The recent discovery that some Asian microhylid frogs frequent the dung piles of elephants has gotten these obscure little anurans into the news, possibly for the first time ever. Microhylids - or narrow-mouthed frogs - are not exactly the superstars of the frog world: they're only really familiar to specialists, despite the fact that (as of June 2009) they contain over 450 species distributed across Africa, Madagascar, the Americas, and Asia. However, some more recent research on the group shows that, like so many animals, they're really quite interesting once you get to know them...
You might be surprised to learn that microhylids in Peru, India, Sri Lanka and perhaps elsewhere have developed close relationships with large spiders. One of the first published discussions of this phenomenon was produced by Crocraft & Hambler (1989). Noting a close association between individuals of the Dotted humming frog Chiasmocleis ventrimaculata and the burrowing theraphosid tarantula Xenesthis immanis in southeastern Peru (but read on), they suggested that the spider - well capable of killing and eating a frog of this size - used chemical cues to recognise the frogs. Young spiders have sometimes been observed to grab the frogs, examine them with their mouthparts, and then release them unharmed. Microhylids are probably unpalatable due to their skin toxins, and this might explain how this association arose in the first place [the image above shows a tarantula walking over a Dotted humming frog. Photo by Emanuele Biggi from here on Anura.it. Used with permission].
Crocraft & Hambler (1989) noted that the frog seemed to benefit from living in proximity to the spider by eating the small invertebrates that were attracted to prey remains left by the spider. The frog presumably also benefits by receiving protection: small frogs like this are preyed on by snakes and large arthropods, yet this frog is protected by a formidable spider bodyguard. Hunt (1980) suggested that the spider might gain benefit from the presence of the frog: microhylids specialise on eating ants, and ants are one of the major predators of spider eggs. By eating ants, the microhylids might help protect the spider's eggs. Hmm, interesting...
In an unpublished masters report from 2002, Jolene Csakany examined the relationship observed between the Dotted humming frog and two kinds of theraphosid, again in Peru. Csakany was unable to identify the spiders concerned: she noted that Crocraft & Hambler's (1989) identification of X. immanis might be incorrect as this spider is otherwise thought to be absent from Peru. Furthermore, X. immanis has some bright pink on its dorsal surface, whereas the spiders observed by Csakany were either robust and solid black, or less robust, and with red hairs on their abdomens. The black spider might be a new species of Pamphobeteus, known locally as the chicken spider (due to an anecdotal account where one carried off a chick!), but the fact that Csakany observed two different kinds of Peruvian tarantula suggests that humming frogs might have formed relationships with more than one tarantula species. Csakany placed skin from humming frogs onto the body of a frog that does not seem to have any special relationship with tarantulas and is ordinarily eaten by them (the Lowland tropical bullfrog Leptodactylus andreae, a leptodactylid. Csakany used one of its synonyms: Adenomera andreai [sic]). After grabbing the skin-wearing Leptodactylus specimens, the spiders examined them, and released them unharmed. Again, this supports the hypothesis that the tarantulas recognise 'partner' frogs after receiving certain chemical signals [adjacent image shows Pamphobeteus nigricolor, from wikipedia].
Another relationship between a microhylid and a spider was reported on Rameshwaran Island (off the south-east coast of India) by Siliwal & Ravichandran (2008). These authors reported that they first became alerted to the possibility of an unusual relationship between the arboreal tarantula Poecilotheria and the microhylid Kaloula taprobanica* after seeing individuals of both species emerge from the same tree hole, and then stand in close proximity without the spider showing any predatory interest in the frog (recall that big spiders will ordinarily eat small frogs if the situation allows). And Poecilotheria is a large, aggressive tarantula, quite capable of killing and eating small frogs [image above shows a close relative of K. taprobanica, K. baleata, from wikipedia. Image below, from Siliwal & Ravichandran (2008), shows K. taprobanica on the left, the spider on the right, and the shared tree hole in the middle].
* The species name is wrongly spelt taprobranica [sic] in the paper. A bit embarrassing, perhaps, as Taprobane is the old name for Sri Lanka.
More recently, Karunarathna & Amarasinghe (2009) reported close relationships between the microhyline Ramanella nagaoi and the theraphosids Poecilotheria ornata and P. cf. subfusca in Sri Lanka. The frog and the tarantulas shared tree holes, and a number also contained eggs and/or juveniles of the spider, or eggs and/or juveniles of the frog, or eggs and/or juveniles of both 'partner' species. Karunarathna & Amarasinghe also cite a very obscure published report by G. Miller from 2003 where a South American microhylid (this time the Bolivian bleating frog Hamptophryne boliviana) was observed in close association with the theraphosid Xenesthis immanis. Unlike Kaloula and Ramanella (which are both microhyline microhylid), Hamptophryne is a gastrophrynine, as is Chiasmocleis. For the significance of this, read on.
Complex relations: commensalism... or mutualism?
The various papers you've just been reading about frequently refer to these microhylid-tarantula associations as examples of commensalism. Commensalism, as I'm sure you know, is the phenomenon whereby species strike up a relationship that is beneficial to one, but has no real cost or benefit to the other. So, if a small, insectivorous bat sleeps in the roof of the house you build, the bat is benefiting from your house, but you essentially gain nothing*, and nor does the bat exact any sort of cost on you or the resources you rely on. If these microhylids and spiders do have a commensal relationship, I presume the thinking is that the frog receives protection from predators thanks to its association with the spider, but that the spider gets nothing in return [adjacent pic from wikipedia].
* On this occasion, let's pretend that the bat eats something inconsequential to human life, rather than piles of mosquitoes.
However, as we've already seen, there are indications that things are more complicated than this. The frogs seem to benefit through their association with a large, formidable predator: presumably, the risk of predation from snakes and so on is lessened thanks to the presence of the spider, and indeed the snakes, geckos, mantids and other frog-eating predators normally found in Sri Lankan tree holes were absent from those frequented by the spider Poecilotheria. Karunarathna & Amarasinghe (2009) reported how several Poecilotheria were seen attacking individuals of Hemidactylus depressus (a gecko) after the latter tried eating the eggs of the frogs the spiders were sharing their tree holes with. The frogs also seem to benefit from the fact that the leftovers of the spiders' meals provide food for their tadpoles (Karunarathna & Amarasinghe 2009), and attract small insects that are eaten by the frogs (Siliwal & Ravichandran 2008). As mentioned above, the spider seems to benefit in that the frogs eat the ants that might ordinarily attack the spider's eggs. Due to their small size, ants are presumably difficult for the spiders to deal with, and they might be effectively helpless against them.
So, both the frogs and the tarantulas seem to benefit from the association of their 'partner'. If this is so, then we're not seeing commensalism, but mutualism. Mutualism is more sophisticated than commensalism, and describes the condition whereby both species gain benefit from the relationship. In extreme forms of mutualism, both species are utterly reliant on the other. It's possible that things might be heading that way, but there are no indications as yet that microhylids or tarantulas have become that specialised, given that all of the species discussed here can survive without a 'partner' [in the photo below, a group of tarantulas are feeding on a frog. Yet, nearby, a 'partner' microhylid (a Chiasmocleis) is in no danger from attack. Again the photo is by Emanuele Biggi, available here on Anura.it. Used with permission. Be sure to visit his site to see this and other images at larger size].
As hinted at above, the fact that the mutualistic relationships discussed here occur on at least two continents, and among frogs (and spiders) that belong to distinct lineages, indicates that these relationships have evolved more than once. Furthermore, they might prove more widespread than realised so far, and more species should be examined with this behaviour in mind. Indeed there are even indications that the mutualism described here is not unique to microhylids, as Powell et al. (1984) reported an association between the Tungara frog Engystomops pustulosus (formerly Physalaemus pustulosus)* and tarantulas of the genus Aphonopelma in Mexico.
* Engystomops is a leiupeurid: Leiupeuridae (named in 1850) is another recently recognised hyloid frog clade, this time extracted from the old, inclusive version of Leptodactylidae by Grant et al. (2006). Leiupeurids are hypothesised to be the sister-taxon to the bufonid + nobleobatian clade (termed Agastorophrynia).
Many thanks to Søren Rafn for the assistance!
And if you're in need of a tutorial on microhylids and where they fit within Anura, see Of short-heads, shovel-snouters and squeakers: an afrobatrachian's tale (part I).
Refs - -
Foelix, R. F. 1982. Biology of the Spiders. Harvard University Press, Cambridge, Mass.
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.
Hunt, R. H. 1980. Frog sanctuary in a tarantula burrow. Natural History 89 (3), 48-53.
Powell, R., Little, L. W. & Smith, D. D. 1984. Eine Wohngemeinschaft von Physalaemus pustulosus (Cope, 1864) (Salientia: Leptodactylidae) mit einer bodenbewohnenden Vogelspinne. Salamandra 20, 273-274.
Karunarathna, D. M. S. S. & Amarasinghe, A. A. T. 2009. Mutualism in Ramanella nagaoi Manamendra-Arachchi & Pethiyagoda, 2001 (Amphibia: Microhylidae) and Poecilotheria species (Aracnida [sic]: Thereposidae [sic]) from Sri Lanka. Taprobanica 1, 16-18.
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Curious little things.
I wonder if these froglets are simply not highly poisonous or disgusting for a spider? And, for other animals, for that matter.
I can imagine that dendrobatid frog might sit next to a spider without worrying to be eaten.
Hi Jerzy. I should indeed have mentioned in the article the fact that microhylids are unusually toxic, with poison glands distributed throughout the skin. It has been proposed that this might have evolved as a response to ant predation: some microhylids spend time sitting right in the middle of ant colonies where small frogs would normally get eaten alive. Some microhylids also produce unusually sticky skin secretions that prevent or discourage arthopod attacks.
So, the toxicity of microhylids probably does play a role in this relationship. Nevertheless, the fact that both the spiders and the frogs seem to gain from the association still indicates that mutualism has evolved.
I had no idea...
:-o
This frog-spider stuff has been out there in the literature since the eighties, and I only know hear of it? Damn, I need to get out more (or would that be 'less'?).
Don't praying mantises have similar problems with ants that attack their newborn young? Might there perhaps also be some frog-mantis mutualistic association somewhere in the world?
Out of topic:
Go to PLOSOne and meet the three new Australian dinosaurs: Australovenator, a "proto-Carcharodontosaurid"; WIntonotitan, a basal titanosauriform; and Diamantinasaurus, an advanced lithostrotian.
Yeah yeah, dinosaurs dinosaurs bloody dinosaurs. Frogs are much more interesting.
Having said all that, keep an eye on SV-POW!
Amazing. I knew about such a partnership from the BBC series Weird Nature, but didn't realise how widespread this partnership was.
- "so many animals [are] really quite interesting once you get to know them"
As author Dodie Smith comments in the original novel of The Hundred and One Dalmatians: "In fact, usual dogs are really more unusual than unusual dogs."
- "the snakes, geckos, mantids and other frog-eating predators normally found in Sri Lankan tree holes were absent from those frequented by the spider Poecilotheria."
And after viewing these photos I can assure you that I too will remain absent from these tree holes. Looks like Shelob's family album. :-)
Seriously, Darren, thanks for the pointer to Emanuele Biggi's anura.it. A nice site which I would never have discovered otherwise.
- "if a small, insectivorous bat sleeps in the roof of the house you build, the bat is benefiting from your house, but you essentially gain nothing"
Um, this relationship also often shows mutualistic aspects, as according to the cliche "a single bat can eat up to 1000 mosquitoes in one hour." Some people build bat boxes to entice the little exterminators to move in. In China and Japan the bat is a traditional symbol of good fortune - I've always guessed for this reason.
Fascinating!
Looks clear how the toxic froglets can live along the adult tarantula, but isn´t so clear how the spiderlings aren´t eaten by the frog partner(perhaps they born too big to be eaten, after all,a common name of microhylids is "narrowmouths".....)
Oh! I remember seeing this on The Most Extreme.
Those are remarkable images! It does seem likely that the young spiders are not generally good prey for the frogs due to size, but immediately after hatching they are probably on the same scale as much of the frog's prey. Since it seems like the tarantulas do engage in a form of brood care, though (the photoset you link to says as much, and shows it, for one of the species), it's probably just a bad idea for the frogs to do so. This might be acquired for mutualism, or commensalism.
wicked cool. Sort of amazing that something like a tarantula, which we think of as automatons always performing the algorithm of bigger or smaller, if smaller, then pounce, can cohabitate with something else in the same size class. A similar arthropod-vertebrate mutualism are the gobies and shrimp that share a burrow, but in that case neither organism would ordinarily be a deadly predator of the other. This thing must really have relied upon the frog being highly distasteful for it to get started at all. Think of how male tarantulas have to be constantly and carefully tapping and plucking to keep female tarantulas in the "mate" and not "eat" mindset...and even that sometimes fails. What is the communication here so that the spider isn't always 'accidentally' pouncing...smells I guess?
I guess. It seems to me that accidentally pouncing on a highly toxic frog and dying (zero benefit) would carry a higher selective penalty than accidentally pouncing on a conspecific, which might cost a mating opportunity (unless the pounce is post-hookup) but does deliver a big meal, and might thin out the competition for food and living space. One wonders how many of those "accidental" acts of cannibalism are actually accidental.
Matt-I wasn't implying the cannibalism is accidental. merely that in either case predation by the spider is unintentional (from the mutualist's or males POV) but might occur. Mostly I mentioned that to draw attention to the fact that constant communication must occur for the predation impulse to be suppressed. This must also be the case for the frog. I am wondering how the spider isn't constantly like, hey, that thing is smaller than me...let's check it out! followed by pouncing and realizing, You again?
Alternatively, maybe constant chemical signals aren't important, but somehow the spider must track, 'remember' or 'recognize' its cohabitor.
Well, what is missing is that frogs spare hatchling spiders, and indeed that adult frogs prefer holes with spiders over holes without spiders. They are protected by their poison in any case.
I think it is missing a proof that really it is a regular commensalism or symbiosis.
But, fascinating Attenborough-documentary-worthy observation in any case.
BTW - I recall that tropical bats also have astonishing hiding places.
Has nothing been published on this relationship in North America? Gastrophryne and tarantulas in (e.g.) Texas and Oklahoma?
I know that they coinhabit burrows.
As an aside, wouldn't something that kills and eats its prey from the inside out be relatively immune to skin toxins? Unless it is something really virulent and has a mode of action such that the spider doesn't even need to ingest it to feel the effects
I vaguely remember a nature documentry (or book/magazine article?) skimming over spider/frog - I had no idea it was so widespread. Great stuff as usual :)
That last picture is awesome. What's the next step in this research?
This is very timely review of a greatly neglected area of research. When I was in school I was amazed by a microhylid -- I believe Kaloula sp that was sitting on a red ant nest. The ants were dismembering a lizard nearby. They would dart towards this frog and then scuttle away.Kaloula could be distinguished from all other frogs in their nocturnal orchestra in our town due to its peculiar grating call. I have seen Microhyla rubra in holes of the type that Chilobrachys spiders use. I have never seen the two together in the same hole but they did co-occur in the same forest. So this might be a relationship to explore. Another incredibly beautiful microhylid Melanobatrachus also lived in the mountains not far from where I went to school but sadly we were hardly aware that the species had gone missing for a while.
Ah, I gotcha. Not the why, for which there is a plausible selective story, but the how, as in how does the spider remember not to eat the frog. That is a good question. Ditto the slurping the prey inside out and skin toxins. I got nothin'.
It's nuts that people yap about pyramids, UFOs, etc. when the really interesting, really unsolved mysteries are right under our feet.
Do you expect an ur-spider - ur-frog pairing, and these are all their descendants, or is this a case of multiple convergence?
The baby spiders probably sound distinctive enough to the frog - they possibly have a completely different acoustic footprint as they walk, run, move compared to any insect, and possibly a unique acoustic signature to that particular species or family, so the frog is likely to distinguish on that basis. Likewise the spider regarding froglets.
All pictures I've seen so far are with female spiders, or individuals of unspecified sex. Do these frogs only associate with females?
Thanks to all for comments, I'm glad this has stirred up so much interest. Hopefully I'll come back to the subject in the future: the main constraint is lack of useable images (a persistent problem when writing about obscure herps).
Sven (comment 18): Hunt's 1980 article (cited above) is about the association of the Texas narrow-mouthed toad Gastrophryne olivacea with the tarantula Aphonopelma. There's also a Breene (1996) that discusses this relationship: I haven't see this reference and think that it's a tarantula book.
Nathan (comment 24): I would say that this behaviour has arisen independently on several occasions as different microhylids and tarantulas have found themselves sharing the same burrows or tree holes. However, it remains to be seen how widespread this sort of thing is.
Really interesting article. I've never read about this before. You'd think it'd have come up in one of the nature documentaries...
"..the arboreal tarantula Poecilotheria .."
What amazing markings!
I've seen this in Mexico on several occasions: frogs and tarantulas.
Note that the "Brachypelma vagans" might be a different species, and I am really not sure if the frogs are actually "rain frogs".
Darren,
I most likely have better pictures of what I've observed in Mexico. I have for sure a video of frogs hopping around a tarantula. I'll try to upload this video to YouTube later on.
Feel free to contact me.
Tarantula's don't so much eat their prey from the inside out as after striking down with their fangs and injecting the venom then proceed to chew the food item until it's a mushy mess, suck out the liquid bits and leave the hard parts as a bolus. This means were they to dine of the frog they would receive a substantial does of poison which is probably incentive enough not to eat the frog.
These discarded remnants of meals do attract scavengers; in captive tarantulas here in the UK minute springtails are often found in spiders tanks feeding on the remains of meals. They're easy to deal with if you keep the tank clean but don't present any sort of threat to the spider.
I think the reason all the images show females (although the first image could be a male - it has a small abdomen and rather spindly legs) is because females tend to stay in the locality of their burrow/hole/tube web whereas mature males will wander far and wide in their search for a mate.
Poecilotheria are indeed wonderful spiders. They are popular with tarantula keepers because of their spectacular markings, quick growth rates and high interest value. They can be kept communally in large tanks (there is some debate about how viable this is) and breed easily; there is a ready market for captive-bred spiderlings. Some of the more recent additions to the hobby are equally incredible animals, especially P. metallica which is a bright iridescent blue in mature females (tarantuala males often have the duller markings of the two sexes).
You might be interested to know that a report in British Tarantula Society Journal Vol. 20 No. 4 written by A. Hooijer and entitled 'Interesting Encounter in Tamarindo, Costa Rica' where he found a microhylid frog he identified as Physalaemus pustulosus co-habiting with an Alphonopelma seemanni in a burrow on an abandoned road.
Excellent article!
Thanks for further comments. John: I'm really interested in seeing the images you have and will email you. Stu, thanks for the info. Note that Engystomops pustulosus (formerly Physalaemus pustulosus) is not a microhylid, but a member of the obscure little group Leiupeuridae.
P. metallica? Really?
I'll have to add that to my list of pop-culture inspired taxonomic names.
Wikipedia says that P. metallica was named in 1889 (and that the species name refers to its metallic blue sheen), so I don't think that Ulrich et al. (who started in... 1981?) have much to do with it, alas.
If you can see them, they're not minute, but utterly gigantic. Minute springtails are about the size of an average ciliate :o)
When I was on holiday in sri lanka, I remember seeing frogs several times, and then perhaps trapping them TEMPORARILY under a mug or something, and then when i came to release them getting a huge shock because a spider was there, with no trace of frog whatsoever.
Thanks for the article by the way, I found it very helpful :)
Heh. Just a little blurb to inform everyone that this post has been linked to in an article on Cracked (a humour website) entitled The 6 Most Unlikely Partners in the Animal Kingdom.