The different groups of Lissamphibia – Part 1

The different groups of Lissamphibia – Part 1

As exposed in the previous article, lissamphibians, or modern amphibians, is a monophyletic clade including four groups: Albanerpetontidae, Apoda, Salientita, and Urodela. Let have a focus on the two least known: the mysterious apods and the cute albanerpetontids!

I)              Albanerpetontidae

Figure 1: Representation of an albanerpetontid (credits: nix).

Probably the least known clade among lissamphibians, mostly because it is extinct (and therefore not truly “modern”), but also because its position within Lissamphibia or as a sister-group is still open to debate (Matsumoto and Evans, 2018). Albanerpetontids constitute a small group of amphibians, salamander-like forms, that occurred from the Middle Jurassic to the Late Pliocene (Gardner et al., 2003; Venczel and Gardner, 2005; Delfino and Sala, 2007).

Albanerpetontid are found either in vertebrate microfossil assemblage, in fissure fills, or in floodplain deposits. The fossil record is mostly located in Laurasia, the supercontinent grouping North America, Europe, an Asia, although one occurrence is from the Early Cretaceous of Morocco. Up to date, 5 genera and 13 species have been described, and more material has been attributed to undetermined genera or species. However, some of these descriptions may require a revision, since the phylogeny of this group retains some issues.

Figure 2: Cladogram of Albanerpetontidae, with their time and geographical range.

One of the major problems with albanerpetontid lies in their material mostly biased toward fragmented and isolated elements. However, despite this issue, Albanerpetontids are characterized by a small set of synapomorphies easily recognizable:

1.     the fused and dorsally ornamented frontal;

2.     the “mortise and tenon” interdentary joint, where right and jaw dentary symphysis bear an interdigitating joint;

3.     the amniote-like atlas-axis complex involving a tripartite facet;

4.     the chisel-shaped, non-pedicellate, tricuspid teeth.

Very few complete specimens are available (McGowan and Evans, 1995), which befog their identification and study for systematics, especially in the Mesozoic period. Indeed, as it can be hard to recognize, the post-cranial skeleton bears very few characteristics and it is not included in systematics analyses. Furthermore, fused frontals are not only a synapomorphy of the group, but they can also be used as diagnostic features to segregate the different species.

Figure 3: Frontals from different genera of albanerpetontids (from Matsumoto and Evans, 2018)

Their morphology would suggest their fossorial ecology (Estes and Hoffstetter, 1976). They supposedly lived in humid soil near freshwater ponds, where the skull would be used as a ram or a shovel, feeding on arthropods with tough chitinous shell (Wiechmann, 2000), thanks to the shearing bite allowed by their dentition (Gardner, 2001).

However, albanerpetontids constitute one major group of microvertebrates from the Late Jurassic of Portugal. Indeed, they represent one of the most abundant taxa in Guimarota mine, with thousands of remains recovered, but hundreds have also been found in the Lourinhã Formation (Wiechmann, 2003; Guillaume et al., 2019), and they are now under description.

II)            Apoda

Figure 4: Representation of an apod (credits: Manimalworld).

Another poorly known amphibian clade outside herpetology. They are a small group of vermiform animals that occurred in the Early Jurassic. One of their difficulties lies in the scarcity of their fossil record, especially for the Mesozoic period (Jenkins and Walsh, 1993; Evans and Sigogneau‐Russell, 2001; Jenkins et al., 2007). The known species fit poorly within the modern clades, which require the use of molecular data to understand their evolutionary pattern (Roelants et al., 2007; Zhang and Wake, 2009; Wilkinson et al., 2011; Schoch, 2014).

Figure 5: Cladogram of Apoda, with the occurrence of some noticeable fossil species.

Due to their highly specialize morphology, apods share a unique set of synapomorphies:

1.     the trunk greatly elongated, exhibiting an increase of presacral vertebrae, ranging from 95 to 285;

2.     as a consequence, and as other vertebrates with similar adaptation, lungs are asymmetric, the right one being the larger;

3.     the skin is segmented with primary and secondary rings, the former correlating with myosepta;

4.     male individuals display a phallodeum, an unpaired, intromittent organ formed by a projected portion of the cloaca;

5.     the absence of limbs and girdles in all extant and extinct species, with the unique exception of Eocaecilia, the most basal taxon;

6.     the short tail skeleton, which can be even lost in some species;

7.     the presence of a massive skull, weakly fenestrate or entirely closed, with solid fusion of the different bones;

8.     as a consequence, eyes are largely reduced, or can even be covered by dermal bones in some species;

9.     the presence of a tentacular organ between the eye and the nose, used a chemosensory.

The extant groups have a tropical distribution, and molecular analyses suggest their dispersal road may be linked to the breaking of Gondwana during the Cretaceous (Zhang and Wake, 2009). However, the early radiation should have occurred before the breaking of Pangea (Roelants et al., 2007; Wilkinson et al., 2011). As reflected by their skull morphology, they are fossorial and nocturnal animals. They live mostly in the topsoil layers and occupy a full range of environment: decaying plant material, humus, wet mud of riverbanks, or fully aquatic habitats. They usually feed on earthworms and arthropods (beetles and termites), but the biggest species can also prey on lizards, snakes, and even small birds!

Figure 6: Geographic distribution of extant apods.

Nowadays, no apods are living in Portugal and unfortunately, none have been found in the fossil record neither. However, if we are not focusing on them in Lourinhã, it does not mean they should be forgotten! We still have a lot to learn about them, especially since recent studies may suggest a different path in their evolution (Pardo et al., 2017), and we will go back on this when we talk on the origin of Lissamphibia.

Next time, we will see the Batrachia, the clade that groups both Salientia and Urodela, the best-known amphibians. Until then, stay home and be safe!

Bibliography

Delfino, M., and B. Sala. 2007. Late Pliocene Albanerpetontidae (Lissamphibia) from Italy. Journal of Vertebrate Paleontology 27:716–719.

Estes, R., and R. Hoffstetter. 1976. Les Urodèles du Miocène de La Grive-Saint-Alban (Isère, France). Bulletin Du Muséum National d’Histoire Naturelle, 3e Série 398:297–343.

Evans, S. E., and D. Sigogneau‐Russell. 2001. A stem-group caecilian (Lissamphibia: Gymnophiona) from the Lower Cretaceous of North Africa. Palaeontology 44:259–273.

Gardner, J., S. Evans, and D. Sigogneau-Russel. 2003. New albanerpetontid amphibians from the Early Cretaceous of Morocco and Middle Jurassic of England. Acta Paleontologica Polonica 48:301–319.

Gardner, J. D. 2001. Monophyly and affinities of albanerpetontid amphibians (Temnospondyli; Lissamphibia). Zoological Journal of the Linnean Society 131:309–352.

Guillaume, A. R. D., M. Moreno-Azanza, and O. Mateus. 2019. New lissamphibian material from the Lourinhã Formation (Late Jurassic, Portugal). Abstract of Papers Society of Vertebrate Paleontology 79th Annual Meeting 112.

Jenkins, F. A., D. M. Walsh, and R. L. Carroll. 2007. Anatomy of Eocaecilia micropodia, a limbed caecilian of the Early Jurassic. Bulletin of the Museum of Comparative Zoology 158:285–365.

Jenkins, P. A., and D. M. Walsh. 1993. An Early Jurassic caecilian with limbs. Nature 365:246–250.

Matsumoto, R., and S. E. Evans. 2018. The first record of albanerpetontid amphibians (Amphibia: Albanerpetontidae) from East Asia. PloS One 13:e0189767.

McGowan, G., and S. Evans. 1995. Albanerpetontid amphibians from the Cretaceous of Spain. Nature 373:143–145.

Pardo, J. D., B. J. Small, and A. K. Huttenlocker. 2017. Stem caecilian from the Triassic of Colorado sheds light on the origins of Lissamphibia. Proceedings of the National Academy of Sciences 114:E5389–E5395.

Roelants, K., D. J. Gower, M. Wilkinson, S. P. Loader, S. D. Biju, K. Guillaume, L. Moriau, and F. Bossuyt. 2007. Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences 104:887–892.

Schoch, R. R. 2014. Amphibian Evolution: The Life of Early Land Vertebrates. John Wiley & Sons, Oxford, 276 pp.

Venczel, M., and J. D. Gardner. 2005. The geologically youngest albanerpetontid amphibian, from the lower Pliocene of Hungary. Palaeontology 48:1273–1300.

Wiechmann, M. F. 2000. The albanerpetontids from the Guimarota mine; pp. 51–54 in Guimarota: a Jurassic ecosystem. Verlag Dr. Friedrich Pfeil, Munich.

Wiechmann, M. F. 2003. Albanerpetontidae (Lissamphibia) aus dem Mesozoikum der Iberischen Halbinsel und dem Neogen von Süddeutschland. Doctoral dissertation, Freie Universität Berlin, Berlin pp.

Wilkinson, M., D. San Mauro, E. Sherratt, and D. J. Gower. 2011. A nine-family classification of caecilians (Amphibia: Gymnophiona). Zootaxa 2874:41–64.

Zhang, P., and M. H. Wake. 2009. A mitogenomic perspective on the phylogeny and biogeography of living caecilians (Amphibia: Gymnophiona). Molecular Phylogenetics and Evolution 53:479–491.

Introduction to modern amphibians

Introduction to modern amphibians

Let’s talk about amphibians! When it comes to those cute, little animals, living both in water and on land, everyone has in mind the small frogs and salamanders that dwell in ponds and rivers. One can also consider the newts or the unique axolotl, an animal keeping a neotenic form. Few would include those limbless worm-like animals, the caecilians. However, if identifying amphibians may seem trivial nowadays, because of their peculiar characteristics, such as their ontogeny, the actual term “Amphibia” appears to be quite loose in systematics.

Here is the first article of a series that will present you the coolest vertebrates and all the problematic brought by this group.

Figure 1: Some example of modern amphibians. Clockwise, a South American caecilian, a fire salamander, Paedophryne amauensis (the smallest vertebrate known), a common reed frog, a Pacific newt, and an axolotl.

I)              An obscure definition for a mysterious clade: problematic in taxonomy.

First, we need to understand what an amphibian is. Amphibia comes from the Greek ἀμφίβιος (amphíbios), which “both kinds of life” or “living on both sides”. For a long time, it was used to describe animals that could reside at once in water and on land. However, taxonomic problems quickly rose with this wide application. On the one hand, it appeared that modern “amphibians” were closely related together than with any tetrapod group, forming a clade then named Lissamphibia. And on the other hand, more and more fossil taxa were identified as “amphibians”, the term referring then to any non-amniote tetrapod.

In other words, Amphibia became, sensu lato, a paraphyletic grade, including Lissamphibia, but also temnospondyls, lepospondyls, and all the stem-tetrapod taxa (which illustrate the transition from water to land, such as Ichthyostega or Acanthostega). Since then, biologists and paleontologists are not agreeing on what should be called “Amphibia”. Nonetheless, common ground can be found.

Figure 2: Evolution of Amphibia taxonomy. On top, the old-fashion way, where Amphibia (dark purple) was referring to all animals living both in water and on land, and can be used in ecological context (=amphibious). On bottom, the necessity to respect taxonomy and splits the groups of stem-tetrapods (blue) and stem-amniotes (red), and where Amphibia is synonymous of Batrachomorpha, the most inclusive clade containing Lissamphibia (light purple) and their stem-taxa. Modified from Benton, 2014.

From an ecological point of view, it is still acceptable to refer to “amphibians” for animals sharing this unique way of life. However, it would require distinguishing stem-tetrapods, stem-lissamphibians, and stem-amniotes. Also, since they are not the only vertebrates to have adopted the environment of the land-water interface through Evolution (nowadays, seals and crocodiles illustrate such adaptations), some authors would rather refer to them as “amphibious taxa” (van der Valk, 2012).

And from a systematic point of view, Amphibia would now be defined to include lissamphibians and their stem-groups, which would make it synonymous of Batrachomorpha. On the same note, Lissamphibia will then be comprised by all modern taxa and their stem relatives, namely Apoda (the caecilians), Salientita (frogs), and Urodela (salamanders and newts). Some authors argue that the extinct Albanerpetontidae would also be part of Lissamphibia.

II)            An overview of Lissamphibia.

Lissamphibians are represented today by over 8,000 species (AmphibiaWeb, 2020), with a worldwide distribution with the exception of Antarctica. Although the biggest diversity is observed in tropical regions, some species extant up to the North Pole and down to Tierra del Fuego, the meridional-most point of South America. Among the most common features shared by lissamphibians are the four digits or double occipital condyles, but those characteristics are also found in non-lissamphibian fossils.

Nonetheless, molecular analysis strongly supported both the group’s monophyly and its position as sister-group of amniotes. On top of that, lissamphibians shared a set of physiological, ecological and osteological autapomorphies:

1.     they are ectotherm animals, which means they rely mostly on environment to control the heat of their temperature;

2.     their skin is rich in glands with a thin stratum corneum (the outermost layer of epidermis);

3.     their eyes are covered by an eyelid;

4.     they have a tricameral heart, with three chambers: two atria and one ventricle;

5.     their ontogeny involves a larval stage with external gills going through metamorphosis, and therefore a biphasic life-cycle;

6.     their skeleton is poorly ossified, either because of loss, reduction or fusion of the bones, notably in the skull;

7.     their gonads have large fat bodies, used as an extra source of energy;

8.     their teeth are bicuspid, usually with attached to the inner jaw (pleurodonty), where the crown and the root are not fused but connected by fibrous poorly mineralized tissue (pedicelly), giving flexibility;

9.     they have a canalis perioticus, a channel that connects the perilymphatic sac and the perilymphatic cistern in the inner ear

10.  they have a papilla amphibiorum, which is the second sense receptor in the inner ear and works within 600 to 1000 Hz range;

11.  the radius and the ulna articulate with a single enlarged, ossified structure on the humerus (radial condyle).

Figure 3: Pedicellate teeth, as represented by the three modern amphibian orders. A, the salamander Amphiuma means. B, the caecilian Gymnopis mexicanus. C, the frog Rana occipitalis. D, the leptodactylid frog Calyptocephalus gayi. From Carroll, 2009.

Among additional features, can be noted the intermaxillary glands, the short ribs and the palatal opening between the pterygoid and the parasphenoid, but those also occurred in other Paleozoic taxa, such as temnospondyls.

Next time, we’ll see the different groups that constitute Lissamphibia.

Bibliography and recommended sources

AmphibiaWeb. 2020. Browse by Family. AmphibiaWeb. Available at http://amphibiaweb.org:8000/lists/index.shtml. Accessed March 24, 2020.

Benton, M. J. 2014. Vertebrate Palaeontology, 4th ed. John Wiley & Sons, Chichester, 480 pp.

Carroll, R. L. 2009. The Rise of Amphibians: 365 Million Years of Evolution. Johns Hopkins University Press, Baltimore, MD, 544 pp.

Schoch, R. R. 2014. Amphibian Evolution: The Life of Early Land Vertebrates. John Wiley & Sons, Oxford, 276 pp.

van der Valk, A. 2012. The Biology of Freshwater Wetlands, 2nd ed. Oxford University Press, New York City, NY, 296 pp.