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.
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People working with vertebrates should not complain about inavailability of literature.
Otherwise, nice piece. I am looking forward to reading the rest of your series.
Is there a post about poisonous in the making? I would really like to see one.
love, m
Thank you for posting this. I have always liked amphibians since I was a child, and now share that love with my 4 year old daughter. Transferring a curiosity to a scientific understanding is one of the great adventures of living, and you are helping us here with this blog.
Off to a toadally great start, Darren! Looking forward to more of this literary bufonic plague.
The darker side of toads:
http://www.npr.org/templates/story/story.php?storyId=6376594
That was just an excuse to use some bad puns, right?
Thanks for positive thoughts - tons more to come.
That's surprising. After all, toads are completely toothless.
Rhinella, right?
Names, not taxa, are defined. :-)
On dietary habits of toads, David says (comment 7)...
Is it? Cane toads (in particular) are well known for sitting outside beehives, eating and eating and eating bees until they can't fit any more into the stomach. Big toads manage to subdue stinging and largish prey without trouble. There are photos showing Cane toads eating snakes 30 cm long or more: will feature all this later in the series.
And, yup, the R. was short for Rhinella (used earlier in article, if you check. Tsk tsk).
Wonderful! When my family used to vacation on Maui, I caught toads every night, including some really massive specimens. They are very easy to catch, as they don't really hop: you just get behind them, reach down, and pluck them up at their midsection. They inflate themselves, sure, but after a few minutes they calm down. I always wondered what kind of toad I was catching...
On a semi-related note, I just got Robert Carroll's new "The Rise of Amphibians" book. It's wonderful, I didn't know amphibians were so diverse in the past.
Darren, yes I'd better watch out or the bad puns will Rana amok.
Had my kid been a son, I was seriously considering the name Bufo.
BTW - why so few cool amphibians are found in captivity?
It would be nice to see eg. Hyla faber in a zoo.
Actually, we *could* use another series of super-expensive, weighty tomes on the bird families of the world, once the relationships have all been nailed down and reorganized properly (and with decent references this time too).
And as far as understudied groups go, toads are hardly in the worst shape. Think of the poor echiuran fans, for example.
Zach @ 9, I have been thinking of buying that book. I guess I will. It will be #2 on my list, after a certain recent book about dinosaurs authored by a certain tetrapod zoology blogger ...
amend #14 to read ... I guess I will now, with your recommendation, thanks for the tip. ...
Yeah, sure, but 2 paragraphs earlier, and... with those empty lines and topic breaks between paragraphs, I wasn't sure if it was still the same R..
Well, most of them aren't amphibians.
And it's not just nomenclature. Be warned that Carroll is conservative in phylogenetic matters, too... which means... he still does phylogenetics as an art, not as a science. For the last 20 years, his students and their students have been trying to explain to him how cladistics works, and he still hasn't understood it. Most of his phylogenetic hypotheses consist of taking two taxa, comparing them, finding similarities, saying "oh, how similar", and concluding an ancestor-descendant relationship. (Also, Carroll seems to think that "sister-group" is newspeak for "ancestor". <headdesk>) No attempt to add an outgroup so it becomes possible to tell which of the similarities are derived similarities; no attempt to add more taxa to see if others are perhaps even more similar to one of the original two; just the two, and "oh, how similar".
You'll learn a lot about biodiversity in time and space, anatomy, and perhaps functional morphology from that book. But phylogeny... be careful.
How do scorpion-eating toads avoid getting stung? Given anuran anatomy, a scorpion could even sting them in an eyeball while inside the toad's mouth.
Darren,
I do hope this recent heightened interest in toads means you'll be addressing that strange phenomenon of toads being found in very unexpected places, be it inside rocks or at the bottom of Loch Ness:
http://news.bbc.co.uk/2/hi/uk_news/scotland/highlands_and_islands/66189…
Really, how does a toad end up crawling along the bottom of a lake like that?
I should note that predators in the relevant areas are slowy learning techniques for hunting cane toads in Australia.
Quolls flip them onto their belly, kites eat only the eyes, and crows do just fine. I'm sure there were more references, but this was word of mouth on Fraser Island last time I was there.
I had been under the impression that Bufo had been found to be polyphyletic, and I was steeling myself to abandon it. Am I hallucinating, or have there been recent upsets?
Jerzy:
I think this species is now called Hypsiboas faber. (Historically, Hyla has been an almost equally big taxonomic wastebasket as Bufo and Rana have been.)
Bufo can radically shrink this way (and indeed this is happening, as now mentioned in the next post), but it cannot completely disappear: the type species, Bufo bufo, must be called Bufo -- unless we manage to sink it into another genus, which is extremely improbable; pretty much only Rana has priority over Bufo.
The name Bufo is also retained for the closest relatives of B. bufo, though there aren't many of those, AFAIK.
hundreds of species; cosmopolitan; origin date back to Cretaceous.
I think it's hard to believe that this genus was not a wastebasket for a huge and old cluster of homogeneous creatures. If we plot a predictable genealogical tree for so many species (all around the world), we may assume that they came from a Cretaceous ancestor, perhaps older than the placentals' common ancestor. I think Bufo should be raise to a family (Bufonidae) or even an order (Bufoniformes?).
Please note that all crocodilians were placed by Linneus into genus Lacerta (together with lizards), and later to their single own genus, Crocodilus, then later to a few genera Caiman, Crocodylus, Alligator, Gavialis), later raised to subfamilies, families and now currently seen as superfamilies (Gavialoidea, Alligatoroidea, Crocodyloidea).
Fair enough, but an origin in the Cretaceous is now debatable: this was based on the assumption that Baurubatrachus from the Upper Cretaceous could act as a calibration point for the crown of Nobleobatrachia (Pramuk et al. 2008) (Nobleobatrachia = the hyloid clade that includes hemiphractids, hylids and bufonids, but not myobatrachoids). If (as is plausible) Baurubatrachus is not a member of Nobleobatrachia, but of a more inclusive hyloid clade ('clade x'), then 'clade x' has its oldest calibration point in the Late Cretaceous, and all included clades are younger than Pramuk et al. (2008) concluded. Van Bocxlaer et al. (2009) went with this and estimated the bufonid stem at 63 Ma (+/- 9.3) and the crown at 55 Ma (+/- 8). This agrees with the fossil record: the oldest toads are Paleocene.
For a previous (but now dated!) discussion of toad antiquity on Tet Zoo go here.
Refs - -
Pramuk, J. B., 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.
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
I haven't had many toad encounters in recent years. When I was a kid in New Jersey, small toads were so common in the summer that the residential streets would end up with a carpet of squashed toad after a couple of months, and I'd occasionally encounter a really massive one, but after my family moved to Colorado, I hardly ever saw one.
Though on one trip to New Mexico, we were doing a little horseback riding around dusk, and there were a large number of toads around, some more gracile than the others. We dubbed them "dairy toads" and "beef toads" (though they were probably just males and females) and practiced herding them.
... and (addendum to comment 24) I've just remembered: if the Marilia Formation (source of Baurubatrachus) is Late Maastrichtian, those mentions of 83 Ma for the calibration point are almost 20 million years too old! Someone should have told Van Bocxlaer et al. I might.
I really hope Pramuk et al. didn't get that calibration point from me (MarjanoviÄ & Laurin 2007, Syst. Biol.). Because⦠I had used an outdated source that called Baurubatrachus Campanian, and had failed to read the rest of the same fucking page, where it says MarÃlia Fm, which is Maastrichtian!
However, even if B. is not a ceratophryid (and why shouldn't it be? What have I missed?), the contemporary Beelzebufo is, and that means there were Cretaceous nobleobatrachians.
How could Paleocene Bufo-ancestors reach Australia and Africa from South America?
Even regarding Bufo as Paleocene-aged, this is the age of almost all South American endemic placental orders.
Response to David (comment 27): yes, there were evidently Maastrichtian nobleobatrachians (of course). But the point here is that authors (Pramuk et al. 2008) had previously used the nobleobatrachian Baurubatrachus as a calibration point for a nobleobatrachian clade that it does not demonstrably belong to. Pramuk et al. (2008) only cite Báez & Perà (1989) in connection with Baurubatrachus, so you're off the hook on this one :)
While I'm here, is this paper as widely known as it should be? .....
Graur, D. & Martin, W. 2004. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends in Genetics 20, 80-86.
Oh, I'm reading now Pramuk's abstract. Forgive my mistake, there's no Bufos in Australia and Madagascar.
And I couldn't find an ultimate age for Marilia Formation. Brazilian dinos Uberabatitan, Baurutitan and Trigonosaurus came from there. Trigonosaurus' paper stated a putative Maastrichtian age, but it's not undebated.
JS Lopes, comment 28, asks...
They didn't reach Australia (so far as we know), but as for Africa: it seems that (contrary to traditional ideas) over-water dispersal was important in amphibian biogeography, so this would be my guess. And there are reasons for thinking that toads in particular are good at over-water dispersal: more on this soon. Meanwhile, see...
Vences, M., Vieites, D. R., Glaw, F., Brinkmann, H., Kosuch, J., Veith, M. & Meyer, A. 2003. Multiple overseas dispersal in amphibians. Proceedings of the Royal Society of London B 270, 2535-2442.
I had forgotten that trans-Beringian dispersal for the Old World bufonid clade is now thought more likely. So, toads originated in the Americas some time around the K/Pg boundary, invaded the Old World once (if you accept phylogenies where all Old World taxa are nested within a New World clade: see Van Bocxlaer et al. 2009), and here diversified into separate African, Eurasian and Indian clades. The big controversy is whether 'Out of India' or INTO India was more important, with recent phylogenies supporting the latter for toads (but not for all amphibians). Over-water dispersal to Africa from the Americas does remain possible however... bring on those Paleocene African fossils :)
What was the position of Proto-Caribbean microplate(s) near K/T borderline? It was next to North America or South America? I suspect a complex pattern of pathways to both landmasses. Maybe Late Cretaceous Northern immigrants (eutherians and metatherians) became nested in Caribbean proto-islands before reach South America in Paleocene. Unfortunately Northern South American paleobiogeography are still scarcely known. ALmost all fossil Late Cretaceous sites came from Argentinan Patagonia, Peru or Southeastern Brazil. I know that was found a promising site in Colombia - I hope it will bring good news to understand SA fauna.
Nice article!
If you ever get time to visit other anura-based sites, you are welcomed to check out my site: www.ifrog.us.
I love the little critters and spend many hours a day studying and researching them.
Have a groovy day!
I don't know, but I've seen it cited a few times, and most of the errors it decries are no longer being committed. Well, some anyway. :-)
Loads of terrestrial crocodiles also come from there, and all papers I've seen on them say Maastrichtian.
JS Lopes wrote:
During the Maastrichtian the Caribbean arc was close to Yucatán in the north and to South America in the south (
map here). There is evidence of subaerial exposure in some of the islands (paleosols, conglomerates, karst) so immigration from NA or SA to the Caribbean could have been possible. In fact, according to Roca et al. (2004) the Caribbean insectivores arrived to the region during the Cretaceous. Fossils of charophytes serve as evidence of availability of brackish or freshwater; there is also evidence of archosaurs from this
Campanian deposit in Puerto Rico, unfortunately, no idea weather it was a marine or terrestrial form, the fossil looks like roadkill.
I've always been fond of toads since I was a little girl, and even now when I see one, I'll generally go charging off in an attempt to capture it. The only toads I've seen around here have been Bufo americanus. Interestingly, none of the toads I ever caught ever inflated or foamed poison, they only made a distressed *meep* noise and tried to crawl out of my hand. Not much of a survival strategy there.