Journal of Systematic Palaeontology: page 1 of 23

doi:10.1017/S1477201908002460 C© The Natural History Museum

The intrarelationships and

evolutionary history of the

temnospondyl family

Branchiosauridae

Rainer R. SchochStaatliches Museum fur Naturkunde, Rosenstein 1, D-70191 Stuttgart, GermanyE-mail: schoch.smns@naturkundemuseum-bw.de

Andrew R. MilnerDepartment of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UKE-mail: andrew.milner@nhm.ac.uk

SYNOPSIS The larval or paedomorphic branchiosaurid temnospondyls, inhabitants of many Permo–Carboniferous freshwater lakes across Europe, have never been analysed cladistically. In the presentwork, we have analysed the relationships between all the well-defined species of the clade, withthe following results: (1) despite homoplasies shared with amphibamids, the family Branchiosaur-idae forms a well-supported monophylum; (2) if Micropholis is considered to be an amphibamid,then Branchiosauridae have arisen within the Amphibamidae and could be considered to be a cladeof paedomorphic amphibamids; (3) the closest relatives of branchiosaurids are the amphibamidsAmphibamus and Platyrhinops; (4) the stratigraphically oldest genus Branchiosaurus, here rep-resented by its only well-known species B. salamandroides, forms the most basal offshoot of theBranchiosauridae; (5) the remainder of the branchiosaurids fall into two clades referred to as theMelanerpeton-clade and Apateon-clade, respectively; (6) the Melanerpeton-clade is morphologicallymore diverse than the Apateon-clade; (7) within the Melanerpeton-clade, Schoenfelderpeton andLeptorophus are sister groups; (8) within Apateon, A. kontheri forms the basal-most taxon, followedby A. gracilis, A. pedestris, A. dracyiensis and the sister-taxa A. caducus and A. flagrifer.

An evolutionary scenario suggests that branchiosaurids originated by invention of a key innova-tion: specialized pharyngeal denticles, housed in gill clefts, served as a filter-feeding device focussingon plankton. The group diversified in part, by patterns of delayed development of the upper jaw andcheek resulting in a kinetic maxilla, thereby permitting manipulation of the oral margin during suctionfeeding. It can be shown that within the Apateon-clade, the second component evolved along differ-ent lines into rather different adaptational directions, producing a range of morphotypes controlledby minor heterochronic changes.

KEY WORDS Temnospondyli, Dissorophoidea, Branchiosauridae, ontogeny, phylogeny, evolutionaryscenario

Contents

Introduction 2

Material 2

Analysis 3

Taxa 3Outgroups 3Ingroups 5

Characters 8

Results 11Relationships 11Robustness of nodes 11

Diagnoses of Branchiosauridae 13

Branchiosauridae Fritsch, 1879 13

Affinities of poorly known branchiosaurids 13

Evolutionary history of the Branchiosauridae 14

2 R. R. Schoch and A. R. Milner

Palaeobiological implications 14Evolutionary scenario 15Phylogeny and stratigraphy 18

Acknowledgements 21

References 21

Introduction

Branchiosaurids are small Palaeozoic temnospondyl amphi-bians with external gills, poorly ossified skeletons and anoverall immature appearance. The first specimen to be col-lected, Apateon pedestris Meyer, was also the first Palaeo-zoic tetrapod to be recognised as such, being noted by Meyer(1844, 1848, 1858) during his investigations of the Permo–Carboniferous vertebrates from the Central European Rotlie-gend facies. The Rotliegend – a term adopted from Germanminers’ parlance and literally meaning ‘Red Beds’ – forms asequence of sediments deposited in freshwater lakes and riverbanks in the Permo–Carboniferous of Middle Europe. Withinthe Rotliegend, branchiosaurids are mostly found in greyshales and limestones that formed in large freshwater lakes.By the end of the nineteenth century, more adequate mater-ial had emerged, permitting Gaudry (1875), Fritsch (1876,1878, 1879), and Credner (1881) to add numerous observa-tions to Meyer’s findings. They established a firm basis forthe classification of the Branchiosauridae, a group that hadfirst been recognised and named by Fritsch (1879). The fam-ily was based on the type genus and species Branchiosaurussalamandroides Fritsch from the Gas Coal of Nyrany nearPlzen, western Czech Republic.

In his revision of the branchiosaurids from the Saar-Nahe Basin, Boy (1971) argued for the neotenic state of thegroup and subsequently Boy (1972) produced a phylogeneticinterpretation of its intrarelationships. He also clarified thatMicromelerpeton and its relatives (Micromelerpetontidae), asecond group of paedomorphic dissorophoids that had longbeen confused with branchiosaurids, form a clade of theirown. Boy (1972) forms the major landmark in branchiosauridresearch, as he clarified the monophyletic status, the system-atic position and the proper composition of the family, afterdecades of major confusion had left temnospondyl systemat-ics in a problematic state (Romer 1947; Heyler 1957; Watson1963). The morphology of branchiosaurids and its develop-mental changes were covered in depth by Boy (1972, 1978,1986, 1987a), Milner (1982, 1986), Werneburg (1986, 1987,1988a-c, 1989a, b, 1990, 1991, 1996, 2001a, b), and Schoch(1992, 1998, 2002a, b, 2004).

Branchiosaurids have long been considered to be Cent-ral European endemics and no critically diagnostic finds canyet be confirmed for North America. Boy (1987a) discussedthe North American reports (Romer 1939; Milner 1982) not-ing that they provide tantalising but insufficient anatom-ical information, because the crucial regions – the base ofthe parasphenoid and the palatine–ectopterygoid complex –were too poorly preserved or hidden by the overlying mand-ibles. Recently, however, diagnostic branchiosaurid materialhas been collected in Sardinia in the West Mediterranean(Werneburg et al. 2007). In a further recent paper, Shishkin(1998) attributed new material of the enigmatic temnospon-

dyl Tungussogyrinus from Siberia to the Branchiosauridae,but the available anatomical evidence is equivocal, beyondthe fact that this taxon is a dissorophoid.

A thorough phylogenetic understanding of the Bran-chiosauridae is not merely an end in itself, but is necessitatedby the current debate on dissorophoid intrarelationships andtheir bearing on the ancestry of the modern lissamphibianorders, the salamanders, anurans and gymnophionans. In re-cent decades, branchiosaurids have been suggested as close,if not immediate lissamphibian relatives (Milner 1988, 1993;Trueb & Cloutier 1991; Schoch 1995; Gardner 2001; Schoch& Carroll 2003; Ruta et al. 2003; Anderson 2007; Carroll2007; Ruta & Coates 2007; but see Laurin & Reisz 1997 andLaurin 1998 for disagreement) and in this context, numerousbranchiosaurid characters have been highlighted that may ormay not be phylogenetically informative. In order to assessthe significance of these characters for a broader phylogeneticinvestigation, the relationships within the Branchiosauridaemay be critical. So far, the distribution of character-states sig-nificant for dissorophoid relationships has been reported to behighly variable across the Branchiosauridae. Therefore it iscrucial to establish the ancestral (primitive) condition of thisgroup in as much detail as possible. The present study is thusexclusively focused on branchiosaurid intrarelationships.

Material

The taxonomic and descriptive work on the Branchiosaur-idae forms a large body of literature. It is based on manyhundreds of specimens from several Permo–Carboniferousbasins across Central Europe. These basins are (from westto east): the basin of Autun (Massif Central, France), theSaar-Nahe Basin (Rheinland-Pfalz, southwest Germany), theSaale Basin (which includes the Thuringian Forest region,northern Thuringia and Saxony-Anhalt, central Germany),the Dohlen Basin (Saxony, east Germany), the PodkrkonoseBasin (Czech Republic), and the Lower Silesian Basin(Czech Republic).

Particularly rich collections exist for Apateon pedes-tris Meyer, A. caducus (Ammon), and A. gracilis (Cred-ner) (Boy 1972, 1978, 1988, 1995; Werneburg 1991; Schoch1992, 2002a). Good collections with a broad size-rangeamong specimens are available for Branchiosaurus sala-mandroides Fritsch, Apateon dracyiensis (Boy), Leptorophustener (Schonfeld), M. humbergense (Boy), and Schoenfelder-peton prescheri (Boy) (Boy 1978, 1987a; Werneburg 1988a,2001a). In addition to the available descriptions, 742 bran-chiosaurid and 137 other temnospondyl specimens (used asoutgroups) have been studied by the authors:

Humboldt Universitat, Museum fur Naturkunde, Ber-lin, Germany (MB): Platyrhinops lyelli (Am.48, 331),

Relationships and evolutionary history of branchiosauridae 3

Sclerocephalus sp. (Am.1203, 1291, 1293, 1294, 1301–1309, 1313, 1316, 1323), Cheliderpeton sp. (1274–1276, 1281, 1284, 1289, 1312), Micromelerpeton cred-neri (Am.1197–1210, 1180–1196, 1260, 1261, 1335–1337, 1343–1347), Apateon pedestris from the Saar-Nahe Basin in Germany (Am.274, 1062–1092, 1125–1174, 1299, 1316–1319, 1321–1323, 1340–1341), A.pedestris from Autun in France (Am. 977), A. cadu-cus (1262–1264), A. flagrifer (Am.297, 976), A. gracilis(Am.55, 363, 364, 370, 374, 376, 402–406, 412–413,398, 399, 945), Melanerpeton humbergense (Am.1265–1269).

Institut und Museum fur Geologie und Palaontologie,Tubingen, Germany (GPIT): Sclerocephalus sp. (Am105).

Johannes-Gutenberg Universitat, Mainz, Germany(GPIM): Apateon pedestris and A. caducus (1230–1840).

Landesamt fur Umwelt und Geologie, Freiberg/Sachsen,Germany (LFUG): Apateon gracilis (13612).

Staatliches Museum fur Naturkunde, Stuttgart, Germany(SMNS): Sclerocephalus sp. (51307, 51309, 51314,51367, 51373, 51377, 51398, 54989, 81711, 81833,81851–81854, Micromelerpeton credneri (51243,51282, 51310, 51312, 51313, 51315, 51318, 51323,51326–51328, 51331, 51332, 51338, 51368, 54978,54991–54994, 56135, 56137). Apateon gracilis (91016–91028).

Narodnı Muzeum, Prague, Czech Republic (NMP): Bran-chiosaurus salamandroides (M332, 336–338, 341, 346,353), Mordex laticeps (M335, 349, 351, 352, 356, 357).

Naturhistorisches Museum, Vienna, Austria (NMW): Bran-chiosaurus salamandroides (1983–32-4, 1983–32-16,1983–32-25, 1983–32-37), Mordex laticeps (1898-X-21,1983–32-18, 1983–32-26).

Department of Palaeontology, The Natural History Mu-seum, London, UK (BMNH): Balanerpeton woodi(R10952–10955, R12014–12016).

Hunterian Museum, University of Glasgow, Glasgow, UK(GLAHM): Balanerpeton woodi (V2051, V2052).

Department of Geology, National Museum of Scotland, Ed-inburgh, UK (NMS.G.): Balanerpeton woodi (1985.4.1,1985.4.2, 1987.7.32, 1990.79.3, 1991.47.2).

University Museum of Zoology, Cambridge University, UK(UMZC): Balanerpeton woodi (T1261, T1312, T1313).

New Mexico Museum of Natural History, Albuquerque,USA (NMMNH): Milnererpeton huberi (P 3696).

Analysis

The phylogenetic analysis was supported by the softwarepackages PAUP 3.1 (Swofford 1991) and MacClade 2.0(Maddison & Maddison 1992). In the main analysis, 40 char-acters and 17 ingroup taxa were considered, polarity beingdetermined by two well-known outgroup taxa: the primitivetemnospondyl Balanerpeton woodi Milner & Sequeira andthe stereospondylomorph Sclerocephalus haeuseri Goldfuss.

The analysis was performed in the branch-and-boundand heuristic search modes with characters treated altern-atively in Acctran and Deltran modes. All characters wereordered, because the outgroups are well known and their ple-siomorphic state in the present discussion are not a matter ofdebate. Multistate characters were also ordered, referring tothe detailed knowledge of ontogenetic character transform-ations in both branchiosaurids (Boy 1974; Schoch 1992,2002a) as well as in Micromelerpeton (Boy 1972, 1995),Platyrhinops (Carroll 1964; Clack & Milner 1994; Schoch2002b), and Sclerocephalus (Schoch 2003). By that, we ac-cept the axiom that evolutionary character transformationcorrelates with ontogenetic character transformation. The ba-sic idea behind this is that evolution works by modification ofexisting ontogenetic trajectories (Alberch et al. 1979; Wake& Larson 1987). It does not imply the simplistic Haeckelianview of recapitulation, nor even the more general von Baerianview, because these make statements about phylogenetic po-larity, which is not accepted here. It is implied only thatontogenetic transformations happen in an ordered sequence,which evolution may change in either direction. For instance,paedomorphosis often results in a reversal of ontogenetic po-larity by evolution (with the adults of the descendant similarto the larvae of the ancestor), while the sequence itself isoften retained.

The PAUP analysis found two most parsimonious topo-logies, with a tree length of 109 steps, a consistency indexof 0.62, a retention index of 0.75, and a rescaled consistencyindex of 0.47 (Fig. 5A). A bootstrap analysis with 10,000random additional replicates was performed in order to elu-cidate the robustness of single nodes, giving high supportfor Platyrhinops + Amphibamus (97%), A. caducus + A.flagrifer (89%), and the Dissorophoidea (87%). Reasonablerobustness was found for the Branchiosauridae (77%), thethree wide-headed Apateon species A. dracyiensis + (A. ca-ducus + A. flagrifer) (79%), the Melanerpeton-clade (68%),and the Apateon-clade (57%). Poorly supported nodes areBranchiosauridae + (Amphibamus + Platyrhinops) (0%) andpost-Branchiosaurus branchiosaurids.

Taxa

Outgroups

1. Balanerpeton woodi Milner & Sequeira. Morphologicallywell-known and also plesiomorphic in most character-states, Balanerpeton is the stratigraphically oldest temno-spondyl, but is morphologically clearly advanced in somecharacters beyond the condition in Dendrerpeton, Coch-leosaurus, and Edops (Milner 1993; Milner & Sequeira1994; Holmes et al. 1998). However, it is distinctly smal-ler than most stem-stereospondyls (Eryops, Scleroceph-alus, Archegosaurus) and therefore forms a particularlyappropriate outgroup to the Branchiosauridae and otherdissorophoids. Balanerpeton is found in Early Carbon-iferous (Visean) lake deposits at East Kirkton in Scotland(Milner & Sequeira 1994).

2. Sclerocephalus haeuseri Goldfuss (Figs 1H, 2B1, 2D1).This is the best known among the more advanced Permo-Carboniferous temnospondyls (Boy 1988, 1993; Schoch2003). It probably belongs to the stereospondyl stem

4 R. R. Schoch and A. R. Milner

Figure 1 Cranial character-states referred to in the phylogenetic analysis. A-D, skull roof in dorsal view; E-G, skulls in lateral view; H-I, palatesin ventral view. A, Micromelerpeton credneri (after Boy 1995); B, Branchiosaurus salamandroides (NMP M332); C, Schoenfelderpeton prescheri(after Boy 1987); D, Apateon dracyiensis (after Werneburg 2001a); E, Micromelerpeton credneri (after Boy 1995); F, Apateon pedestris (after Boy1987); G, Apateon dracyiensis (after Werneburg 2001a); H, Sclerocephalus sp. (Schoch 2003); I, Apateon pedestris (after Boy 1987, Schoch1992). Abbreviation: LEP, lateral exposure of palatine.

Relationships and evolutionary history of branchiosauridae 5

Figure 2 Postcranial character-states referred to in the phylogenetic analysis. A, complete skeletal reconstruction of large Apateon pedestris;B, interclavicles (B1: Sclerocephalus sp.; B2: Melanerpeton humbergense; B3: Apateon pedestris); C, branchial dentition (C1, Micromelerpetoncredneri; C2, Mordex laticeps; C3, Apateon pedestris); D, humeri (D1, Sclerocephalus sp.; D2, Micromelerpeton credneri; D3, Micropholis stowii).

(Schoch & Milner 2000), sharing some derived character-states with archegosauroids and rhinesuchids (Boy 1990,1996; Yates & Warren 2000). The genus Sclerocephalussensu stricto, occurs abundantly in the Lower Rotliegendof the Saar-Nahe Basin (southwestern Germany) and fur-ther specimens have been found in the Thuringian ForestBasin (central Germany). In the former region, it covers awide range of localities and stratigraphical horizons, ob-viously exemplifying intra-basin evolutionary trends. Inthis analysis, we use the Sclerocephalus haeuseri mater-ial from the Meisenheim Formation (upper part of LowerRotliegend section). Despite the presence of some poten-tially confusing morphological variation, Sclerocephalusis particularly suited to serve as an outgroup, becausethere is a consensus that it is much closer to the dissor-ophoids than to Balanerpeton, and in addition there is alarge body of ontogenetic data available for this taxon(Boy 1988; Schoch 2003). With these data in mind, thecomparably large adult size should not pose problems forthe definition of character-states, as the characters in bran-chiosaurids may be compared with all stages of ontogenyin Sclerocephalus.

Ingroups

3. Ecolsonia cutlerensis Berman, Reisz & Eberth. (Source:Berman et al. 1985). This is the one of the few well-

prepared and described representatives of the large dis-sorophoids although it does not have dissorophid-typearmour and therefore cannot represent the Dissorophidaesensu stricto. It stems from the Lower Permian CutlerFormation of New Mexico (Berman et al. 1985). Wehave omitted more certain dissorophid taxa (e. g. Dis-sorophus, Broiliellus, Cacops), as these need substantialpreparation and redescription, being too poorly knownin many critical characters.

4. Micromelerpeton credneri Bulman & Whittard (Figs 1A,2C, 2D2). (Sources: Boy 1972, 1995; Witzmann & Pfret-zschner 2003). This is a well-known species formingpart of a small clade of mostly neotenic dissorophoids,the Micromelerpetontidae. This monophyletic familyencompasses a range of species falling into four gen-era, Limnogyrinus, Branchierpeton, Micromelerpetonand Eimerisaurus. Micromelerpeton is now known froma range of morphotypes, three of which have been form-ally named as species (Boy 2002a). Within the clade,Boy (2002b) has recognised a confusing degree of par-allel evolution. Therefore, we have confined our usage ofMicromelerpeton as an ingroup taxon to the type species.Although it is more derived than the less well-knowntaxa Limnogyrinus and Branchierpeton, it is knownby numerous ontogenetic stages, and furthermore thecharacter-states in which it is autapomorphic are ratherobvious (Boy 1995, 2002b).

6 R. R. Schoch and A. R. Milner

5. Platyrhinops lyelli (Wyman). (Sources: Carroll 1964;Clack & Milner 1994; Schoch 2002b). This taxon isa representative of the Amphibamidae, a small cladeof miniaturized dissorophoids (i. e., in the 15–30 mmadult skull size range) with marked affinities to extantamphibians (Bolt 1969). Platyrhinops is from the lateMiddle Pennsylvanian of Linton, Ohio and Asturian(= Westphalian D) of Nyrany, Czech Republic.

6. Amphibamus grandiceps Cope (Sources: Watson1940; Milner 1982). This taxon forms the smallestterrestrial dissorophoid, and was found in the late MiddlePennsylvanian of Mazon Creek, Illinois.

7. Micropholis stowii Huxley (Sources: Broili & Schroder1937; Boy 1985; Schoch & Rubidge 2005). Stratigraph-ically by far the youngest dissorophoid (lowermost Tri-assic of South Africa), Micropholis is similar to Am-phibamus and Platyrhinops in some features.

8. Branchiosaurus salamandroides Fritsch (Figs 1B, 3A).(Sources: Fritsch 1876, 1879; Milner 1986; Boy 1987a;Werneburg 1987). This is the earliest known bran-chiosaurid from the Asturian (= Westphalian D) ofNyrany, Czech Republic. The material used here is arestricted subset of B. salamandroides as listed in thecurrent literature. Work in progress by ARM and SEKSequeira indicates that B. salamandroides is a compositeof three separate taxa. Much of the material describedby Fritsch (1879) and Werneburg (1987) appears to bejuvenile or larvae of the trematopid Mordex laticeps, asdoes at least some of the material referred to by Boy(1987a), e. g. the reconstruction of the skull roof figuredby him (Boy 1987a, fig. 2a). Here, we refer only to thefew unambiguous specimens from Nyrany (as listed inthe ‘Material’ section) for our comparisons.

9. Apateon pedestris Meyer (Figs 1F, 2A, 3D, 4E).(Sources: Boy 1972, 1978, 1987a; Schoch 1992, 2004).This relatively small species has long formed the stereo-typical branchiosaurid, including French material ori-ginally described as Protriton petrolei, German mater-ial long referred to the genus Branchiosaurus, and theoriginal material of Apateon pedestris of Meyer (1844).Although the ontogeny is not known in as much detail asin the following species, large quantities of A. pedestrisspecimens are present in numerous collections aroundthe world; most of them stem from a single horizon (so-called Odernheim-Bank, or L-O 8 of Boy & Fichter1982). A. pedestris has a wide stratigraphical range,spanning some recently calculated 3 Myr (Koniger etal. 2002). If the most recent absolute age data are cor-rect, A. pedestris ranged from the Gzhelian well into theAsselian (Boy & Schindler 2000).

10. Apateon gracilis (Credner) (Fig. 3B). (Sources: Cred-ner 1881; Boy 1987a; Werneburg 1988b, 1991, 2003;Schoch & Frobisch 2006). This is a small bran-chiosaurid similar to Branchiosaurus salamandroidesin general skull morphology, but sharing a range ofcharacters with all Apateon species, among which it ismost similar to A. pedestris. A. gracilis was describedfrom the Autunian in the very restricted locality ofNiederhaslich near Dresden. Subsequently, Werneburg(1988b) has assigned material from the Oberhof Form-ation in Thuringia to this species. Werneburg (1989a)emphasized the large orbits of gracilis and consideredit more closely related to the genus Melanerpeton, and

referred it to that genus. Our analysis does not sup-port Werneburg’s assignment and we have prejudgedthis conclusion by referring to this species as Apateongracilis. This species has recently been recognised as un-dergoing metamorphosis at 16 mm skull length (Schoch& Frobisch 2006). Character-states 17 and 22 are basedon metamorphosed specimens of A. gracilis.

11. Apateon caducus (Ammon) (Fig. 3E). (Sources: Am-mon 1889; Boy 1972, 1978, 1987a). This is the bestknown branchiosaurid, a large-growing broad-headedform, of which an extensive growth series has beenstudied (Schoch 1992, 2004). It is known exclusivelyfrom the higher parts of the Lower Rotliegend sequence(Gzhelian/Asselian boundary of STD 2002) of the Saar-Nahe Basin.

12. Apateon kontheri Werneburg. (Source: Werneburg1988c). A poorly known species from the Upper Gold-lauter Beds of Thuringia, represented by a few adultspecimens only.

13. Apateon flagrifer (Whittard) (Fig. 3F). (Sources:Werneburg 1986; Boy 1987a). A relatively large,broad-headed species forming the most abundant bran-chiosaurid in the Thuringian region and including theholotype of Watson’s (1963) Branchiosaurus brachy-rhynchus (Werneburg 1989a).

14. Apateon dracyiensis (Boy) (Figs 1D, 1G, 3D). (Sources:Boy 1986, 1987a; Werneburg 1988a, 2001a, 2002). Asmall-growing species with immature features such asa rudimentarily developed jugal and a persisting gapbetween the maxilla and the cheek. Werneburg (1988c)reviewed the status and nomenclature of A. dracyiformisBoy, referring it to A. dracyiensis, a procedure that wefollow. (A. dracyiensis was introduced as a linguistic-ally correct replacement for A. dracyi by Werneburg1988c).

15. Melanerpeton humbergense (Boy) (Figs 4C, 4F).(Sources: Boy 1972, 1974, 1978, 1987a). The only spe-cies of Melanerpeton in the Saar-Nahe Basin. A relat-ively large branchiosaurid with disproportionately hugeorbits and a slender interorbital region.

16. Leptorophus tener (Schonfeld) (Fig. 4B). (Sources:Schonfeld 1911; Boy 1986, 1987a; Werneburg 1988a).A large species with remarkably long snout and a tri-angular skull outline. Found at Clennen in Saxony, oc-curring in reworked pebbles probably of Lower Permianage.

17. Schoenfelderpeton prescheri Boy (Figs 1C, 4A).(Sources: Schonfeld 1911; Boy 1986, 1987a; Werneburg1988a). Described from reworked pebbles from Clennenin Saxony and later from the Goldlauter Formation atTabarz in Thuringia. The most aberrant branchiosaurid,it has a combination of larval features (e. g. short maxilla,dentition) and adult characters (otic notch).

18. Melanerpeton sembachense Werneburg (Fig. 4D).(Source: Werneburg 1989b). Generally very similar toM. humbergense, this form is abundant in the IlmenauFormation of Thuringia and constitutes the stratigraph-ically oldest evidence of Melanerpeton.

19. Melanerpeton eisfeldi Werneburg. (Source: Werneburg1988c). This species from Friedrichroda in Thuringia isa large, perhaps the largest, branchiosaurid reaching 34mm skull length. Originally referred to Branchiosaurusbrachyrhynchus, the material was identified as large

Relationships and evolutionary history of branchiosauridae 7

Figure 3 Cranial morphology of selected branchiosaurids, all showing skull roof in dorsal view. A, Branchiosaurus salamandroides (NMPM332); B, Apateon gracilis (after Werneburg 1991); C, Apateon dracyiensis (after Werneburg 2001a); D, Apateon pedestris (after Schoch 1992);E, Apateon caducus (after Schoch 1992); F, Apateon flagrifer (after Boy 1987). Abbreviations: EO, exoccipital; F, frontal; J, jugal; L, lacrimal; M,maxilla; N, nasal; P, parietal; PF, postfrontal; PM, premaxilla; PO, postorbital; PP, postparietal; PRF, prefrontal; QJ, quadratojugal, SQ,squamosal, ST, supratemporal; T, tabular.

8 R. R. Schoch and A. R. Milner

Figure 4 Cranial morphology of selected branchiosaurids. A-D, skull roof in dorsal view, E-F, palate in ventral view. A, Schoenfelderpetonprescheri (after Boy 1986); B, Leptorophus tener (after Boy 1986); C, Melanerpeton humbergense (after Boy 1978); D, Melanerpetonsembachense (after Werneburg 1989b); E, Apateon pedestris (after Boy 1987); F, Melanerpeton humbergense (after Boy 1978). Abbreviations:EC, ectopterygoid; M, maxilla; Pl, palatine; PS, parasphenoid; PT, pterygoid; QJ, quadratojugal; VO, vomer.

Melanerpeton by Werneburg (1988c, 1989a). The skullroof is poorly known in large specimens, and smallerindividuals assigned to the same species are hardly dia-gnostic beyond family level. In consequence, we reliedonly on the large specimens in our analysis.

Characters

The Branchiosauridae form one of the best-known famil-ies among the Temnospondyli, principally because of thelarge number of available specimens and the excellent

Relationships and evolutionary history of branchiosauridae 9

preservation typical of many Rotliegend localities. The os-teology of the skeleton has been covered in great detail inmore than twenty publications over the last thirty years, start-ing with Boy’s (1972) paper on the composition and defin-ition of the family, which focused on Apateon pedestris (asBranchiosaurus petrolei) from the Saar-Nahe Basin. In addi-tion, most branchiosaurid species are known from a range ofgrowth stages, which make developmental changes readilyrecognized across the group.

Despite this history of descriptive work, there havebeen few attempts to analyze branchiosaurid intrarelation-ships. A probable reason for this hesitation is the sup-posedly high number of homoplasies that were expectedto appear, triggered by the observation in extant salaman-ders that neoteny has repeatedly resulted in raised levels ofhomoplasy (Wake 1996). These homoplasies have been ar-gued to be parallelisms rather than convergences, i.e. theresult of repeated simple modifications of shared develop-mental pathways (Boy 1987a), and comparison of early on-togenies within the genus Apateon supports this (Boy 1974,1978; Schoch 1992). A second reason why branchiosaur-ids have been reported to be especially problematic is thehigh frequency of individual variation. Based on numerouspaedomorphic characters, neoteny has also in this case beenmentioned by Boy (1971) as an explanation for the immaturemorphology and the retention of gills in branchiosaurids wellinto large stages, and this explanation has been accepted eversince. There is very good reason for this hypothesis and in-deed neoteny is a major factor that produces highly variablemorphotypes in salamanders (Hanken 1984).

The following list includes all characters that havebeen analyzed in this study, and multistate characters havebeen ordered wherever ontogenetic character transformationprovides insight into likely pathways for evolutionary modi-fications.

1. Interorbital width/skull length. Narrow (Fig. 1B), notexceeding 0.26 (0), or moderately wide with valuesbetween 0.27 and 0.3 (1), or broad (Fig. 1D) with val-ues markedly beyond 0.3 (2). The clustering of thesemorphometric character-states is clear-cut and order-ing is based on arithmetic rather than ontogenetic ar-guments, since interorbital space proves to be stable inbranchiosaurid ontogeny (Boy 1978; Schoch 1992). Theprimitive condition is clear even in Balanerpeton, whenthe smallest juvenile specimen is drawn into considera-tion (Milner & Sequeira 1994).

2. Prefrontal-postfrontal contact. Prefrontal and post-frontal are either sutured on the dorsal side (Fig. 1B)or always well separated (1). There can be no doubtabout the primitive condition as indicated by numerousavailable outgroup taxa, but for the Dissorophoidea thecase is less clear. However, the stratigraphically oldest(but not necessarily the most plesiomorphic) taxa of mi-cromelerpetontids and amphibamids both have pre- andpostfrontals firmly sutured and so the occurrence of thischaracter-state in branchiosaurids is therefore regardedas primitive.

3. Postfrontal. The postfrontal has a narrow posteromedialpart in the primitive condition (with the exception of Mi-cromelerpeton), Melanerpeton, Leptorophus, Schoen-felderpeton and A. pedestris. In most Apateon species– A. gracilis, A. caducus, A. flagrifer and A. dracyiensis

– the postfrontal is posteromedially extended (Fig. 1D)(1), while in Branchiosaurus salamandroides both stateshave been observed.

4. Contact between maxilla and quadratojugal. These areeither sutured in early ontogenetic stages (0), or growthof the maxilla is slowed down with late suturing (1), orelements fail to meet (Figs 1D, 1G), leaving a gap inthe cheek (2). The three states are obviously correlatedwith ontogenetic character transformation (2>1>0), andoutgroup comparison indicates clearly that the adult state(0) is the primitive condition.

5. Jugal-lacrimal contact. The jugal is clearly sutured tothe lacrimal (0), or is separated by it by either a gap or alaterally exposed palatine (1).

6. Shape of supratemporal. Primitively, the anterior portionof the supratemporal is blunt and not much narrower thanthe greatest width of the element (Fig. 1D) (0). In mostMelanerpeton, Leptorophus and Schoenfelderpeton, theanterior end is pointed to give the element a triangularoutline (Fig. 1C); the squamosal compensates this spacewith a medial projection (1).

7. Medial suture of supratemporal. The supratemporal iswide with a straight or convex medial suture (0), ormuch narrower and medially concave (1). The derivedstate is interpreted as having evolved twice, which issuggested not only by incongruence, but also by thepolymorphic variation in A. caducus as contrasted withthe Melanerpeton-clade where this character-state ap-pears to have been fixed.

8. Parietal/frontal width. In all outgroups, the parietalis wider than the frontal, and this is also the casein Melanerpeton, Leptorophus, Schoenfelderpeton, andBranchiosaurus (0). In Apateon dracyiensis, A. caducusand A. flagrifer both elements are of equal width, irre-spective of the width and shape of the supratemporal (1).A. gracilis, A. pedestris and A. kontheri have retained theprimitive condition throughout ontogeny.

9. Postparietal length. Primitively, the postparietal islonger than the tabular (0). In Micromelerpeton, it is onlyslightly longer than the tabular, but still has a rectangularoutline. Within Apateon, the postparietal is substantiallyshortened and overplated by the parietal anteriorly in A.caducus and A. dracyiensis with only its posteriormostmargin exposed on the dorsal side (1).

10. Length of posterior skull table. In the primitive condi-tion, the skull table is elongated with extended supratem-porals and parietals (Fig. 1A) (0), a state that is retainedin Melanerpeton Leptorophus, and Schoenfelderpeton.In Branchiosaurus and all species of Apateon, the pos-terior skull table is foreshortened as indicated by theblunt and stout shape of parietals and supratemporals(Fig. 1B) (1).

11. Jugal anteriorly abbreviated. Irrespective of its lost con-tact to the lacrimal, the jugal may be either anteri-orly long (Figs 1A, 1B, 1E, 1F) (0), or it may lackthe anterior process and end bluntly (Figs 1C, 1F, 1G)(1).

12. Occipital flange. Postparietal and tabular with continu-ous, narrow flange of equal width (Fig. 1A) (0), or flangeformed by wide paired posterior processes of the post-parietal (Fig. 1B) (1), or flange restricted to the mid of thepostparietal region, but projecting well to the posterior(Fig. 1D) (2).

10 R. R. Schoch and A. R. Milner

13. Supratemporal and tabular laterally constricted. Thelateral margin of the supratemporal and tabular is straight(0), or concave because of a medial expansion of the oticnotch (1).

14. Intertemporal absent. The presence of an intertemporalis a heritage from the earliest tetrapods (0), while in mosttemnospondyls, this bone is absent (1).

15. Morphology of tabular horn. The tabular horn developseither continuously from the posterolateral corner of thetabular (0), or is set off from the skull table by a groove,irrespective of its relative size (1).

16. Size of tabular horn. The tabular horn is poorly estab-lished in the primitive condition, forming small or tinypointed projections from the main body of the tabular(0), while in Branchiosaurus and some Apateon species,the horns are generally much larger, occupying nearlyhalf the area of the element (1). The derived state devel-ops into a very large and posteromedially curved tabularhorn in large adults (Fig. 3E) (Schoch 1992), which isan autapomorphy if compared with outgroups across theTemnospondyli.

17. Distance of otic notch to orbit. Primitively, the suturebetween supratemporal and squamosal is long and theorbit is well separated from the otic notch (Fig. 1A) (0).In the derived condition, the otic notch is much expandedanteriorly by an abbreviated squamosal-supratemporalsuture, and the squamosal is foreshortened in its medi-almost part.

18. Width of maxillary shelf. The main dentigerous bodyof the maxilla is slender in the primitive condition(Fig. 1E) (0), while in Apateon it is markedly broadened,especially in adult and/or large specimens (Fig. 1F) (1).

19. Bicuspidity. The crowns of marginal and palatal teethare primitively monocuspid (0), but are clearly bicuspidin derived amphibamids (1).

20. Nasal/frontal width. Primitively, the nasal is muchbroader than the frontal (0), while in the derived con-dition nasal and frontal differ little in width (Fig. 1C)(1).

21. Postorbital separated from supratemporal. In the prim-itive condition, the supratemporal has a broad suturewith the postorbital (0). In Leptorophus (Fig. 4B) andSchoenfelderpeton (Fig. 4A), a posterolateral projectionof the postfrontal keeps the tiny postorbital apart fromthe supratemporal (1), see Boy (1986) and Werneburg(2001b).

22. Quadrate condyle position. The jaw articulation is wellposterior to the occipital articulation (0), whereas in thederived state, both joints are at the same level (1).

23. Parasphenoid, basal plate. The basal plate of the paras-phenoid has slightly concave lateral margins in the prim-itive condition (0), which is greatly accentuated in thederived state where large anterior and posterior lateralprojections have developed (Fig. 1I) (1).

24. Marginal elements of palate. The palatine ramus ofpterygoid, ectopterygoid, and palatine are reduced in allbranchiosaurids (characters 23, 24). In Branchiosaurusand Apateon these elements are still well-ossified androbust, bearing numerous tiny teeth arranged in severalrows or one row of large teeth (Fig. 4E) (0). In the de-rived condition, these elements are extraordinarily del-icate and poorly ossified, and have either few denticlesor are edentulous (Fig. 4F) (1).

25. Pterygoid-vomer contact. The anterior ramus of thepterygoid is either long and sutured with the vomer lat-erally (0), or well-separated from the vomer, with partof the palatine forming the margin of the interpteryg-oid vacuity (1). This character-state is clearly definedin both branchiosaurids and Micromelerpeton, whileSclerocephalus and all other plesiomorphic temnospon-dyls have the primitive state (Milner 1993).

26. Pterygoid, lateral flange. The base of the palatine ramusof the pterygoid has a straight parasagittal lateral margin(0), while in the derived condition the palatine ramusbears an upcurved lateral projection, here called the lat-eral flange (1). We avoid the term ‘transverse flange’,because this is restricted to a different anatomical struc-ture in amniotes.

27. Width of palatine and ectopterygoid. These elementsare either attached to the maxilla throughout their lat-eral margins (Fig. 1H) (0), or the ectopterygoid andthe posterior portion of the palatine are well separatedfrom the maxilla, with the palatine attaining a Y-shapedoutline (Fig. 1I) (1). This character forms the secondrobust support for the monophyly of the Branchiosaur-idae. In addition to its uniqueness among temnospon-dyls, this state differs essentially from the highly de-rived condition in amphibamids where the palatine andectopterygoid are extremely slender but attached to themaxilla, giving distinctly wider interpterygoid vacuitiesthan in branchiosaurids or dissorophids, for instance.The peculiar branchiosaurid condition is acquired earlyin development (Schoch 1992) and was maintained wellinto the largest growth stages (Boy 1978; Werneburg1991).

28. Anterolateral region of palatine. This has either a nar-row lateral process clearly shorter than the main bodyof the element (0), or prominent branch forming thecentre of the bone (1). The derived state characterizesall branchiosaurids.

29. Ectopterygoid. This forms a slender elongate elementin the primitive condition, which is retained in bran-chiosaurids (Figs 4E, 4F) (0). In Apateon caducus(Fig. 3E) and A. flagrifer it is abbreviated and secondar-ily wider than in the primitive branchiosaurid condition(1).

30. Parasphenoid, carotid foramina. The carotid foraminaand grooves are on the basal plate (Fig. 4E) (0), or altern-atively they are situated on the sides of the cultriformprocess (1).

31. Parasphenoid, denticle field. This region either bearsa raised deltoid area densely covered with denticles(Fig. 1H) (0), or a poorly defined area with loosely setpits (Fig. 4F) (1), or remains entirely smooth (Fig. 1I)(2). The plesiomorphic state is found consistently inthe outgroups, and it is probably the primitive condi-tion for dissorophoids. In branchiosaurids there are onlytwo well-known species that retain what appears to bea rudimentary denticle field (1), Branchiosaurus sala-mandroides and Melanerpeton humbergense (Fig. 4F).In Schoenfelderpeton this region has an irregular surfacebut there is not even a denticle field, while all Apateonspecies are characterized by smooth surfaces apart fromsome very old specimens of A. pedestris (Schoch 1992),which indicate that this character-state might have beenpostponed in development.

Relationships and evolutionary history of branchiosauridae 11

32. Branchial dentition. Primitively, there are four rows ofbranchial denticles which are attached to rectangular oroval platelets bearing a total of 3–10 denticles (Fig. 2C1)that form a ratchet, as two of the outgroups indicate (0),or there are six rows of isolated denticles with a singlepoint (Fig. 2C2), or multi-ended (Fig. 2C3) (1).

33. Presacral count. Primitively a total of 25–29 presacralvertebrae are present (0), while fewer than 24 presac-rals is clearly derived (1). All branchiosaurid specieshave fewer than 24 presacrals as an average, and mosthave only around 20 (Fig. 2A) (Boy 1972, 1978, 1987a).The reduction of the presacral count to fewer than 24is observed in the Amphibamidae as well, but there itis clearly a derived character-state characterizing only asingle species, Amphibamus grandiceps, while the prim-itive condition for the family is 24 presacrals (Clack &Milner 1994; Daly 1994).

34. Interclavicle. The interclavicle is rhomboidal and at leastas large as the posterior skull table (Fig. 2B1) (0), orpentagonal to quadrangular, reaching half the size of theposterior skull (Fig. 2B2) (1), or much abbreviated andtransversely oval, at best reaching the size of the post-parietals (2). Boy (1987a) has mentioned ontogeneticchanges in the morphology of the interclavicle, suggest-ing that state (1) preceded state (2) ontogenetically inthe most advanced clade (Apateon pedestris through A.dracyiensis). The interclavicle of Melanerpeton humber-gense departs from all other morphologies, but may bemost readily derived from that of other Melanerpeton-clade species or Branchiosaurus.

35. Humerus, foramen. An entepicondylar foramen piercesthe humerus in the primitive condition (0), and is lost inthe derived state (Fig. 2D) (1).

36. Humerus, morphology. The humerus length:waist ratiois 3:4 in Dendrerpeton, Balanerpeton, Sclerocephalus(Fig. 2D) (0); 4:6 in Micromelerpeton and the bran-chiosaurid Schoenfelderpeton (Fig. 2D2) (1), and 6:10in amphibamids (Fig. 2D3) and most branchiosaurids(2). We admit that this character may be problematicwhen the profound ontogenetic changes in large temno-spondyls are considered (e.g., Schoch 1999; Pawley &Warren 2006), but for comparisons among small dissor-ophoids and especially branchiosaurids it does appear tobe informative.

37. Dorsal osteoderms. The lateral and dorsal osteodermsare usually covered with numerous fine rings of accre-tion e.g. in Sclerocephalus and in the Melanerpeton-group (0), whereas in other taxa they are smooth or withradiating striations (1).

38. Ventral osteoderms (‘gastralia’). Spindle-shaped ventralosteoderms fully ossified (0), or absent (1). This is onlyrecognized in large specimens, where osteoderms arefully formed (Boy 1987a). The plesiomorphic character-state is present only in Branchiosaurus, while all otherbranchiosaurids lack spindle-shaped ventral osteodermsin adult stages.

39. Supinator process. A supinator process is present nearthe distal end of the humerus (0), or is absent (1).The derived state is present in one of the outgrouptaxa (Balanerpeton) and in all branchiosaurids andamphibamids.

40. Anterior ribs. The anterior trunk ribs have widened ends(0; Fig. 2A), or are simple rods without distal expan-

sion (1). The apomorphic character-state is present inthe amphibamids Platyrhinops, Amphibamus, and Mi-cropholis.

Results

Relationships

1. The Branchiosauridae are monophyletic with respect toall other ingroups analyzed here (Fig. 5A).

2. Within the Dissorophoidea, Micromelerpeton forms themost basal taxon, followed by the slightly more derivedEcolsonia and finally a clade formed by branchiosauridsand amphibamids. Within this, Micropholis is the sistergroup of all the others, which then fall into Amphibamus+ Platyrhinops on the one hand and the Branchiosauridaeas a whole on the other hand (Fig. 5A). If Micropholisis considered to be an amphibamid (Schoch & Rubidge2005) then this implies that the Amphibamidae are para-phyletic with respect to the Branchiosauridae, i.e. that theBranchiosauridae are a subgroup of paedomorphic am-phibamids. However, in view of the continuing researchin this area we feel it would be premature to modify thefamily-level systematics of these genera.

3. The Branchiosauridae encompass a single basal taxonfrom the Upper Carboniferous (Branchiosaurus salaman-droides) and a clade comprising all the other species asits sister taxon (Fig. 5A).

4. The post-Branchiosaurus branchiosaurids fall into twoclades, a five-species group comprising Melanerpetonhumbergense, M. sembachense, M. eisfeldi, Leptorophustener and Schoenfelderpeton prescheri (here referred toas the Melanerpeton-clade), and a larger group that en-compasses all the species of Apateon (Apateon-clade) ex-amined during this work (Fig. 5A).

5. Within the Melanerpeton-clade, L. tener and S. prescheriare sister taxa; M. humbergense and M. sembachense forma grade of uncertain relationships and M. eisfeldi is themost primitive form (Fig. 5A).

6. The intrarelationships within the Apateon-clade have beenresolved as follows: A. gracilis and A. kontheri form anunresolved trichotomy with all other species of Apateon.Obviously the poor knowledge of A. kontheri does notallow for a more detailed resolution. The more derivedspecies of Apateon form a clade composed of A. pedestrisas the most basal species, followed by A. dracyiensis andthen the monophyletic A. flagrifer and A. caducus.

Robustness of nodes

1. A sister-group relationship between the Branchiosauridaeand the two amphibamids Platyrhinops and Amphibamusis supported by one step Bremer support and two unequi-vocal synapomorphies (10, 12) (Fig. 5A). The close re-lationship between Amphibamus and Platyrhinops is stillmore robust, indicated by a high Bootstrap (97%), a 4-stepBremer support, and two unambiguous synapomorphies(13, 19).

2. The monophyly of the Branchiosauridae is supportedby a 77% Bootstrap value, a Bremer support of threesteps, and two unambiguous synapomorphies (22R, 27)(Fig. 5A).

12 R. R. Schoch and A. R. Milner

Figure 5 Phylogenetic analysis of the Branchiosauridae. A, Consensus of two most parsimonious trees; B. Alternative patterns of relationshipwithin Melanerpeton-group. Black rectangles represent nodes defined by unequivocal synapomorphies, grey rectangles represent nodesdefined by equivocal synapomorphies (reversals and homoplasies).

3. The monophylum formed by the Melanerpeton-clade andthe genus Apateon is suggested by a Bremer Support oftwo steps and three synapomorphies (?4, 11∗ 33–2).

4. The Melanerpeton-clade is supported by a Bootstrap of68% and one unambiguous synapomorphy (24) (Fig. 5A).

5. A sister group relationship of Schoenfelderpeton pres-cheri and Leptorophus tener is indicated by a Bootstrapof 52% and two unambiguous synapomorphies (21, 30)(Fig. 5A).

6. The monophyly of Apateon is supported by a Bootstrap of57% and three unambiguous synapomorphies (15, 18, 37).

7. A monophylum formed by A. pedestris, A. dracyiensis, A.flagrifer and A. caducus is supported by a 63% Bootstrap,but no unambiguous synapomorphies (Fig. 5A).

8. The hypothesis that the broad-headed species A. dracyi-ensis, A. flagrifer and A. caducus are monophyletic issupported by a 79% Bootstrap, 2 Bremer steps, andby two equivocal derived character-states (16∗, 34–2∗)(Fig. 5A).

9. Finally, the sister group relationship between A. flag-rifer and A. caducus is indicated by a 89% Boot-strap, a 2-step Bremer support, and one unambiguous

Relationships and evolutionary history of branchiosauridae 13

synapomorphy (29) plus an equivocal character-state(?7∗) (Fig. 5A).

Diagnoses of Branchiosauridae

The above analysis results in the following critical diagnosesfor the Family Branchiosauridae and its constituent generaas follows. All characters are derived unless specified asprimitive.

Branchiosauridae Fritsch, 1879

DIAGNOSIS. Palatine with prominent process extendingfrom centre of bone laterally to the maxilla; six rows of isol-ated branchial denticles which are slender and multi-ended;21–22 presacral vertebrae (reversed to longer in some forms).

CONTENT. The genera Branchiosaurus, Apateon, Melaner-peton, Leptorophus and Schoenfelderpeton.

Branchiosaurus Fritsch, 1876

DIAGNOSIS. Plesiomorphic branchiosaurid with no autapo-morphies. Retains prefrontal-postfrontal contact (shared asreversal with Apateon dracyiensis); retains anteriorly exten-ded jugal; retains ventral osteoderms.

CONTENT. Branchiosaurus salamandroides Fritsch, 1876.

Post-Branchiosaurus clade

DIAGNOSIS. Prefrontal-postfrontal contact lost (reversed inA. dracyiensis); maxilla sutures with quadratojugal late indevelopment or not at all; jugal anteriorly abbreviated; noossified ventral osteoderms.

CONTENT. Apateon, Melanerpeton, Leptorophus andSchoenfelderpeton.

Apateon Meyer, 1844

DIAGNOSIS. Tabular horn separated from skull table by agroove; tooth-bearing region of maxilla broad; dorsal osteo-derms smooth or with radiating striations.

CONTENT. Apateon pedestris, A. gracilis, A. caducus, A.kontheri, A. flagrifer, A. dracyiensis.

‘Melanerpeton-group’

DIAGNOSIS. Palatine, ectopterygoid and palatine ramus ofpterygoid all extremely delicate, poorly ossified and withfew or no denticles.

CONTENT. Melanerpeton, Leptorophus and Schoenfelder-peton

Melanerpeton Fritsch, 1878

DIAGNOSIS. This genus appears to be paraphyletic with re-spect to the Leptorophus-Schoenfelderpeton group and hasno autapomorphies.

CONTENT. M. humbergense, M. sembachense, M. eisfeldi.

Leptorophus-Schoenfelderpeton group

DIAGNOSIS. Clade characterised by postorbital separatedfrom supratemporal; carotid foramina and grooves situatedon sides of the cultriform process.

CONTENT. Leptorophus, Schoenfelderpeton.

Leptorophus Bulman & Whittard, 1926

DIAGNOSIS. Long triangular skull; anterior parts of nasaland vomer elongated; prefrontal and postfrontal very close;elongated narial openings; maxilla extends far posteriorly;quadrate condyles posterior to occipital condyles; vomer withlong posteromedial processes, which is unique among bran-chiosaurids.

CONTENT. Leptorophus tener.

Schoenfelderpeton Boy, 1986

DIAGNOSIS. Skull overall broad with enlarged otic notch;posterior skull table wider than in Melanerpeton and Lept-orophus; supratemporal anteriorly pointed; postfrontal maybe subdivided; humerus very short, represented only by ossi-fied mid-shaft. Altogether this is probably the most neotenicspecies of branchiosaurid.

CONTENT. Schoenfelderpeton prescheri.

Affinities of Poorly Known

Branchiosaurids

There is a range of branchiosaurids or potential branchiosaur-ids that are too inadequately known to permit their inclusionin a reasonable phylogenetic analysis. These are either basedon immature specimens or on incomplete/poorly preservedmaterial. Here, we attempt to fit these taxa into the proposedphylogenetic concept by referring to the available evidence ofderived character-states. They fall into the following groups:

a) Branchiosaurids forming diagnostically distinct speciesbut being insufficiently known:1. Melanerpeton pusillum from Olivetın near Broumov,

Czech Republic was studied in depth by Werneburg(1986) and discussed by Boy (1987a, as Apateon). Itspalate is not well-known, which precludes thoroughassessment of relationships. The skull roof resemblesthat of Melanerpeton humbergense most closely, butappears more juvenile; the maxilla does not reach thequadratojugal, at least not in the smaller specimens,while the shape of supratemporal and parietal is verysimilar to other species of the Melanerpeton-clade.On the other hand, Boy (1987a) emphasized similar-ities with Apateon in the more robust morphology ofthe palate. While an assessment of its affinities clearlyrequires complete material, we regard it most parsimo-nious to leave M. pusillum in the genus Melanerpeton,until a complete description becomes possible. Thisseems the most practical procedure, since M. pusil-lum is the type species of the genus and if it provedto be distinct from the attributed species, Melaner-peton should be abandoned in favour of Leptorophusfor those species.

14 R. R. Schoch and A. R. Milner

2. Apateon intermedius (Werneburg, 1996) from theStephanian D of Stutzerbach in Thuringia is more sim-ilar in the few well-preserved regions to Melanerpetonthan to Branchiosaurus or Apateon, but the palatalelements are too poorly preserved to allow detailedcomparisons and analysis of character-states as dis-cussed in the present context. The main character-state it shares with the Melanerpeton-clade is theshape of the supratemporal combined with an elong-ated posterior skull table. According to Werneb-urg, it also preserves a prefrontal-postfrontal con-tact while the interorbital width is small as in Bran-chiosaurus and Melanerpeton. Phylogenetic analysisof the few available data puts this taxon in an un-resolved trichotomy with the two major clades ofbranchiosaurids.

b) Poorly diagnostic branchiosaurids whose assignment ishampered by juvenility of the only known specimensand/or the lack of (aut)apomorphic character-states:3. Branchiosaurus fayoli (Thevenin, 1906) from the

Stephanian C of Commentry, Allier, France, has beenbriefly discussed by Boy (1987a) who assigned it toBranchiosaurus sensu stricto on the basis of symple-siomorphies plus the absence of synapomorphies ofeither of the other genera. It retains ventral osteoderms,a primitive character-state shared within the familyonly by B. salamandroides. The palate is, however,too little known to reasonably diagnose the species,and including it in the present discussion would onlyraise more questions, although it marks a stratigraph-ically interesting occurrence.

4. Melanerpeton arnhardti (Werneburg, 1988b) fromLochbrunnen in Thuringia is a small branchiosauridwith affinities to M. humbergense but too juvenile topermit definitive assignment. In contrast to M. sem-bachense and M. eisfeldi, this species has a wide nasallike M. humbergense.

5. ? Apateon umbrosus (Fritsch, 1879) is based on a fewvery poorly preserved specimens from Olivetın nearBroumov, Czech Republic. Morphologically, the fewpreserved remains could pertain to any branchiosaurid,although the wide interorbital region points to thegenus Apateon.

c) Taxa claimed by other authors to be either branchiosauridsor close to the Branchiosauridae, but which lack criticalsynapomorphies of the Branchiosauridae.i) Milnererpeton huberi (Hunt et al. 1996, 2002) from

the Upper Pennsylvanian Wild Cow Formation ofNew Mexico is a branchiosaur-like specimen. Theholotype and only specimen is a tantalizing discov-ery which unfortunately lacks any clear evidence onthe morphology of the palatine, ectopterygoid andpterygoid but clearly possesses elongated and singlebranchial denticles. Although similar to those of truebranchiosaurids, these denticles differ markedly by be-ing very long and needle-shaped, as well their singleends. Otherwise, the morphology of the palate andoccipital rim of the skull table is much more similarto branchiosaurids, notably the genus Apateon, thanto amphibamids sensu stricto. The synapomorphiesshared by Platyrhinops and Amphibamus are all ab-sent, but still the available information is too poor asto permit further assignment.

ii) Tungussogyrinus bergi (Efremov 1939, 1953;Shishkin 1998) is from the Permo-Triassic BugariktaFormation of the Tunguska Basin, Siberia. As in theformer case, the specimens do not allow any clear as-signment to the Branchiosauridae, although the mor-phology and configuration of the palatine, parasphen-oid, and pterygoid is quite similar to that of bran-chiosaurids. However, Shishkin (1998) also describedclear-cut differences between Tungussogyrinus and allbranchiosaurids, which in concert with the lack ofclear branchiosaurid synapomorphies makes his refer-ral doubtful. For instance, there is no evidence for theexistence of branchial denticles.

Evolutionary History of The

Branchiosauridae

Palaeobiological implications

Boy (1972) developed aspects of an evolutionary scenario,which attracted little attention at the time but since parts of ithave recently been published in English (Boy & Sues 2000),it has begun to be cited (Carroll 2002). In the following, weshall expand on Boy’s arguments by including developmentaland morphological observations that have been publishedsince. The main question of this section is: given that thephylogenetic hypothesis employed here is correct, how canthe recognized patterns (synapomorphies, autapomorphies,homoplasies, and symplesiomorphies) be interpreted in anadaptational context?

There is reason to hypothesize that the Branchiosaur-idae originated by evolution of a key innovation, parts ofwhich have been reconstructed by Boy (1972, 1978). Thishypothesis is supported by (i) the unique status of all bran-chiosaurids, which is both developmentally and morpholo-gically well-defined, and (ii) the palaeoecological data fromthe Rotliegend lake deposits that document the evolutionarysuccess of the clade.

The branchial skeleton typical of temnospondyl larvaeconsisted of mostly cartilaginous ceratobranchial bars thatstiffened the three gill clefts on each side. (The presence ofexactly three gill clefts is indicated by the frequent preserva-tion of three external gills in several branchiosaurid species).The epithelium surrounding these bars housed small oss-icles of variable shape and size that bore tooth-like denticles(Fig. 2C1). These are known from a range of taxa, includ-ing the dissorophoids Micromelerpeton and Branchierpeton(Boy 1972, 1995; Boy & Sues 2000; Schoch & Milner 2000).These ossicles appear to have occurred in four rows, one rowon each gill bar. Many authors have confused these dermalossicles and the denticles they bear with gill rakers, whichare actually endoskeletal structures growing out of the cerato-branchials, but in our view (Schoch 2001) they are two func-tionally convergent but non-homologous structures. There-fore, we see no continuity between the branchial denticles ofbranchiosaurids and the gill rakers of salamanders, as Carroll(2007) has assumed.

In branchiosaurids, the branchial ossicles formed ajaw-like apparatus that may have served (i) to hold backprey items or organic detritus in the process of leaving thepharyngeal cavity with the water current, and (ii) to form a

Relationships and evolutionary history of branchiosauridae 15

zipper-like, tightly interfingering apparatus providing tightclosure of the gill cleft when necessary during feeding.This hypothesis is supported by the apparent occurrence ofbranchial denticles in Recent salamanders (Worthington &Wake 1971) and the functioning of similar, albeit cartilagin-ous processes of the ceratobranchials, so-called gill rakers.While branchial denticles and gill rakers are of differentembryological and histological origin and must not be con-fused (Schoch 2001), the branchial ossicles of temnospon-dyls could well have served both functions (their morpho-logy suggests them to be homologues of branchial denticlesin salamanders, rather than gill rakers).

Branchiosaurids have a rather different pharyngeal den-tition: they lack the platelets to which the denticles are at-tached in other temnospondyls, but have an increased numberof denticles in six rows – in a 1.2.2.1 configuration on the fourbranchial arches, thus lining each gill-slit with two opposingrows of denticles. The denticles have numerous, brush-likebranches (Fig. 2C3) instead of a single pointed crown (Boy1972, 1978, 1986). These branches are remarkably variablein their orientation and distance to each other, and often theyare curved as if they had been flexible. Based on very richevidence, Boy (1978) suggested that these ‘brushes’ werenot fully mineralized, allowing for considerable flexibility;our observations agree with this suggestion throughout. Anadditional observation is the occurrence of denticles with aball-shaped base, suggesting that each element was moveablyattached to the ceratobranchial. This however also occurs injuveniles of Mordex and Platyrhinops from Nyrany wherethe ossicles are less brush-like (Fig. 2C2) and may be a morewidespread post-micromelerpetontid feature within the Dis-sorophoidea (Milner, pers. obs.).

Together these observations suggest that branchiosaur-ids had acquired an unorthodox pharyngeal apparatus thatpermitted filtration of tiny items borne by the water current.Filter-feeding for planktonic prey seems to be the most plaus-ible explanation. It seems logical that branchiosaurids wereable to explore a promising niche by this mechanism, andthat no other lower tetrapod clade seems to have achievedthis at that time. Filter-feeding as the primary mechanismwould explain the retarded growth of the maxilla and thecheek elements in many branchiosaurids. Interestingly, largerspecimens of some Apateon species (A. pedestris and A. ca-ducus, Boy 1978) had abandoned (resorbed?) the brush-likeends of their branchial denticles, if not the whole denticle,which coincides with a consolidation of the cheek and anenlargement of the tooth arcade in the upper jaw.

Evolutionary Scenario

All phylogenetic analyses (Boy 1972, 1978; this study) sug-gest that there was a basal dichotomy in the phylogeny ofbranchiosaurids, giving rise to the morphologically diverseMelanerpeton-clade and the morphologically conservativegenus Apateon (Fig. 6). The exact position of the Westphaliangenus Branchiosaurus does not critically affect this matter.Whatever its position, it represents the primitive conditionmore completely than any other branchiosaurid. We cannotbe certain that it did not metamorphose. The most primit-ive Apateon, A. gracilis, metamorphosed at about 15–18 mmskull length (Schoch & Frobisch 2006) and we know of noB. salamandroides with a skull length greater than 12 mm(ARM pers. obs.). If Branchiosaurus did metamorphose, then

full neoteny developed twice, once within the Apateon cladeand once at the base of the Melanerpeton clade.

The large number of presently known Apateon speciesmay be a product of the diversified landscape in CentralEurope, which was located in the middle of the Variscanorogen. The Saar-Nahe Basin lakes appear to have been pop-ulated by different species from the Saale and ThuringianBasins (e. g. Saar-Nahe: Boy et al. 1990, Thuringia: Werneb-urg 2001b).

Melanerpeton-clade species were less abundant andtheir generally larger size probably permitted them to oc-cupy different niches in lake ecosystems. It has been arguedthat these niches were eventually occupied by micromel-erpetontids instead (Boy 1995). The majority of Apateonspecies appear to have been without competitors and werethus successful invaders in almost every preserved lake. Inthe Thuringian region, Melanerpeton was more common andmore speciose, although most species recognized by Werneb-urg (1989a) may in fact represent a chronological sequenceof a lineage evolving in the same basin.

The dichotomy between the Melanerpeton clade andApateon does not correlate with the acquisition of obviousevolutionary innovations, and many phylogenetic trends ob-viously occurred in parallel in both groups; some of themoccurred even more than twice.

The intrarelationships and ecological adaptations ofApateon species are better understood also because they arepreserved in greater detail, larger quantities and are repres-ented by broader size ranges. The geologically oldest bran-chiosaurid, B. salamandroides, retained primitive featureslike spindle-shaped ventral osteoderms and a rudimentarydenticle field on the parasphenoid, the significance of whichis difficult to assess. The adaptational background of thisnovelty is difficult to assess because of its complexity. AsBoy (1972) noted, it is probably correlated with the jaw mus-culature, one of the main functional complexes that occupythis region. (The other critical units are the hindbrain andotic capsules, which probably remained relatively unaffectedbecause of their internal position). An abbreviation of themuscle-bearing cavity implies either a rearrangement or re-duction of adductor musculature, caused by a decrease innumber of muscles, or (more likely) simply a reduction oftheir physiological diameter. However, the abbreviation ofthe skull coincides with a markedly smaller size than in theancestral condition, which is indicated both by the outgroupsand by its sister taxon, the Melanerpeton clade. Given thatsmaller animals can function with disproportionately smallermuscle masses and average diameters (surface to volume ra-tio), the postorbital abbreviation may be just a by-product ofa scaling effect. This hypothesis is supported by the observa-tion that – throughout branchiosaurids and other temnospon-dyls – the postorbital skull and cheek in particular underwentstrong allometric growth in later larval development (Boy1972; Witzmann & Pfretzschner 2003). In branchiosaurids,this is best exemplified by moderately large or large speciessuch as Melanerpeton humbergense, Apateon pedestris andA. caducus (Boy 1978; Schoch 1992).

The origin of the genus Apateon involved two innov-ations: (1) a marked broadening of various skull elementsresulting in a greater skull height, and (2) a general shorten-ing of the interclavicle with a concomitant pronunciationof the posterior process, and a taxonomically more con-strained outline of the element. The first change includes four

16 R. R. Schoch and A. R. Milner

Figure 6 Evolutionary scenario for the origin and diversification of the Branchiosauridae as suggested by this work. The origin of theBranchiosauridae was made possible by a key innovation (filter-feeding), which was then elaborated and modified along various lines. Neoteny,a probable factor already in the most ancient and plesiomorphic taxon, played a major role in branchiosaurid evolution. In the scenario depictedhere, the capacity to metamorphose into fully terrestrial adults was regained once in Apateon gracilis. An alternative scenario would be that B.salamandroides still metamorphosed (no large individuals are known) and neoteny evolved twice, once at the base of the Melanerpeton cladeand once within the Apateon clade post-A. gracilis.

apparent synapomorphies: the broadening of the palatine,the frontal, the maxilla, and the cheek elements (especiallyjugal and quadratojugal). This indicates that the robustness ofthe monophyletic concept for Apateon may be grossly over-weighted, but there are contra arguments, as well: within theMelanerpeton clade, a broadening of the cheek bones ap-parently occurred in parallel, but neither the palatine nor thefrontal were altered in this direction. Instead, skull width wascontrolled by the widening of the cheek and the retention ofrelative large orbits, interpreted here as a primitive character-state for the Branchiosauridae. The broader and higher skullof Apateon does not strictly correlate with other, eventuallysignificant changes, only that in those species that did meta-morphose, skull width was markedly increasing in adults.

Broad skulls have been mentioned by Schmalhausen (1968)to have an impact on buccal respiration, which is selectedfor in terrestrial adults. This, however, explains only the pro-nounced adult shift in skull width, which is managed by abroadening of the postorbital and squamosal in the first range(Werneburg 1991; observations by the authors). The skull ofApateon is wider than that of Branchiosaurus and the primit-ive condition, even in small larvae, indicated by the morpho-logy of the palatine and frontal in tiny larvae (Schoch 1992).Schoenfelderpeton also has a wider skull than its relatives,though this results from rather different causes (apomorphicmorphology of the supratemporal, squamosal, tabular, andparasphenoid). However, Schoenfelderpeton also has a veryshort maxilla and a wide open cheek which is found in many

Relationships and evolutionary history of branchiosauridae 17

lineages within the genus Apateon, where the maxilla reachedthe cheek much later than in the ancestral condition or notat all.

The posteriorly free short maxilla, an open cheek, anda palatine and ectopterygoid not tightly suturing with themaxilla co-occur in many branchiosaurids. This conditionwas certainly a transitional stage for Branchiosaurus andMelanerpeton, which is demonstrated in small larvae ofMelanerpeton, but in Apateon it was extended and sometimespersisted in adult stages, likewise in Schoenfelderpeton. Ourargumentation is based on the following observations: (1)the short maxilla indicates that the gape was rather short,(2) the maxilla was not tightly attached to the palatine, (3)the premaxilla and maxilla were not tightly sutured either,but had a slightly overlapping contact if at all, and (4) thebasicranial articulation remained unossified, thus was prob-ably moveable. We speculate that the maxilla was at leastslightly moveable, being loosely attached to the premaxillaand the palatine lateral branch by means of connective tis-sue. This speculation is supported by detailed investigationof extant salamander larvae (Ranodon, Ambystoma, Dicamp-todon), where such a construction is established. (We do notclaim this situation to be homologous, but the parallels arecompelling and suggest it is functionally analogous).

In many modern species among aquatic salamandersand teleosts, the mouth margin can be modified by rotationof the maxilla, by that forming a rounded, anteriorly-facingmouth (Larsen 1963; Lauder & Shaffer 1993; Deban & Wake2000). This mechanism evolved independently in salamanderlarvae and teleosts. The similarities are largely at the func-tional level, as morphology differs broadly between theseclades. The main point is that both mechanisms employ acontrolled mode of suction-feeding in which intracranial kin-etism creates a buccal cavity that guarantees (1) a focused,directional suction of prey and (2) an increased suction effectdue to the expansion of the buccal floor by a posteroventralpull of the hyobranchial apparatus. This mechanism is usefulfor both feeding on single large prey and suspension feeding,because the main factor is the increased water volume thatcan be dealt with. The findings on branchiosaurids suggest aroughly similar mechanism, although it remains unclear howlarge the impact of a moveable maxilla might have been. Yeteven if the maxilla remained immobile, suction was probablygenerated by hyobranchial depression. The hyobranchial ap-paratus of branchiosaurids compares well with that of larvalsalamanders (Boy 1974).

If the concept of modified suction-feeding in bran-chiosaurids has any explanatory value, the recognized dis-tribution of morphologies among the different clades ofApateon permits a heuristic narrative to be constructed. Thefirst cornerstone of the branchiosaurid key innovation wastheir modified branchial “dentition” which allowed suspen-sion feeding. The second cornerstone is formed by the lightconstruction of the palate, especially the reduced maxillo-palatine contact. If this was a means to generate elaboratedsuction, it was certainly as significant as the first innova-tion. It is likely that both novelties formed an adaptationallyintegrated whole, although this is almost impossible to prove.

There is substantial evidence that ontogeny was subjectto change in the evolutionary history of the Apateon-clade.Apateon gracilis and A. pedestris are relatively small formsof which the former reached metamorphosis at a skull lengthbeyond 15 mm (Werneburg 1991; Schoch & Frobisch 2006).

Both species went through an extended phase in which thecheeks remained unossified and the maxilla short, suggestingelaborate suction-feeding that focused on planktonic nutri-tion. Prior to transformation in A. gracilis, the gape wasgreatly expanded, larger teeth appeared, and the maxilla andcheek were consolidated. Postcranial features indicate thattransformed Apateon gracilis was terrestrial and thus gravityand biting force were the important factors replacing suction.While metamorphosis here can be argued to be inherited froma more general dissorophoid condition, the extended phaseof suction feeding can be regarded the major innovation ofApateon. In the more derived species (A. dracyiensis, A. flag-rifer and A. caducus) metamorphosis was not reached and,more importantly, larval feeding diverged into quite differentadaptational directions. In A. caducus and probably also inA. flagrifer, the maxilla grew at an accelerated rate comparedwith A. gracilis or A. pedestris, and consolidated early in de-velopment (Schoch 1992). Thus, gape size and a stronger, lessregular dentition (conical instead of needle-shaped) indicatean early ontogenetic diet change from suspension to carni-vory, which is confirmed by intestine fillings (Boy 1995). A.caducus was evidently not selective of prey, engulfing bothA. pedestris and its own larvae (observation by RRS).

A. caducus grew to larger documented size than mostother Apateon species and remained neotenic into the lateststages, as branchial denticles indicate. However in large spe-cimens, the denticles changed in being more robust andlacking brush-like branches (observation by RRS). Its rel-ative Apateon dracyiensis evolved in the opposite direction:it abandoned the consolidation of the maxilla entirely andreduced adult size even further than A. pedestris and A. gra-cilis. The skull became still broader and higher, suggesting areinforced, or at least modified, suction mechanism.

This partial scenario for the Apateon-clade rests on thehypothesis that selection for intensified suction-feeding wasof major significance. The evolutionary pattern of paedo-morphosis is most evident within Apateon, and this patternmay be best explained by the evolutionary process of neotenyin the traditional sense. The actual processes involved arebeyond reasonable speculation, however. For instance, thereis no way to find out whether Apateon caducus was (1) grow-ing at an accelerated rate by maintaining life span, or (2)extending life span, or both. Likewise, it is not appropriate tospeculate about the nature of neoteny in advanced Apateonspecies; whether it was facultative or obligatory. There maywell have been terrestrial forms in the hinterland whose en-vironments were simply not preserved (Boy 1971, 1972),yet there is a strong physical argument against this, and weshall expand on this theme in the section on branchiosauridorigins.

The most clear-cut synapomorphy of the Melanerpeton-clade, the delicate palate elements, is difficult to explain.As with all ‘reduction characters’, such a phenomenon ishardly explained in functional terms or even in terms of nat-ural selection. In the Melanerpeton-clade, the dentition ofthe pterygoid, palatine and ectopterygoid is rudimentary oreven absent, concurring with the delicate state of these ele-ments; especially the posterior portion of the palatine andthe entire ectopterygoid are mere rudiments. As in mostspecies of Apateon, the branchial denticles have brush-likeends and suggest a certain amount of filter feeding. We havealready argued that planktonic prey was probably exploredby the first branchiosaurids, and there are no apparent further

18 R. R. Schoch and A. R. Milner

specializations in the Melanerpeton-clade. However, thecombination of early consolidated cheeks and maxillae withreduced palatal elements and dentition indicates a shift inimportance from the palatal to the marginal dentition. InApateon instead, the plesiomorphic, heavier palatal dentitionis retained and the palatine bone is even more robust thanin the primitive condition, as indicated by outgroups. TheMelanerpeton clade, it seems, combined filter-feeding with alarge gape useful for occasional capture of larger prey items,while the degeneration of palatal teeth suggests that manip-ulation of prey items in the buccal cavity was less important.From this ground pattern, Leptorophus and Schoenfelder-peton diverged into rather different adaptational directions.

Leptorophus tener may be readily derived from an an-cestor similar to M. humbergense or M. sembachense, whichwould both also neatly match stratigraphically. Both of thelatter taxa lack clear autapomorphies. L. tener had acquireda triangular, much elongated skull with posteriorly exten-ded cheeks, a strong and well-consolidated maxilla, and adeep and well-ossified mandible; an intermediate form maybe exemplified by M. eisfeldi, a large but still poorly knownelaboration of M. sembachense. (However, the sequence M.sembachense – L. tener – M. eisfeldi appears partially re-versed in stratigraphical succession). The characteristic fea-tures of L. tener indicate an accentuation of jaw musculatureand an increased biting force. The skull furthermore appearsbetter consolidated, including the basicranial region, in com-parison with Apateon and Schoenfelderpeton. In all knownbranchiosaurids and contrasting teleosts, there is no evidencethat suction-feeding was supported by intracranial kinetism.The only evidence, though rather ambiguous, is the wideoverlap between the squamosal and supratemporal, whichmay have permitted some movement of cheek against skulltable (Boy 1972).

Schoenfelderpeton is a highly paedomorphic genuscharacterized by the retarded development of the maxilla,an open cheek in adults, and a particularly poorly developedpectoral limb. On the other hand, the otic notch indicatesthat Schoenfelderpeton had an elaborate middle ear which isotherwise not found in this family – eventually indicating anadult specialization. The numerous tiny teeth of the maxillasuggest that it focused on different prey items, or a differentmode of feeding, as compared with other branchiosaurids.The ectopterygoid is edentulous and has almost vanished,indicating that the skull roof posed few supporting demandson the palate.

Finally, the origin of the Branchiosauridae remains tobe discussed. It falls within the dissorophoids, some of whichappear to metamorphose from aquatic larvae (Milner 1982).There is some evidence that Mordex laticeps, the larvae ofwhich co-occur with true Branchiosaurus salamandroides inthe Nyrany deposit, underwent similar larval stages as bran-chiosaurids (Milner & Sequeira, unpublished results). Theyseem to have possessed similar single branchial denticleson spherical bases, although lacking their brush-like ends(Fig. 2C2). This indicates that a certain degree (or precondi-tion) of filter-feeding, perhaps as a short-term seasonal activ-ity by larvae in ephemeral water-bodies, probably evolvedbefore branchiosaurids originated, and thus is not necessar-ily exclusive to the clade. What remains mysterious is thewidespread, almost ubiquitous neoteny among branchiosaur-ids, given that adults are not just lacking from the depositsfor some unknown reason. The latter possibility, which has

been always cited as an alternative to obligate neoteny, is notparticularly plausible, because at least during the breedingseason putative adults of branchiosaurids should have vis-ited the breeding water bodies, and under these conditionsbe at least as frequent as adult Sclerocephalus or Onchiodon,which are mostly found in concert with their own larvaeacross the Variscan mountain range. Thus, obligate neotenyis probable for most branchiosaurids, and Boy & Schindler(2000) have recently discussed some aspects that might becritical to the present debate.

The Variscan orogen is generally believed to havereached considerable elevations during the late Carbonifer-ous (Wagner & Lyons 1995). Ziegler & Gibbs (1996) cal-culated elevations between 1,000 and 2,000 metres for thecentral ranges of the orogen, and this has in turn been takenas a reason to suggest a strong seasonality for these regions,in addition to a thinner atmosphere, decreased atmospherichumidity, intensified UV, and a lower oxygen level (Bailey1998). At comparable elevations today, the physiologicalactivity and taxonomic diversity of modern amphibians issignificantly reduced and the existence of terrestrial formsis increasingly restricted, as elevation increases (Duellman& Trueb 1986). Given that the gross dimension of the cal-culated elevations is correct, terrestrial temnospondyl am-phibians might not have survived in the higher regions ofthe Variscan mountain ranges. Neoteny, hitherto an exploit-able option when required, could have become an obligation.Likewise, the miniaturization recorded in dissorophoids andparticularly in branchiosaurids, might reflect selection pres-sures posed by high elevations.

Interestingly, this scenario might explain the hypothes-ized obligatory neoteny in most branchiosaurids. A furthersupport for this concept is that larger temnospondyls such asMicromelerpeton or Sclerocephalus did apparently not trans-form into terrestrial adults in most lakes of the Rotliegendtime (Schoch 2002b), while their relatives in the lowlandsof south-central North America (Texas, New Mexico, Ok-lahoma) transformed into terrestrial morphotypes such asDoleserpeton annectens (50–100 mm body size), Cacopsaspidephorus (1 m) or even Eryops megacephalus (2.5 m).

Phylogeny and Stratigraphy

Branchiosaurids are such characteristic faunal elements thatthey have been used as biostratigraphical index fossils acrossEuropean Permo-Carboniferous basins (Boy 1987b; Werneb-urg 1989a; Werneburg & Schneider 2006; for a critique seeSteyer 2000 and reply by Werneburg 2003). Although theabsolute ages of many Rotliegend strata remain unclear, re-cent efforts have helped clarify at least part of the sequencein the Saar-Nahe basin, shifting the base of the occurrencesof many branchiosaurids down into what is now undoubtedlyconsidered the Upper Carboniferous (Fig. 7).

The stratigraphical range of branchiosaurids may reflecttrue presence, but it is likely that sedimentary facies and eco-logy have had a major impact on this range. For instance, inthe Saar-Nahe Basin, the oldest occurrence of branchiosaur-ids is in lake deposits, and remains as such throughout thesection. In intermediate phases during which coal swampsor anastomosing rivers dominated the sedimentary regime,branchiosaurids were not preserved (Boy & Schindler 2000).This is in agreement with observations in other basins, withfew exceptions. The oldest known branchiosaurid remain,

Relationships and evolutionary history of branchiosauridae 19

Figure 7 Stratigraphical occurrence and range of branchiosaurids across Middle Europe. Taxa analyzed in the present paper in bold, poorlyknown taxa in normal type. Taxa grouped according to the regions where they occur. Absolute age data from Davydov et al. (2005) and Konigeret al. (2002), the latter marked with an asterisk.

Branchiosaurus salamandroides, stems from a coal-bearinglowland lake deposit rather than a coal measure (Milner1987).

The stratigraphically oldest branchiosaurids belong tothe genus Branchiosaurus, namely B. salamandroides fromthe Asturian (Moscovian) and B. fayoli from the Stephanian C(Gzhelian). This agrees with the concept that Branchiosaurusconstitutes the most primitive taxon (e. g. Boy 1987a; impli-citly: Boy & Sues 2000) suggesting Branchiosaurus mightbelong to the stem lineage of both the Melanerpeton-cladeand Apateon.

In our analysis, strict parsimony analysis has come tothe same result. This appears particularly comfortable, be-

cause there remains a wide stratigraphical gap between theMoscovian reports of Branchiosaurus and either of the Per-mian branchiosaurid lineages whose earliest reports are notolder than Gzhelian (Fig. 7). In the alternative case, in whichBranchiosaurus belonged to either of the two stem lineages,at least two major ghost lineages would have to be assumed,(i) the branching of the Melanerpeton clade, and (ii) the di-vergence of Apateon gracilis from Branchiosaurus salaman-droides. Thus, from a purely stratigraphical point of view,the most parsimonious morphology-based hypothesis alsoappears to be the most likely scenario.

The Melanerpeton clade makes its occurrence witha form originally described as Apateon intermedius by

20 R. R. Schoch and A. R. Milner

Table 1 Character matrix. All characters ordered, including multiple states. Taxon abbreviations are as follows: Amp.: Amphibamusgrandiceps; Bal.: Balanerpeton woodi; cad.: Apateon caducus; dra.: Apateon dracyiensis; Eco.: Ecolsonia cutlerensis; eis.: Melanerpetoneisfeldi; flag.: Apateon flagrifer; gra.: Apateon gracilis; hu.: Melanerpeton humbergense; kon.: Apateon kontheri; Mic.: Micropholis stowii;Mim.: Micromelerpeton credneri; ped.: Apateon pedestris; Plat.: Platyrhinops lyelli; pre.: Schoenfelderpeton prescheri; sal.: Branchiosaurussalamandroides; Scl.: Sclerocephalus haeuseri; sem.: Melanerpeton sembachense; ten.: Leptorophus tener.

OUTGROUP INGROUP1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19

Nr. Character Bal. Scl. Eco. Mim. Plat. Amp. Mic. sal. ped. gra. cad. kon. flag. dra. hu. ten. pre. sem. eis.

1 Interorb. width 0 0 0 0 2 2 0 0&1 1 0 2 1 2 2 0 0 1 0 12 Pre-/postfront. 0 0 1 1 0 0 1 0 1 1 1 1 1 0 1 1 0&1 1 13 Postfr. med. ext. 0 0 0 1 0&1 1 0&1 0 0 1 1 1 1 1 0 0 0 0 04 Max.-qujug. contact 0 0 0 0 0 0 0 ? 2 2 1 1 2 2 1 1 2 1 15 Jugal 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 16 Suprat. shape 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0&1 ?7 Suprat. medial suture 0 0 0&1 0 0 0 0 0 0 0 1 0 1 0 1 1 1 1 ?8 Par., fr. width 0 0 1 0 1 1 1 0 0 0 1 0 0&1 1 0 0 0 0 09 Pp., Tab. length 0 0 0 0 1 1 0&1 1 0&1 1 1 1 0&1 1 0 0 0 0 ?

10 Po. skull short 0 0 0 0 1 1 0 1 1 1 1 1 1 1 1 1 1 1 111 Jugal anterior length 0 0 0 0 0 0 1 0 0 1 1 1 1 1 1 1 0 1 112 Occip. flange 0 0 0 0 1 1 0 1 1 1&2 2 0&1 0&1 1 1 2 1 1 ?13 St, Ta lateral narrow 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 014 Intertemporal absence 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 115 Tab. horn end 0 0 0 0 0 ? 0 ? 1 1 1 1 1 1 0 0 0 0 ?16 Tab. horn area 0 0 0 0 0 ? 0 1 1 0 1 0 0&1 1 0 0 0 0 017 Ot. notch-orb. dist. 0 0 0 0 1 1 0 0 0 1 0 0 0 0 0 0 0 0 018 Max. shelf wide 0 0 0 0 0 ? 0 0 1 1 1 1 1 1 0 0 0 0 019 Bicuspidity 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 020 Nasal-frontal 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 021 Po. separ. from st. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0&1 ?22 Quadrate behind occiput 0 0 0 0 0 0 0 1 1 0 1 1 1 1 1 0 1 1 123 Parasp. process. 1 0 1 0 ? ? 1 0&1 1 1 1 1 ? 0&1 0 0 0 0 024 Pterygoid delicate 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 125 Pterygoid-vomer 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 126 Pterygoid flange 0 0 1 0&1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 027 Palatine/ectopterygoid 0 0 0 0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 028 Palatine post. red. 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 1 129 Ectopterygoid 0 0 0 0 0 0 0 0 0&1 0 1 0 1 0 0 0 0 0 030 Carot. for. parasph. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 031 Denticle field parasph. 0 0 2 0 0 0 0 2 2 2 2 2 2 2 1 2 1 1&2 232 Branchial dentition ? 0 ? 0 ? ? ? 1 2 2 2 2 2 2 2 2 2 2 233 Presacral count 0 0 ? 0 0 1 1 1 1 1 1 1 1 1 1 1 ? 1 134 Interclavicle 0 0 1 1 1 1 1&2 1 2 1 2 1 2 2 1 1 1 2 135 Humerus, foramen 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 136 Humerus ratio 0 0 2 1 2 2 2 2 2 2 2 2 2 2 1 1 1 2 237 Dorsal osteoderms ? 0 ? 0 ? 0 ? ? 1 1 1 1 1 1 0 0 0 ? 038 Ventral osteoderms 0 0 0 0 1 0 0 0 1 1 1 1 1 1 1 1 1 1 139 Supinator process 1 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 140 Anterior ribs 0 0 ? 0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0

Werneburg (1996) but which shares derived character-stateswith Melanerpeton rather than Apateon. L. tener cannot bedated accurately. M. humbergense is from the Middle Au-tunian, while Schoenfelderpeton prescheri from Tabarz isfrom beds of slightly younger age. The chronology of branch-ing of the Melanerpeton-clade remains unresolved also fromstratigraphical evidence, as a relatively derived form – M.sembachense, a close relative or ancestor of L. tener – appearsbefore the most plesiomorphic species (M. humbergense).Unless a rather unparsimonious case is true, the fossil recordmust be interpreted as having major gaps.

In several Rotliegend basins, the stratigraphical occur-rence of branchiosaurids has been recorded in detail (Werneb-

urg 1990; Boy et al. 1990). However, the correlation of theseoccurrences across basin boundaries, and the chronostrati-graphic correlation in general, remain unclear in many re-spects (e.g. Boy & Schindler 2000; Menning et al. 2005;Werneburg & Schneider 2006). The main problem is therecognition of the Carboniferous-Permian boundary. Re-cent advances in this area have been made by Koniger(2000) and Koniger et al. (2002) who have argued thatthe lowermost Rotliegend Remigiusberg and AltenglanFormations of the Saar-Nahe Basin, date radiometricallyaround 300 Ma, corresponding to Stephanian D, whichfalls within the Gzhelian (Menning et al. 2005). Thus, thefirst stratigraphical occurrence of the genus Apateon in the

Relationships and evolutionary history of branchiosauridae 21

Remigiusberg Formation is made by A. pedestris within theUpper Carboniferous, followed by A. caducus in the Saar-Nahe Basin and A. dracyiensis and A. flagrifer in the SaaleBasin (with A. dracyiensis only later appearing in the AutunBasin) (Fig. 7). The first occurrence of A. dracyiensis andA. flagrifer has been recorded in the Manebach Formation,which Boy & Schindler (2000) suggested as equivalent of theQuirnbach Formation in the Saar-Nahe Basin, but accordingto Menning et al. (2005) it would correlate with the Meis-enheim Formation (Gzhelian-Asselian boundary). Of the re-maining Apateon species, A. kontheri and A. gracilis appearmuch later in the chronological succession as listed here (Boyet al. 1990; Boy & Schindler 2000; Werneburg 1989a). Thelate appearance of A. gracilis is the one anomaly in relationto our analysis. In the analysis presented here, the primitivemetamorphosing A. gracilis is the sister-taxon to most of theother Apateon species including A. pedestris, which first ap-pears in the latest Carboniferous (Fig. 7). A. gracilis musttherefore be part of a lineage extending back to the Carbon-iferous and cannot be confidently treated as a late-appearingtaxon of high biostratigraphical value, as used by Werneburg& Schneider (2006). This is particularly applicable to thedating of the Niederhaslich Formation in the Dohlen basin.The stratigraphical position of this formation (e.g. Roscher& Schneider 2005: fig. 1) is based entirely on the presenceof A. gracilis, there being no plants, blattid insects, fishes orisotope dates to provide supporting or contradictory data (op.cit. p. 286).

Acknowledgements

We thank Sandy Sequeira, Florian Witzmann, Jurgen Boyand Ralf Werneburg for many fruitful discussions and theLeverhulme Trust for Award F/07 112/B giving financial sup-port for A.R.M. The manuscript was significantly improvedby suggestions from Dr Jason Anderson and an anonymousreferee, and by the editorial work of Dr Andrew Smith.

References

Alberch, P., Gould, S. J., Oster, G. F. & Wake, D. B. 1979. Size andshape in ontogeny and phylogeny. Paleobiology 5: 296–317.

Ammon, L. 1889. Die permischen Amphibien der Rheinpfalz. Straub:Munich, 119 pp.

Anderson, J. S. 2007. Incorporating ontogeny into the matrix: a phylo-genetic evaluation of developmental evidence for the origin of modernamphibians. Pp. 182–227 in Anderson, J. S. & Sues, H. D. (eds), Majortransition in the evolution of life. Indiana University Press: Blooming-ton, 417 pp.

Bailey, R. G. 1998. Ecoregions. The ecosystem geography of the oceansand continents. Springer: New York, 176 pp.

Berman, D. S., Reisz, R. R. & Eberth, D. A. 1985. Ecolsonia cutlerensis,an Early Permian dissorophid amphibian from the Cutler Formation ofnorth-central New Mexico. New Mexico Bureau of Mines and MineralResources 191: 1–32.

Bolt, J. R. 1969. Lissamphibian origins: possible protolissamphibian fromthe Lower Permian of Oklahoma. Science 166: 888–891.

Boy, J. A. 1971. Zur Problematik der Branchiosaurier (Amphibia, Karbon-Perm). Palaontologische Zeitschrift 45: 107–119.

— 1972. Die Branchiosaurier (Amphibia) des saarpfalzischen Rot-liegenden (Perm, SW-Deutschland). Abhandlungen des hessischenLandesamtes fur Bodenforschung 65: 1–137.

— 1974. Die Larven der rhachitomen Amphibien (Amphibia: Temno-spondyli; Karbon-Trias). Palaontologische Zeitschrift 48: 236–268.

— 1978. Die Tetrapodenfauna (Amphibia, Reptilia) des saarpfalzischenRotliegenden (Unter-Perm; SW-Deutschland). 1. Branchiosaurus.Mainzer geowissenschaftliche Mitteilungen 7: 27–76.

— 1985. Uber Micropholis, den letzten Uberlebenden der Dissorophoidea(Amphibia: Temnospondyli; Unter-Trias). Neues Jahrbuch fur Geolo-gie und Palaontologie Monatshefte 1985: 29–45.

— 1986. Studien uber die Branchiosauridae (Amphibia: Temnospondyli)1. Neue und wenig bekannte Arten aus dem mitteleuropaischen Rot-liegenden (? oberstes Karbon bis unterstes Perm). PalaontologischeZeitschrift 60: 131–166.

— 1987a. Studien uber die Branchiosauridae (Amphibia: Temnospon-dyli; Ober-Karbon – Unter-Perm). 2. Systematische Ubersicht. NeuesJahrbuch fur Geologie und Palaontologie Abhandlungen 174: 75–104.

— 1987b. Die Tetrapoden-Lokalitaten des saarpfalzischen Rotliegenden (?Ober-Karbon-Unter-Perm; SW-Deutschland) und die Biostratigraphieder Rotliegend-Tetrapoden. Mainzer geowissenschaftliche Mitteilun-gen 16: 31–65.

— 1988. Uber einige Vertreter der Eryopoidea (Amphibia: Temnospon-dyli) aus dem europaischen Rotliegend (? hochstes Karbon-Perm). 1.Sclerocephalus. Palaontologische Zeitschrift 62: 107–132.

— 1990. Uber einige Vertreter der Eryopoidea (Amphibia: Temnospon-dyli) aus dem europaischen Rotliegend (? hochstes Karbon–Perm) 3.Onchiodon. Palaontologische Zeitschrift 64: 287–312.

— 1993. Uber einige Vertreter der Eryopoidea (Amphibia: Temnospon-dyli) aus dem europaischen Rotliegend (? hochstes Karbon-Perm). 4.Cheliderpeon latirostre. Palaontologische Zeitschrift 67: 123–143.

— 1995. Uber die Micromelerpetontidae (Amphibia: Temnospondyli).1. Morphologie und Palaookologie des Micromelerpeton credneri(Unter-Perm; SW-Deutschland). Palaontologische Zeitschrift 69: 429–457.

— 1996. Ein neuer Eryopoide (Amphibia: Temnospondyli) ausdem saarpfalzischen Rotliegend (Unter-Perm; Sudwest-Deutschland).Mainzer geowissenschaftliche Mitteilungen 25: 7–26.

— 2002a. Uber die Micromelerpetontidae (Amphibia: Temnospondyli).2. Micromelerpeton ulmetense n. sp. und Micromelerpeton (?) boyiHeyler. Neues Jahrbuch fur Geologie und Palaontologie Abhandlun-gen 223: 241–274.

— 2002b. Uber die Micromelerpetontidae (Amphibia: Temnospondyli).3. Eimerisaurus n. g. Neues Jahrbuch fur Geologie und PalaontologieAbhandlungen 225: 425–452.

— & Fichter, J. 1982. Zur Stratigraphie des saarpfalzischen Rotlie-genden (? Ober-Karbon – Unter-Perm; SW-Deutschland). Zeitschriftder deutschen geologischen Gesellschaft 133: 607–642.

— & Schindler, T. 2000. Okostratigraphische Bioevents im Gren-zbereich Stephanium/Autunium (hochstes Karbon) des Saar-Nahe-Beckens (SW-Deutschland) und benachbarter Gebiete. Neues Jahr-buch fur Geologie und Palaontologie Abhandlungen 216: 89–152.

— & Sues, H. D. 2000. Branchiosaurs: larvae, metamorphosis and het-erochrony in temnospondyls and seymouriamorphs. Pp. 1150–1197 inH. Heatwole & R. L. Carroll (eds) Amphibian Biology 4: 973–1496.Surrey Beatty & Sons: Chipping Norton, N.S.W.

—, Meckert, D. & Schindler, T. 1990. Probleme der lithostratigraph-ischen Gliederung im unteren Rotliegend des Saar-Nahe-Beckens(? Ober-Karbon – Unter-Perm; SW-Deutschland). Mainzer geowis-senschaftliche Mitteilungen 19: 99–262.

Broili, F. & Schroder, J. 1937. Beobachtungen an Wirbeltieren der Kar-rooformation. XXV. Uber Micropholis Huxley. Sitzungsberichte derBayerischen Akademie der Wissenschaften, mathematisch naturwis-senschaftliche Abteilung 1937: 19–57.

Bulman, O. M. B. & Whittard, W. F. 1926. On Branchiosaurus andallied genera. Proceedings of the Zoological Society of London 1926:533–579.

Carroll, R. L. 1964. Early evolution of the dissorophid amphibians. Bul-letin of the Museum of comparative Zoology Harvard University 131:161–250.

— 2002. The origin and early radiation of terrestrial vertebrates. Journalof Paleontology 75: 1202–1213.

22 R. R. Schoch and A. R. Milner

— 2007. The Palaeozoic ancestry of salamanders, frogs, and caecilians.Zoological Journal of the Linnean Society 150, Supplement 1: 1–140.

Clack, J. A. & Milner, A. R. 1994. Platyrhinops from the Upper Car-boniferous of Linton and Nyrany, and the family Peliontidae (Am-phibia; Temnospondyli). Pp. 185–192 in D. Schweiss & U. Heidtke(eds) New results on Permo-Carboniferous Fauna, Pollichia-Buch 29,199 pp.

Credner, H. 1881. Die Stegocephalen (Labyrinthodonten) aus dem Roth-liegenden des Plauenschen Grundes. 2. Theil. Zeitschrift der Deutschengeologischen Gesellschaft 33: 298–330.

Daly, E. 1994. The Amphibamidae (Amphibia: Temnospondyli), with adescription of a new genus from the Upper Pennsylvanian of Kansas.University of Kansas Miscellaneous Publications 85: 1–59.

Davydov, V. I., Schmitz, M. D., Snyder, W. S. & Wardlaw, B. R. 2005.Progress toward development of the Cisuralian (Lower Permian) times-cale (biostratigraphy, chronostratigraphy, radiometric calibration). Pp.48–55 in S. G. Lucas & K. Zeigler (eds) The Nonmarine Permian,New Mexico Museum of Natural History and Science Bulletin 30.Albuquerque, 362 pp.

Deban, S. & Wake, D. B. 2000. Aquatic feeding in salamanders.Pp. 65–94 in K. Schwenk (ed.) Feeding. Academic Press: New York,537 pp.

Duellman, W. & Trueb, L. 1986. The biology of amphibians. McGrawHill: New York, 670 pp.

Efremov, J. A. 1939. The first representative of the early tetrapods fromSiberia. Comptes Rendus de l’Academie des Sciences de l’ URSS 23:106–110.

— 1953. The second find of a Permian amphibian in the Tunguska Basinof Siberia. Doklady Akademiya Nauk SSSR 91: 943–946.

Fritsch, A. 1876. Ueber die fauna der Gaskohle des Pilsner und RakonitzerBeckens. Sitzungsberichte der koniglich-bohmischen Akademie derWissenschaften Prag 1875: 70–79.

— 1878. O novem jesteru z permskych vapencu u Broumovo. Vesmır 7:249.

— 1879. Fauna der Gaskohle und der Kalksteine der PermformationBohmens. Vol. 1, part 1. Selbstverlag: Prague.

Gaudry, A. 1875. Sur la decouverte de batraciens dans le terrain primaire.Bulletin de la Societe geologique de France 3: 299–306.

Gardner, J. D. 2001. Monophyly and affinities of albanerpetontid am-phibians (Temnospondyli; Lissamphibia). Zoological Journal of theLinnean Society of London 131: 309–352.

Hanken, J. 1984. Miniaturization and its effects on cranial morphology inplethodontid salamanders, genus Thorius (Amphibia: Plethodontidae).I. Osteological variation. Biological Journal of the Linnean Society 23:55–75.

Heyler, D. 1957. Revision des Branchiosaurus de la region d’Autun.Annales de Paleontologie 43: 47–111.

Holmes, R., Carroll, R. L. & Reisz, R. 1998. The first articulated skel-eton of Dendrerpeton acadianum (Temnospondyli, Dendrepetontidae)from the Lower Pennsylvanian locality of Joggins, Nova Scotia, anda review of its relationships. Journal of Vertebrate Paleontology 18:64–79.

Hunt, A. P., Lucas, S. G. & Berman, D. S. 1996. A new amphibamid(Amphibia: Temnospondyli) from the Late Pennsylvanian (MiddleStephanian) of central New Mexico, USA. Palaontologische Zeitschrift76: 125–126.

—, — & — 2002. Milnererpeton, a replacement name for the temnospon-dyl genus Milneria. Palaontologische Zeitschrift 76: 125–126.

Koniger, S. 2000. Verbreitung, Fazies und stratigraphische Bedeutungdistaler Aschentuffe der Glan-Gruppe im karbonisch-permischen Saar-Nahe-Becken (SW-Deutschland). Mainzer geowissenschaftliche Mit-teilungen 29: 97–132.

—, Lorenz, V., Stollhofen, H. & Armstrong, R. A. 2002. Origin,age and stratigraphic significance of distal fallout ash tuffs from theCarboniferous-Permian continental Saar-Nahe Basin (SW Germany).International Journal of Earth Sciences 91: 341–356.

Larsen, J. H. Jr. 1963. The cranial osteology of neotenic and transformedsalamanders and its bearing on interfamilial relationships. Universityof Washington, PhD thesis, 205 pp.

Lauder, G. V. & Shaffer, H. B. 1993. Design of feeding systems inaquatic vertebrates: major patterns and their evolutionary interpreta-tions. Pp. 113–149 in J. Hanken & B. K. Hall (eds) The Skull, Volume3. University of Chicago Press: Chicago, 460 pp.

Laurin, M. 1998. The importance of global parsimony and historicalbias in understanding tetrapod evolution. Part I. Systematics, middleear evolution, and jaw suspension. Annales des Sciences naturellesZoologie, 13e serie 19: 1–42.

— & Reisz, R. R. 1997. A new perspective on tetrapod phylogeny. Pp.9–59 in S. S. Sumida & K. L. Martin (eds) Amniote origins, completingthe transition to land. Academic Press: London, 510 pp.

Maddison, W. P. & Maddison, D. R. 1992. MacClade: Analysis of phylo-geny and character evolution. Sinauer: Sunderland/Mass.

Menning, M., Gast, R., Hagdorn, H., Kading, K.-C., Simon, T., Szur-

lies, M. & Nitsch, E. 2005. Zeitskala fur Perm und Trias in der Strati-graphischen Tabelle von Deutschland 2002, zyklostratigraphische Kal-ibrierung der hoheren Dyas und Germanischen Trias und das Alter derStufen Roadium bis Rhaetium 2003. Newsletters on Stratigraphy 41:173–210.

Meyer, H. v. 1844. Briefliche Mitteilung an Professor Bronn. Neues Jahr-buch fur Mineralogie 1844: 336–337.

— 1848. Apateon pedestris aus der Steinkohlen-Formation vonMunsterappel. Palaeontographica 1: 153.

— 1858. Reptilien aus der Steinkohlen-Formation in Deutschland. Palae-ontographica 6: 59–220.

Milner, A. R. 1982. Small temnospondyl amphibians from the MiddlePennsylvanian of Illinois. Palaeontology 25: 635–664.

— 1986. Dissorophoid amphibians from the Upper Carboniferous ofNyrany. Pp. 671–674. in Z. Rocek (ed.) Studies in Herpetology. CharlesUniversity: Prague, 754 pp.

— 1987. The Westphalian tetrapod fauna. Journal of the Geological So-ciety of London 144: 495–506.

— 1988. The relationships and origin of living amphibians. Pp. 59–102 inM. J. Benton (ed.) Phylogeny and classification of the tetrapods, vol.1: amphibians, reptiles, birds. Systematics Association Special Volume35 A, Oxford: Clarendon Press, 377 pp.

— 1993. The Paleozoic relatives of lissamphibians. Herpetological Mono-graphs 7: 8–27.

— & Sequeira, S. E. K. 1994. The temnospondyl amphibians from theVisean of East Kirkton, West Lothian, Scotland. Transactions of theRoyal Society of Edinburgh: Earth Sciences 84: 331–361.

Pawley, K. A. T. & Warren, A. 2006. The appendicular skeleton ofEryops megacephalus Cope, 1877 (Temnospondyli: Eryopoidea) fromthe Lower Permian of North America. Journal of Paleontology 80:561–580.

Romer, A. S. 1939. Notes on branchiosaurs. American Journal of Science237: 748–761.

— 1947. Review of the Labyrinthodontia. Bulletin of the Museum ofComparative Zoology Harvard College 99: 1–368.

Roscher, M. & Schneider, J. W. 2005. An annotated correlation chartfor continental Late Pennsylvanian and Permian basins and the marinescale. Pp. 282–291 in S. G. Lucas & K. E. Zeigler (eds) The nonmarinePermian. New Mexico Museum of Natural History and Science Bulletin30: 362 pp.

Ruta, M. & Coates, M. I. 2007. Dates, nodes, and character conflict:addressing the lissamphibian origin problem. Journal of SystematicPalaeontology 5: 69–122.

—, — & Quicke, D. L. J. 2003. Early tetrapod relationships revisited.Biological Reviews 78: 251–345.

Schmalhausen, I. I. 1968. The origin of terrestrial vertebrates. London:Academic Press, 314 pp.

Schoch, R. R. 1992. Comparative ontogeny of early Permian bran-chiosaurid amphibians from southwestern Germany. Developmentalstages. Palaeontographica A 222: 43–83.

— 1995. Heterochrony and the development of the amphibian head. Pp.107–124 in K. McNamara (ed.) Evolutionary Change and Hetero-chrony. J. Wiley: Chichester, 286 pp.

— 1998. Homology of cranial ossifications in urodeles: significance ofdevelopmental data for fossil basal tetrapods. Neues Jahrbuch fur Geo-logie und Palaontologie Monatshefte 1998: 1–25.

Relationships and evolutionary history of branchiosauridae 23

— 1999. Comparative osteology of Mastodonsaurus giganteus (Jaeger,1828) from the Middle Triassic (Lettenkeuper: Longobardian) of Ger-many (Baden-Wurttemberg, Bayern, Thuringen). Stuttgarter Beitragezur Naturkunde B 278: 1–175.

— 2001. Can metamorphosis be recognised in Palaeozoic amphibians?Neues Jahrbuch fur Geologie und Palaontologie Abhandlungen 220:335–367.

— 2002a. The early formation of the skull in extant and Paleozoic amphi-bians. Paleobiology 28: 278–296.

— 2002b. The evolution of metamorphosis in temnospondyls. Lethaia 35:309–327.

— 2003. Early ontogeny of the Permo-Carboniferous temnospondylSclerocephalus. Palaeontology 46: 1055–1072.

— 2004. Skeleton formation in the Branchiosauridae: a case study incomparing ontogenetic trajectories. Journal of Vertebrate Paleontology24: 309–319.

— & Carroll, R. L. 2003. Ontogenetic evidence for the Paleozoic an-cestry of Salamanders. Evolution and Development 5: 314–324.

— & Frobisch, N. B. 2006. Metamorphosis and neoteny: alternativepathways in an extinct amphibian clade. Evolution 60: 1467–1475.

— & Milner, A. R. 2000. Handbuch der Palaoherpetologie, Volume 3B,Stereospondyli. (P. Wellnhofer, series editor). Pfeil: Munich. 203 pp.

— & Rubidge, B. S. 2005. The amphibamid Micropholis stowii from theLystrosaurus Assemblage Zone of South Africa. Journal of VertebratePaleontology 25: 502–522.

Schonfeld, G. 1911. Branchiosaurus tener Schonfeld. Ein neuer Stego-cephale aus dem Rotliegenden des nordwestlichen Sachsen. Sitzungs-berichte und Abhandlungen der naturwissenschaftlichen GesellschaftIsis 1911: 19–43.

Shishkin, M. A. 1998. Tungussogyrinus – a relict neotenic dissorophoid(Amphibia, Temnospondyli) from the Permo-Triassic of Siberia. Pa-leontological Journal 32: 521–531.

Steyer, J.-S. 2000. Are European Paleozoic amphibians good stratigraphicmarkers? Bulletin de la Societe geologique de France 171: 127–135.

Swofford, D. 1991. Paup: phylogenetic analysis using parsimony, Version3.1. Illinois Natural History Survey: Champaign.

Thevenin, A. 1906. Amphibiens et reptile du terrain houiller de France.Annales de Paleontologie 2: 145–163.

Trueb, L. & Cloutier, R. 1991. A phylogenetic investigation of the inter-and intrarelationships of the Lissamphibia (Amphibia: Temnospon-dyli). Pp. 223–313. in H.-P. Schultze & L. Trueb (eds) Origins ofthe higher groups of tetrapods – controversy and consensus. CornellUniversity Press: Ithaca, 724 pp.

Wagner, R. H. & Lyons, P. C. 1997. A critical analysis of the higherPennsylvanian megafloras of the Appalachian region. Review of Pa-laeobotany and Palynology 95: 255–283.

Wake, D. B. 1996. Introduction. Pp. xvii–xxv. in M. J. Sanderson & L.Hufford (eds), Homoplasy. Academic Press, 339 pp.

— & Larson, A. 1987. Multidimensional analysis of an evolving lineage.Science 238: 42–48.

Watson, D. M. S. 1940. The origin of frogs. Transactions of the RoyalSociety of Edinburgh 60: 195–231.

— 1963. On growth stages in branchiosaurs. Palaeontology 6: 540–553.Werneburg, R. 1986. Die Stegocephalen der Goldlauterer Schichten

(Unterrotliegendes, Unterperm). Teil I: Apateon flagrifera (Whitt.).Freiberger Forschungshefte C 410: 88–101.

— 1987. Dissorophoiden (Amphibia, Rhachitomi) aus dem Westfal D(Oberkarbon) der CSSR. Branchiosaurus salamandroides Fritsch,1876. Zeitschrift fur geologische Wissenschaften 15: 681–690.

— 1988a. Die Stegocephalen (Amphibia) der Goldlauterer Schichten(Unterrotliegendes, Perm) des Thuringer Waldes. Teil III: Apateondracyiensis (Boy), Branchierpeton reinholdi n. sp. und andere.Veroffentlichungen des Naturkundemuseums Erfurt 1988: 80–96.

— 1988b. Die Amphibienfauna der Oberhofer Schichten (Unterrotlie-gendes, Unterperm) des Thuringer Waldes. Veroffentlichungen aus demNaturhistorischen Museum Schleusingen 3: 2–27.

— 1988c. Die Stegocephalen der Goldlauterer Schichten (Unterrotlie-gendes, Unterperm). Teil II: Apateon kontheri n. sp., Melanerpetoneisfeldi n. sp. und andere. Freiberger Forschungshefte C 427: 7–29.

— 1989a. Labyrinthodontier (Amphibia) aus dem Oberkarbon und Un-terperm Mitteleuropas. Systematik, Phylogenie und Biostratigraphie.Freiberger Forschungshefte C 436: 7–57.

— 1989b. Die Amphibienfauna der Manebacher Schichten (Unterrotlie-gendes, Unterperm) des Thuringer Waldes. Veroffentlichungen aus demNaturhistorischen Museum Schleusingen 4: 55–68.

— 1990. Dissorophoiden (Amphibia) aus dem Grenzbereich Karbon/Permder Saale-Senke und des Ilfelder Beckens (DDR). Zeitschrift fur geo-logische Wissenschaften 18: 665–677.

— 1991. Die Branchiosaurier aus dem Unterrotliegend des Dohlener Beck-ens bei Dresden. Veroffentlichungen aus dem Naturhistorischen Mu-seums Schleusingen 6: 75–99.

— 1996. Temnospondyle Amphibien aus dem Karbon Mitteldeutschlands.Veroffentlichungen aus dem Naturhistorischen Museum Schleusingen11: 23–64.

— 2001a. Apateon dracyiensis – eine fruhe Pionierform der Bran-chiosaurier aus dem Europaischen Rotliegend. Teil 1: Morphologie.Veroffentlichungen aus dem Naturhistorischen Museum Schleusingen16: 17–36.

— 2001b. Die Amphibien- und Reptilienfaunen aus dem Permokarbon desThuringer Waldes. Beitrage zur Geologie von Thuringen 8: 125–152.

— 2002. Apateon dracyiensis – eine fruhe Pionierform der Bran-chiosaurier aus dem Europaischen Rotliegend. Teil 2: Palaookologie.Veroffentlichungen aus dem Naturhistorischen Museum Schleusingen17: 17–32.

— 2003. The branchiosaurid amphibians from the Lower Permian ofBuxieres-les-Mines, Bourbon l’Archambault (Allier, France) and theirbiostratigraphic significance. Bulletin de la Societe geologique deFrance 174: 343–349.

— & Schneider, J. W. 2006. Amphibian biostratigraphy of the Permo-Carboniferous. Pp. 201–215 in S. G. Lucas, G. Cassins, & J. W.Schneider (eds) Non-Marine Permian Biostratigraphy and Biochrono-logy. Geological Society London, Special Publications, 265: London,344 pp.

—, Ronchi, A. & Schneider, J. W. 2007. The early Permian branchiosaur-ids (Amphibia) of Sardinia (Italy): systematic palaeontology, palaeo-ecology, biostratigraphy and palaeobiogeographic problems. Palaeo-geography, Palaeoclimatology, Palaeoecology 252: 383–404.

Witzmann, F. & Pfretzschner, H. U. 2003. Larval ontogeny of Micromel-erpeton credneri (Temnospondyli, Dissorophoidea). Journal of Verteb-rate Paleontology 23: 750–768.

Worthington, R. D. & Wake, D. B. 1971. Larval morphology and on-togeny of the ambystomatid salamander, Rhyacotriton olympicus. TheAmerican Midland Naturalist 85: 349–365.

Yates, A. M. & Warren, A. A. 2000. The phylogeny of the ‘higher’ tem-nospondyls (Vertebrata: Choanata) and its implications for the mono-phyly and origins of the Stereospondyli. Zoological Journal of theLinnean Society 128: 77–121.

Ziegler, A. M. & Gibbs, M. T. 1996. Approaches to Permian worldclimates and biogeography. Permophiles 29: 44–46.