After a brief hiatus we return to the remarkable world of toads, and this time round we look at reproductive biology. As a western European person, the toad species I'm most familiar with (the Common toad Bufo bufo and Natterjack Epidalea calamita [see later articles for details on the name changes]) are seasonal breeders that turn up at ponds early on in the year [Common toad mating ball shown here, photo by Neil Phillips] and produce strings of hundreds or thousands of eggs (between 400 and 7500). There are other toad species that are even more fecund, with individuals of some species (like the American toad Anaxyrus americanus and Cane toad Rhinella marina) producing more than 20,000 eggs on occasion: if you put an egg string from one of these species into a straight line, it would be up to 20 m long. You might think that no-one will ever see an egg string even approaching that length, given that the toads wind the strings around plants and debris. However, the egg strings of species that lay their eggs in streams or rivers sometimes become un-entangled by heavy rains and are then swept downstream: Shannon & Werler (1955) reported seeing a doomed string belonging to a Mountain toad Incilius cavifrons that was about 14 m long.
Having mentioned streams and rivers, it's interesting that even those species that normally breed in lakes or ponds will sometimes lay their eggs in fast-flowing water. How successful this strategy might be is a good question, given that the tadpoles lack adaptations for this habitat and would presumably be swept rapidly downstream [Cane toad eggstring shown below, from the Kimberley Cane toad-busting site].
The jet black, poisonous tadpoles of species like the Common toad and Natterjack take about 12 weeks to develop, and by July or August hundreds of metamorphosed toadlets are leaving the water. This pattern will be familiar to people who know the toads of Europe, Asia, northern Africa and North America. A common, and reasonable, assumption is that temperate-zone toads emerge from hibernation and only then start heading towards the breeding pond. You might be surprised to learn that at least some toads of temperate regions actually start moving toward their breeding ponds in September: it's just that cold snaps in the following months stop them from progressing, and cause them to seek out refugia for hibernation (Sinsch 1992).
Toads are diverse in reproductive biology, and some produce small or very small clutches compared to the more familiar species. Examples include the Asian stream toads (Ansonia*), where females may only produce 75-85 eggs per ovary, and the southeast Asian flathead toads or dwarf toads (Pelophryne) whose clutches (laid in shallow puddles, leaf axils, tree holes and even in such places as broken bottles) may consist of less than 20 eggs (in cases between 5 and 10). Various tropical species, including many of the South American stubfoot toads (Atelopus), lay their eggs in fast-flowing streams and have torrent-adapted tadpoles equipped with sucker-like mouthparts or belly suckers [adjacent image shows ventral surface of a Rio Viego toad Rhinella chrysophora tadpole, with belly sucker indicating strong adaptation for stream environment. From McCranie et al. (1989)].
* The monophyly of which has recently been contested. More on that later.
Some species native to arid regions are opportunistic breeders that mate and produce eggs whenever it rains. In such species, the tadpoles may metamorphose in an incredibly rapid time. A total development time of less than two weeks has been reported for the African Taita dwarf toad Mertensophryne taitana (MÃ¼ller et al. 2005). Viviparity has evolved more than once in toads: read on.
Some toads engage in amplexus long before they reach the breeding pond, with the males grabbing hold of animate objects while on their way to the pond, each time hoping for the best (female anurans must be very strong as, in cases, they're able to surmount high obstacles and cling to the bottom of fast-flowing streams, all the while carrying a male who is at least half as heavy as she is). Females therefore typically arrive with a male already attached, though males may then fight over the females within the pond and sometimes drown them in the process. These species are typically explosive breeders that have very short breeding seasons. Other species have longer breeding seasons, and in these the males usually have large vocal sacs and call loudly to attract females [Asian common toads Duttaphrynus melanostictus in amplexus shown here, image by Andrew Johnson Â©, used with permission].
Ear loss and semaphore
At least some toads (like the Cameroon toad Amietophrynus superciliaris) are entirely voiceless, and the repeated loss of hearing organs (the tympanum and its associated structures) among toads suggests that airborne sounds are unimportant to several taxa. It's worth noting here that the development of the tympanum is delayed in post-metamorphic toads, so a juvenile toad that lacks a tympanum does not necessarily grow into an adult that lacks one too by (De La Riva 2004).
However, some species definitely do lack eardrums and other ear structures as adults. How then do the males and females find each other? That's a good question and, for most earless taxa, no-one yet knows. However, it's recently been discovered that earless stubfoot toads that inhabit cascade stream environments with high levels of ambient noise (specifically, the Panamanian gold frog Atelopus zeteki: shown here*) use semaphore - waving actions of their forelimbs - in order to attract attention (Lindquist & Hetherington 1998 and references therein). Also worth noting is that the loss of ear components is not necessarily such a problem in species that are still vocal, as some anurans have co-opted the body wall and lungs as sound-transmission organs (Ehret et al. 1990). We clearly need more answers on how the males and females of non-vocal, earless species find each other.
* This species now seems to be extinct in the wild. Many South American highland toad species are threatened with extinction by the spread of the Bd chytrid fungus. For an introduction to the global amphibian crisis please go here.
How to grab and inseminate females
Amplexus (the action whereby males clasp hold of females) is usually axillary in toads (that is, males grab females around the chest), but inguinal amplexus (where the male grabs the female in front of her hindlimbs) is practised by a few species, including the African tree toads (Nectophrynoides), the Pico Blanco toad Incilius fastidiosus, Holdridge's toad I. holdridgei, the plump toads (Osornophryne) and the Colombian species Rhinella cristinae (Graybeal & de Quieroz 1992, VÃ©lez-R. & Ruiz-C. 2002). In the inguinal amplexus used by some Nectophrynoides African tree toads (Malcolm's Ethiopian toad N. malcolmi) and by some Nimba toads (Nimbaphrynoides), the male clings to the female's ventral surface (Mattison 1987). In the larger clade that includes Bufonidae, axillary amplexus is the norm, indicating that inguinal amplexus is derived for toads, not primitive.
Some species of South American stubfoot toad (Atelopus) remain in amplexus for an amazing length of time: a few weeks is apparently fairly common; more incredibly, Dole & Durant (1974) reported individuals of the Rednose stubfoot A. oxyrhynchus to join in amplexus in December, to begin migration towards the breeding streams in April or May, and to spawn in May or June. In one case, a pair remained in amplexus for a staggering 125 days. During this period of prolonged amplexus, the male declines in condition, becoming thinner and thinner. It's been suggested that prolonged amplexus has evolved because the individuals of the species concerned (inhabitants of high-altitude moorland) are widely spaced out and that meetings must be taken advantage of (Mattison 1987).
As is fairly common in anurans, male toads have stronger arms than females, and they also have special roughened or spicule-covered patches on the hands or fingers that help them to maintain amplexus [those of B. bufo are shown here, from Mattison (1987)]. These 'nuptial excrescences' become larger and more obvious during the breeding season and are hence seasonal secondary sexual characteristics. Skin texture may also change for the breeding season (usually becoming smoother), and the vocal sac and associated vocal slits of males also enlarge at this time.
Viviparity has evolved more than once within toads. It's practised by the African tree toads Nectophrynoides liberiensis and N. occidentalis and by Loveridge's snouted toad Mertensophryne micranotis. African tree toads as a whole are sometime said to be viviparous, but in fact some have a tadpole stage, and others (N. tornieri and N. viviparus) are ovoviviparous (that is, the eggs develop into froglets inside the body of the mother, but are nourished by their own yolk rather than by uterine means). Again it's worth making the point that reproductive diversity in anurans is staggering, with just about everything and anything conceivable being practised by some group or other [new species of Tanzanian Nectophrynoides shown here: photo by P. Whitehorn. Check out those poison glands].
Obviously, viviparity can only evolve in species where internal fertilisation occurs. How did internal fertilisation evolve in toads? We don't really know, but there's some indication that it might be an 'accidental' consequence of inguinal amplexus: the implication being that inguinal amplexus brings the male's vent into closer, more enduring contact than does axillary amplexus. In plump toads, a 'cloacal tube' is said to project from the male's vent (the only descriptions are vague and unhelpful), and it has been suggested that this might represent a step towards internal fertilisation.
More toads soon. You know you love it.
For previous articles in the monumental, ground-breaking toad series see...
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
- We need MORE FROGS
Refs - -
De la Riva, I. 2004. Taxonomic status of Bufo simus O. Schmidt, 1857 (Anura: Bufonidae). Journal of Herpetology 38, 431-434.
Dole, J. W. & Durant, P. 1974. Movements and seasonal activity of Atelopus oxyrhynchus (Anura: Atelopidae) in a Venezuelan cloud forest. Copeia 1974, 230-235.
Ehret, G. Tautz, J. & Schmitz, B. 1990. Hearing through the lungs: lung-eardrum transmission of sound in the frog Eleutherodactylus coqui. Naturwissenschaften 77, 192-194.
Graybeal, A. & de Queiroz, K. 1992. Inguinal amplexus in Bufo fastidiosus, with comments on the systematics of bufonid frogs. Journal of Herpetology 26, 84-87.
Lindquist, E. D. & Hetherington, T. E. 1998. Semaphoring in an earless frog: the origin of a novel visual signal. Animal Cognition 1, 83-87.
Mattison, C. 1987. Frogs & Toads of the World. Blandford, London.
McCranie, J. R., Wilson, L. D. & Williams, K. L. 1989. A new genus and species of toad (Anura: Bufonidae) with an extraordinary stream-adapted tadpole from northern Honduras. Occasional Papers of the Museum of Natural History, the University of Kansas 129, 1-18.
MÃ¼ller, 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.
Shannon, F. A. & Werler, J. E. 1955. Notes on amphibians of the Los Tuxtlas range of Veracruz, Mexico. Transactions of the Kansas Academy of Science 58, 360-386.
Sinsch, U. 1992. Seasonal changes in the migratory behaviour of the toad Bufo bufo: direction and magnitude of movements. Oecologia 76, 390-398.
VÃ©lez-R., C. M. & Ruiz-C., P. M. 2002. A new species of Bufo (Anura: Bufonidae) from Colombia. Herpetologica 58, 453-462.
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Everything that's orange is a poison gland!?!
Yes. Quite a few bufonids (mostly Andean members of Rhinella) have poison glands on their limbs, and even on their hands and feet as is the case here.
I used to teach amphibian reproduction to our vet students. Even though I'm far from an expert on it, it was always a hit, as it tended to blow some minds. Parental care, elaborate social/reproductive behavior, you name it, amphibians do what "only good endotherms should do." And then the caecilians, oh man, they break pretty much all the reproduction "rules." I miss that lecture. I'd have stolen plenty from this article if I was still doing it; nice one Darren!
I was disabused of most of the preconceptions here exploded before they got time to stabilize to proper preconceptions in my head, but they make me wonder what preconceptions that did solidify will turn out to have been known to be wrong all along. What should I discover next - eusocial squamates? macropredatory tardigrades? I was going to say sexual trimorphism but I actually know that one to exist. Toolmaking by chaetognaths? Sperm-whale-grade aquaticism in a marsupial? In an anuran?
Great stuff darren. Im rather fond of toads and thanks for using my photo/Bufo porn :)
If a 14m egg string can stay intact while in a flooded stream, that must be some serious protein holding it together.
I'm curious about the poison. Are the poisons secreted by all toads similar, and are they really (principally?) psychoactive alkaloids?
What? All this about nuptial pads without mentioning Paul Kammerer or neolamarckism?
Excellent. More toads. Will we learn something about the desert spadefoot toad? I recall something about their incredible transformation in times of stress where a percentage metamorphose into canibals, becoming much larger and thereby surviving into the next generation - ?
Spadefoot toads are actually not true toads, but Darren did cover them back in 2007- http://scienceblogs.com/tetrapodzoology/2007/10/those_transitional_anur…
Toads are even uglier then people!
Andreas Johansson @ #4: I was going to say sexual trimorphism but I actually know that one to exist
In *what*? That sounds freaky...
I am a water gardening enthusiast and have a question I hope someone can help me with. I was discussing tadpoles with friends and said that as tadpoles go through their metamorphosis when they reach a certain level of maturity they will release a pheromone (?) that keeps other tadpoles from maturing, thus explaining why so many tadpoles don't mature in ponds. (I realize bullfrog tadpoles take two years to mature). I'm sure I read this somewhere trustworthy but can't remember where. I'm assuming there is an evolutionary mechanism at work, perhaps eliminating competitors?
Of course, I could be wrong. Could someone shed some light on this discussion or direct me to some research in this area.