapted and semi-fossorial species that live amongst fallen leaves or in terrestrial burrows or fissures, deposit their eggs inside or under logs, and have terrestrial tadpoles (Heyer & Crombie 1979).

Variation in hindfoot webbing among Cycloramphus species. Note the range from having large webs to small webs to none at all. Image from Heyer (1983).

The two groups don’t appear to be clades, with stream-adapted species forming a paraphyletic grade with respect to the more terrestrial ones (Weber et al. 2011). Furthermore, there are also two species (C. bandeirensis and the recently described C. organensis) that occur beneath rocks in open highland regions and hence represent a third ‘ecotype’. It seems that the two species concerned are not closely related (Weber et al. 2011).

Oh, and: yes, terrestrial tadpoles – these are a thing for several anuran groups. More on them below.

Spines are present on the thumbs of C. ohausi (Heyer 1983). Elsewhere in anurans, spikes or spines are present on the thumbs or wrists of males where they are either used in fighting or in gripping females during amplexus. C. ohausi is unusual in that both sexes apparently have spines. Quite what this means for behaviour isn’t clear; I haven’t read any behavioural observations that might illuminate things and am interested to know if there’s anything out there. Are the females fighting with one another, or with males, or is this a defensive adaptation?

A male individual of C. boraceiensis (one of many species named by Heyer in 1983) guarding the egg clutch he fertilised. Photo (c) Ariovaldo Giaretta, CC BY-SA 2.5.

‘Stream-dwelling’ tadpoles, but not as we know it

As is the case with so many anuran groups, the reproductive biology of these frogs is diverse. Some Cycloramphus species produce egg strings and others produce egg clumps; some have free-swimming tadpoles, others produce tadpoles that are laid on land and supplied with large yolk stores (Heyer 1983). Some species guard their eggs, the male sticking with the clutch and attacking and pushing away and even biting foreign objects that approach the eggs (Giaretta & Cardoso 1995). The tadpoles are long-tailed, slender animals with big, dorsally located eyes, a low tailfin that’s restricted to the tail’s distal half, and a flattened belly that has an unusual flap-like structure that extends posteriorly. They don't have a belly sucker like that present in some other tadpoles, but their flattened belly and associated 'flap' might be antecedent to the evolution of such a structure (Aguayo et al. 2009). It should be noted that tadpoles have only been described for a handful of species. As noted above, some are stream-dwellers and others are terrestrial, completing their development thanks to the presence of an attached yolk store.

Montage of Cycloramphus tadpoles, the images from Heyer (1983). Top to bottom: C. fuliginosus, C. duseni, and C. boraceiensis. They are not exactly to scale and, in life, are between 27 and 42 mm long in total.

We should note that the term ‘stream-dweller’ is misleading, however, since these aren’t tadpoles that swim along in the water column. Rather, they constantly cling to, and feed from, rocks that are not submerged but are covered by the thin films of water that result from splash or spray and hence they technically live above the water surface. Tadpoles of this sort (those of C. boraceiensis and C. duseni) have also been discovered on vertical rock wall seeps at quarries and road cuts – not at stream edges at all (Heyer 1983). Presumably, the frogs chose to lay eggs at these spots as they mimicked conditions naturally occurring around waterfalls and other places where water flows. As you might predict, the terrestrial tadpoles don’t need these features and their feeding apparatus “appears embryonic” (Heyer 1983, p. 325). Terrestrial tadpoles of this sort are also present in another taxon included in Cycloramphidae by Frost et al. (2006), Zachaenus.

The decline and disappearance of Cycloramphus

Things are not looking good for many of the Cycloramphus species. This is is C. boraceiensis. Photo (c) Ariovaldo Giaretta, CC BY-SA 2.5.

Now for the depressing part. The conservation status of many Cycloramphus species is extremely worrying. Frogs across Brazil – in both lowland and highland habitats – have severely declined or even wholly disappeared in recent years for reasons linked to pollution, unusual weather events, and the spread of chytridiomycosis (or Bd) (Lips et al. 2005). Furthermore, some or many species are extremely restricted in distribution (in fact, several good questions about their biogeography and limited ranges remain unanswered: Heyer & Maxson 1982)... as a result, they might be very vulnerable to even very localised events (Weber et al. 2011). [Adjacent photo by Ariovaldo Giaretta.]

During the 1980s, Ron Heyer returned to the sites where he had documented numerous new Cycloramphus populations and species during the 1970s. The animals had disappeared and are suspected to have become extinct (Heyer et al. 1988); similar disappearances of other populations were noted in the 1990s. Young et al. (2004) noted that “no-one has seen 13 of the 18 stream-dwelling Cycloramphus species in the last 20 years”. This is a depressing way to end an article, but... there it is.

The original idea behind this article was to write about all taxa included in the large version of Cycloramphidae proposed by Frost et al. (2006). Alas, time has not allowed this luxury.

For previous Tet Zoo articles on frogs and toads, see...

Refs - -

Aguayo, R., Lavilla, E. O., Vera Candioti, M. F. & Camacho, T. 2009. Living in fast-flowing water: morphology of the gastromyzophorous tadpole of the bufonid Rhinella quechua (R. veraguensis group). Journal of Morphology 270, 1431-1442.

Frost, D. R. 2014. Amphibian Species of the World: an Online Reference. Version 6.0 (30th December 2014). Electronic Database accessible at American Museum of Natural History, New York, USA.

Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sá, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., 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 297, 1-370.

Giaretta, A. A. & Cardoso, A. J. 1995. Reproductive behaviour of Cycloramphus dubius Miranda-Ribeiro (Amphibia, Anura, Leptodactylidae). Revista Brasileira de Zoologia 12, 233-237.

Heyer, W. R. 1983. Variation and systematics of frogs of the genus Cycloramphus (Amphibia, Leptodactylidae). Arquivos de Zoologia. São Paulo 30, 235-339.

- . & Crombie, R. I. 1979. Natural history notes on Craspedoglossa stejnegeri and Thoropa petropolitana (Amphibia: Salientia, Leptodactylidae). Journal of the Washington Academy of Sciences 69, 17-20.

- . & Maxson, L. R. 1982. Neotropical frog biogeography: paradigms and problems. American Zoologist 22, 397-410.

- ., Rand, A. S., da Cruz, C. A. G. & Peixoto, O. L. 1988. Decimations, extinctions, and colonizations of frog populations in southeast Brazil and their evolutionary implications. Biotropica 20, 230-235.

Lips, K. R., Burrowes, P. A., Mendelson, J. R. & Parra-Olea, G. 2005. Amphibian declines in Latin America: widespread population declines, extinctions, and impacts. Biotropica 37, 163-165.

Pyron, A. R. & Wiens, J. J. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61, 543-583.

Weber, L. N., Verdade, V. K., Salles, R. de O. L., Fouquet, A., & de Carvalho-e-Silva, S. P. 2011. A new species of Cycloramphus Tschudi (Anura: Cycloramphidae) from the Parque Nacional da Serra dos Órgãos, southeastern Brazil. Zootaxa 2737, 19-33.

Young, B. E., Stuart, S. N., Chanson, J. S., Cox, N. A., & Boucher, T. M. 2004. Disappearing Jewels: the Status of New World Amphibians. NatureServe, Arlington, Virginia.