I've said it before and I'm sure I'll be saying it again: as a life-long zoology nerd, one of my greatest frustrations has always been the fact that there are so many animals that get mentioned - only ever mentioned - but never elaborated upon. I've always liked Axolotls Ambystoma mexicanum, and among the world's unusual amphibians this has got to be one of the most familiar, thanks of course to its widespread use in the pet trade and as a laboratory animal [assortment of captive axolotls show above]. As everyone knows, the Axolotl is neotenous: it retains juvenile characters into sexual maturity, and even an adult is essentially an unmetamorphosed larva, exhibiting a perennibranchiate morphology (meaning that external gills are obvious). Unlike a metamorphosed salamander, a neotenous one retains external gills and a tail and body fin, lacks moveable eyelids, and of course is obligatorily aquatic. The books always say that the Axolotl is far from unique, but in fact one of several similar neotenous, perennibranchiate mole salamanders. What: there are other species like this? Well yes there are, and that's what we're going to look at here...
To begin with, it's worth saying more about A. mexicanum, the Axolotl [wild-type Axolotl shown here, image © EDGE]. Little known is that the wild population of this species is entirely restricted to Mexico's Lake Xochimilco and Lake Chalco, and here they are critically endangered thanks to the pollution, habitat degradation and water extraction and resulting desiccation that has occurred. Use of the animals for food and medicinal purposes, and predation from introduced fish, have also contributed to axolotl decline, and a 2004 survey failed to capture any axolotls in areas where they had formerly occurred (they aren't thought to be locally extinct, however, as specimens continue to show up in local markets). A. mexicanum is one of the larger members of its group, with some individuals reaching 45 cm in total length (although this is exceptional and half this length is more normal).
The word 'axolotl' ('ajolote' in Spanish*) is usually thought to mean 'water dog' (it is probably not coincidental that other, non-ambystomatid perennibranchiate salamanders are today termed 'mudpuppies' and 'waterdogs'), but it also has links to the concept of ugliness or monstrousness and is also often translated as 'water monster' (Smith 1969). All neotenous mole salamanders were originally termed axolotls, as were the larvae of metamorphosing species like the Tiger salamander A. tigrinum, and indeed this is still the case among laypeople (some people even, apparently, use 'axolotl' as the name for any larval salamander). Herpetologists, however, have restricted the name to the perennibranchiate species A. mexicanum, and animals from this population have been well known to scientists since 1864 when a shipment of individuals were sent to Paris. Lake Xochimilco animals were again sent to Paris in 1868, and these Parisian axolotls were the ancestors of virtually all of the laboratory axolotls bred forever afterwards.
* Which confuses things, because this name is today used for Bipes, the limbed amphisbaenians [Tiger salamander shown below]
Early confusion as to whether perennibranchiate individuals should be given their own species or genus relative to metamorphosed individuals, and arguments as to whether A. mexicanum should be regarded as conspecific with the metamorphosing Tiger salamander, mean that the Axolotl has a complex nomenclatural history involving several appeals to, and actions of, the ICZN.
The Axolotl's distinctive morphology and highly endangered status mean that it's among the top 100 EDGE amphibians: you'll recall from a previous Tet Zoo article (here) that EDGE species are Evolutionarily Distinct and Globally Endangered. The EDGE website on globally endangered amphibians can be found here, and here you can find a huge amount of information on endangered mole salamanders and other species. Nine mole salamanders are on the EDGE list, and several of them are the poorly known neotenous, axolotl-like species I referred to above.
The tiger salamander complex
The Axolotl and Tiger salamander are mole salamanders, or ambystomatids, a group of exclusively American salamanders consisting of 33 or so species (we previously looked briefly at them in the second caudate article). The Tiger salamander - if recognised as a single species (read on) - is supposedly distributed over virtually the whole of continental North America, comprising between five and seven subspecies. Closely related to the Tiger salamander are an addition 13 or so species, all of which are unique to Mexico, and the Tiger salamander and its Mexican relatives are grouped together as the 'tiger salamander complex' on the basis of morphological and genetic data. The California tiger salamander A. californiense might be the sister-taxon to the tiger salamander complex. However, DNA work has indicated that 'the Tiger salamander' is not really one species that is monophyletic with respect to the other members of the tiger salamander complex (Shaffer 1993, Shaffer & McKnight 1996) [adjacent image shows California tiger salamanders together with Barred tiger salamanders A. tigrinum mavortium, and hybrids of the two. Barred tiger salamanders have been introduced to California and have been hybridizing with native California tiger salamanders for 50-60 years: the resulting hybrids are fitter than their parent species and mean that pure California tiger salamanders are declining (Fitzpatrick & Shaffer 2007)].
Sorting out the taxonomy and phylogenetic relationships of the different Tiger salamander populations is a rather involved subject that need not concern us here, but one of the most interesting results of this work is the discovery that various of the Mexican neotenous members of the tiger salamander complex are very recently diverged and in fact may be 'among the most recently derived vertebrate species known' (Shaffer & McKnight 1996, p. 430).
Among the most recently named of mole salamanders is another neotenous species, Anderson's salamander A. andersoni: it's also on the EDGE list, and was only named in 1984 (Krebs & Brandon 1984). During field work in 1967, mole salamander expert James D. Anderson discovered a distinctive population of aquatic mole salamanders in and near Laguna de Zacupa (or Lake Zacupa) in Michoacan, Mexico. While clearly planning to describe the Laguna de Zacupa animals as a new species, Anderson died before publishing this work, and in 1970 the species was 'discovered' anew by Ronald A. Brandon and Ronald Altig. By combining Anderson's notes and draft manuscript with new data, Brandon and Salome Krebs later published the species, naming it after Anderson. A. andersoni is a robust, relatively short-tailed species with a reddish-brown background colour and numerous black spots. Its webbed, flattened toes are particularly short and it has a low number of gill rakers compared to other neotenous mole salamanders. A prominent keel is present on the lateral side of the hindfoot. In total length it reaches 21 cm [A. andersoni shown in adjacent image, image © EDGE].
The robust body, short tail and relatively small body fin of A. andersoni suggest that it's a bottom-living species that inhabits running water, and collected specimens came from the stream that ran into Laguna de Zacupa. As with some other neotenous species, in its wild state A. andersoni has only ever been seen in its perennibranchiate stage. Individuals have spontaneously metamorphosed in the laboratory however, and in a few cases the metamorphosed animals lived on for a couple of years. Like the metamorphosed individuals of other neotenous species, these animals seemed to have trouble properly sloughing their skin (Krebs & Brandon 1984).
Taylor's salamander A. taylori is another neotenous, perennibranchiate species on the EDGE list, and like the Axolotl it is extremely restricted in distribution, being unique - so far as we know - to one body of water, Mexico's saline Laguna Alchichica. Yes, saline: what makes A. taylori particularly remarkable is that it is specialised for life in saline water (Taylor 1943) [UPDATE: see comments. The claim that Laguna Alchichica is saline is not at all clear-cut]. It's still true that lissamphibians cannot tolerate the sorts of salinities that amniotes can, but it is not true that anurans or caudates are thoroughly unable to deal with at least some salinity. Brackish water can be tolerated by the larvae and adults of some species: some frogs have even been reported to briefly swim in the sea as an escape tactic. Within Laguna Alchichica, A. taylori lives in deep water, occurring at depths below 30 m. The lake has a maximum depth of 64 m, but - as is typical for deep lakes - is thought by local people to be bottomless [A. taylori shown in adjacent image, © EDGE].
Phylogenetic studies indicate that A. taylori is part of an 'eastern Mexican' mole salamander clade that also includes A. andersoni, A. mexicanum and at least some 'A. tigrinum' populations (Shaffer 1993). A. taylori is yellowish with small dark spots on its dorsal surface.
Are neotenous mole salamanders particularly closely related to one another, or has neoteny simply cropped up repeatedly among different mole salamander lineages? Actually, both possibilities are supported by different parts of the cladogram. Some neotenous taxa really are very close relatives (e.g., A. andersoni and A. taylori) and may have shared a neotenous common ancestor (note that some neotenous species are still capable of metamorphosing when conditions allow, so they can function as polymorphs, phasing in and out of a neotenous lifestyle). Other neotenous species, like the Lake Pátzcuaro salamander A. dumerilii and Lake Lerma salamander A. lermaense, do not group closely with other neotenous species but with those that exhibit metamorphosis, and hence presumably evolved their neoteny separately [adjacent image shows A. dumerilii, image © EDGE].
I had planned to write more about the obscure axolotl-like species, but conference preparation and a long list of other jobs are calling, so I have to leave it there. Please visit the EDGE amphibians site if you want more information. Remember also that we're trying to bring the global amphibian crisis to wider attention this year, and that 2008 is Year of the Frog. If you're concerned about the plight of axolotls and the many other endangered amphibians of the world, please do add your name to the Amphibian Ark online petition.
Refs - -
Fitzpatrick, B. M. & Shaffer, H. B. 2007. Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proceedings of the National Academy of Sciences 104, 15793-15798.
Krebs, S. L. & Brandon, R. A. 1984. A new species of salamander (family Ambystomatidae) from Michoacan, Mexico. Herpetologica 40, 238-245.
Shaffer, H. B. 1993. Phylogenetics of model organisms: the laboratory axolotl, Ambystoma mexicanum. Systematic Biology 42, 508-522.
- . & McKnight, M. L. 1996. The polytypic species revisited: genetic differentiation and molecular phylogenetics of the tiger salamander Ambystoma tigrinum (Amphibia: Caudata) complex. Evolution 50, 417-433.
Smith, H. M. 1969. The Mexican axolotl: some misconceptions and problems. BioScience 19, 593-597, 615.
Taylor, E. H. 1943. A new ambystomid salamander adapted to brackish water. Copeia 1943, 151-156.
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Great post! These are some of the most fascinating animals ever, in my opinion...I first "discovered" them when I read Gould's Ontogeny and Phylogeny in high school, and have been fascinated by them ever since. Glad to see they're getting some press time!
Wow!!! Synchronicity! I read the Axolotl's Tale by Dawkins yesterday, and now you elaborate on the same topic!!! Could it get any better?
One thing I was wondering... Those gills seems pretty vulnerable to attack by predators... Are they protected in any way? I don't know, venom or so?
Salamanders have unparalleled regenerative abilities and can regrow limbs, external gills and even internal organs!
Thanks for comments.
So, how salty is Laguna Alchichica?
What are axolotls used for in local markets? Are they kept as pets?
I have often noticed that this "The books always say that the [insert name] is far from unique, but in fact one of several similar [describe species]" happens. It's great that you took the time to build on that.
As a side point, can anyone comment on the success of EDGE? It's an incredible idea, but by only focusing on sufficiently unique animals aren't they really limiting themselves? It is still one of my favorite organizations though.
Super post, Darren, as always. I was a salamander nerd before becoming a mammal nerd, so was most interested in the topic. The photo of the tiger salamander looks a lot like a Dicamptodon sp. which are also neotenic. Our species of Dicamptodon in the San Francisco bay area is still holding its own and the larvae can easily be seen in the creeks in Marin county -- right across of the Golden Gate bridge from SF.
Taylor said that sodium and potassium (together?) are at 2,570 ppm and chloride is roughly the same (2595 ppm). He does refer to the lake as being both "saline" and "brackish" (in the title!) and I'm pretty sure that it is within the range of what is considered brackish (500-30,000 ppm). A more recent paper on the phytoplankton in the lake refers to it as a "deep, tropical, hyposaline lake" - it gives the salinity as 8.5 g/l.
Oliva, Guadalupe et al. 2001. Phytoplankton dynamics in a deep, tropical, hyposaline lake. Hydrobiologia 466: 299306.
I can still hardly wrap my mind around amphibians briefly swimming out at sea...
Now, does anyone have a reference for frogs swimming in the sea...?
Thanks again for comments, much appreciated - especially the data on salinity in Laguna Alchichica, which I hadn't gotten round to chasing up. Responses...
- Why do local people buy axolotls from markets? Mostly for food, but also for alleged (and undoubtedly mythical) medicinal benefits. Salamanders are said to taste like a cross between fish and chicken, not that I've tried (nor ever will).
- I suppose the big Tiger salamander pictured above does look a bit Dicamptodon-ish. But doesn't Dicamptodon always have that marbled or network-like pattern, plus it never has yellowish coloration like this. Anyway, I don't think you were challenging the id Chris, just noting the comparison. Interesting to hear that you started out as a salamander-nerd. To those who haven't done so, CHECK OUT CHRIS' BLOG (Camera Trap Codger).
- Frogs swimming in the sea? Annandale (in Boulenger 1920) said of Fejervarya cancrivora (the ranid formerly known as Rana cancrivora) 'Individuals are frequently found in brackish water, and I have seen one jump into the sea from a rock and swim ashore apparently without suffering' (p. 24). Shaw (1934) reported seeing Pseudepidalia raddei (the bufonid formerly known as Bufo raddei) jump into the sea and swim away when disturbed. These citations are listed with others in Schmidt (1957): an article which also cites occurences of frogs and tadpoles in estuaries and tidal pools.
Refs - -
Boulenger, G. A. 1920. A monograph of the south Asian, Papuan, Melanesian, and Australian frogs of the genus Rana. Records of the Indian Museum 20, 1-226.
Schmidt, K. P. 1957. Amphibians. In Hedgpeth, J. W. (ed) Treatise on Marine Ecology and Paleoecology. Volume 1. Ecology. Geological Society of America Memoir 67, 1211-1212.
Shaw, T.-H. 1934. Notes on specimens of Radde's toad from Cehfoo. China Journal 20, 197-199.
Our own (European) green toad is also pretty tolerant to salinity and drying.
I add my sympathies to all times when amazing animal fact which I once learned from semi-popular book turned to be not-completely certain, not unique etc. So, axolotl is not unique neotenic larva, crab-eater frog is not only amphibian tolerating brackish water, Baikal seal is not the only freshwater one, Calvaria tree was not extinct together with dodo, Stephen island wren was not wiped out by a single cat etc.
It's really great to see this post - I did my MS thesis work on this complex.
Unfortunately, the phylogeny is not settled - we cannot really say whether some neotenic species are more closely related than others at this point. Despite good geographic clades in the original allozyme study (Shaffer, 1984), The mtDNA analysis (Shaffer and McKnight 1996) showed only very small differences between all the Mexican species - leading others to suggest that there were far fewer species in existance (or one large polytypic species). The mtDNA paper itself concluded that they were among the most recent species on earth.
Weisrock and colleagues (2006) recently showed that the poor mtDNA resolution was due to rare hybridization events leading to introgression. This is becoming a common problem with mtDNA studies of recent radiations like the A. tigrinum complex. The study also showed that there were definite species boundaries for most of the named taxa based on ESTs from a number of nuclear genes. Running a Bayesian phylogenetic analysis of Weisrock's data shows A. taylori to be distantly related to the sister species A. andersoni and A. dumerilii, not the relationship mentioned in the post. Since the latter two live across the mountains from A. taylori, this makes sense.
Speaking of A. andersoni, it wasn't the only unnamed population Anderson found. The American Museum of Natural History in New York has cabinets full of Ambystoma spp. brough back from his expedition to Mexico. The ones that belong to definite species have already been assigned. These specimens are completely unidentified and unnamed. Most are from isolated habitats without named taxa. A. andersoni was the only species Anderson had begun to describe in his extensive field notes. Nowadays, unidentified species are just called A. velasci (Mexican Tiger Salamander) - which only confuses things.
There is a lot of work to be done on this group - I'm glad it's getting the attention it deserves.
Wow, thanks for that Lollia. I based my comments on phylogenetic relationships on Shaffer's older work, but it looks like I should have checked...
Weisrock, D. W., Shaffer, H. B., Storz, B. L., Storz, S. R. & Voss, S. R. 2006. Multiple nuclear gene sequences identify phylogenetic species boundaries in the rapidly radiating clade of Mexican ambystomatid salamanders. Molecular Ecology 15, 2489-2503.
Dammit, I had missed this paper. Anyway, I look forward to seeing more work done on these neat animals - I deliberately avoided discussing hybridisation and ideas about species boundaries because it so quickly becomes a confusing mess... :)
It definitely does, but you can't throw up your hands and call everything A. velasci - or A. tigrinum, which I've been noticing people use lately in reference to A. mavortium and A. velasci, so recently removed from that mother taxon. It's not exactly fair that dozens of small populations of nearly identical salamanders (Bolitoglossa)can be named as distinct species based mainly on molecular differences, while dozens of morphologically distinct ambystoma populations are grouped as a single species with a huge range because the molecular differences aren't great enough. At least that's my opinion. :) Who decided molecules take precendence anyway!
Speaking of species, there also a more recently named species than A. andersoni - A. silvensis (Webb 2004) from Durango. It's partially neotenic and is sympatric with A. rosaceum.
In high country southwest New Mexico we have "properly" metamorphosed individuals rather resembling the boldly black and yellow spotted ones in the fourth photo. We also have gilled individuals looking rather like the one in the lower left photo in the first group, mostly in cattle watering "tanks". Might you or Lollia have any clarification of where these might fit in the Ambystoma complex?
Of course the ones in the tanks might be descended from Mexican ones used for bait, but who would put them there? The only fish in tanks are goldfish, which ranchers add because they allegedly keep the algae down.
Based on the location, they are likely Ambystoma mavortium mavortium or A. m. nebulosum
The neotenes in your tanks are likely descended from the proper salamanders wandering around your yard. A. mavortium is a variable species, and there will be neotenic individuals who attempt remain aquatic (it's genetic). There are semi-permanent axolotl-like populations in Colorado that are actually larger than transformed adults. However, most of the time, the paedomorphs die when their little cattle pond dries out. I
t's a gamble, but sometimes it pays off, particularly when the terrestrial environment is bad (its associated with high altitudes, low temperatures, high terrestrial predation, dry land). Since salamanders have to breed in ponds anyway, the neotenes can mate with the transformed individuals and each other the next season, so they are not exactly isolated by metamorphic failure. The Axolotl may have speciated when the breeding season of the neotenic individuals shifted away from that of the terrestrial population, since terrestrial Mexican Tiger Salamanders breed in their habitat as well.
Thanks for the refs.
Thanks, Lollia-- ALL your criteria apply here. The neotenics are often larger, the land here is high, dry, and cold in the winter. Maybe they get into the ponds in rare wet years and stay until the ponds dry up--??
ANother interesting post. Especially the salt tolerant salamader. I knew marsh frogs could tolerate at least slightly brackish water, but hypersaline lakes! - thats impressive for a fish, let alone a lissamphibian
That's likely what's happening. They may have an escape valve as well, since axolotls can occasionally be forced transform by lowering the water level enough to stress them. Usually they die trying. A salamander from a non-neotenic species may be able to transform before the pond dries out (this hasn't been tested on non-neotenic species, so don't quote me).
I should have mentioned that the non-neotenic species in southern areas and Mexico have much longer larval stages to begin with. An A. mavortium from New Mexico likely remains a larva for up to two years before transforming, and reaches adult size (8-12 inches). So neoteny is likely foremost a timing issue - metamorphosis is delayed so long that they become sexually mature before it can happen. In northern areas (like the Midwest), tiger salamanders tend to transform much earlier at very small sizes - because of the change of seasons. At one point I had a fully transformed juvenile tiger salamander who was smaller than a three month old axolotl. This is more like the outgroup taxon of the complex, the California Tiger Salamander (A. californiense), which actually transforms two months after hatching in vernal pools and never exhibits neoteny.
Neil: That was hyposaline, not hypersaline. A hyposaline lake would be one with low salinity.
Indeed, the heart! Half, anyway. Becker reports accidental discovery while collecting salamander blood by cutting away half the heart and pipetting out the cavity. It turns out that if you stitch up the chest, the cavity fills with blood, which clots. Then the blood cells de-differentiate, and some re-differentiate to heart muscle, while the rest wander off (presumably) to make themselves useful elsewhere. The whole process takes just a few hours, and the new heart is pumping blood after only four.
(Becker & Selden, "The Body Electric". He credits discovery to an assistant whose name escapes me, but that Google insists was Sharon E. Chapin. See also http://www.nature.com/nature/journal/v248/n5444/abs/248145a0.html .)
Leaves me speechless.
It does, however, explain why mammals don't do that: if we tried, given our fast metabolism and high body temperature, the only result would be aggressive cancer.
David: Also, our erythrocytes don't have nuclei.
This is something I notice about "living fossil" sorts of creatures. Maybe it's illusory. Living with the same body plan in one eon and out another, they evidently aren't experimenting with big, visible phenotypic changes. (Or, those experiments failed, or are now not recognizably them.) However, their ancestors had the same capacity for variation as ours did. Can we say that a creature that hasn't changed in visible ways is more likely to have changed in other interesting ways, e.g. biochemically? I'm thinking of ginkgo, coelecanthus, salamander, amoeba, horseshoe crab.
Sure, but the white blood cells still do.
I could do with your help. I'm in Mexico city right now attempting to film Axolotl in the wild. I've just been to a market and been illegally offered several species under the name Axolotl - one looked like te real deal. I've bred them many times in captivity at home and I've also bred thre most likely other species A.tigrimun. So I like to tjink I can idendentify them pretty well - however I cannot find any useful key to these Ambystomid larvae. Is there any?? It just I have people doubting what I saw and without purchasing the animal concerned I cannot be 100% sure.
Hi Nick (wow - I assume you are 'the' Nick Baker?). I'll see if I can send you some pdfs. Thanks for your help with the EDGE amphibians site by the way.
Darren this is THE Nick Baker (well with 99% certainty) as he was asking for help with Axolotl on his website forum before it went down.
Hope the film goes well nick :)
8 g/L ain't saltwater.
The salamander's own blood is about 9 g/L. No major osmoregulatory problems until the environment is hypertonic. In fact, they probably save energy on osmoregulation compared to freshwater species.
Oh yeah, sorry (I'm guessing your comment is inspired by my mention of 'salt water salamanders' in the African softshell article). But - the lake is more saline than a normal lake, right?
hey i have managed to evolve my axolotls by feeding them thyroid glands the thyroxine contained in these gland is enough to change these water dwelling creatures into land based creatures
tay how old are you
beleive it or not i am only 15
Tay, that's not evolution. It's metamorphosis. Evolution means descent with heritable modification â individuals cannot evolve, unless they're Pokemon.