Arrow Poison and Arrow without Poison

Central and South America are home to a remarkable diversity of frogs, coming in nearly all the shapes and sizes a frog can possibly come in. Among this diversity, probably the most famous representatives are the arrow-poison frogs of the Dendrobatidae.

Two dendrobatid frogs of two different subfamilies: dyeing dart frog Dendrobates tinctorius (Dendrobatinae, left) and phantasmal poison frog Epipedobates tricolor (Colostethinae, right), copyright H. Krisp. Offhand, has someone been playing silly buggers with dendrobatid species names? Dendrobates auratus is green and black, not gold, and I'm sure I only see two colours on that E. tricolor.

The Dendrobatidae are themselves a diverse family, with somewhere in the area of two hundred currently recognised species. Many of these have only recently been recognised: nearly half of the currently known species have been named since 1985 (Grant et al. 2006). There are also ninety or so species in the closely related family Aromobatidae that were historically treated as dendrobatids and still may be in some sources. The Dendrobatidae are currently divided between three subfamilies: about half the species belong to the subfamily Dendrobatinae, a bit less than a quarter to the Colostethinae, and close to sixty species are placed in the genus Hyloxalus that forms its own subfamily (Grant et al. 2006).

Panama rocket frog Colostethus panamensis, copyright Brian Gratwicke.

Members of the Dendrobatidae are best known, of course, for their remarkable toxicity, associated with bright, striking warning colours. The name 'arrow-poison frog' reflects this trait as an arrow scraped across a frog's skin would pick up some of the frog's own lethality. The toxin, comprising various alkaloids, is not produced directly by the frog itself but is instead acquired through its arthropod diet. Most of the alkaloids sequestered by arrow-poison frogs come from ants (Darst et al. 2005) but other potential sources include beetles, millipedes and oribatid mites. However, not all dendrobatids are toxic and colourful. In fact, these features are largely characteristic of the Dendrobatinae only. Members of the Colostethinae and Hyloxalus are mostly cryptic in coloration and largely do not sequester alkaloids. The distinction is not an unshakeable rule: some non-dendrobatine dendrobatids are quite colourful in their own right and a handful of colostethines (members of the genus Epipedobates) are toxic, having seemingly evolved the ability to secrete alkaloids independently of the dendrobatines. Laboratory studies indicate that at least some non-toxic colostethines are able to consume alkaloid-bearing prey without ill effects, suggesting that alkaloid resistance is ancestral for the family as a whole.

Male Hyloxalus nexipus carrying tadpoles, copyright Santiago Ron.

More characteristic of dendrobatids as a whole is their breeding behaviour. As a rule, dendrobatids are more or less terrestrial, not habitually living in water, though many species are found alongside the margins of water bodies and may dive into the water to escape danger. Others will be found among leaf litter or be completely arboreal. Eggs are laid in damp terrestrial locations such as under leaves; males may deposit their sperm before or after the female deposits her eggs. Hatching tadpoles are then carried on the back of one of the parents to a suitable body of water such as a pool or stream. In members of the Dendrobatinae, tadpoles are deposited in phytotelmata, water-filled hollows in vegetation (such as in the cenre of bromeliads or holes in trees). Adelphobates castaneoticus, found in Pará in Brazil, has a habit of using the fallen husks of Brazil nuts. In some species, tadpoles are transferred one at a time; in others, groups of tadpoles will be carried en masse. In most genera, the male parent is the primary or sole transporter of tadpoles. Females of some species may also carry tadpoles; in others, a female finding an unattended cache of eggs will simply eat them. In the dendrobatine genus Oophaga, tadpole transport is the sole responsibility of the female. Following deposition, developing tadpoles of many species live on a diet of detritus. Others, particularly among the phytotelm-inhabiting species, are carnivorous, feeding on insects and other aquatic vertebrates, or even on their own siblings. In the aforementioned Oophaga, the transporting female will also lay a deposit of unfertilised eggs at the same time as she drops off the tadpoles. As well as providing food for the developing larvae, these eggs may also carry a shot of alkaloids to provide a head start in developing their defenses.

Strawberry poison-dart frogs Oophaga pumilio, two different colour morphs, copyright Pavel Kirillov.

Despite their often bright colours, many dendrobatids are poorly known due to cryptic habits and many species are only found in restricted ranges. As well as the usual threats to their survival from habitat destruction and the like, many dendrobatid species are threatened by collection for the pet trade. Their bright colours make dendrobatids popular specimens and captive individuals lose their toxicity if not provided with the prey from which alkaloids are derived. Unfortunately, about a quarter of dendrobatid species are currently recognised as endangered, many severely so. The highest diversity of endangered species is in the northern Andean region, in Venezuela, Colombia and Peru, which is also the centre of diversity for the family as a whole (Guillory et al. 2019). Urgent action may be required if we are to preserve these tiny, shiny, toxic beauties.

REFERENCES

Darst, C. R., P. A. Menéndez-Guerrero, L. A. Coloma & D. C. Cannatella. 2005. Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. American Naturalist 165 (1): 56–69.

Grant, T., D. R. Frost, J. P. Caldwell, R. Gagliardo, C. F. B. Haddad, P. J. R. Kok, D. B. Means, B. P. Noonan, W. E. Schargel & W. C. Wheeler. 2006. Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History 299: 1-262.

Guillory, W. X., M. R. Muell, K. Summers & J. L. Brown. 2019. Phylogenomic reconstruction of the Neotropical poison frogs (Dendrobatidae) and their conservation. Diversity 11: 126.

Monkey Frogs

Following my last post, it looks like we're staying in the Neotropics for a while longer. The leaf frogs or monkey frogs of the Phyllomedusinae (a subfamily of the tree frog family Hylidae) are perhaps the most famous group of frogs to be found in South America. One particular species, the red-eyed tree frog Agalychnis callidryas, would for many people be the first image that comes to mind when they picture a frog, owing to its regular appearance in popular media.

The aforementioned red-eyed tree frog Agalychnis callidryas, copyright Carey James Balboa.

The phyllomedusines are a group of about sixty species of slender, arboreal frogs that live as ambush predators of invertebrates. The inner digits of the hands and feet are opposable and can be used to grasp slender twigs while adhesive pads at the ends of the digits allow the frog to grip onto flat surfaces such as leaves. Darren Naish at Tetrapod Zoology (Wayback Machine version; the current iteration of Tetrapod Zoology is at tetzoo.com) has described leaf frogs as superficially resembling "slow-climbing primates like lorises". Phyllomedusines will perch with all four hands and feet firmly grasping the substrate, waiting for suitable prey to inadvertently stray too close. Prey is captured by means of a highly protrusible tongue, not found in other hylids. In at least some species, light markings are present on the outer toes which may be drummed while in ambush to attract prey. Bertoluci (2002) suggested that the movement of these light patches in Phyllomedusa burmeisteri may resemble those of a worm or caterpillar but I would suggest that merely the appearance of the small moving points alone may pique a wandering arthropod's interest while the camouflaged remainder of the frog blends into the background.

Orange-legged tree frog Phyllomedusa oreades, copyright Danielvelhobio.

Though phyllomedusines begin their lives as aquatic tadpoles, their eggs are laid in clutches outside the water, in locations such as on leaves, tree trunks, rock crevices, etc. In some species, one or more leaves are folded together to construct a nest in which the eggs are laid. Some phyllomedusines in the genera Agalychnis and Cruziohyla are capable of gliding by means of extensive webbing on enlarged hands and feet and/or skin flaps on arms and legs. Interestingly, possession of gliding ability in phyllomedusines is correlated with explosive breeding patterns, suggesting that its main function is to facilitate synchronised movement of members of a population between their usual upper canopy habitat and suitable breeding locations near ground-level water bodies (Faivovich et al. 2009). Females of the two gliding genera (or sometimes a mating pair) may also spend time sitting in water prior to egg-laying; during this time, the female draws water into her bladder that she will then release over the eggs while laying them. In the majority of phyllomedusines (except Agalychnis) egg masses contain a mixture of eggs and empty, eggless capsules. In those species that construct nests from folded leaves, these extra capsules act as the glue holding the leaf surfaces together. Their function in other species is less obvious; they may help to protect the egg mass from drying out.

Upon hatching, the tadpoles will wriggle out of the egg mass to drop into a nearby body of water, whether a pond, a stream, or a pool of water collected in the hollow of a tree. After a childhood spent scraping algae for food, they will eventually transform into a new generation of frogs, ready to ascend once again into the trees above.

REFERENCES

Bertoluci, J. 2002. Pedal luring in the leaf-frog Phyllomedusa burmeisteri (Anura, Hylidae, Phyllomedusinae). Phyllomedusa 1 (2): 93–95.

Faivovich, J., C. F. B. Haddad, D. Baêta, K.-H. Jungfer, G. F. R. Álvares, R. A. Brandão, C. Sheil, L. S. Barrientos, C. L. Barrio-Amorós, C. A. G. Cruz & W. C. Wheeler. 2010. The phylogenetic relationships of the charismatic poster frogs, Phyllomedusinae (Anura, Hylidae). Cladistics 26: 227–261.

Hydromantes: Salamanders in Different Places

There are times when biogeography is able to throw us some real puzzlers: organisms whose distribution seems to defy expectations. Among these mysteries, special mention must be made of the salamanders of the genus Hydromantes.

Gene's cave salamanders Hydromantes genei courting, copyright Salvatore Spano.

Hydromantes is a genus containing a dozen species from among the lungless salamanders of the family Plethodontidae. Plethodontids are the most diverse of the generally recognised families of salamanders, with over 450 known species found mostly in Central and South America. Hydromantes, however, is a geographically isolated genus in this family with its species found in two widely separated regions: California in western North America, and mainland Italy and Sardinia in Europe. Though some authors have advocated treating the species found on each continent as separate genera, both morphological and molecular studies have left little doubt that the group represents a discrete clade.

Distinctive features of Hydromantes compared to other plethodontids include feet with five, partially webbed toes and a weakly ossified, flattened skull (Wake 2013). Members of this genus capture prey with a projectile tongue which is the most extensive of any amphibian, extending up to 80% of the animal's total body length (Deban & Dicke 2004). There are some differences between North American and European species notable enough for the recognition of separate subgenera (there is something of a gigantic clusterfuck surrounding the names of said subgenera but the details are far too tedious to relate here). The three North American species of the subgenus Hydromantes have bluntly tipped tails that they use as a 'fifth leg' when navigating smooth and/or slippery surfaces, whereas the European species have unremarkable pointed tails. Historically, the North American Hydromantes species have been poorly known, being isolated to restricted ranges. Hydromantes shastae is found in limestone around Lake Shasta whereas H. brunus is found in a small area of mossy talus habitat along the Merced River in the foothills of the Sierra Nevada (Rovito 2010). The third species, H. platycephalus, is found at higher altitudes in the Sierra Nevada, well over 1000 m above sea level. Individuals found living on steep slopes are known to escape predators by tightly coiling their bodies and simply rolling down the slope (García-París & Deban 1995). A molecular analysis of H. platycephalus and H. brunus by Rovito (2010) identified the former species as derived from within the latter, and Rovito suggested that H. brunus may have originated in a remnant population from when H. platycephalus moved into lower altitudes during the Ice Age.

Mt Lyell salamander Hydromantes platycephalus, copyright Gary Nafis.

The seven or eight European species are mostly placed in the subgenus Speleomantes; a single species, Hydromantes genei, is divergent enough to be placed in its own subgenus Atylodes (though most recent studies have indicated that the European Hydromantes overall form a discrete clade). Hydromantes genei and three species of Speleomantes are found in caves on the island of Sardinia; the remaining Speleomantes species on mountains of mainland Italy. Molecular analysis suggests that H. genei became isolated on Sardinia about nine million years ago, with the ancestors of the Sardinian Speleomantes arriving later about 5.6 million years ago when the Mediterranean dried out during what is known as the Messinian Salinity Crisis (Carranza et al. 2008). The absence of any Hydromantes on neighbouring Corsica is something of a mystery, and it has been suggested that they may have been present there in the past before going extinct.

Extinction also seems the most likely explanation for Hydromantes' unusual distribution. The fossil record for the genus is minimal, and provides little information not already available from living species, but molecular dating attempts agree that the division between European and North American Hydromantes happened too recently to be related to the tectonic separation of the two continents. Such a scenario would also leave open the Hydromantes' absence in eastern North America. The description in 2005 of the Korean lungless salamander Karsenia koreana demonstrated the presence of plethodontids in eastern as well as far western Eurasia, and it seems possible that Hydromantes dispersed into Eurasia via the Bering Strait landbridge, becoming widespread across the continent before extinction reduced it to the isolated relicts it is today.

REFERENCES

Carranza, S., A. Romano, E. N. Arnold & G. Sotgiu. 2008. Biogeography and evolution of European cave salamanders, Hydromantes (Urodela: Plethodontidae), inferred from mtDNA sequences. Journal of Biogeography 35: 724–738.

Deban, S. M., & U. Dicke. 2004. Activation patterns of the tongue-projector muscle during feeding in the imperial cave salamander Hydromantes imperialis. Journal of Experimental Biology 207: 2071–2081.

García-París, M., & S. M. Deban. 1995. A novel antipredator mechanism in salamanders: rolling escape in Hydromantes platycephalus. Journal of Herpetology 29 (1): 149–151.

Rovito, S. M. 2010. Lineage divergence and speciation in the web-toed salamanders (Plethodontidae: Hydromantes) of the Sierra Nevada, California. Molecular Ecology 19: 4554–4571.

Wake, D. B. 2013. The enigmatic history of the European, Asian and American plethodontid salamanders. Amphibia-Reptilia 34: 323–336.

Riding a Frog's Pouch

Most people are familiar with the concept of marsupials, the group of mammals whose young spend the earliest part of their life nurtured within a pouchon their mother's underside. Kangaroos, koalas, wombats—all have their established place in popular culture (even if a person can't really ride inside a kangaroo's pounch, and anyone trying to is likely to find themselves picking their intestines off the floor). But perhaps less people are aware that a nurturing pouch is not unique to marsupial mammals: among others, there are some frogs that do it too.

Horned marsupial frog Gastrotheca cornuta female carrying eggs, copyright Danté B. Fenolio.

The marsupial frogs are found over a great part of South America, being particularly diverse in upland regions. Many (particularly members of the genus Hemiphractus) are somewhat gargoyle-ish beasts with flattened heads and/or prominent 'horns' above the eyes. Until recently, marsupial frogs were usually classified as a subfamily of the treefrog family Hylidae but more recent phylogenetic studies have agreed on the polyphyly of the latter family in its broad sense. As a result, the marsupial frogs are now placed in their own distinct family, the Hemiphractidae, as part of a broader association of a number of South American frog families. The influential phylogenetic study of amphibians by Frost et al. (2006) suggested that the marsupial frogs themselves were polyphyletic and divided them between no less than three families (Hemiphractidae, Cryptobatrachidae and Amphignathodontidae) but more recent studies have agreed on their monophyly. Frost et al.'s results are generally thought to have resulted from their poor coverage of members of this clade.

So what makes them marsupials? In all hemiphractids, the female carries her eggs after fertilisation until they hatch. In three of the five recognised genera (Hemiphractus, Cryptobatrachus and Stefania), the eggs are carried exposed on the surface and the young hatch directly as fully-formed froglets without a free-living tadpole stage. In the other two genera, Flectonotus and Gastrotheca (the latter genus being the most diverse in the family), the eggs are contained in a pair of pouches on the female's back. In some Gastrotheca species the eggs hatch into froglets as in the other genera, but in other Gastrotheca and in Flectonotus they hatch into tadpoles that the female then releases into a suitable pool of water.

Female Spix's horned treefrog Hemiphractus scutatus carrying a load of young froglets, copyright Santiago Ron.

Considering that a tadpole stage in development is evidently the original condition for frogs as a whole, it might be assumed the tadpole-bearing hemiphractids represent the basal taxa in the group with loss of the tadpole being derived. But intriguingly, recent phylogenetic analyses have indicated that the tadpole-bearing Gastrotheca occupy quite deeply nested positions in the hemiphractid family tree (Wiens et al. 2007; Flectonotus is placed as the sister taxon of all other hemiphractids, more as one might expect). This has led to the suggestion that the presence of tadpoles in Gastrotheca may represent a reversal to the original condition from direct-developing forebears. Now, I'm going to admit up front that I tend to be skeptical about claims for the reappearance of complex characters (and only partially because such studies never fail to cite that "stick insects re-evolved wings" thing of which I've already said I'm not a fan). In their analysis of breeding trajectories in hemiphractids, Wiens et al. (2007) found that, if one assumed that loss of the tadpole stage was equally likely to its gain, then the hemiphractid phylogeny supported a re-gain of tadpoles. However, if one presumed that loss was more likely than gain, then their analysis supported multiple losses with the tadpole-bearing Gastrotheca retaining the ancestral state. Nevertheless, they argued that a re-gain was more likely. Tadpole-bearing hemiphractids are all inhabitants of high altitudes where their young are often the only tadpoles about, suggesting that competition with other frogs excludes them from lower altitudes. Assuming multiple origins of direct development would require that the low-altitude hemiphractids evolved from low-altitude tadpole-bearers of which there is no current sign. But could it be that more recent changes in the South American environment changed the competitive regime for hemiphractids? Have the frog lineages that supposedly exclude them for lower altitudes been in the area for as long as the hemiphractids have? On the other hand, hemiphractids are unusual among direct-developing frog in that their embryos still develop some tadpole-like features (such as an incipient beak) only to lose them before emerging from the egg. Could this retention of ancestral features in an incipient form made it easier for them to re-establish at a later date?

The only living frog with mandibular teeth, Gastrotheca guentheri, copyright Biodiversity Institute, University of Kansas.

There is an evolutionary reversal among hemiphractids that seems more unequivocal, however: one species, Gastrotheca guentheri, is the only known frog in the modern fauna to have teeth in the lower jaw (Wiens 2011). There are a number of other frogs (including some other hemiphractids) in which the lower jaw has tooth-like serrations but G. guentheri is the only species with honest-to-goodness teeth. There seems little doubt that this is a true reversal; for G. guentheri to be the only living frog species to retain the ancestral state would require close to two dozen independent losses with no sign of the feature's retention elsewhere. In this case, while other frogs do not have teeth in the lower jaw, many of them do have teeth in the upper jaw (in some, such as Hemiphractus species, these upper teeth may be modified into prominent fangs for prey capture). So the genes for tooth development are still in place; presumably, G. guentheri has been able to re-develop its lower teeth through the genes for upper teeth being effectively re-deployed to take action elsewhere.

REFERENCES

Frost, D. R., T. Grant. J. N. Faivovich, R. H. Bain, A. Haas, C. F. B. Haddad, R. O. de Sá, A. Channing, M. Wilkinson, S. C. Donnellan, C. J. Raxworthy, J. A. Campbell, B. L. Blott., P. Moler, R. C. Drewes, R. A. Nussbaum, J. D. Lynch, D. M. Green & W. C. Wheeler. 2005. The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1–370.

Wiens, J. J. 2011. Re-evolution of lost mandibular teeth in frogs after more than 200 million yeatrs, and re-evaluating Dollo's Law. Evolution 65 (5): 1283–1296.

Wiens, J. J., C. A. Kuczynski, W. E. Duellman & T. W. Reeder. 2007. Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead? Evolution 61 (8): 1886–1899.

East Asian Forest Frogs

Black-striped frog Sylvirana nigrovittata, from here.

One group of animals that has somewhtat flown (or at least hopped) under the radar here at Catalogue of Organisms is the frogs. Frogs are perhaps one of the most instantly recognisable of all terrestrial animal groups, with a combination of features that is truly unique (see this post at an older iteration of Tetrapod Zoology for a list of some of their eccentricities—I mean, the things don't have a rib-cage. Maybe fish can get away with those sorts of shenannigans, but I expect any vertebrate crawling around on land to be fully skeletoned up, thank you.) Frogs come in a wide range of shapes and sizes, but perhaps the group most often thought of as the classic 'frogs' are the members of the family Ranidae. A large proportion of these mostly smooth-skinned, long-legged frogs were classified until recently in a single genus Rana. This was always seen as something of a generalised group, characterised as much by the absence of the derived features of other ranid genera such as the torrent-dwelling Amolops as by anything else. As such, it was long expected that more detailed studies of ranid relationships would lead to the Rana monolith being broken down somehow. In 1992, Alain Dubois presented a classification of the Ranidae in which he divided Rana between a number of subgenera, some of which were further divided into sections and species groups. This classification was presented by Dubois as explicitly provisional: the arrangement of taxa was based on overall similarities rather than any explicit analysis, and was largely intended to provide some sort of starting point for future analyses.

One of the new taxa recognised by Dubois (1992) was Sylvirana, which he erected as a new subgenus of Rana containing an assortment of species found in southern and eastern Asia. Members of this group had a foot with an external metatarsal tubercle, suction pads on digit III of the fore foot and digit IV of the hind foot but often not on fore digit I, and males with a humeral gland and internal or external subgular vocal sacs. Their tadpoles had long papillae along the edge of the lower lip, and often had dermal glands. As indicated by the name, species of Sylvirana were mostly found in forests.

Günther's frog Sylvirana guentheri, copyright Thomas Brown.

When the broad genus Rana was later carved up by Frost et al. (2006), they recognised Sylvirana as a separate genus (albeit without quite the same composition as Dubois' version). Since then, the status of Sylvirana has shifted around a bit; some authors have sunk it into a broader Old World tropical genus Hylarana on the grounds of non-monophyly. Oliver et al. (2015) conducted a molecular phylogenetic analysis of the Hylarana group that lead them to propose Sylvirana as the name for a clade of southeast Asian frogs that they recovered. A number of Indian species previously assigned to Sylvirana formed a separate clade that they recognised as a distinct genus Indosylvirana. Morphological differences between Sylvirana and Indosylvirana are slight, but males of the former have a larger humeral gland: three-quarters the length of the humerus vs two-thirds the length in Sylvirana. It's worth noting that, although Dubois (1992) recognised a number of ranid taxa as lacking a humeral gland, most if not all of them do indeed possess this gland, just not raised and readily visible externally as in Sylvirana.

The species of Sylvirana sensu Oliver et al. (2015) are generally medium-sized, robust frogs with a shagreenate back and smooth or slightly warty sides. They generally have a dark stripe along the side of the body, becoming broken into dark spots lower down. Widespread species include Sylvirana nigrovittata, commonly known as the black-striped frog (a completely non-distinct name, I have to say, considering that it could apply to any one of dozens of ranid species; Wikipedia calls it the sapgreen stream frog, which on the one hand is a much more distinctive name, but on the other hand suffers from the point that all the individuals I've seen photographed of this species look more brown than green). This species is found over pretty much the entire continental range of the genus, from eastern India and Nepal to Vietnam and Malaysia. Also widespread is Günther's frog S. guentheri, which is found in southern China, Taiwan and Indochina. This species is also found in Guam where it was first recorded in 2001 and has since become well-established (Christy et al. 2007). It is believed to have made its way there as a stowaway in shipments of aquaculture stock though, as it is itself captured for food in its native range, it is not impossible that it may have been introduced deliberately.

REFERENCES

Christy, M. T., J. A. Savidge & G. H. Rodda. 2007. Multiple pathways for invasion of anurans on a Pacific island. Diversity and Distributions 13: 598–607.

Dubois, A. 1992 Notes sur la classification des Ranidae (Amphibiens Anoures). Bulletin Mensuel de la Société Linnéenne de Lyon 61 (10): 305–352.

Frost, D. R., T. Grant, J. Faivovich, R. H. Bain, A. Haas, C. F. B. Haddad, R. O. de Sá, A. Channing, M. Wilkinson, S. C. Donnellan, C. J. Raxworthy, J. A. Campbell, B. L. Blotto, P. Moler, R. C. Drewes, R. A. Nussbaum, J. D. Lynch, D. M. Green & W. C. Wheeler. 2006. The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1–370.

Oliver, L. A., E. Prendini, F. Kraus & C. J. Raxworthy. 2015. Systematics and biogeography of the Hylarana frog (Anura: Ranidae) radiation across tropical Australasia, Southeast Asia, and Africa. Molecular Phylogenetics and Evolution 90: 176–192.

The Tuna-Lizards

The classic ichthyosaur Ichthyosaurus communis, from here.

Ichthyosaurs have long been one of the most famous examples of convergent evolution. These Mesozoic marine reptiles, as any textbook will tell you, evolved a body form similar to that of modern dolphins and sharks, and presumably held a similar niche as fast-swimming apex predators. But interesting as that might be, it's certainly not all there is to be said about ichthyosaurs.

The classic ichthyosaurs that said textbooks will usually depict are members of the clade Thunnosauria that first appeared in the upper Triassic (Thorne et al. 2011). Thunnosaurs differ from other ichthyosaurs in having a relatively short tail, shorter than the trunk, and hindfins that are much shorter than (usually less than half as long as) the forefins (Maisch & Matzke 2000). The name 'Thunnosauria' appropriately means 'tuna-lizards': as with modern tunas, the compact body of the thunnosaurs indicates greater specialisation for more powerful, tail-driven swimming.

Cast of the short-beaked Ichthyosaurus breviceps, from Charmouth Heritage Coast Centre.

In the Lower Jurassic, thunnosaurs are represented by the genera Ichthyosaurus and Stenopterygius, though the known fossil record for the former is earlier than that of the latter. Both genera are represented by hundreds (if not thousands in the case of Stenopterygius) of known specimens from Europe (Motani 2005): primarily England for Ichthyosaurus, Germany for Stenopterygius. Stenopterygius grew up to 4 m in length; Ichthyosaurus would have been somewhat smaller (Maisch & Matzke 2000). One species of Ichthyosaurus, I. breviceps, stands out for its particularly short and robust rostrum in comparison to other species. Another potential Lower Jurassic thunnosaur is Hauffiopteryx typicus, which also has a distinctively small rostrum, but in this case a particularly fine and slender one (Maisch 2008).

Mounted skeleton of Ophthalmosaurus icenicus, from the British Natural History Museum.

During the Lower Jurassic, the thunnosaurs were among a number of ichthyosaur lineages present. By the time of the Upper Jurassic, all surviving ichthyosaurs (with one possible exception*) belonged to a single thunnosaur lineage, the Ophthalmosauridae. Unfortunately, for most of the Middle Jurassic the ichthyosaur fossil record is missing, and a gap of more than ten million years separates Stenopterygius from Ophthalmosaurus. The only break in this gap is the Argentinan Chacaicosaurus cayi, which sits a few million years later than Stenopterygius. Intriguingly, Chacaicosaurus is not only intermediate in age, it is intermediate in morphology: while its skull is similar to that of Ophthalmosaurus, its forefin is more similar to that of Stenopterygius. As noted by Maisch & Matzke (2000), "It appears as if Chacaicosaurus cayi is one of the rare forms that are true structural intermediates".

*The possible exception is the Upper Jurassic Nannopterygius enthekiodon, some features of which suggest that it occupies a more basal Stenopterygius-grade position (Maisch & Matzke 2000). Unfortunately, it has not yet been adequately described and included in a formal phylogenetic analysis. This is rather frustrating: Nannopterygius promises to be a quite distinctive animal, with greatly reduced fins and long spinal processes on the anterior tail vertebrate.

Reconstruction of Platypterygius bannovkensis, by Olorotitan. Platypterygius was the latest surviving ichthyosaur genus.

The ophthalmosaurids survived from the late Middle Jurassic to the early Upper Cretaceous. Ophthalmosaurus had a slender rostrum with reduced dentition, while other genera such as Brachypterygius and Platypterygius had higher, more robust rostra with their full complement of teeth. Some ophthalmosaurids grew very large: Platypterygius reached up to 9 m. The name Ophthalmosaurus means 'eye lizard', and reference to the large eyes of this ichthyosaur seems to be de rigeur for any popular book in which it features, together with some speculation that it may have been a nocturnal hunter. However, a quick scan through the various ichthyosaur skulls illustrated by Maisch and Matzke (2000) indicates that ichthyosaur eyes were generally large. Those of Ophthalmosaurus were not the largest; the eyes of Eurhinosaurus longirostris are particularly ridiculous, with orbits filling almost the entire side of the cranium! So perhaps the question should not be why Ophthalmosaurus had large eyes, but why those ichthyosaurs without large eyes had reduced them.

REFERENCES

Maisch, M. W. 2008. Revision der Gattung Stenopterygius Jaekel, 1904 emend. von Huene, 1922 (Reptilia: Ichthyosauria) aus dem unteren Jura Westeuropas. Palaeodiversity 1: 227-271.

Maisch, M. W., & A. T. Matzke. 2000. The Ichthyosauria. Stuttgarter Beiträge zur Naturkunde Serie B (Geologie und Paläontologie) 298: 1-159.

Motani, R. 2005. True skull roof configuration of Ichthyosaurus and Stenopterygius and its implications. Journal of Vertebrate Paleontology 25 (2): 338-342.

Thorne, P. M., M. Ruta & M. J. Benton. 2011. Resetting the evolution of marine reptiles at the Triassic-Jurassic boundary. Proceedings of the National Academy of Sciences of the USA 108 (20): 8339-8344.

Tortoise Resurrection

In a subsequent portion of this narrative I shall have frequent occasion to mention this species of tortoise. It is found principally, as most of my readers may know, in the group of islands known as the Gallipagos... They are frequently found of an enormous size... They can exist without food for an almost incredible length of time, instances having been known wher they have been thrown into the hold of a vessel and lain two years without nourishment of any kind - being as fat, and, in every respect, in as good order at the expiration of that time as when they were first put in... They are excellent and highly nutritious food, and have, no doubt, been the means of preserving the lives of thousands of seamen employed in the whale-fishery and other pursuits in the Pacific.

--Edgar Allen Poe, The Narrative of Arthur Gordon Pym of Nantucket

For sailors in tropical oceans before the invention of refrigeration, keeping supplies of food was a serious issue. It was a permanent challenge to keep supplies fresh and edible, and indeed, much of the time stores failed at both. Under such conditions, the giant tortoises of the Galapagos islands and the Mascarenes and other islands in the Indian Ocean would have been seen as nothing short of miraculous. Tortoises could be captured easily and kept in the hold of a boat for extended periods without feeding, only slaughtered when they were actually required for eating. As a result, ships that were in a position to do so often took on tortoises in large number, and Charles Darwin apparently recorded single vessels taking up to 700 individuals at a time. By modern standards the idea of seven hundred starving tortoises crammed into a single hull seems unthinkably cruel, but doubtless the sailors who otherwise faced another six months of decomposing ship's biscuit saw things differently.


Geochelone becki, the Volcano Wolf tortoise. Photo by Joe Flanagan.

Unfortunately, such intense harvesting took an inevitable toll. Tortoise numbers declined rapidly, and many went extinct. Honneger (1981) lists three extinct species of tortoise from the Galapagos (including Geochelone abingdoni from Pinta island, which is technically not yet extinct but which only survives in the form of a single captive male) and at least six extinctions from the Seychelles and Mascarenes. Extinct populations on the Galapagos islands of Rabida and Santa Fe may have represented further undescribed species.

However, a paper published yesterday in the Proceedings of the National Academy of Sciences adds a remarkable coda to the history of one of the "extinct" species, the Floreana tortoise Geochelone elephantopus. Using DNA extracted from museum specimens collected on Floreana before the population disappeared, Poulakakis et al. (2008) have demonstrated that G. elephantopus may not be quite as extinct as previously thought. Instead, anomalous genetic haplotypes previously identified in some living individuals of Geochelone becki, a species found on the Volcano Wolf at the northern end of Isabela, the largest island in the Galapagos, indicate descent from G. elephantopus. These individuals would appear to be descendants of past hybridisations between native Volcano Wolf tortoises and introduced Floreana tortoises.

Such a situation is quite believable. As a result of the widespread transport of tortoises for food, many tortoises ended up on islands to which they were not native*. Tortoises were regularly imported to Réunion in the Mascarenes after the native population became extinct. Living populations of giant tortoises on the Granitic Islands of the Seychelles probably descend from imports from Aldabra rather than representing the species originally found there (Honegger, 1981). According to Poulakakis et al. (2008), some 40% of the Volcano Wolf tortoises tested showed evidence of Floreana ancestry, so the genetic legacy of Geochelone elephantopus is alive and well, at least in hybrid form.

*Potentially a serious issue for taxonomy, as researchers cannot assume that species names based on inadequate type material necessarily represent the species native to the island the type was collected on. Honegger (1981), for instance, cast doubt on whether Geochelone gouffei, known from a single specimen found on Farquhar Island in the Seychelles, actually originated there.

This still leaves a significant problem - most conservation policies do not cope well with hybrids. A number of species worldwide, such as the black stilt (Himantopus novaezelandiae) in New Zealand, are regarded as endangered because of the risk of hybridisation with related species. The red wolf (Canis rufus) and the Florida panther (Puma concolor coryi) represent two 'endangered' taxa in the United States for which the suggestion that their histories could have been compromised by hybridisation led to the suggestion that they should be abandoned as worthwhile conservation targets. However, the disappearance or decline of a species in its pure form due to hybridisation with another species is a different proposition from its decline due to replacement by that species. The genetic legacy of the declining species may still persist. Overemphasis on species "purity" may actually hinder the conservation of endangered taxa, especially if natural hybrid zones with related taxa exist in the first place (Allendorf et al., 2001). If there are no purebred Florida panthers, should that mean that there is no place for panthers in Florida?

REFERENCES

Allendorf, F. W., R. F. Leary, P. Spruell & J. K. Wenburg. 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology and Evolution 16 (11): 613-622.

Honegger, R. E. 1981. List of amphibians and reptiles either known or thought to have become extinct since 1600. Biological Conservation 19: 141-158.

Poulakakis, N., S. Glaberman, M. Russello, L. B. Beheregaray, C. Ciofi, J. R. Powell & A. Caccone. 2008. Historical DNA analysis reveals living descendants of an extinct species of Galápagos tortoise. Proceedings of the National Academy of Sciences of the USA 105 (40): 15464-15469.

Some History of the History of Tetrapods

Titanophoneus potens, a Permian synapsid (image from Kheper).

Benton, M. J. (ed.) 1988. The Phylogeny and Classification of the Tetrapods. The Systematics Association Special Volume 35A & 35B. Clarendon Press: Oxford.

One interesting thing about comparing different fields of research is the different time-scales we work in when it comes to what constitutes a "recent" publication. As an invertebrate taxonomist, I think nothing of delving into stuff that was written in the 1950s or even earlier. A developmental geneticist is likely to regard anything more than a few years old as ancient history. Vertebrate palaeontology lies between these two extremes, but certainly 1988 was a long time ago for the tetrapods.

As a result, I suspect that Phylogeny and Classification of the Tetrapods can't really tell us much about the current state of tetrapod classification. What does make it interesting, though, is what it says about the state of vertebrate palaeontology at the time. The late 1980s were certainly interesting times, not just in vertebrate palaeontology but in systematics in general. The cladistic revolution was gathering speed. Molecular phylogeny was making its first faltering steps, and challenging a few orthodoxies.

The Phylogeny and Classification of the Tetrapods was published in two volumes, and even that says something about changes in focus since. The second volume was devoted entirely to the mammals (about 5,400 living species). Everything else - amphibians, reptiles, birds, about 24,000 living species - took up only the first volume. Birds in particular warrant a single chapter, as do living amphibians (that latter point possibly hasn't changed much). Dinosaurs (the non-birdy type, that is) barely rate a mention. The dinosaur renaissance was in its early stages at the time - for comparison, Bakker's The Dinosaur Heresies, a book I personally don't think much of but which became something of a focal point for changing views on the big lizards, was first published in 1986. (It was also in 1988 that Gregory S. Paul's Predatory Dinosaurs of the World first hit the shelves, in which Paul copped a certain degree of ridicule for his decidedly heterodox reconstructions of dinosaurs covered in feathers - Paul has since, of course, been able to carry around a big bag of harsh words and force his critics on this point to eat them.) Of course, it should be noted that despite its palaeontological bent, ultimately the main focus of Phylogeny and Classification of the Tetrapods is on the relationships between living tetrapods.

Despite all that has changed since then, some parts of Phylogeny and Classification of the Tetrapods seem somewhat prescient. Not so much the molecular chapters - that on molecular phylogenetics of tetrapods as a whole has the grim figure of the Haematothermia clade (birds and mammals to the exclusion of reptiles) rear its ugly head, though the authors at least had the sense to recognise this as probably convergence rather than the actual state of affairs. But the mammalian molecular phylogeny chapter gives us some of the early glimmerings of the Afrotheria hypothesis, though that clade was not to be formally recognised until some years later, while the Novacek et al. chapter on the morphological phylogeny of modern mammalian orders is noteworthy for not finding any support for Ungulata.

The prize for best statement in the book, however, has to go to Gaffney & Meylan's chapter on turtles, where, after a description of the apomorphies connecting turtles to their supposed nearest relatives (the captorhinids, in this case), the authors note "And so we reach God's noblest creature - the turtle".

Palaeos page on Stenocybus

A new page is up for critique at Palaeos on the basal dinocephalian Stenocybus acidentatus.

Relict Frog Sex

At least one piece of genetics that almost everyone is familiar with is how our sex is determined - that women possess two X chromosomes while men produce an X and a Y chromosome. What may not be so familiar to most people is that this system is far from universal. Different animals exhibit a wide range of methods of sex determination, both genetic (like our own system) and environmental (such as temperature in crocodiles). In Hymenoptera (ants, bees and wasps) unfertilised eggs produce haploid males, while fertilised eggs produce diploid females. In birds, it is the females that possess two different forms of sex chromosomes (referred to as W and Z), while the male possesses two Z chromosomes. But perhaps the oddest little tale of sex determination (and one I only discovered recently) involves the strange relictual frog genus Leiopelma (the species Leiopelma archeyi is shown in a photo from the page of Dr. Bruce Waldman).

Leiopelma is a small genus of four living species of frog restricted to New Zealand (a further three species are known from sub-fossil remains - Bell et al., 1998). They represent a basal grade of frogs of which the only other member is the "tailed frog" Ascaphus truei from western North America (different studies disagree as to whether Leiopelma and Ascaphus form the sister clade to or are paraphyletic to all other living frogs - Green & Cannatella, 1993; Hay et al., 1995). Leiopelma and Ascaphus retain a number of primitive features that have been lost in other frogs, such nine vertebrae in front of the sacrum and tail-wagging muscles (though the 'tail' of male Ascaphus is actually the copulatory organ). Leiopelma also lack a tadpole stage in their life-cycle, hatching straight out into froglets.

The really remarkable thing about Leiopelma, though, is that of the four species living today, at least three have different methods of sex determination from each other. And within two of those species, there are even different populations that differ in their mode of sex determination!

The most primitive state is perhaps that shown by Leiopelma archeyi, in which most populations don't have distinguishable sex chromosomes. This is the condition in most amphibians, though it has been shown that even in taxa that don't have heteromorphic chromosomes, sex is still determined genetically (Hayes, 1998). However, a heteromorphic W sex chromosome has been recorded in one population of L. archeyi from Whareorino in the King Country (Green, 2002). In other features (including genetic features) the Whareorino L. archeyi are almost indistinguishable from Coromandel populations that lack the W chromosome.

The Whareorino Leiopelma archeyi are therefore more like L. pakeka in sex differentiation. Leiopelma pakeka also has a female-ZW/male-ZZ set-up (Green, 1988)*. There is only a single population of L. pakeka, restricted to Maud Island, which diesn't give much scope for variation.

*The species Leiopelma pakeka was recognised only recently (Bell et al., 1998). Previously it had been regarded as a population of the genetically distinct but morphologically almost identical L. hamiltoni, and its genetic structure was described under the latter name. Leiopelma hamiltoni proper is uber-rare, with a population of less than 300 individuals restricted to less than one hectare of habitat on Stephens Island, and does not seem to have yet been investigated for sex chromosomes.

The ultimate wierdness, however, comes when we look at Leiopelma hochstetteri. Most populations of L. hochstetteri have a single sex chromosome in females, while males lack a sex chromosome. This female-0W/male-00 system is unique - no other animal has it. Not one. In fact, it's so bizarre that not even all L. hochstetteri have it - females of the population on Great Barrier Island lack the lonely W chromosome, and like Coromandel L. archeyi this population does not have morphologically distinct sex chromosomes (Green, 1994). The Great Barrier population also lacks the non-sex-related supernumerary chromosomes (or "B" chromosomes) found in other populations (Green et al., 1993). B chromosomes are small, seemingly dispensable chromosomes that are found in a broad scattering of taxa. In species where they are found, numbers of B chromosomes can vary significantly within and between populations, probably because their lack of significant function means a lack of selective control on their propagation. This variation is also seen in L. hochstetteri, where up to 15 B chromosomes were found in individuals of five different populations. The variation in chromosomes between populations is shown below in a figure from Green (1994).



So how did all this come about? I am not aware of any other group of closely-related organisms showing this much variation in so few species. However, it is possible to imagine ZW chromosomes evolving through differentiation of morphologically indistinct sex-determining chromosomes, and this is what appears to have occurred in Leiopelma pakeka and Whareorino L. archeyi. Leiopelma hamiltoni appears to be more closely related to L. archeyi than L. pakeka (Bell et al., 1998), so it would be very interesting to know whether or not it has distinct sex chromosomes.

As for Leiopelma hochstetteri, the sister taxon to all other Leiopelma, phylogenetic analysis of chromosome characters shows that the Great Barrier population, without the extra W chromosome, is probably sister to all other populations. Green et al. (1993) suggest that the 0W/00 system could evolved from a ZW/ZZ system. Either the Z chromosome may have been lost, or (as the authors of the latter study think more likely) it could have been duplicated, giving a ZZW/ZZ pattern that would be karyotypically indistinguishable from 0W/00.

REFERENCES

Bell, B. D., C. H. Daugherty & J. M. Hay. 1998. Leiopelma pakeka, n. sp. (Anura: Leiopelmatidae), a cryptic species of frog from Maud Island, New Zealand, and a reassessment of the conservation status of L. hamiltoni from Stephens Island. Journal of the Royal Society of New Zealand 28 (1): 39-54.

Green, D. M. 1988. Heteromorphic sex chromosomes in the rare and primitive frog Leiopelma hamiltoni from New Zealand. Journal of Heredity 79 (3): 165-169.

Green, D. M. 1994. Genetic and cytogenetic diversity in Hochstetter's frog, Leiopelma hochstetteri, and its importance for conservation management. New Zealand Journal of Zoology 21: 417-424.

Green, D. M. 2002. Chromosome polymorphism in Archey's frog (Leiopelma archeyi) from New Zealand. Copeia 2002 (1): 204-207.

Green, D. M., & D. C. Cannatella. 1993. Phylogenetic significance of the amphicoelous frogs, Ascaphidae and Leiopelmatidae. Ecol. Ethol. Evol. 5: 233-245.

Green, D. M., C. W. Zeyl & T. F. Sharbel. 1993. The evolution of hypervariable sex and supernumerary (B) chromosomes in the relict New Zealand frog, Leiopelma hochstetteri. Journal of Evolutionary Biology 6 (3): 417-441.

Hay, J. M., I. Ruvinsky, S. B. Hedges & L. R. Maxson. 1995. Phylogenetic relationships of amphibian families inferred from DNA sequences of mitochondrial 12S and 16S ribosomal RNA genes. Molecular Biology and Evolution 12 (5): 928-937.

Hayes, T. B. 1998. Sex determination and primary sex differentiation in amphibians: Genetic and developmental mechanisms. Journal of Experimental Zoology 281 (5): 373-399.

Sooglossidae: Deja vu all over again

Every couple of weeks or so I go into the Western Australian Museum library to look over the new journals and see if anything interesting has come out that I've missed. I did so this morning, and among the papers I noticed was van der Meijden et al. (2007) in the Biological Journal of the Linnean Society which established a new genus Leptosooglossus for the frog species previously known as Sooglossus gardineri from the Seychelles (shown above in an adorable image from the Nature Protection Trust of the Seychelles). A second species, Sooglossus pipilodryas, was also transferred into the new genus.

This was all well and good, until a few journals later I came across Nussbaum & Wu (2007) in Zoological Studies which established a new genus Sechellophryne for the frog species previously known as - yep, you know what's coming - Sooglossus gardineri (again, So. pipilodryas was also transferred). Oh dear. Two papers, published very close together in time, coining different names for the same thing.

Before anyone madly leaps to any suspicions, I can't find any obvious signs of plagiarism or claim-jumping in either paper. Both recognised the new genus on the basis of paraphyly of the genus Sooglossus, but van der Meijden et al. only used molecular data, while Nussbaum & Wu only used morphological data. It does seem somewhat incredible that there could be two separate groups of people both working on as small a group as Sooglossidae (only four species restricted to the Seychelles, a small group of islands in the Indian Ocean roughly the size of a postage stamp) and unaware of each other, but I can't find any obvious indications otherwise (if there is any sort of scandal, I'm chucking in a vote that it be referred to as 'Bubblegate'). It is good that the two papers using completely different methods agree so much in their results.

So the next question becomes - which is the correct name to use? The van der Meijden et al. paper was in the July issue of the journal it appeared in, while Nussbaum & Wu appeared in a May issue. So the first round would appear to favour Sechellophryne over Leptosooglossus. However, the cover date of a journal issue is not necessarily identical to the actual print release date, which is what is supposed to determine priority. The online release date for van der Meijden et al. (which may not be identical to the print release date, but is usually at least an indication) is given as 5th July at the journal website. Unfortunately, the website for Zoological Studies doesn't appear to list specific release dates, and there doesn't appear to be one on the paper. If anyone out there in the know is able to confirm the release date for me, I would be quite grateful (it suddenly occurs to me that I should have looked inside the cover or on the table of contents or such of the journal itself, but I'm no longer at the museum and can't do that now - d'oh!). Again, at the moment Sechellophryne appears to be the senior name unless proven otherwise.

Oh, and if you're wondering why Bubblegate, it's a reference to one of my partner's current favourite jokes (warning - PG rating):

Three frogs are brought before the court. As the first frog is taken to the stand, the judge asks the bailiff for his name and crime, to which the bailiff replies, "This is Frog, and his crime is blowing bubbles in the pond". The second frog is taken in, and again the judge asks for his name and crime. The bailiff replies, "This is Frog-Frog, and his crime is blowing bubbles in the pond". The third frog is then brought in, and the judge asks, "I suppose this is Frog-Frog-Frog?" "No," replies the bailiff, "this is Bubbles".

REFERENCES

Meijden, A. van der, R. Boistel, J. Gerlach, A. Ohler, M. Vences & A. Meyer. 2007. Molecular phylogenetic evidence for paraphyly of the genus Sooglossus, with the description of a new genus of Seychellean frogs. Biological Journal of the Linnean Society 91: 347-359.

Nussbaum, R. A., & S.-H. Wu. 2007. Morphological assessments and phylogenetic relationships of the Seychellean frogs of the family Sooglossidae (Amphibia: Anura). Zoological Studies 46 (3): 322-335.

Taxon of the Week #3: Rana

The taxon that has been chosen to receive the coveted Taxon of the Week spot today is the frog genus Rana. Rana is a large primarily Holarctic genus of frogs, and probably the inspiration for most depictions of frogs in the world (see the page on Wikipedia and linked pages for images). Well-known species are the edible frog (Rana × esculenta - actually not a true species but a hybrid) and the European common frog (Rana temporaria).

I thought I'd look up the info on Rana over lunchtime. Pretty soon, my head was swimming. The genus Rana has been hit with two major investigations in recent years, both of which have received some frosty responses. Frost et al. (2006) in their investigation of the 'Amphibian Tree of Life' divided Rana between more than fifteen smaller genera to remove its previous paraphyly (for instance, the above-mentioned Rana esculenta would become Pelophylax esculentus). As happens with any wholesale name change, there has been quite a bit of outcry at the idea of having to update the filing systems. Also, a number of authors have felt that the number of taxa sampled by Frost et al. was not enough to inspire confidence in their results. The review by Wiens (2007) was particularly vitriolic - the scientific equivalent of attempting to hold the subject down and kick them repeatedly in the teeth. Smith and Chiszar (2006) have suggested the more mollifying approach of treating Frost et al.'s various genera as subgenera, though unless one was willing to accept a paraphyletic genus this would also require sinking some well-established genera such as Staurois within Rana. Division of the genus Rana was also supported by Che et al. (2007).

The other cause of debate was perpetrated by Hillis & Wilcox (2005), who investigated the phylogeny of New World species of 'Rana' (most of which would belong to Lithobates in the Frost et al. system). The problem came when Hillis & Wilcox suggested a whole series of subgeneric taxa for nested groups of species that they defined according to the rules of the PhyloCode, but also allowed for use under the ICZN as subgenera. Debate promptly exploded about whether Hillis & Wilcox's names were validly published and usable (Dubois, 2006, 2007; Hillis, 2007). Compared to this argument, Frost et al.'s division appears quite simple. I may return to this in a later post, if my brain doesn't implode first. Check out the Dubois (2006) paper in particular - Dubois thinks that the answer to our problems is to make the ICZN more complicated. No. Thank. You.

REFERENCES

Che, J., J. Pang, H. Zhao, G.-F. Wu, E.-M. Zhao & Y.-P. Zhang. 2007. Phylogeny of Raninae (Anura: Ranidae) inferred from mitochondrial and nuclear sequences. Molecular Phylogenetics and Evolution 43 (1): 1-13.

Dubois, A. 2006. New proposals for naming lower-ranked taxa within the frame of the International Code of Zoological Nomenclature. Comptes Rendus Biologies 329 (10): 823-840.

Dubois, A. 2007. Naming taxa from cladograms: A cautionary tale. Molecular Phylogenetics and Evolution 42 (2): 317-330.

Frost, D. R., T. Grant, J. Faivovich, R. H. Bain, A. Haas, C. F. B. Haddad, R. O. de Sá, A. Channing, M. Wilkinson, S. C. Donnellan, C. J. Raxworthy, J. A. Campbell, B. L. Blotto, P. Moler, R. C. Drewes, R. A. Nussbaum, J. D. Lynch, D. M. Green & W. C. Wheeler. 2007. The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1-370.

Hillis, D. M. 2007. Constraints in naming parts of the Tree of Life. Molecular Phylogenetics and Evolution 42 (2): 331-338.

Hillis, D. M., & T. P. Wilcox. 2005. Phylogeny of the New World true frogs (Rana). Molecular Phylogenetics and Evolution 34 (2): 299-314.

Smith, H. M., & D. Chiszar. 2006. Dilemma of name-recognition: why and when to use new combinations of scientific names. Herpetological Conservation and Biology 1 (1): 6-8.

Wiens, J. J. 2007. Review: The Amphibian Tree of Life. Quarterly Review of Biology 82: 55-56.