I forget how it started now, but lately I’ve been very, very interested in toads (yes, toads), so much so that I’ve felt compelled to write about them. The problem is that toads – properly called bufonids – are not a small group. On the contrary, this is a huge clade, distributed worldwide and containing about 540 species in about 38 genera (as of October 2009). So, there are a lot of species to write about, and covering all or most of them is quite the challenge. But it’s the sort of challenge I like…
As is so often the case with amphibian and reptile groups, accessible literature that reviews and discusses these animals is thin on the ground, by which I mean all but unavailable. Indeed, this is a complaint I’ve made several times on Tet Zoo before: there are numerous excellent books that review, on a species by species (or, at least, genus by genus) basis, the mammals and birds of the world, but amphibians and reptiles consistently get short shrift. When will publishers start rectifying this? We don’t need yet another series of super-expensive, weighty tomes on the bird families of the world…. please, please give us some comprehensive herp books! In the continuing absence of such, one has to accrue a huge collection of primary literature and/or field guides. Field guides are very nice, but (1) many of the more exciting regions of the world (zoologically speaking) are either served poorly, or not at all, and (2) some really, really good field guides are prohibitively expensive (as you might have guessed, this fact inspired the recent rant about book prices) [adjacent image, from wikipedia, shows an Asiatic toad Bufo gargarizans].
In view of all this, my aim here on Tet Zoo is to provide at least some basic information on all those toads you never hear anything about, though the better known and more familiar taxa will be covered too. As will be explained later, our views on toad taxonomy have changed much in recent years as new phylogenetic work has confirmed that the members of the biggest and most diverse genus – Bufo (traditionally containing over 250 species) – are actually scattered all about the bufonid tree and are not close kin after all.
Introducing the toads
Toads are familiar to people worldwide, whether they live in the tropics or the temperate regions: they occur on all major landmasses with the exception of Madagascar, Antarctica, Australasia, and various cold and oceanic regions. Having said that they’re absent from Australasia, they occur there now of course, thanks to the introduction of the Cane or Marine toad Rhinella marina [Australian Cane toad merchanise shown here, from wikipedia]. More on that later. Anyway, toads are even relatively familiar to those of us living here in western Europe, where the herpetofauna is so woefully pathetic.
An average toad is a stout, broad-snouted, terrestrial anuran with dry, warty skin, proportionally short limbs that make it good at excavating burrows but poor at leaping, and large poison glands – the parotoid glands (sometimes incorrectly spelt ‘paratoid’, even in the technical literature) – at the back of the head. The burrowing abilities are pretty impressive: winter burrows used by hibernating European toads can sometimes extend as much as three metres below ground. Sexual dimorphism is the norm in toads: females are generally larger than males, and the sexes also often differ in colour and markings. As we’ll see, there’s a lot more to toad diversity than this. There are small, climbing forms, brightly coloured forms that don’t look like ‘toads’ at all, and weird forms with pointed, protruding snouts or giant bony head crests.
Toads are generally predators of small invertebrates (particularly ants), but the larger species will eat millipedes, scorpions, stinging insects like bees and wasps, and small tetrapods like lizards, snakes and other anurans. While anurans in general only recognise animate objects as food sources, at least some toads – the famous and well-studied Cane toad in particular – will eat inanimate objects, including dog food. More remarkable still, Cane toads in Florida have been reported to eat kitchen refuse including sweet corn, broccoli, avocado and rice (Alexander 1965). The reliance of many toads on ants raises the question of how they cope with large numbers of these highly toxic prey. We don’t really know, but a fascinating report of mud-eating in a South American common toad R. margaritifera has led to the suggestion that at least some toads might neutralise insect toxins by ingesting soil (McCracken & Forstner 2006) [photo of R. margaritifera indulging in geophagy shown here, from McCracken & Forstner (2006)].
What are toads?
To begin with, toads – members of the group Bufonidae – are monophyletic. Ford & Cannatella (1993) defined Bufonidae as a node-based clade that includes ‘the most recent common ancestor of living bufonids [Bufo, Frostius, etc., as listed in Frost (1985)], and all its descendants’ (p. 108). Proposing a phylogenetic definition like this is risky: if just one of those 38-odd specifiers was found to be, say, a poison-dart frog, then the content and inclusiveness of Bufonidae would become substantially modified. To date, all of the taxa included within Bufonidae by Ford & Cannatella (1993) have been recovered as part of a clade that conforms with traditional usage, but someone should probably publish a better definition to be on the safe side.
Without doubt, toads are part of Neobatrachia: the enormous anuran clade that includes the familiar ranid frogs, the tree frogs and so on, and excludes primitive frogs (like tailed frogs and New Zealand frogs), pipoids (African clawed frogs and relatives), disc-tongued frogs and spadefoot toads. Neobatrachia (defined as node-based by Ford & Cannatella (1993)) has often been divided into two major groups: the ranoids and the hyloids. The latter group, variously termed Hyloidea, Hyloides or Bufonoidea (it includes tree frogs, glass frogs, leptodactylids, horned frogs and poison-dart frogs, as well as toads), is a clade in some studies (e.g., Hay et al. 1995, Ruvinsky & Maxson 1996, Frost et al. 2006). However, some authors have argued that it’s a paraphyletic assemblage, essentially being a grade that contains all those neobatrachians that aren’t ranoids (e.g., Ford & Cannatella 1993) [‘consensus’ sort of cladogram for hyloids shown here: previously used and discussed here].
Regardless of this controversy, phylogenies generally find Bufonidae to be close to the mostly South American poison-dart frogs (dendrobatids), and to various obscure little South American clades that have only recently been removed from the old, inclusive version of Leptodactylidae, such as Cycloramphidae (the mouth-brooding frogs and their relatives) and Hylodidae (the spinythumb frogs and their relatives)*. Frost et al. (2006) named Agastorophrynia (meaning ‘near kinsman toads’) for the dendrobatid + bufonid clade. More recently, Grant et al. (2006) recovered a phylogeny where Bufonidae formed a clade with a poison-dart frog + hylodid clade, named Nobleobatia therein. Rather than finding cycloramphids to be the sister-taxon to the agastorophrynians, Grant et al. (2006) recovered leuiperids in this position: this is another small group of obscure, mostly South American hyloids (they also occur in Mexico and Central America). They lack common names and were previously included within Leptodactylidae. Phylogenies that recover paraphyly of Hyloidea/Hyloides/Bufonoidea typically find Bufonidae to be in between tree frogs and leptodactylids (e.g., Báez et al. 2009).
* Incidentally, Leptodactylidae sensu lato and Bufonidae have been merged on occasion, but this is not currently considered correct.
Several recent efforts have been made to produce a comprehensive phylogeny for Bufonidae, with the most important works being Graybeal (1997), Pauly et al. (2004), Frost et al. (2006), Pramuk (2006), Pramuk et al. (2008) and Van Bocxlaer et al. (2009). Attempts have been made (primarily by Alain Dubois) to divide Bufonidae into subfamilies, but this hasn’t been widely accepted, plus the obvious non-monophyly of some of the proposed groups has resulted in their rejection by some workers (Graybeal & Cannatella 1995). The phylogenetic studies agree in many respects: an assortment of South American taxa (including taxa sometimes grouped together as the ‘atelopids’ or ‘atelopines’) are basal in the tree, and Bufo of tradition (Bufo sensu lato from hereon) is wildly paraphyletic with respect to many long-recognised genera (more on this later).
When writing this series of toad articles (yes, there’s a series), I’ve relied extensively on Frost et al. (2006), predominantly because this was the first study that acted decisively on the acknowledged paraphyly of Bufo sensu lato: the authors created (or resurrected from synonymy) an unavoidable plethora of new generic names. As is well known, and as we’ve seen here before, Frost et al. (2006) has been criticised as ‘fatally flawed’ (Wiens 2007; see also Vences 2007) and there are concerns that some of its conclusions are erroneous. I’m sure there are, indeed, some problems, but in fact some or many of the relationships recovered by Frost et al. (2006) don’t seem at all unreasonable in light of other studies, and for a response to the ‘fatally flawed’ claim see Frost et al. (2007). Also particularly invaluable was the AMNH Amphibian Species of the World site, maintained by Darrel Frost and citable as Frost (2009) [Ansonia spinulifer shown here, courtesy of John C. Murphy, used with permission]. More on toads soon!
For previous articles on hyloid anurans see…
- Britain’s lost tree frogs: sigh, not another ‘neglected native’
- Ghost frogs, hyloids, arcifery.. what more could you want?
- Green-boned glass frogs, monkey frogs, toothless toads
- It’s the Helmeted water toad!
- Horn-headed biting frogs and pouches and false teeth
- More wide-mouthed South American horned frogs
- Tiny pterosaurs and pac-man frogs from hell
- We need MORE FROGS
Refs – –
Alexander, T. R. 1965. Observations on the feeding behavior of Bufo marinus (Linne). Herpetologica 20, 255-259.
Báez, A. M., Moura, G. J. & Gómez, R. O. 2009. Anurans from the Lower Cretaceous Crato Formation of northeastern Brazil: implications for the early divergence of neobatrachians. Cretaceous Research 30, 829-846.
Ford, L. S. & Cannatella, D. C. 1993. The major clades of frogs. Herpetological Monographs 7, 94-117.
Frost, D. R. 2009. Amphibian Species of the World: an Online Reference. Version 5.3 (12 February, 2009). Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/ American Museum of Natural History, New York, USA.
– ., 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.
– ., 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. 2007. Is The amphibian Tree of Life really fatally flawed? Cladistics 23, 1-11.
Grant, T., Frost, D. R., Caldwell, J. P., Gagliardo, R., Haddad, C. F. B., Kok, P. J. R., Means, D. B., Noonan, B. P., Schargel, W. E. & Wheeler, W. C. 2006. Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History 299, 1-262.
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.
Hay, J. M., Ruvinsky, I., Hedges, S. B. & Maxson, L. R. 1995. Phylogenetic relationships of amphibian families inferred from DNA sequences of mitochondrial 12S and 16S ribosomal RNA genes. Molecular Biology and Evolution 12, 928-937.
McCracken, S. F. & Forstner, M. R. J. 2006. Bufo margaritifer (South American common toad). Geophagy. Herpetological Review 37, 72-73.
Pauly, G. B., Hillis, D. M. & Cannatella, D. C. 2004. The history of a Nearctic colonization: molecular phylogenetics and biogeography of the Nearctic toads (Bufo). Evolution 58, 2517-2535.
Pramuk, J. B. 2006. Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence. Zoological Journal of the Linnean Society 146, 407-452.
– ., Robertson, J. B., Sites, J. W. & Noonan, B. P. 2008. Around the world in 10 million years: biogeography of the nearly cosmopolitan true toads (Anura: Bufonidae). Global Ecology and Biogeography 17, 72-83.
Ruvinsky, I. & Maxson, L. R. 1996. Phylogenetic relationshipf among bufonoid frogs (Anura: Neobatrachia) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 5, 533-547.
Wiens, J. J. 2007. Book review: the amphibian tree of life. Quarterly Review of Biology 82, 55-56.
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 Wester Ghats-Sri Lanka biodiversity hotspot. BMC Evolutionary Biology 2009, 9:131 doi:10.1186/1471-2148-9-131
Vences, M. 2007. The amphibian tree of life: Ideologie, Chaos oder biologische Realität? Zeitschrift für Feldherpetologie 14, 153-162.