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Dwarf mountain toads and the ones with the doughnut-headed tadpoles

The views expressed are those of the author and are not necessarily those of Scientific American.


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Cladogram based on Van Bocxlaer et al. (2010). Click to enlarge.

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As you’ll know if you’ve been following Tet Zoo for any length of time, I’ve been slowly working my way through the toads of the world for the past few years – yes, all of them, more or less. Seeing as there are about 540 living toad species, this may take a while. I’m currently dealing with that section of the cladogram that seems pretty much dominated by African lineages [the adjacent cladogram - a massively simplified version of the one generated by Van Bocxlaer et al. (2010) - is shown here]. Different studies have produced somewhat different cladograms, but there’s some support for what I’ve been calling the ‘African clade’ [note its position in the adjacent cladogram]. Recent articles introduced the concept of the ‘African clade’ and also covered the 20-chromosome toads. Here, we embark on a look at more members of the ‘African clade’…

The dwarf mountain toads

Capensibufo, the two species of cape toads, mountain toadlets or dwarf mountain toads (C. tradouwi and C. rosei), is poorly known and restricted to South Africa. Long included in Bufo*, they were given their own generic name in 1980. Recent work suggests that they’re close relatives of the also southern African Vandijkophrynus species and also of Mertensophryne and Amietophrynus (Van Bocxlaer et al. 2010).

* For those who haven’t read the previous articles in this series – or aren’t otherwise well-versed in toad taxonomy and phylogeny – an enormous number of bufonid lineages, now known to be well removed from Bufo in the strictest sense (the Eurasian Common toad B. bufo and its close relatives), were originally lumped in to Bufo due to overall phenetic resemblance. See Bidder’s organ and the holy quest for synapomorphies.

Both Capensibufo species lack any trace of digital webbing (a character seen elsewhere among toads only in the South American Truebella species [discussed here]). They produce small clutches of relatively large eggs. Populations conventionally classified as C. rosei (read on) lack a tympanum and columella (the loss of these structures seems to be a familiar theme in toad evolution). Tolley et al. (2010) found that neither currently recognised species is monophyletic and that the numerous distinct lineages recovered within this group of toads require a modified taxonomy. It’s pretty evident that we’re gong to end up with a taxonomy where there are rather more than two species [adjacent photo shows C. tradouwi; from www.grenouilles.free.fr].

As is the case with other earless anurans, much mystery surrounds the way in which earless C. rosei individuals find each other during the breeding season. Intriguingly, the inguinal area in these animals becomes swollen and pink at this time, leading some herpetologists to suggest that odiferous chemical attraction is involved. Tandy & Keith (1972) discussed a 1965 case in which hundreds of (mostly male) C. rosei were discovered packed closely together “like sardines” under rotting reeds fringing shallow breeding pools on Table Mountain. They described this aggregation as “the densest we have ever observed in anurans” (p. 133).

The one with the doughnut-headed tadpoles

Mertensophryne, the African forest toads or dwarf toads or snouted frogs, are remarkable in that their tadpoles have a doughnut-shaped structure on the top of the head. One species now included in Mertensophryne, the Chirinda forest toad M. anotis of Zimbabwe and Mozambique, was given the new generic name Stephopaedes – meaning ‘crown-bearing young’ – specifically for this character (Channing 1978: Channing was removing this taxon from Bufo sensu lato, and it had not been included in Mertensophryne when he was writing). That tadpole is shown in the adjacent diagrams (from Channing 1978).

The young of some African forest toads develop incredibly quickly. In a case reported by Müller et al. (2005), those of the Taita dwarf toad M. taitana hatched from their eggs after two days, and had fully metamorphosed within 11 days! This is one of the most rapid metamorphisms reported for any anuran.

What on earth is that doughnut - or crown – on the tadpole’s head for? Dissection shows that it contains a rich net of capillaries not present elsewhere on the body, and it’s kept in contact with the air while the rest of the tadpole is submerged. Given that these tadpoles inhabit stagnant pools, it’s therefore conceivable that the crown might act as an accessory respiratory surface, and this is supported by the fact that the tadpoles keep the crown in contact with the water surface when the water becomes warm and hence low in oxygen content (Müller et al. 2005). It’s also been suggested that the crown might help to keep surface scum away from the eyes and nostrils (Broadley, in Channing 1978).

Mertensophryne was originally a monotypic taxon (Schmidt’s snouted frog M. schmidti was the first member of the genus to be named), but the fact that a group of African toads exhibit Mertensophryne-like characters (such as a digital reduction [only four toes on the feet], absence of the columella and unusual structures on the heads of the tadpoles) has led some workers to suggest that these species belong in the genus too. These latter species were conventionally included in Bufo and known as the ‘Bufo taitanus group’. If Frost et al. (2006) are right in expanding Mertensophryne in this way, then it’s an important African radiation that includes at least 14 species (note that other authors, including Grandison (1980), Graybeal (1997) and Müller et al. (2005), had previously proposed an affinity between Mertensophryne, Stephopaedes and the ‘Bufo taitanus group’). While the characters mentioned a moment ago might plausibly be synapomorphies of this enlarged Mertensophryne, subtle differences in the anatomy of the ‘doughnut’ imply that it might not be homologous across the group [Adjacent photo shows M. micranotis, photographed in Tanzania. Photo from the Vladimir Dinets Homepage].

Tihen (1960) noted that species included within Mertensophryne possess a reduced presacral vertebral formula compared to many other toads – there are only seven presacral vertebrae (eight is normal for toads). Tihen (1960) also referred to extensively developed quadratojugal and palatine bones in the skull. As usual, it would be nice to know if these peculiarities relate to any specific aspect of behaviour or ecology, but (so far as I can tell) no obvious correlations have been reported.

Poynton’s toads and Van Dijk’s toads

Southern pygmy toad (Poyntonophrynus vertebralis), photo by Marius Burger.

Possibly closely related to Mertensophryne is another African toad assemblage conventionally included within Bufo, the ‘Bufo vertebralis group’. These toads possess small tympana and flattened, poorly developed parotoid glands. Frost et al. (2006) argued that DNA evidence published by Cunningham & Cherry (2004) demonstrates that the toads in this group form a clade that they named Poyntonophrynus. The name honours South African herpetologist J. C. Poynton [adjacent P. vertebralis image - by Marius Berger - from the University of Cape Town’s Avian Demography Unit page].

Vandijkophrynus Frost et al., 2006 is the new name proposed for the ‘Bufo angusticeps group’, a southern African group that seems to form a clade with Capensibufo [V. angusticeps - the Sand toad of the South African Cape Flats - is shown below. Image by Trevor and Margaret Hardaker of the excellent Our Wildlife Adventures, used with permission]. This time the generic name commemorates “Eddie Van Dijk, noted South African herpetologist and indefatigable tadpole specialist” (Frost et al. 2006, p. 220). The toads included in this group are proportionally short-legged and at least some have smooth skins. The Sand toad is one of the best known species, and – as suggested by its name – it’s mostly restricted to areas of sandy soil. It has been reported to eat snails on occasion. Vandijkophrynus toads tend to have a dark, reticulate pattern on their dorsal surface, and males have particularly large testes. Smooth skin and hypertrophied testes are also seen in Capensibufo, and consequently an affinity between these two groups of species has long been suggested. It’s recently been apparently confirmed by analysis of mitochondrial and nuclear DNA (Van Bocxlaer et al. 2010).

Sand toad (Vandijkophrynus angusticeps). Photo (c) Trevor Hardaker.

And that’s where we’ll end for now. More toads real soon.

For previous articles in the Tet Zoo toads series see…

For previous articles on hyloid anurans see…

Refs – -

Channing, A. 1978. A new bufonid genus (Amphibia: Anura) from Rhodesia. Herpetologica 34, 394-397.

Cunningham, M., & Cherry, M. (2004). Molecular systematics of African 20-chromosome toads (Anura: Bufonidae) Molecular Phylogenetics and Evolution, 32 (3), 671-685 DOI: 10.1016/j.ympev.2004.03.003

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.

Grandison, A. G. C. 1980. Aspects of breeding morphology in Mertensophryne micranotis (Anura: Bufonidae): secondary sexual characters, eggs and tadpole. Bulletin of the British Museum (Natural History), Zoology 39, 299-304.

Graybeal, A. 1997. Phylogenetic relationships of bufonid frogs and tests of alternate macroevolutionary hypotheses characterizing their radiation. Zoological Journal of the Linnean Society 119, 297-338.

Müller, H., Measey, G. J. & Malonza, P. K. 2005. Tadpole of Bufo taitanus (Anura: Bufonidae) with notes on its systematic significance and life history. Journal of Herpetology 39, 138-141.

Tandy, M. & Keith, R. 1972. Bufo of Africa. In Blair, W. F. (ed). Evolution in the Genus Bufo. University of Texas Press, Austin, pp. 119-170.

Tihen, J. A. 1960. Two new genera of African bufonids, with remarks on the phylogeny of related genera. Copeia 1960, 225-233.

Tolley, K. A., de Villiers, A. L., Cherry, M. I. & Measey, G. J. 2010. Isolation and high genetic diversity in dwarf mountain toads (Capensibufo) from South Africa. Biological Journal of the Linnean Society 100, 822-834.

Van Bocxlaer, I., Loader, S. P., Roelants, K., Biju, S. D., Menegon, M. & Bossuyt, F. 2010. Gradual adaptation toward a range-expansion phenotype initiated the global radiation of toads. Science 327, 679-662.

Darren Naish About the Author: Darren Naish is a science writer, technical editor and palaeozoologist (affiliated with the University of Southampton, UK). He mostly works on Cretaceous dinosaurs and pterosaurs but has an avid interest in all things tetrapod. His publications can be downloaded at darrennaish.wordpress.com. He has been blogging at Tetrapod Zoology since 2006. Check out the Tet Zoo podcast at tetzoo.com! Follow on Twitter @TetZoo.

The views expressed are those of the author and are not necessarily those of Scientific American.





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  1. 1. Jerzy New 10:27 am 11/24/2011

    So many curious unknown little things!

    Link to this
  2. 2. David Marjanović 2:59 pm 11/24/2011

    Photo from the Vladimir Dinets Homepage].

    Link broken; you probably forgot the http:// .

    Link to this
  3. 3. naishd 3:20 pm 11/24/2011

    Thanks; now fixed.

    Darren

    Link to this
  4. 4. vdinets 1:38 pm 11/25/2011

    Doesn’t the photo of Capensibufo clearly show the tympanum?

    Link to this
  5. 5. naishd 8:13 pm 11/25/2011

    Doesn’t the photo of Capensibufo clearly show the tympanum?

    Ha, you’re dead right – it does. This is because C. tradouwi possesses a tympanum and I was wrong in saying that all Capensibufo species lack one. It turns out that only C. rosei (sensu lato) lacks a tympanum; C. tradouwi possesses one (Channing 2001). Thanks for pointing this out, I’m now going to correct the text.

    Channing, A. 2001. Amphibians of Central and Southern Africa. Cornell University Press, Ithaca & London.

    Darren

    Link to this
  6. 6. Halbred 3:41 pm 11/28/2011

    So this might be a stupid question, but are frogs & toads the only amphibians to go through a tadpole phase? And if so, how did that evolve? Hell, even if tadpoles are more widespread in amphibians, how did that evolve? Tadpoles have such a distinct morphology from adults.

    If this has been covered already on Tet Zoo, I must have missed it.

    Link to this
  7. 7. naishd 4:07 pm 11/28/2011

    Halbred: all excellent questions, and questions that are not actually asked enough. All three modern amphibian clades go through a larval stage, but only anurans (frogs and toads) have what should be called tadpoles. We know that at least some temnospondyls – a group that may or may not include the ancestors of living amphibians – also had larvae, but metamorphosis was nowhere near as profound as that of modern forms. As for the distinctive anatomy of tadpoles: this raises loads of really interesting questions, and by peculiar coincidence I’m thinking a lot about them right now and aim to write about tadpoles on Tet Zoo some time soon. To date, the longest Tet Zoo article on tadpoles is the 2007 one here.

    Darren

    Link to this
  8. 8. David Marjanović 4:25 pm 11/29/2011

    at least some temnospondyls [...] also had larvae

    The same holds for many, presumably all, seymouriamorphs.

    Tadpoles: early larval stages are expanded and get added features like the gill lid which covers the external (!) gills and the fake-jaw cartilages; late larval stages (and the development of the sexual organs and stuff) are squeezed into metamorphosis.

    metamorphosis was nowhere near as profound as that of modern forms

    And in most of the few temnospondyls for which growth series are known, there was no recognizable metamorphosis at all, just gradual development – no two adult features developed at the same time.

    Link to this
  9. 9. David Marjanović 4:26 pm 11/29/2011

    (On the lack of definable metamorphosis, too, the same holds for seymouriamorphs.)

    Link to this
  10. 10. Spookpadda 10:16 am 03/12/2012

    Thanks again for a good summary of these four groups and how they fit in. I’m really enjoying your blog so please excuse the long comments.

    Work over the past decade has resulted in excellent definition of these four groups and a real improvement of biogeographic and biological understanding, each being a reasonable radiation of species restricted to a subcontinental region. Mertensophryne, Poyntonophrynus, Capensibufo and Vandijkophrynus are each clearly monophyletic clades, cohesive within and well distinct from any of the other groups. Their phylogenetic insertion is still very foggy – in Bocxlaer et al 2010 none of the branches joining them to each other or to other toads has any credible support. Despite the tantalizing evolutionary science possibilities of revealing something about earlessness, voicelessness, sexual selection (huge testes), tuberculosity, size change and the origin of the 20-chromosome toads. With the exception of Capensibufo, the majority of species in each group have not been included in molecular analyses and there are likely to be some surprises.

    The monophyly of Mertensophryne (including Stephopaedes and the Bufo taitanus group) was hinted at by many morphological characters. The suggestion that the tadpole crowns may not be homologous is unconvincing. Poynton (1991) Bull. Mus. Comp. Zool. 152: 451-72 summarized the morphological evidence in great detail based on good samples. He found the differences in tadpoles, ecology and skeletons to be slight but surprisingly plumped for recognition of both genera based on relatively minor differences in external morphology and ossification of the skull. Our 2004 study showed Stephapaedes anotis and Bufo lindneri (in the “taitanus group”) carrying closely related mitochondrial DNA, well diverged from other groups. The silver bullet was the tadpole description of B. taitanus. The additional molecular evidence since then makes this interesting group incontestable.

    With “the conceit of hindsight” resistance to lumping them was perverse. In addition to the unique tadpole Mertensophryne sensu lato share a suite of traits separating them from other African toads, such as broad, flattened parotoid glands, paired subarticular tubercles, lack of ear elements (columella and tympanum), and a ventrally directed cloaca (with the accompanying suggestion of internal fertilization). The whole genus is adapted to breeding in very small pockets of water – small hollows in trees or even snail shells. Strangely, despite the absence of outer and middle ear elements M. anotis is recorded as having a call.

    The major problem for this group is that the genus was based on M. micranotis (not M. schmidti), which is a very small frog (adults 16 – 24 mm) and this species shows several features that occur in other very small frogs such as skeletal reduction, digital reduction and increased ossification of the skull (The unrelated Didynamipus shows similar changes). The toe character applies only to M. micranotis and is a reduction not a loss; there are still 5 toes but the outer one is very short. In fact the number of vertebrae in M. micranotis varies from 6 – 8, with 7 as the mode (suggesting that it is an evolutionary reduction in progress). As in Capensibufo, this is another species lacking webbing. Incidentally, the photo that you show is an Amietophrynus (A. brauni?), not Mertensophryne – the toad shown is too large, has clearly raised parotoid glands and a tympanum.

    A couple of other features that you don’t mention – Poyntonophrynus, like Mertensophryne, have doubled subarticular tubercles and peculiar rosette arrangements of dorsal tubercles. They have been suggested as a group demonstrating the SW – NE arid corridor in Africa, with related species in Namibia and Somalia as shown by some birds and mammals, but the two NE species, P. lughensis and P. parkeri have not been properly evaluated.

    Vandijkophrynus are universally knobble skinned, as in the lovely pic that you include – none are smooth skinned. In addition to the enlarged testes some populations in this genus also show mating aggregations and reduction or absence of a call. This was the one group of toads that Blair and colleagues were unable to hybridise with others.

    Capensibufo rosei populations vary in the extent to which they have lost their ear elements – some have a tympanum – possibly due to cryptic species. The Tolley et al 2010 study did not find that the currently recognized species are not monophyletic. Rather, they showed that there are two divergent clades among populations assigned to C. tradouwi and the relationship between these and the monophyletic C. rosei are unresolved (forming a basal polytomy). They suggest that this each group may be a radiation of several closely related species. It remains likely that the described taxa actually are monophyletic entities – as would be expected on biogeographic grounds. As you comment, C. tradouwi has an ear, it calls in small choruses and breeds in mountain wetlands. It is still possible to see the spectacular breeding aggregations of Capensibufo rosei, which occurs in small puddles over a short period of time. Measey & Tolley from the South African National Biodiversity Institute have have been studying the how and why of this phenomenon. Unfortunately there is only one remaining site on the Cape Peninsula and the status of populations elsewhere is uncertain.

    Link to this
  11. 11. em_cressey 8:52 am 05/6/2012

    Hi there.
    I am interested in finding out a little more about the record of the mass aggregation of C.rosei on Table Mountain, discussed by Tandy and Keith (1972). I recently finished my MSc thesis on the phylogenetics and population genetics of the Peninsula lineages of C. rosei. Additionally I compiled all records (museum data, field notes and anecdotal accounts) in an attempt to assess the extent of decline, the previous distribution of the species and to direct search effort in the field. I have no access to Blair’s 1972 book and was wondering if the author of this article may be able to tell me anything more about this record. I have two records from Table Mountain for 1965, both obtained from museum specimen accession notes. One specimen was collected by J. Visser and the other by C.E. Gow. Does this info collaborate with the record mentioned in this article? Although my thesis is complete, I am in the process of submitting for publication, thus this info would very helpful.

    Kind Regards

    Emily

    Link to this

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