BRANCHIOSAURIDAE (Boy & Sues, 2000)

Carroll, Robert L., 2007, The Palaeozoic Ancestry of Salamanders, Frogs and Caecilians, Zoological Journal of the Linnean Society 150, pp. 1-140 : 79-93

THE BRANCHIOSAURIDAE

Among which late Palaeozoic and early Mesozoic tetrapods can the largest number of these features be recognized?

Prior to the Middle Jurassic, we still lack fossils of any taxa that exhibit derived characters that are uniquely homologous with those of extant adult salamanders. However, thousands of specimens are known from the Upper Carboniferous and Lower Permian that resemble the larvae of modern urodeles. As primitive members of all extant salamander families have extensive periods of larval development, and several families are entirely neotenic, knowledge of early development among Palaeozoic amphibians is clearly of great importance in establishing their ancestry. In this regard, it is ironic that Laurin & Reisz (1997) specifically excluded evidence from larval stages in their attempt to establish the relationships of the modern amphibian groups.

Fortunately, the conditions of deposition during the Late Carboniferous and Early Permian favoured the preservation of early developmental stages of amphibians in a great number of lake deposits in Germany, France, the Czech Republic, and the UK, as well as at Mazon Creek in the USA ( Milner, 1980, 1982; Shabica & Hay, 1997; Boy & Sues, 2000; Schoch & Milner, 2005). Both major groups of Permo-Carboniferous amphibians are represented. We will look first at the lepospondyls. Tiny juveniles (as small as 2 cm in skull–trunk length and with centra length less than 1 mm) of all major groups of lepospondyls are known ( Carroll, 2000a; Anderson, 2002, 2003). Specimens of tiny aïstopods, adelogyrinids, lysorophids, microsaurs, and nectrideans resemble one another in precocial ossification of their vertebral centra as complete cylinders ( Fig. 51 ). This mode of development is derived relative to that of the most primitive salamanders (e.g. the extant hynobiids Ranodon tsinpaensis , Ranodon sibericus , and Hynobius maculosus ) ( Boisvert, 2002; C. A. Boisvert, 2004) and a primitive Jurassic salamander ( Fig. 48A ), in which the arches ossify prior to the centra. Aïstopods, adelogyrinids, and lysorophids are particularly improbable sister taxa of salamanders, as their girdle and limbs are either completely absent or highly reduced, and the vertebral column is greatly elongated. Microsaurs and nectrideans have relatively normal limbs, but no specific synapomorphies with either frogs or salamanders.

Another distinctive feature of juvenile lepospondyls is that they lack evidence of external gills, although many are found in the same deposits as larval labyrinthodonts, in many specimens of which conspicuous external gills are preserved ( Milner, 1980; Boy & Sues, 2000). It is because of the presence of external gills that larval labyrinthodonts have long been referred to as branchiosaurs. However, these gilled larvae clearly belong to two divergent clades, the temnospondyls and the discosauriscid anthracosauroids. These groups are distinguished by many features of their adult anatomy, including the dominance of intercentra and the presence of a four-toed manus in the temnospondyls vs. dominance of pleurocentra and a five-toed manus in the anthracosauroids ( Boy & Sues, 2000). Both of these features preclude the close affinities of anthracosauroids and modern amphibians.

Among the temnospondyls, many larvae can be identified as representing early growth stages of previously recognized Palaeozoic amphibians that share few, if any, characters suggestive of salamanders. On the other hand, other larvae belong to distinct taxa that cannot be associated with particular adult labyrinthodonts, and metamorphose only very late, or not at all. These are grouped in two families, the Micromelerpetontidae and the Branchiosauridae ( Fig. 52 ), belonging to the superfamily Dissorophoidea ( Boy & Sues, 2000; Schoch, 1992, 2004; Schoch & Milner, 2005). Larvae of the Branchiosauridae , of which Apateon is the best known example, share a great many aspects of their development, especially that of the skull and hyoid apparatus, with modern salamanders ( Schoch & Carroll, 2003).

The skull

Cranial development among Palaeozoic amphibians follows two distinct patterns. The vast majority, including most labyrinthodonts and lepospondyls as well as their sister taxa among Upper Devonian fish, ossify all the dermal bones of the skull roof, palate, and lower jaws essentially simultaneously ( Schoch & Carroll, 2003; Witzmann & Pfretzschner, 2003; Witzmann, 2006). All the bones form a close-fitting mosaic, in even the smallest known fossils ( Fig. 53 ). In contrast, most Late Carboniferous and Early Permian members of the Branchiosauridae ossify the dermal bones of the skull gradually during larval development in a relatively consistent sequence ( Schoch, 1992, 2002). The first bones to ossify are those associated with grasping prey: the tooth-bearing bones of the palate, and the margins of the upper and lower jaws – the premaxilla, maxilla, vomer, palatine, pterygoid, dentary, coronoids, and anterior end of the parasphenoid. These are followed by the squamosal and midline bones of the skull roof, and later the circumorbital bones and those at the back of the skull table ( Figs 54 , 55 ; Table 1). This is essentially the same sequence as that of primitive living salamanders ( Rose, 2003; C. A. Boisvert, 2004), but is very different from that of extant anurans or caecilians.

A striking feature of branchiosaurids is the early elaboration of the squamosal (relative to the circumorbital bones), which extends from the back of the skull table as a laterally oriented jaw suspension, much as in the salamander families Hynobiidae , Salamandridae , and Ambystomatidae , as well as the recently illustrated (but unnamed) larval salamander from the Middle Jurassic of China ( Gao & Shubin, 2003) ( Fig. 48 ). In common with these families, there is initially a long gap in the margin of the cheek between the maxilla and the jaw suspension, and both the squamosal and underlying pterygoid have a mobile articulation with the skull. In Apateon , the dorsal end of the squamosal loosely underlaps the supratemporal (which actually ossifies slightly later, along with the quadratojugal, postparietal, and nasal). The distal end of the squamosal is firmly attached to the quadrate and pterygoid, whose medial basipterygoid process has a V-shaped surface that would have permitted mediolateral movement relative to the parasphenoid. The configuration of these bones suggests that the distal end of the suspensorium could have moved in a mediolateral arc that would have allowed the oropharyngeal chamber to expand laterally in the course of suction feeding.

The skull bones in the smallest known larvae (in which the endolymphatic sacs still retain a calcium reserve) form an open lattice that would allow the mouth and pharynx great flexibility to expand laterally and ventrally to accommodate prey during suckand-gape feeding. In contrast, the most mature specimens of Apateon ( Figs 54 E 1 , 56 ) have the same complement of dermal bones as other advanced temnospondyls, in which they form a highly integrated skull for grasping and biting prey.

The retention of mobile joints between the jaw suspension and the skull roof and base of the braincase in hynobiids, ambystomatids, and some salamandrids suggests that expansion of the cheek may be possible in the larvae of living salamanders. Deban & Marks (2002) reported that video sequences from a dorsal perspective in Desmognathus marmoratus , Gyrinophilus porphyriticus , and Pseudotriton ruber (all primitive plethodontids) revealed slight lateral expansion of the branchial region during suction feeding. However, the lateral expansion contributed only slightly to the increase in buccal volume.

During later larval development in Apateon , the prefrontal, postfrontal, lacrimal, postorbital, and jugal ossify in succession, after which the maxilla extends posteriorly to make contact with the quadratojugal, greatly reducing the mobility of the jaw suspension. In the final stage of development, the skull acquires the rugose ornamentation of adult temnospondyls, and the ceratobranchials become ossified or calcified. An even more striking change occurs in the marginal dentition. During larval growth, the teeth of both Apateon and modern salamanders are long and slender, without the gap between the base and crown that characterizes the pedicellate teeth of the adults. However, in large specimens of Apateon , the marginal teeth acquire the pedicellate structure of adult salamanders ( Fig. 56 ). Boy & Sues (2000) argue that the very large size of the interpterygoid vacuities in more mature branchiosaurids, and their position beneath the expanded orbits, may have enabled branchiosaurids to use the retractor bulbi muscles, as in modern salamanders and frogs, to force the food down the throat.

The bones forming the anterior margin of the orbit are the last to ossify in modern salamanders, and the bones forming the posterior margin of the orbit and the back of the skull table in primitive tetrapods are lost completely. The adult cranial anatomy of modern hynobiids, ambystomatids, and salamandrids could have evolved from animals resembling Apateon by truncating ossification early in development, before the appearance of the posterior circumorbital bones and those at the posterior margin of the skull table, while retaining the gap between the maxilla and the squamosal. Ossification of endochondral bones of the skull, the quadrate, elements of the braincase (except the exoccipitals), and the articular of the lower jaw is long delayed in branchiosaurids, as in most Palaeozoic amphibians.

As was discussed in the descriptive sections, both frogs and caecilians show sequential ossification of the dermal bones of the skull roof, but each extant order has a different sequence, resulting in a succession of distinctive geometric patterns.

In contrast to other habitually aquatic temnospondyl labyrinthodonts, most branchiosaurids lack conspicuous lateral-line canal grooves on the skull bones. This does not indicate that they lacked the sensory structures associated with the lateral-line canal system, but simply that it did not sink into the bone but remained suspended in the overlaying soft tissue, as in modern salamanders ( Duellman & Trueb, 1986). Postcranial lateral-line canals have been demonstrated in the branchiosaurids Apateon and Melanerpeton , where they are supported by rows of denticles ( Werneburg, 2004).

Hyoid apparatus

Larvae of branchiosaurids and those of primitive living salamanders also have significant similarities in their hyoid apparatus. The endochondral elements of Apateon are only poorly ossified, but have been reconstructed by Boy & Sues (2000) ( Fig. 57 ) as being comparable to those of ambystomatids. Both groups have columnar to narrowly triangular gill rakers (pharyngeal denticles) associated with the ceratobranchials. In modern salamanders, they are arranged so as to fit together like the teeth of a zipper to close the external gill openings. As shown by Lauder & Schaffer (1985), and Lauder & Reilly (1988), this is necessary to maintain an effective vacuum during suction feeding in modern salamanders, as was presumably the case for branchiosaurids. Gill rakers in modern salamanders The individual denticles of primitive branchiosaurids are typically in the shape of slender cones, narrowing to a single tip. Such a configuration closely resembles that of the pharyngeal denticles of modern salamander larvae. This is also the shape of the denticles in the most mature specimens of Apateon , in which the skull roof is fully ossified but the ceratobranchials are calcified or ossified, indicating that the specimen is a neotenic adult. In less mature specimens of Apateon and other advanced branchiosaurids, the shape of the denticles changes during growth. The smallest individuals have simple denticles, but as they mature, additional slender processes grow successively from near the base of the crown. The largest specimens of Apateon caducus have up to six, and some later branchiosaurids have as many as 11 Schoch & Milner (2004). Such subdivision of the crown produces an admirable structure for the filtering of tiny particles of food. Nothing equivalent has been described in modern salamanders. It may have been a unique adaptation to the apparently planktonic feeding of the Carboniferous branchiosaurs, living in the many large, but isolated, lakes of the 2000-m-high Variscian mountains of central Europe, as described by Boy & Sues (2000) and Schoch & Milner (2004). are also described as being important in filtering out small particles of food, which are then swept back into the digestive tract ( Deban & Wake, 2000).

In modern larvae ( Fig. 57D ), the gill rakers are arranged in six rows. Ceratobranchials I and IV each support one row, while ceratobranchials II and III each support two rows. Together, these form an interlocking pattern that closes the three gill slits. This is exactly the arrangement of the gill rakers observed in Apateon and other advanced branchiosaurids. In nearly all other Palaeozoic amphibians for which larvae are known, the branchial denticles are attached in patches to thin plates of bone that are arranged in four rows, each attached to separate ceratobranchials. This pattern is retained in the close sister taxon of the branchiosaurs, the Micromelerpetontidae , and can be traced back to their ancestors among sarcopterygian fish such as Eusthenopteron ( Figs 10A , 57A ).

Vertebrae

As is the case for the development of the skull, knowledge of the vertebrae of branchiosaurs is confined primarily to the larvae. As in other labyrinthodonts, the neural arches formed as paired elements that ossified in an anterior–posterior sequence. The intercentra and pleurocentra either ossified only very late in ontogeny, or remained cartilaginous throughout the life of the animal. Both the structure and sequence of development of the vertebrae were highly distinct from those of most extant salamanders, in which the centra both chondrify and ossify prior to the arches. If salamanders evolved from branchiosaurids, it must be assumed that the initially paired pleurocentra fused to form a cylindrical structure closely integrated with the neural arch, and that the intercentra were completely lost, at some time between the Lower Permian and the Middle Jurassic, by which time fully modern salamander centra had evolved.

The research of C. A. Boisvert (2004) has demonstrated that a major change in the sequence of development occurred within basal salamanders (the Hynobiidae ), among which three primitive species retain the plesiomorphic sequence of chondrification and ossification of the neural arches prior to the centra. This supports other evidence that salamanders had evolved from labyrinthodonts rather than lepospondyls, in which the centra always ossified prior to the arches, at a very early stage of development.

Appendicular skeleton

As with the skull and vertebrae, sequential development is also evident in the appendicular skeleton of branchiosaurids, but this also occurs in other Palaeozoic labyrinthodonts. In most Palaeozoic tetrapods, the dermal shoulder girdle ossified essentially simultaneously with the dermal skull, and well before the endochondral girdles and other elements of the postcranial skeleton. In Micromelanerpeton ( Fig. 53 ), which may be considered a plesiomorphic sister taxon of branchiosaurids, only the body outline is evident behind the pectoral girdle at an early larval stage. In branchiosaurids, the dermal bones of the shoulder girdle ossify more slowly and are of reduced size in the adults. This might be expected in a sister taxa of salamanders, in which these bones are lost entirely. The pubis is also slow to ossify in most branchiosaurids, as is the case in primitive living salamanders (e.g. Hyn. nigrescens , Fig. 17 ), and fails to ossify in others.

The limbs of all early tetrapods ossify in an essentially proximal-to-distal sequence, except for a delay in ossification of the carpals, tarsals, and ends of the limb bones. Ossification of the carpals and tarsals is very much delayed in branchiosaurs, for which this part of the skeleton is known in very few specimens.

The most striking feature of limb development in branchiosaurids is the sequence of ossification across the digital arch ( Figs 58 , 59 ). As early as 1910, Schmalhausen recognized that salamanders were unique among living tetrapods in the sequence of development of the distal portion of the limbs ( Schmalhausen, 1910). In all anurans and amniotes that have been studied, development occurs in a posterior-to-anterior (or postaxial-to-preaxial) direction – the ulna ahead of the radius, the fibula ahead of the tibia, and the digits and associated elements of the wrist and ankle from the fourth to the first. Salamanders alone chondrify and ossify these elements in the opposite direction ( Erdmann, 1933; Shubin & Wake, 2003). Holmgren (1933, 1939) used this distinct pattern of development to argue that salamanders had evolved their limbs independently from all other tetrapods, as a result of their origin from a different group of fish, the Dipnoi .

A pattern very close to that of modern salamanders can also be recognized in the Palaeozoic branchiosaurid Apateon ( Schoch, 1992; Fröbisch NB, Carroll RL, Schoch RR, 2007). At an early stage in development ( Figs 58 , 59 ), the radius is distinctly larger and more differentiated than the ulna, and the tibia is more advanced than the fibula. Carpals and tarsals are very slow to ossify in all branchiosaurids, if they appear at all, and their sequence cannot be determined. However, the metapodials and digits show a consistent pattern of ossification in the sequence II– III–I–IV–(V), uniquely comparable to that of modern salamanders. Surprisingly, the first elements of the autopodium (the hands and feet) to ossify in Apateon are the terminal phalanges of the manus. These appear at stage III ( Fig. 58A ), leaving a great gap distal to the ulna and radius. A similar pattern is seen in the living salamanders Ranodon sibiricus , Salamandrella keyserlingii , and Ambystoma mexicanum . It has been suggested that the early development of the extremities of the manus and pes may help to keep the smallest larvae suspended above the sediments of the water bodies in which they develop. The next elements to ossify in Apateon are the metapodials, which also appear in the sequence II–III–I–IV–(V). They in turn are followed by the medial phalanges, in the same order. The preterminal phalanges ossify from proximal to distal.

No Palaeozoic taxa other than branchiosaurs are known to show this dominance of the preaxial elements of the limbs or the precocial ossification of the terminal phalanges. As such, this appears as an important synapomorphy with salamanders that is logically associated with their life histories, based on great prolongation of the larval stage. However, despite the unique sequence of development, the anatomy of the most mature specimens, specifically the nearly identical phalangeal count, remains very similar to that of other dissorophoids and early temnospondyls ( Table 2), and supports an ultimate common ancestry. Observations of primitive extant salamander larvae show the importance of the first and second digits in locomotion and attachment to vegetation, as well as their having a sensory role ( Vorobyeva et al., 2000; Shubin & Wake, 2003), which may have served as a force of selection for the switch from postaxial to preaxial dominance in development of the digital arch in ancestral caudates.

Life-history traits

Although branchiosaurids are not unique among Palaeozoic amphibians in their prolonged retention of larval characteristics, they are the only group known to have larvae very similar to those of primitive modern salamanders. Their prolongation of an aquatic way of life can be associated with a long period of adaptation to the large lake system that existed in central Europe for millions of years in the Late Carboniferous. Most branchiosaurid fossils have been collected from a series of large, long-lasting (on an ecological time scale) lakes in the Czech Republic ( Milner, 1980), France ( Steyer, 2000), and Germany ( Schoch & Milner, 2004, 2005). They suggest very long periods of larval life, and either very late metamorphosis, or neoteny.

One may postulate that the specialized cranial anatomy of the early larvae that characterizes Apateon evolved in response to adaptation to the rich and continuous food resources provided in these long-lasting lake systems. The adaptive advantage for prolongation of the span of larval life may have been the factor that selected for whatever genetic changes were responsible for the slow, sequential sequence of the ossification of the dermal bones of the skull, in contrast to the near synchrony of their ossification in more primitive tetrapods. Great extension of their period of larval life would eventually have had repercussions on other aspects of their anatomy and way of life.

Both branchiosaurids and micromelerpetontids are known almost entirely from larvae. The only branchiosaurid that has certainly reached the level of ossification of the skull and limbs common to the terrestrial adults of modern salamanders is Apateon gracilis from the Middle Autunian (R. R. Schoch & N. B. Fröbisch 2006). Most other branchiosaurids that have been described may have been fully neotentic, with few if any skeletal characters specifically associated with a terrestrial life stage. R. R. Schoch & A. Milner (2004) point out that no specimens showing ossification of endochondral elements of the skull or the carpals and tarsals have been recognized among the hundreds of specimens of larvae of approximately a dozen other branchiosaurid species that have been recognized. In contrast, they cite continuous growth stages, from tiny larvae to highly ossified adults, of the genera Onchiodon and Sclerocephalus , which occur in other localities in Europe over the same time span. They go on to suggest that the apparent absence of adult branchiosaurids may be the result of the probable high altitude of many of the localities in which they have been collected, citing the tendency towards neoteny in some modern salamanders that live in cold environments. However, it should also be noted that the area near the margins of these lakes, where adults might be expected to come to breed, is almost never represented in the sedimentary record of these basins.

The most widely distributed branchiosaurids were small forms, the most common of which was Apateon pedestris . They occurred many kilometres from the shore in the pelagic zone of large, deep, eutrophic lakes with abiotic bottom layers. Prolongation of larval life may have been a very important selective factor in the origin of urodeles, in which the specific structure and function of the larval feeding apparatus is unique relative to all other amphibians.

Specimens that have been described as either branchiosaurs or larval salamanders from the Early Triassic ( Gao et al., 2004) and Late Triassic ( Milner, 2000) suggest that the antecedents of salamanders may have gone through a long period, from the Upper Carboniferous into the Jurassic, during which they were dominated by larval/neotenic forms that would have spent little if any time out of the water. A primarily aquatic way of life may explain the retention of the primitive sequence of vertebral ossification, with the long persistence of an unrestricted notochord running beneath the neural arches prior to the ossification of cylindrical centra. However, in contrast to primitive caecilians, there is no evidence for the retention of separate intercentra.

Synapomorphies of salamanders and advanced branchiosaurids

Although our knowledge of branchiosaurids is limited almost entirely to their larvae, they none the less share numerous synapomorphies with salamanders:

1. specific sequence of ossification of individual bones of the skull and postcranial skeleton

2. retardation in ossification of bones that are either slow to ossify or are lost in modern salamanders

3. jaw suspension without a bony link to the maxilla (at least during development)

4. squamosal with a hinge-like articulation with bones of the skull table and /or otic capsule

5. absence of lateral-lines grooves in the skull bones of late larvae

6. pedicellate teeth in adults but not larvae

7. ceratobranchials become ossified or calcified at the time of maturation in neotenic species

8. pharyngeal denticles not attached proximally to a bony plate, as in most Palaeozoic tetrapods, but appearing as separate elements

9. denticles arranged in six rows that interdigitate across the intervening gill slits

10. loss of bony ventral scales

None of these synapomorphies are known in other Palaeozoic amphibians, and only the presence of pedicellate teeth is also seen in frogs and caecilians.

Other character states, although of a primitive nature, shared between advanced branchiosaurids and primitive salamanders are the ossification of neural arches prior to the centra, a very similar phalangeal formula, and the same number of digits.

The gap between branchiosaurids and crown-group salamanders

Unfortunately, the long-lasting system of lakes, in which a plethora of salamander-like features evolved among branchiosaurids and which was also responsible for their preservation as fossils, did not persist long beyond the base of the Permian. Aside from two fossil assemblages, too poorly preserved to allow determination of whether the specimens were branchiosaurs or primitive salamanders, there remains a gap of approximately 100 million years before the first appearance of crown-group urodeles. We can only guess when, and under what conditions, the sequence of cranial ossification common to branchiosaurs was truncated, and the number of bones present in the larval cranium was retained in the metamorphosed adults.

Although the early larvae of branchiosaurids closely resemble those of Middle Jurassic cryptobranchoids, late larvae or neotenic adults of branchiosaurs retain all the dermal skull bones of other advanced temnospondyl labyrinthodonts. There is no evidence as to whether any branchiosaurids had acquired the anatomical or behavioural characters necessary for the mode of terrestrial feeding present in the most primitive of living salamanders, the hynobiids.

More generally, the changes between the Lower Permian and the Lower Jurassic were as follows:

1. re-emergence or prolongation of life on land

2. termination of growth prior to the development of the following bones of the skull: tabular*, postparietal*, supratemporal*, postfrontal*, postorbital*, jugal*

3. reduction of the sculptured dorsal portion of the squamosal to allow passage of the adductor mandibulae internus (superficialis) out of the adductor chamber and over the otic capsule

4. loss of the otic notch and middle ear cavity associated with the capacity to hear high-frequency, airborne vibrations

5. origin of tongue supported by a modified hyoid apparatus and capable of protrusion

6. change of configuration of the articulating surfaces of the exoccipitals and atlas to limit movement of the head to dorsoventral hinging in the sagittal plane

7. reduction in the number of presacral vertebrae from 20 to 17

8. reduction in the number of dermal bones in the lower jaw from about eight to four

9. formation of cylindrical centra, fused to the neural arch in adults

10. loss of intercentra

11. loss of *cleithrum, *clavicle, and *interclavicle

12. origin of endochondral sternum

13. fusion of distal carpals and tarsals 1 and 2 to form basale commune in the adult

It is important to note that few of these changes require reversal, and many cases of bone loss (*) are presaged by their delayed ossification in the Palaeozoic genera.

One characteristic that appears to change very near the base of the crown group is the loss of sculpturing on the dorsal portion of the squamosal, which allows passage of the adductor mandibulae internus (superficialis) jaw muscle over the otic capsule. This area of sculptured bone is still retained in the Upper Jurassic caudate Karaurus .

Another major change that occurred prior to the appearance of crown-group salamanders involved the nature of the middle ear and hearing. Adults of extant salamanders lack any evidence of the posterior embayment of the squamosal or the middle ear cavity that characterize frogs, or the capacity to respond to highfrequency, airborne sounds. In contrast, all branchiosaurids retain an otic notch, common to other temnospondyls, which appears to be structurally, and therefore presumably functionally, homologous with that of anurans (R. R. Schoch & N. B. Fröbisch (2006). A clearly defined otic notch and a stapes that broadly resembles that of modern frogs is a heritage of temnospondyls ( Robinson, 2005), going back to the Lower Carboniferous, and those of the Lower Permian dissorophoid Doleserpeton are very close to the anuran pattern ( Bolt & Lombard, 1985). Apateon differs only in having a somewhat shallower notch as a result of the more anterior position of the jaw suspension and delayed ossification of the quadrate. Stapes are known for large individuals of Apateon that closely resemble those of small terrestrial temnospondyls, except for the partially unossified footplate. The shaft is compressed anteroposteriorly, and the straight ventral margin of the footplate is hinged or suturally attached to the parasphenoid. This evidence led Boy & Sues (2000) to argue that branchiosaurs were capable of detecting airborne sound. However, a well-developed stapes with a stapedial foramen is present in the stem-group urodele Karaurus and also in hynobiids. These latter species have no place for attachment of a tympanum, and hynobiids have no middle ear cavity.

The question is not whether branchiosaurs could hear airborne sounds, but how important hearing was to their way of life. The persistence of an aquatic way of life, indicated by the presence of external gills in most branchiosaurids over a period of at least 10 million years, and the high degree of specialization of their hyoid apparatus for suck-and-gape feeding, indicate that they had long larval stages, or were facultatively or obligatorily neotenic. As such, they might have found it difficult to make use of an impedancematching middle ear. Despite the presumed selective value of response to high-frequency airborne sound in many Palaeozoic temnospondyls, the otic notch is reduced or lost in several other clades that show a high degree of aquatic adaptation ( Holmes, 2000), and numerous cases of loss of the middle ear are known in modern frogs ( Duellman & Trueb, 1986).

As can be seen in lateral views of the larvae of modern salamanders, their Middle Jurassic relatives, and Apateon ( Fig. 48 ), the functioning external gills extend dorsally over the trunk, above the lateral surface of the skull, which was occupied by the tympanic membrane in terrestrial temnospondyls. These animals clearly could not respire in an aquatic medium and hear airborne sounds at the same time, and nor could they use their gills for respiration if they were exposed to the air.

Over the millions of years during which branchiosaurids adapted to a primarily aquatic way of life, where chemical means of species recognition might have been facilitated, the need to respond to highfrequency vibrations may have been reduced. If there were not strong selective pressures to maintain an impedance-matching middle ear, other forces of selection may have acted to reduce the large middle ear cavity. In modern frogs, this occupies the same general area of the head as the jaw muscles. Salamanders, in contrast, have used this space to greatly enlarge the area of the adductor jaw musculature relative to that of anurans.

It is interesting to note the salamander-like features of the skull that are evident in one of the most primitive of living anurans, Ascaphus . In contrast to most frogs, it has lost the impedance-matching middle ear and stapes, apparently as a result of its adaptation to life in fast-running streams, in which airborne sounds would be difficult to discern. As in hynobiids and ambystomatids, the jaw articulation is anterior to the level of the occiput, and there is no bony connection between the jaw suspension and the maxilla.

The strongest evidence for the presence of an impedance-matching middle ear structure in the ancestors of salamanders is provided by embryological studies of the primitive hynobiid salamanders Ranodon and Hynobius by Schmalhausen (1968:189–190):

The tympanic cavity of anurans is developed as an outgrowth of the dorsal wall of the first visceral fold in the form of an aggregated cellular mass, taking the form of a bubble set on a long pedicel. This cellular mass then loses its connection with the pharyngeal epithelium. The tympanic cavity proper is formed from these primordia only during metamorphosis. It is located anterior to the hyomandibular nerve. The Eustachian tube is formed anew. If one considers the features of the development of the tympanic cavity in anurans, then it is easy to recognize the same process seen in the development of urodele Amphibia.

In Hynobius , the anlage of the dorsal diverticulum of the first visceral fold is considerably larger than in the axolotl or Triton . Its general form is the same: it is a small pyriform formation set on a long pedicel. It is, however, retained much longer without reduction and its original connection to the pharyngeal epithelium sometimes persists until metamorphosis. In one case, in a larva of 33 mm length near metamorphosis, a wellpreserved pear-shaped anteroposteriorly flattened mass of cells set on a long, flat, rather thick pedicel has been observed. In Ranodon , however, this formation is even more strongly developed although the connection of the primordium to the pharyngeal epithelium is broken earlier than in Hynobius .

The rudiments described and especially the epithelial formations developing from this in the larvae of Ranodon , are quite similar to the anlagen of the tympanic cavities of anuran Amphibia, both in their mode of development and in their position between the palatoquadrate cartilage and the hyomandibular nerve.

In summary, he states that evidence from Ranodon and Hynobius ‘gives quite clear indication that in the ancestors of urodele Amphibia there was actually an apparatus for sound transmission from the air, i.e., a tympanic cavity and tympanic membrane’.

Acquisition of salamander characters among branchiosaurids

Although there remains a long gap in time and morphology between advanced branchiosaurids and the adults of crown-group salamanders, there are no other Palaeozoic tetrapods that are known to share as many synapomorphies with urodeles. If advanced branchiosaurs comprised the plesiomorphic sister taxon of urodeles, the next question to ask is how they are related to other Palaeozoic amphibians. We may begin with consideration of the more primitive branchiosaurids (R. R. Schoch & A. R. Milner, 2004).

Although Apateon , and particularly the species Apateon pedestris and Apateon caducus , provide the best known models for comparison with salamanders, there are several other species of Apateon and other genera within the Family Branchiosauridae that should be considered in evaluating the ancestry of salamander characters.

All members of the Branchiosauridae were small, with skulls ranging from 15 to 35 cm in length. Correlated with their small skull size, the orbits were relatively much enlarged. The prefrontal and postfrontal narrowly overlap in primitive species, but are separated from one another to a variable degree in others, and the jugal and lacrimal are separated by the maxilla. The palate was also distinguished by very large interpterygoid vacuities and corresponding reduction of the surrounding bones. The anterior process of the pterygoid is very slender, and the palatine and ectopterygoid are short. In common with other dissorophoids, the anterior ramus of the pterygoid does not reach the vomer. Where there were fangs on the vomers, palatines, and ectopterygoids in more primitive temnospondyls, these teeth are reduced within the Branchiosauridae to the size of the marginal dentition or that of denticles. The squamosal embayment is relatively shallow in Branchiosaurus , but deep in Schoenfelderpeton . Except in Melanerpeton , the jaw articulation does not extend posterior to the level of the occiput.

The body proportions of branchiosaurids resemble those of terrestrial members of other dissorophoid families, with relatively large limbs, short trunk, and large manus. Even in the earliest species, the interclavicle and clavicle were much smaller than those of other temnospondyls. The ilium is slender in primitive genera, but more massive and more nearly vertical in more derived forms.

The most primitive branchiosaurid is Branchiosaurus , known from species from the Westphalian D in both North America and Europe, approximately 8 million years prior to the specimens of Apateon that have just been described ( Milner, 1982). The first described material of Branchiosaurus , Branchiosaurus salamandroides , came from what is now the Czech Republic. This species resembles the more mature specimens of Apateon in the general configuration of the skeleton, but even in the smallest individuals, with skulls little more than 5 mm in length, most, if not all, of the dermal bones were ossified, as in the larvae of most Palaeozoic tetrapods ( Fig. 60 ). That is, Branchiosaurus had not yet evolved the capacity for gradual, sequential ossification of the dermal skull. This genus was also primitive in retaining contact between the prefrontal and postfrontal bones, which are separated by the frontals in the adults of Apateon , and have a rugose area on the posterior plate of the parasphenoid that may reflect the prior presence of denticles that are present in this position in sister taxa of the branchiosaurids, specifically the early amphibamids. Branchiosaurus also retained the bony ventral scales that were lost in later branchiosaurids. It has 24 presacral vertebrae, as opposed to 20–22 in later species.

However, Branchiosaurus did express several derived features shared with later branchiosaurids, including the loss of the bony plates that support the pharyngeal denticles in most primitive temnospondyls. The individual denticles are separate, as in later branchiosaurids, although they usually lack the multiple processes from the tip of the denticle that are elaborated during growth in later branchiosaurids. The jugal failed to reach the lachrymal, and the back of the skull table was reduced, as were the size of the clavicular blade and the interclavicle. Branchiosaurus had also achieved features of the hyoid elements that are similar to those of later branchiosaurs, with early ossification of the hypobranchials and basibranchial ( Fig. 60 ). This condition also resembles that of the primitive caudates, Karaurus and Chunerpeton .

We see within the Branchiosauridae , over the roughly 10 million years between the Westphalian D and the beginning of the Permian, the accumulation of numerous characteristics leading towards salamanders. The most important was the evolution of the capacity to ossify the dermal bones of the skull in a sequential manner, in contrast with the nearly simultaneous mode of ossification in all other Palaeozoic tetrapods, in which nearly all the dermal bones are integrated into a tight-fitting matrix in the smallest known specimens.

Branchiosaurids are, in turn, strongly supported as members of the Superfamily Dissorophoidea (also including the Micromelerpetontidae , the Amphibamidae , and the Trematopidae ) ( Holmes, 2000) by the following synapomorphies: small size of early species compared with all other temnospondyls, very large orbits and interpterygoid vacuities relative to skull size, retention of a movable basicranial articulation, conspicuous otic notch, and a tendency to lose contact between the prefrontal and postfrontal and between the lacrimal and jugal ( Milner, 1982). They share with eryopoids the loss of the intertemporal that is present in earlier temnospondyls. Going further back, the ancestry of dissorophoids, together with many other members of the Temnospondyli , are traceable to the Viséan Balanerpeton ( Milner & Sequeira, 1994) .

Of the characteristics of primitive members of the crown-group urodeles, a few can already be recognized in Balanerpeton : digital and phalangeal count, relatively small body size, arches ossifying before centra, large orbits and interpterygoid vacuities, and general proportions of trunk and limbs ( Fig. 70 ). These, however, are enough to distinguish Balanerpeton from all other clades known from this or earlier time periods in the Palaeozoic, as a plausible sister taxon of salamanders. Thus, one may say with considerable confidence that salamanders have a closer sister-group relationship among the temnospondyls than with any of the other recognized clades of Palaeozoic tetrapods.

In the absence of any knowledge of temnospondyls earlier than Balanerpeton , no characteristics seen in older amphibians are plausibly homologous with any of the distinguishing characters of salamanders.

A nested sequence of synapomorphies leading from early temnospondyls to crown-group urodeles is shown in Fig. 61 .

Figures

Figure 1. Reconstructions of two types of Palaeozoic amphibians that have been hypothesized to be the sister taxa of modern amphibians (Lissamphibia). A, the Upper Carboniferous temnospondyl labyrinthodont Amphibamus grandiceps. Reproduced from Gregory (1950). B, skeletal reconstruction of the Upper Carboniferous lysorophid lepospondyl Brachydectes elongatus. C, dorsal, lateral, and palatal view of the lysorophid Brachydectes elongatus, from the Lower Permian. B, C, modified from Wellstead (1991). Abbreviations used in figures listed on pages 8, 9.

Figure 10. A, dorsal view of the hyobranchial apparatus in the Upper Devonian osteolepiform fish Eusthenopteron. B, C, ventral views of hyobranchial apparatus of larval and adult Salamandra salamandra. D, ventral view of hyobranchial apparatus of larval Rana temporaria. E. Hyoid plate of adult Leiopelma hochstetteri. F, G, hyobranchial apparatus of larval and adult individuals of the primitive caecilian Epicrionops. A, reproduced from Jarvik (1954). B–E, reproduced from Duellman & Trueb (1986). F, G, reproduced from Wake (1989). Coarse stippling is indicative of cartilage. It should be noted that the names of the more distal elements of the hyobranchial apparatus differ from those used by some modern authors (e.g. Deban & Wake, 2000), who refer to the hyobranchials and ceratobranchials as basibranchials and epibranchials. Reilly & Lauder (1988) discussed the homology of these elements and the historical reasons for the use by some authors of a unique terminology for salamanders.

Figure 17. Vertebrae and appendicular skeleton of salamanders. A, anterior view of the atlas of Salamandra salamandra. Reproduced from Francis (1934). B, C, lateral views of atlas and seventh trunk vertebra of Ambystoma opacum. Reproduced from Duellman & Trueb (1986). Note separate articulating surfaces for articulation with double-headed ribs. D, cartilaginous sternum of Salamandra salamandra. Reproduced from Francis (1934). E–K, appendicular elements of Hynobius nigrescens, specimen no. 22513 in the Herpetology Collection of the Museum of Comparative Zoology, Harvard. E, lateral and medial views of the fused scapula and coracoid; the dorsal, anterior, and ventral surfaces are extended in cartilage (coarse stippling). F, ventral view of left humerus. G, left lower forelimb in ventral view. H, I, pelvic girdle in ventral and left lateral view, with femur in place. J, right femur in ventral view. K, left lower hindlimb in dorsal view.

Figure 48. Salamandramorph larvae. A, the oldest described urodele larva, an unnamed genus from the Middle Jurassic of China; skull in primarily dorsal view, trunk and tail in primarily lateral view. Reproduced from Gao & Shubin (2003). B, advanced larval stage of the derived branchiosaurid Apateon (Royal Ontario Museum, no. 44276) from the lowermost Permian locality of Odenheim, Germany, in primarily lateral view. Two external gills are extended dorsally from the trunk. The third gill is lower in position, and pressed against the side of the trunk; a very delicate impression of the caudal fin can be seen above the central portion of the tail. C, sketch of the Apateon larva, emphasizing the outline of the bones. Note that the neural and haemal arches appear prior to the centra, which are not ossified in this specimen.

Figure 51. Skeletons of juvenile lepospondyls. A, the microsaur Hyloplesion longicostatus. Reproduced from Carroll & Gaskill (1978). B, an unnamed adelogyrinid. Reproduced from Carroll (1989). C, the aïstopod Pseudophlegethontia turnulllorum. Reproduced from Anderson (2003). In contrast to the larvae of labyrinthodonts, lepospondyls ossify fully cylindrical centra at a very early stage in development, but show no evidence of external gills.

Figure 52. Skeletal reconstructions of branchiosaurs. A, the micromelerpetontid Micromelerpeton credneri, with four rows of gill rakers, attached to thin bony plates. B, the branchiosaurid Apateon pedestris, with six rows of gill rakers. Reproduced from Boy (1971).

Figure 53. A, pattern of skull roof ossification in the smallest adequately known specimen of the osteolepiform fish Eusthenopteron, in which the dermal bones of the skull ossify essentially simultaneously. Reproduced from Schultze (1984). B, the skeleton of a very small specimen of the branchiosaur Micromelerpeton, in which the skull bones also ossify simultaneously. Scale bars 5 mm in length. Reproduced from Schoch & Carroll (2003).

Figure 54. Comparative views of the sequence of ossification of the dermal skull bones of the uppermost Carboniferous branchiosaurid Apateon caducus (on the left), and the extant salamandrid Notophthalmus viridescens on the right. A1–E1, succession of growth stages illustrated in specimens from the Geological and Palaeontological Institute of Mainz; specimen numbers 1478, 1460, 1464, 1280, and 1530. A2–D2, developmental sequence of cleared and stained specimens of the salamandrid Notophthalmus viridescens (Redpath Museum, McGill University, specimen numbers 5007, and 5009–5011). Bone is red and, where viewed on edge, black; cartilage is blue. Note the very early appearance of the squamosal, when most of the surrounding skull is still cartilaginous. The maxilla, however, ossifies long after the premaxilla.

Figure 55. Diagrammatic illustrations of the sequence of cranial ossification of the uppermost Carboniferous branchiosaurid Apateon caducus on the left and modern hynobiid salamanders on the right. A, uniform grey shading identifies the successive ossification of bones in larger skulls of Apateon. Specimens from the Geological and Palaeontological Institute of Mainz, and numbers in accordance with increasing size: 1310, 1387, 1442, 1779, 1249, 1335, 1601. The millimetre scale at the bottom applies to all but the largest skull. Palatal bones are omitted on the right side to emphasize progressive closing of the gap in the skull margin between the jaw suspensorium and the maxilla. Reproduced from Schoch & Carroll (2003). B–D, growth stages in hynobiid salamanders. Only the palatal and jaw elements are ossified in the smallest specimen. B–D, growth stages in hynobiid salamanders. B, dorsal and palatal views of the skull of an adult specimen of Batrachuperus sinensis (Natural History Museum, London, no. 94-9-15-15). C, late larval stage of Batrachuperus mustersi. Redrawn from Deban & Wake (2000). D, dorsal and palatal views of Ranodon sibiricus. Redrawn from Lebedkina (1979). Ossified bones are in black; surrounding areas are cartilaginous at this stage. Based on an animal 36 mm in length. Scale bars, 1 mm.

Figure 56. Neotenic adult of Apateon from the Lower Permian of Odernheim (Geological and Palaeontological Institute of Mainz, N800). A, complete skull showing calcified or ossified ceratobranchials (cb), with attached branchial denticles. B, enlarged view of teeth from the right dentary as seen through the orbit. Note the clear demarcation between the base and the crown (white arrows). The teeth in larval individuals are slender pegs, showing no trace of pedicellate structure. Scale bars: A, 5 mm; B, 1 mm.

Figure 57. Branchial denticles in Palaeozoic branchiosaurs and a modern salamander. A, branchial tooth plates with attached denticles from the micromelerpetontid Micromelerpeton credneri from Odernheim, Geological and Palaeontological Institute of Mainz, specimen number N226. This typified the primitive pattern for temnospondyls. B, branchial denticles in the branchiosaurid Apateon (Royal Ontario Museum, Canada, 44276). C, reconstruction of hyobranchial elements and branchial denticles of the branchiosaurid Apateon. Reproduced from Boy & Sues (2000). D, branchial denticles associated with the gill slits in Ambystoma tigrinum (Canadian Museum of Nature, Ottawa, 7255).

Figure 58. Sequence of ossification of the bones of the forelimb (top) and hindlimb (bottom) of Apateon. A, stage III, specimen number ATD 6. B, forelimb only, stage IV, ATD 106. C, stage V, ATD 290. D, stage V, ATD 231. Specimens in Figs 58 and 59 are from the Geological and Palaeontological Institute of Mainz. The darker the bones, the greater the level of ossification. *Preaxial side of limb.

Figure 59. Sequence of ossification of the bones of the forelimb and hindlimb of Apateon. A, stage V, ATD 264, hindlimb only. B, stage VI, specimen number 16258, Staatl. Museum für Naturkunde, Stuttgart.

Figure 60. Two specimens attributed to the primitive branchiosaurid Branchiosaurus sp. from the Westphalian D of Mazon Creek, Illinois. Reproduced from Milner (1982). A, skull of United States National Museum 4400 in palatal view. Note the similarity of the hyoid elements to those of the Middle Jurassic salamander Chunerpeton tianyiensis (Fig. 47). B, Yale Peabody Museum 802, showing palate and infillings of the digestive tract.

Figure 61. Nested synapomorphies leading to crown-group urodeles.

Figure 70. The Lower Carboniferous temnospondyl Balanerpeton. A, B, skull in dorsal and palatal views. C, D, lower jaw in lateral and medial views. E, reconstruction of skeleton. F, G, lower forelimbs and hindlimbs. Reproduced from Milner & Sequeira (1994).