Redalyc.On the Squamation of Australerpeton Cosgriffi Barberena

Anais da Academia Brasileira de Ciências ISSN: 0001-3765 [email protected] Academia Brasileira de Ciências Brasil

Dias, Eliseu V.; Richter, Martha On the squamation of Australerpeton cosgriffi Barberena, a temnospondyl amphibian from the Upper Permian of Brazil Anais da Academia Brasileira de Ciências, vol. 74, núm. 3, september, 2002, pp. 477-490 Academia Brasileira de Ciências Rio de Janeiro, Brasil

Disponível em: http://www.redalyc.org/articulo.oa?id=32774310

Como citar este artigo Número completo Sistema de Informação Científica Mais artigos Rede de Revistas Científicas da América Latina, Caribe , Espanha e Portugal Home da revista no Redalyc Projeto acadêmico sem fins lucrativos desenvolvido no âmbito da iniciativa Acesso Aberto Anais da Academia Brasileira de Ciências (2002) 74(3): 477-490 (Annals of the Brazilian Academy of Sciences) ISSN 0001-3765 www.scielo.br/aabc

On the squamation of Australerpeton cosgrifﬁ Barberena, a temnospondyl amphibian from the Upper Permian of Brazil

ELISEU V. DIAS and MARTHA RICHTER

Universidade Federal do Rio Grande do Sul, Instituto de Geociências 91509-900 Porto Alegre, RS, Brasil

Manuscript received on March 5, 2001; accepted for publication on February 26, 2002; presented by Milton Formoso

ABSTRACT Abdominal scales of a juvenile specimen of Australerpeton cosgriffi Barberena 1998 are made of primary compact bone rich in osteocyte lacunae; vascular canals and primary osteons are rare with no sign of remodelling of the tissue by resorption and redeposition. In contrast, the abdominal scales of an adult of the same species shows extensive reworking of the bone tissue. The scale grows by apposition of lamellar bone peripherally around the whole scale; the presence of Sharpey fibers in the periphery of the scales both basally and externally suggests that they remained deeply embedded in the dermis; the embryonic scale is completely remodelled in the adult by resorption and redeposition which produces a cancellous bone with large erosion bays and secondary osteons. Remodelling by resorption and redeposition is confined to the core of the scales and does not affect its periphery, contrary to what happens in sarcopterygians with cosmoid scales. The possible biological functions of the squamation in this species, such as mechanical protection, dry protection, cutaneous respiration, hydrostatic control and calcium reservoir, are discussed. Key words: Temnospondyli, paleohistology, paleobiology, Upper Permian, Rio do Rasto Formation.

INTRODUCTION dev 1984 also possessed a scale cover (Lebedev and Coates 1995). This points to the primitiveness of Rhomboid or round dermal scales are known the scale presence in tetrapods and it seems to be a in many fossil amphibians of distinct groups within remnant character from Osteolepiformes fishes, al- the Temnospondyli such as the Colosteids, Rhine- though their scales differ quite substantially in terms suchoids, Archegosauroids, Trematosauroids and of histological features. Tetrapod dermal bones lack Dissorophoids. The other primitive tetrapod lin- enamel and dentine tissues, for instance, although eage, the anthracosaurs (sensu Gauthier et al. 1988) most living fishes (both sarcopterygians and actino- possessed a very well developed scale covering, a pterigians) also do, a condition acquired indepen- condition found for example in Eogyrinus attheyi dently. No amphibian known so far shows dermal Watson 1926 and in Crassigyrinus scoticus Wat- denticles (odontodes) in the squamation. Amphib- son 1929 where the scales cover almost the entire ians and higher vertebrates apparently lost the ca- body. Basal tetrapods like Tulerpeton curtum Lebe- pacity, seen in fishes, of the trunk neural crest cells Correspondence to: Eliseu Vieira Dias to make teeth and odontodes; only the cranial neural E-mail: [email protected]

An Acad Bras Cienc (2002) 74 (3) 478 ELISEU V. DIAS and MARTHA RICHTER

crest presumably expresses itself forming oral teeth pretation, this "gastralia" composed of scales could and, in certain groups like the urodels and some tem- be homologous with the dermal abdominal ribs of nospondils, tooth-bearing pharyngeal plates (Grave- more derived animals. son et al. 1997, Coates 1996). Consequently, the In conclusion, all the terms, osteoderms, scales dermal bones and squamation of tetrapods are made or gastralia, refer to dermal ossifications and there up exclusively of bone tissue. are no clear distinctions between them. The scales In modern amphibians scales occur in the Gym- or osteoderms of the rhinesuchoid Australerpeton nophiona but their morphological pattern, as de- cosgriffi, resemble fish scales in various aspects and scribed by Zylberberg et al. (1980), is by far differ- here they are called scales for the sake of simplicity. ent from that found in the Temnospondyli amphibian No fossil amphibian scales have been described Australerpeton cosgriffi. from Brazil up to date. The good preservation of the Hook (1983) gave an account of the squamation hard tissues of the specimens and the availability of of some early tetrapods including Colosteus scute- two individuals of different sizes led us to investi- latus Newberry 1856 from the Carboniferous of the gate the structure and histology of the squamation NorthAmerica. He discussed the various terms used of Australerpeton cosgriffi, a species only known to describe the elements of the tetrapod ’armour’and from the continental Rio do Rasto Formation (Up- made a muddled distinction between scales and os- per Permian) of the Paraná Basin in southern Brazil teoderms, basically pointing out the fact that both (Barberena 1998). are structures formed within the dermis, the former The dermal bones and scales of primitive am- presumably deeper and the latter more superficially phibians are known to be highly vascularized and but Hook (1983) did not specify how to quantify this highly reworked through resorption and redeposi- depth. In fact there is no clear functional anatomi- tion of the bone tissue (e.g. Bystrow 1935, Cosgriff cal distinction that justifies choosing between either and Zawiskie 1979). However, comparative histo- of these terms in the case of dermal ossifications of logical studies of amphibians scales are rare. these primitive amphibians. Thin sections of amphibian long bones such as Romer (1956) treated the ventral scales of Pale- femora have shown that the skeletal growth follows ozoic amphibians and those of bony fish as homolo- a pattern similar to modern crocodiles. In both, am- gous by having an essentially protective function and phibians and crocodilies, these bones have growth also homologous in development, because for him, lines that can be used to estimate the minimal age the dermis tends to retain its primitive potentiality of each individual. The type of bone organization of forming bone, and a great number of independent can also provide evidences for ecological inferences groups of tetrapods developed dermal ossifications (Damiani 2000). using this potentiality. Moreover, Hook (1983), like Romer (1956), MATERIAL treated the ventral scales as forerunners of the gas- The skeletons were collected at outcrops of the Rio tralia, the "abdominal ribs" of some primitive tetra- do Rasto Formation along the Ponta Grossa – Apu- pods. There is no consensus about this interpertation carana railroad (Serra do Cadeado region) in the but many authors treat the ventral scales of primitive Paraná State (Fig. 1) by Dr. M. C. Barberena and tetrapods as gastralia. Laurin (1996) described the his colleagues at the Universidade Federal do Rio gastralia of a seymouriamorph as been composed Grande do Sul (UFRGS) at the beginning of the of several scale rows that meet in the midline at a 1980s. Two specimens were used for this study: sharp angle. Milner and Sequeira (1994) also describe a gastralia, composed of elliptical scales, for • UFRGS-PV0319P: A specimen represented by a temnospondyl amphibian. Following this inter- a fragment of the skull table, an almost com-

An Acad Bras Cienc (2002) 74 (3) ON THE SQUAMATION OF Australerpeton cosgrifﬁ 479

Mato Grosso 48º do Sul

Paraná São Paulo 24º Serra do Cadeado area

Paraguay

Santa Catarina Atlantic Ocean Argentina 28º Rio Grande do Sul

Porto Alegre

32º Uruguay 0 300 km 56º 52º Outcrops area of the Passa Dois Group that includes the Rio do Rasto Formation

Fig. 1 – Location map of the Serra do Cadeado region in the State of Paraná, southern Brazil.

plete vertebral column, some bones of the gir- ments of UFRGS-PV0319P and PV0320P fit bet- dles and also some articulated scales. ter on the long-snouted morphotype. Besides, postcranial bones (e.g. femur and clavicle) also differ • UFRGS-PV0320P:An individual with the pos- from those associated with the short-snouted mor- terior part of the skull, many post-cranial bones photype. and some isolated scales. Bageherpeton longignathus Dias and Barber- Within the fossil assemblage of the Rio do Ras- ena 2001, another long-snouted temnospondyl from to Formation in the Serra do Cadeado area there the Rio do Rasto Formation (Dias and Barberena are only two known temnospondyl morphotypes. 2001) was discarded, because it came from a dis- The long-snouted morphotype is attributed to Aus- tinct geographic and stratigraphic position. It was tralerpeton cosgriffi (Barberena et al. 1985, Bar- found in the Rio Grande do Sul State and in upper berena 1998) while the short-snouted morphotype levels within the Rio do Rasto Formation (Barberena remains unidentified (Barberena and Dias 1998). et al. 1985). The material used for histological studies herein was In the amphibian collection at UFRGS yielded identified as Australerpeton cosgriffi mainly based by the Rio do Rasto Formation at the Serra do Ca- on the morphology of the associated skeletal re- deado, there are specimens of Australerpeton cos- mains preserved on both specimens. The skull frag- griffi of distinct sizes, suggesting the presence of an-

An Acad Bras Cienc (2002) 74 (3) 480 ELISEU V. DIAS and MARTHA RICHTER

imals of various ages in the thaphocenosis. We have their mode of articulation. The scales were present no evidence to believe that UFRGS-PV0319P and mainly in the ventral region of the animal as com- PV0320P could represent two biological species. monly found in Temnospondyli. The anteriormost On the contrary, most of the post-cranium remains scale row is in the neck region and the most posterior are similar in both individuals and their small differ- one is apparently at the level of the pelvic girdle. The ences can be more easily interpreted as ontogenetical scales are rhombic in general shape but they vary a or, less probably, due to sexual dimorphism. The little in size and shape throughout the individual. histological evidence described in this paper sup- UFRGS-PV0319P – an young individual of Aus- ports the hypothesis of different ontogenetic stages tralerpeton cosgriffi (Fig. 2A-C). (see discussion). In the post-cranium, the pleu- rocentra are not very well ossified in the smaller At least four assemblages of articulated scales specimen and very well developed in the bigger are preserved ventrally to the vertebral column. No one. Notwithstanding, the discussion of the post- evidence of dorsal scales was found so the scales cranial characters is beyond the scope of this paper cover only the ventral surface of the animal. and will be presented in a future work (Dias and Near the cervical region, the scales are about Schultz, in preparation). Concluding, we assume 18 mm long and their width ranges from 2 to 4 mm. that UFRGS-PV0319P is a young specimen, while They are elongated thin bars, ornamented with long UFRGS-PV0320P is older and may be an adult. and shallow longitudinal grooves. In the anterior For comparison of the dermal skull roof we part of the abdominal region, the scales are slightly used a specimen of the crocodilian Caiman sp. from larger than the anterior ones, measuring 6 to 9 mm Rio Grande do Sul State in the teaching collection in width but with almost the same length, 18 mm. In of the Vertebrate Paleontology Laboratory, as well the posterior part of the abdominal region the scales as the original type series published by Barberena become smaller, ranging from 11 to 14 mm in length (1998) and other partially preserved skulls of Aus- and 4 mm in width. The outline of an isolated scale tralerpeton cosgriffi (UFRGS-PV0237P; UFRGS- of this region is a trapezoid, in which the bigger base PV0320P). is the anterolateral edge and the smaller is the posterior edge (Fig. 2A). When articulated, the exposed surface is lozenge shaped representing almost half DESCRIPTION of the total area of the entire scale (Fig. 2B). The General Morphology and Distribution other half of the scale is excavated anteriomedially, of the Squamation forming an internal articular process that accommo- The osteological description of both specimens dates the preceding overlapping scale. The external whose scale histology is described here will be pre- ornamentation is less pronounced in the abdominal sented elsewhere (Dias and Schultz, in preparation). than in the neck scales and all scales show few blood Most elements of the post-cranium are well pre- vessels crossing the outer surface. At the level of the served and some of them kept their anatomical posi- scapular girdle, there are some articulated scales pre- tion in both specimens. Unfortunately, most of the served in internal view. Their external area is almost scales were dislodged during fossilization, prin- square shaped and the surface seems to be smooth cipally in the adult specimen, so that the original with very small foramina for blood vessels. The an- distribution of the scales is poorly preserved and terior overlapping surface shows some fine furrows prevents a precise reconstruction of the full squa- and a variable number of short nodules, measuring mation in both individuals. However, small blocks no more than 1 mm each (Fig. 2A). of articulated scales were fossilized in the ventral re- UFRGS-PV0320P – an adult individual of Austra- gion of the younger specimen, giving information on lerpeton cosgriffi.

An Acad Bras Cienc (2002) 74 (3) ON THE SQUAMATION OF Australerpeton cosgrifﬁ 481

Fig. 2 –Abdominal scales of a presumed juvenile specimen of Australerpeton cosgrifﬁ Barberena 1998; A. external view of an isolated scale of specimen UFRGS-PV0319P. Scale bar=1cm; B. reconstruction based on the same scale showing the articulation pattern. Scale bar=1cm; C. Histological features observed in a vertical section showing growth lines (arrow) and the embryonic scale of compact bone. Scale bar=1mm.

An Acad Bras Cienc (2002) 74 (3) 482 ELISEU V. DIAS and MARTHA RICHTER

The scales of the adult are variable in size (20- 2. Specimen UFRGS-PV0320P (Figs. 4A-C and 29 mm long and 8-12 mm wide) and in ornamen- 5A-E) (an adult specimen). tation. The trapezoid shape of the scales in the Scale histology. Transverse thin sections of ar- younger specimen develops into a more ellipsoid ticulated scales of this specimen show that all of one in the adult. Frequently, a large number of fine them are entirely made up of cellular bone highly re- blood vessels, lodged in furrows, cross the internal modelled by resorption and redeposition internally. surface of the scale in an almost radial pattern and The bone tissue is compact peripherally and can- they converge to a main region of entrance to the cellous in the core of the scale (Fig. 4A, B and C). scale core (Fig. 3A). Externally, the scales show an The articulation area is composed mainly of compact irregular ornamentation consisting of nodules and bone (Fig. 4C). The osteocyte lacunae are usually some transverse crests and a very small number of well preserved (Fig. 5C). Resorption is therefore vascular openings coming to the out side (Fig. 3B, confined to the ontogenetically older bony layers C and D). of the scale and affects areas of primary lamellar The dermal bones of Australerpeton cosgriffi bone as well as primary osteons. Redeposition oc- show only a single small foramen for each pit or curs around vascular cavities forming secondary os- groove (Fig. 3E). This pattern is similar in Caiman teons. Resorption also forms larger cavities which sp. (Fig. 3F). often truncate primary and secondary osteons lead- ing to total remodelling of the embryonic scale (Fig. Histological Features of the Scales 5B). Vascular canals crossing the scales in all direc- tions suggest that these were deeply embedded in Seven thin sections of dermal scales from these two the dermis. The periphery of the scales contains a specimens of Australerpeton cosgriffi were made large concentration of Sharpey fibber bundles, both and are described below. basally, laterally and superficially (Figs. 4B; 5A, D 1. Specimen UFRGS-PV0319P (a young speci- and E) which also indicates that they were deeply men). embedded in the dermis. Scale histology. Vertical sections of an isolated Growth lines. At least nine growth marked scale and of some articulated scales were made. events were counted in the most peripheral parts of All the scales consist of lamellar (compact) bone the scales which are not too badly affected by re- throughout (Fig. 2C). Primary osteons and vascular working of the bone tissue. The core of the scales, canals are rare. The tissue shows a very high den- corresponding to the embryonic scale, is the site sity of osteocyte spaces and Sharpey fibers, which more heavily affected by resoption and redeposition are distributed at nearly right angles to the entire and also contains the largest vascular cavities (Fig. surface. 4A, B). Growth lines. There are at least five well- Vascularization. The vascular pattern of this marked interruptions in the formation of the bone scale inferred by the thin sections suggests that most which are interpreted as growth lines. The shape of vascular canals run longitudinally in irregular or in the scales is only slightly altered by growth, judging circular rows, giving a trabecular appearance to in- by the course of the growth lines, which are parallel ner portion of the scale, which some authors de- to the former (older) surfaces. There is no evidence scribe as a "honeycomb" bone structure (Cosgriff of remodelling of the bone tissue in this specimen and Zawiskie 1979). This richly vascularized mid- (Fig. 2C). dle portion has only a reduced number of vascular Vascularization. Very few vascular canals of communications to outside. Most of the blood sup- small calibre run across the scale reaching out the ply is therefore provided by the vessels coming from surface. the inner side (Fig. 4A, B and C).

An Acad Bras Cienc (2002) 74 (3) ON THE SQUAMATION OF Australerpeton cosgrifﬁ 483

Fig. 3 – A. Cast of the internal surface of a scale of the adult specimen of Australerpeton cosgrifﬁ Barberena 1998 (specimen UFRGS- PV0320P) showing the radial pattern of furrows produced by blood vessels; B, C and D. External view of adult scales showing ornamentation made up of irregular nodules and crests and the small number of blood vessels reaching out the scale surface. Scale bars = 1 cm. E. External view of the skull table of Australerpeton cosgrifﬁ (UFRGS-PV0237P). Scale bar=2cm. F. External view of the skull table of Caiman sp.. Scale bar = 2 cm. E and F show the pattern of dermal bone ornamentation with a single foramen for each pit or groove.

An Acad Bras Cienc (2002) 74 (3) 484 ELISEU V. DIAS and MARTHA RICHTER

Fig. 4 – Histological features of abdominal scales of UFRGS-PV0320P, an adult specimen of Australerpeton cosgrifﬁ Barberena 1998. A. Cross section. Scale bar = 1mm. B. corresponding drawing; c. crest of external ornamentation; c.b. compact bone; c.c.b., cancellous compact bone; e.b. erosion bay; g.l. growth lines; ost. osteocyte lacunae; p.o. primary osteon; r.l. resorption (reversal) line; S.f. Sharpey ﬁbers; s.o. secondary osteon; v.c. vascular canal. C. Articulated scales showing the area of articulation of two scales (white arrow), as well as large number of vascular canals in the inner side (bottom black arrows) running to the cancellous bone and few of them running to outside. Scale bar=1mm.

An Acad Bras Cienc (2002) 74 (3) ON THE SQUAMATION OF Australerpeton cosgrifﬁ 485

Fig. 5 – Histological features of an abdominal scale of the adult specimen of Australerpeton cosgriffi Barberena 1998. (UFRGS- PV0320P). A. Peripheral region of the scale showing osteocyte lacunae (small arrows) and Sharpey fibers (big arrows). Scale bar = 100µm; B. Resorption lines (arrows) between three osteons. Scale bar = 50µm. C. Detail of osteocyte lacunae (arrow) common throughout the scale. Scale bar = 50µm. D and E. Peripheral area of the scale under polarized light. D. The extensive distribution of Sharpey fibers in the peripheral compact bone as well as in the external limits of the cancellous core. Scale bar = 500µm. E. Detail of the Sharpey fibers (arrows) crossing many growth lines in a crest of the external ornamentation. Scale bar = 250µm.

An Acad Bras Cienc (2002) 74 (3) 486 ELISEU V. DIAS and MARTHA RICHTER

DISCUSSION in amphibians. Olson (1979) also proposed that scales could increase the specific gravity in aquatic The systematic value of dermal scales of Paleozoic forms for hydrostatic function and reduce skin dry- amphibians is limited at present, since the scales ing in terrestrial amphibians. Both functions are of most temnospondyl genera are either usually not plausible for Australerpeton cosgriffi. well described or unknown. Detailed descriptions The physiological function of the scale cover- and histological studies may provide new characters ing in fossil amphibians is controversial. For Romer for systematic studies. (1972), "the scale covering was such as to exclude The external morphology of the scales of a the possibility of any great degree of skin breath- young Australeperton cosgriffi is basically similar to ing in Greererpeton" and he argued that this could patterns found in other temnospondyls such as Platy- be extended for most of the primitive amphibians. oposaurus stuckenbergi Trautschold 1884 and Ura- He also proposed that it is not impossible that some nocentrodon (Rhinesuchus) senekalensis Van Hoe- primitive amphibians have developed a naked skin, pen 1915. The scales are not so elongated in Aus- but this feature seems to have appeared later in am- tralerpeton as they are in U. senekalensis (Van Ho- phibian evolution. epen 1915, Findlay 1968). The shape and size of An opposite idea was presented by Cosgriff isolated scales of the younger specimen ofAustraler- and Zawiskie (1979). Studying the dermal bone peton cosgriffi are similar to the scales of Platy- structure of the rhytidosteid Pneumatostega potamia oposaurus stuckenbergi described by Konzhukova Cosgriff and Zawiskie 1979. They suggest that the (1955 drawings β and δ). dermal ossifications might have been related to a The articulation pattern for Uranocentrodon dermal respiratory apparatus. In this case, not only senekalensis described by Findlay (1968) is similar a well developed honeycombed bone structure is to that of A. cosgriffi, with an elongated articular present, but also a dense network of capillary chan- process in which the articular surface is overlapped nels connected onto the surface by numerous pores by the mesial scales. which open to outside in the valleys between the The chevron – an inverted-V distribution pat- ridge and nodes of the dermal bone sculpture. This tern for the ventral scales – is common in primi- network could carry a copious blood supply to a tive tetrapods. Many authors described this pat- mucous-covered skin where gas exchange was effi- tern in distinct taxa (e. g. Konzhukova 1955 for ciently conducted. Unfortunately, they studied only Platyoposaurus stuckenbergi; Findlay 1968 in Ura- cranial and shoulder girdle dermal bones, leaving nocentrodon senekalensis; Hook 1983 for Colosteus the scales without similar analyses. scutellatus) Unfortunately, due to taphonomic con- Coldiron (1974) argued that there is no consis- ditions, the scales of Australerpeton cosgriffi are tent relationship between cutaneous respiration and scattered in small blocks of scales in the younger in- the type of ornamentation of the bone. For him, the dividual and as isolated scales in the older one and no dermal bone histology of some labyrinthodonts is evidence of the distribution pattern is visible. The a horizontal and irregularly distributed complex of scales of Australerpeton cosgriffi are probably ex- inner vessels, providing an inefficient blood route to clusively present on the ventral surface, as in Platy- the bone surface and then to the skin. He claimed oposaurus stuckenbergi (Gubin 1991). There is no that a more adaptative route should be a less complex evidence of dorsal scales, as in some trematosauri- pathway, because anastomosed canals do not seem ans (Janvier 1992) or dorsal mid line scutes attached to be related to an effective connection to the epi- to the neural arch as in Eryops (Moulton 1974). dermis and that, "if the main function of the canals Protection or defense is the most common func- is to carry blood vessels, those of the lower bone tional interpretation for the presence of squamation layer feeding into this larger middle layer of canals

An Acad Bras Cienc (2002) 74 (3) ON THE SQUAMATION OF Australerpeton cosgrifﬁ 487

would cause a drastic decrease in the blood pressure. since amphibians do not lay eggs with shells. Al- This would be very inefficient for rapid blood flow ternatively, calcium remobilization could be related and efficient oxygen exchange at the skin surface" to extreme environmental stress, such as scarcity of (Coldiron 1974, page 3). Additionally he believed food during the dry season. In Trimerorhachis other that lungs were the main respiratory apparatus at temnospondyl in which the scale histology is known, the labyrinthodont stage and cutaneous respiration bone resorption and redeposition was not observed would have been impossible. (Olson 1979). In this case, the scales are not used The scales of Australerpeton cosgriffi show a as a calcium reservoir, and this could be interpreted small number of pores on their external surface. One as evidence for stable environmental conditions. might expect a larger number if cutaneous respira- The ubiquitous presence of Sharpey fibers in tion was present in those areas. the scales of Australerpeton cosgriffi is indicative of The dermal bones of the skull and shoulder a dermal origin of the whole scale. Sharpey fibers girdle of A. cosgriffi do not show the network of are unknown in endochondral bone (Francillon- capillary channels described by Cosgriff and Za- Vieillot et al. 1990). Moreover, Sharpey fibers dis- wiskie (1979), only a single small foramen for each tributed peripherally around the whole scale (Fig. pit or groove (Fig. 3E). Buffrénil (1982) found in 5A, D and E), indicates that the scales were perma- crocodilian dermal bones a vascular system similar nently embedded in skin and strongly anchoraged to that described in temnospondyl amphibians by one to another within the dermis. This can be an- Bystrow (1935, 1947) and Coldiron (1974). Exter- other evidence against dermal respiration function nally, the dermal bone ornamentation of Caiman sp. for the scales of Australerpeton cosgriffi. shows a similar pattern of a single foramen (or even The distinctive pattern of dermal bone orna- more than one in some areas) for each pit or groove mentation, consisting of grooves and sub-circular (Fig. 3F), which is common in living crocodil- pits is typically (but not exclusively) found in poik- ians. Nevertheless, differences in the morphogen- ilothermic amphibious tetrapods. Temnospondyli esis of the ornamentation between crocodilians and andAnthracosauria labyrinthodont amphibians, cro- temnospondyls suggest an independent evolutionary codilians, aetosaurs thecodonts, some cotylosaurs origin for this character. Based on the similarities of (Captorhinidae, Pareiasauridae) frequently show dermal skull bones morphology between crocodil- such pits and grooves (Buffrénil 1982). The cara- ians and Australerpeton cosgriffi, and the fact that pace of the turtle Drazinderetes tethyensis Head, the former do not breath through their skin, one may Raza and Gingerich 1999, from the Eocene of Pak- conclude that cutaneous respiration was not present istan, also presents superficial bone ornamentation in that amphibian. However this does not imply that (Head et al. 1999) that is in a way similar to the der- areas lacking scales and dermal bones could not be mal bone ornamentation found in temnospondyls. sites for this type of gas exchange. The carapace is composed of enlarged ribs which Another function for the complex bone struc- are of endochondral origin. It is not common to ture of the inner portion of the adult scale could this kind of bone to developed superficial ornamen- be as a calcium reservoir. The ecologically similar tation. In this case, the ornamentation is probably recent animals such as breeding females of african related to anchorage of the dermal scutes. The pat- crocodiles do mobilize calcium from the dorsal os- tern of bone ornamentation in Australerpeton cos- teoderms maybe used to make up the egg shells griffi dermal bones (Fig. 3E) also can be related (Hutton 1986). In Australerpeton cosgriffi the re- to skin anchorage or, following Coldiron (1974), a sorption and redeposition of bone tissue in the adult bone-strengthening function. scales could be an evidence for calcium reservoir The process of scale growth in Australerpeton function but hardly related to the breeding season, cosgriffi is similar to that of some osteolepiform

An Acad Bras Cienc (2002) 74 (3) 488 ELISEU V. DIAS and MARTHA RICHTER

fishes like Gogonasus andrewsae Long 1985 in calcium reservoir function. Cutaneous respiration is which only the last-formed layer of laminar material discarded in Australerpeton cosgriffi at least in areas extends around the scale margin onto the articulat- covered by the scales and dermal bones. The dis- ing surface; internally, as a result of this peripheral tribution of Sharpey fibers around the whole scale growth, the cancellous layer resorbs another lam- is indicative that these scales were strongly anchor- inar layer (Long et al. 1997). Australerpeton cos- aged and deeply embedded into the dermis. griffi shows a marginal growth similar to that seen in Gogonasus andrewsae, but in the latter, the growth ACKNOWLEDGMENTS affects the whole external surface of the scale, leav- M. Richter is indebted to Prof. Wolf-Ernst Reif for ing growth lines all around, not only on the border his hospitality in Tübingen in 1998-99. The thin line. At the same time, internally, growth also pro- sections were made by Mrs. Indra Gill-Kopp. The ceeds by resorption and redeposition of new osteons histological study was partially carried out at the making up for the expansions of the cancellous com- Eberhard-Karls Universität Tübingen during a Post- pact bone layer. This externally ubiquitous growth Doc by MR sponsored by PUCRS and CNPq (fel- of the compact bone also is additional indication that lowship 20.3461/86-0). the scales were deeply embedded in the dermis (Fig. E.V. Dias thanks Prof. Dr. Cesar Leandro 4A-C). Schultz (UFRGS) who made useful comments on The climatic model for the Rio do Rasto Forma- the manuscript and MSc. Lílian Timm (UFRGS) tion is of semi-arid conditions with a slightly more for some bibliography and discussions on bone his- humid season and a dry and hot season (Ragonha tology of reptiles. CNPq for the financial support 1989). If each growth line possibly corresponds (process 143207/1996-2). to a seasonal (annual) growth, then the specimen The authors also thank Prof. Dr. Vitor Paulo UFRGS-PV0319P is, by this criterion, at least 5 Pereira (UFRGS) for the use of the Optic Micro- years old and UFRGS-PV0320P is at least 9 years scope Lab (Curso de Pós-Graduação em Geoquí- old. The second could be much older than 9 years mica), Prof. Gerson Terra for the use of the mi- but the remodelling of the embryonic scales to form croscope of the Convênio UFRGS-Petrobras, where the cancellous bone in the core of the scale precludes they completed the histological study and Mr. Luís an exact count. Flávio Lopes (UFRGS) who developed some of the It is worth noticing that the remodelling of the photographs. scales of this extinct amphibian followed a distinct pattern to those observed in sarcopterygian fishes. In fossil sarcopterygians with cosmoid scales, for RESUMO instance, reworking affected the topmost layers of Escamas abdominais de um espécime juvenil de Austra- the scales, forming theWestoll lines (for an overview lerpeton cosgriffi Barberena 1998 são compostas de osso see Janvier 1996) and does not affect the embryonic primário compacto rico em lacunas de osteócitos; canais scale area, as we observe in Australerpeton cosgriffi. vasculares e osteons primários são raros, não havendo sinais de remodelamento do tecido por reabsorção e re- deposição. Ao contrário, as escamas abdominais de um CONCLUSIONS adulto da mesma espécie mostra um extenso retrabalha- The most plausible presumed functions for the scales mento dos tecidos ósseos. A escama cresce por deposição of Australerpeton cosgriffi are calcium reservoir, de osso lamelar perifericamente ao redor de toda sua su- hydrostatic equilibrium and mechanical protection. perfície; a presença de fibras de Sharpey na periferia da The high rate of resorption and remodelling seen in escama tanto basal com externamente sugere que elas per- the cancellous compact bone layer is evidence for a maneciam profundamente envolvidas pela derme; a es-

An Acad Bras Cienc (2002) 74 (3) ON THE SQUAMATION OF Australerpeton cosgrifﬁ 489

cama embrionária é completamente remodelada no adulto tralian Triassic temnospondyl amphibians: prelimi- por reabsorção e redeposição formando uma camada in- nary data. Mod Geol 24: 109-124. terna esponjosa de osso com grandes baías de erosão e Dias EV and Barberena MC. 2001. A Temnospondyl osteons secundários. O remodelamento por reabsorção e Amphibian from the Rio do Rasto Formation, Upper redeposição é confinado ao núcleo da escama e não afeta a Permian of Southern Brazil. An Acad Bras Cienc 73: sua periferia, ao contrário do que acontece nos peixes sar- 135-143. copterígeos com escamas cosmóides. São discutidas as Findlay GH. 1968. On the struture of the skin in Ura- possíveis funções biológicas das escamas na espécie, tais nocentrodon (Rhinesuchus) senekalensis Van Hoe- como proteção mecânica, proteção contra perda d’água, pen. Palaeont Af 11: 15-21. respiração cutânea, controle hidrostático e reserva de cál- Francillon-Vieillot H, Buffrénil V de, Castanet cio. J, Géraudie J, Meunier FJ, Sire JY,Zylberberg L and Ricquès A. de 1990. Microstructure and min- Palavras-chave: Temnospondyli, paleohistologia, pale- eralization of vertebrate skeletal tissues. In: Carter obiologia, Permiano Superior, Formação Rio do Rasto. JG. (Ed.) Skeletal biomineralization: Patterns, Pro- cesses and Evolutionary Trends. 1, Van Nostrand REFERENCES Reinhold, New York, p. 471-530. Gauthier JA, Kluge AG and Rowe T. 1988. The early Barberena MC. 1998. Australerpeton cosgriffi n.g., evolution of the Amniota. In: The Phylogeny and n.sp., a Late Permian Rhinesuchoid amphibian from classification of the tetrapods. Vol. 1; Amphibia, Brazil. An Acad Bras Cienc 70: 125-137. Reptiles, Birds (ed. MJ Benton), Syst Assoc Spec Barberena MC and Dias EV. 1998. On the presence of Vol 35A: 103-155. a short-snouted Rhinesuchoid amphibian in the Rio Graveson AC, Smith MM and Hall BK. 1997. Neu- do Rasto Formation (Late Permian of Paraná Basin, ral crest potential for tooth development in a Urodele Brazil). An Acad Bras Cienc 70: 465-468. Amphibian: Development and Evolutionary signifi- Barberena MC, Araújo DC and Lavina EL. 1985. cance. Dev Biol 188: 34-42. Late Permian and Triassic tetrapods of Southern Bra- Gubin YM. 1991. (Permian archegosauroid amphibians zil. Nat Geog Res 1: 5-20. of the USSR). Trudy Pal Inst Akad Nauk SSSR 249: Bystrow AP. 1935. Morphologische untersuchungen 1-138 (in Russian). der Deckknochen des Schädels der Wirbeltiere. Acta Head JJ, Raza SM and Gingerich PD. 1999. Drazin- Zool 16: 65-141. deretes tethyensis, a new large trionychid (Reptilia: Bystrow AP. 1947. Hydrophilous and zenophilous Testudines) from the marine Eocene Drazinda forma- labyrinthodonts. Acta Zool 28: 137-164. tion of the Sulaiman range, Punjab (Pakistan). Contr Buffrénil V de 1982. Morphogenesis of bone ornamen- Mus Paleont Univ Mich 30: 199-214. tation in extant and extinct crocodilians. Zoomor- Hook RW. 1983. Colosteus scutellatus (Newberry), a phology 99: 155-166. primitive Temnospondyl amphibian from the Middle Coates M. 1996. The Devonian tetrapod Acanthostega Pensylvanian of Linton, Ohio. Am Mus Nov 2770: gunnari Jarvik: Postcranial anatomy, basal tetrapod 1-41. interrelationships, and patterns of skeletal evolution. Hutton JM. 1986. Age determination of living Nile Trans R Soc Edi 87: 363-421. crocodiles from the cortical stratification of bone. Coldiron RW. 1974. Possible functions of ornament in Copeia 1986: 332-341. labyrinthodont amphibians. Occ Pap Mus Nat Hist Janvier P. 1992. Les écailles des Trématosaures (Tetra- Univ Kansas, 33: 1-19. poda; Temnospondyli): nouvelles données sur les Cosgriff JW and Zawiskie JM. 1979. A new species of Trématosaures du Trias Inférieur de Madagas- the Rhytidosteidae from the Lystrosaurus Zone and a car. Bull Mus natl Hist nat Paris serie 4, 14, section review of the Rhytidosteoidea. Palaeont Af 22: 1-27. C, 1: 3-13. Damiani RJ. 2000. Bone histology of some aus-

An Acad Bras Cienc (2002) 74 (3) 490 ELISEU V. DIAS and MARTHA RICHTER

Janvier P. 1996. Early vertebrates. Clarendon Press, Moulton JM. 1974. A description of the vertebral col- Oxford, 393 p. umn of Eryops based on the notes and drawings of Konzhukova ED. 1955. Platyops stuckenbergi, Trauts- A.S. Romer. Breviora 428: 1-44. chold – an archegosauroid labyrinthodont from the Olson EC. 1979. Aspects of the biology of Trimero- lower zone of the Cis-Uralian Upper Permian. Trudy rhachis (Amphibia, Temnospondyli). J Paleont 53: Palaeont Inst 49: 89-127. 1-17. Laurin M. 1996. A reappraisal of Utegenia, a Permo- Ragonha EW. 1989. Placas Dentárias de Dipnoi no Carboniferous seymouriamorph (Tetrapoda: Batra- Grupo Passa-Dois (P-Tr) da Bacia do Paraná. Apre- chosauria) from Kazakhstan. J Vert Paleont 16: 374- ciações Ambientais, Climáticas, Cronológicas e es- 383. tratigráﬁcas. In: Congresso Brasileiro de Pale- Lebedev OA and Coates MI. 1995. The postcranial ontologia, 11, Curitiba, 1989. Anais... Curitiba, skeleton of the Devonian tetrapod Tulerpeton curtum SBP. 1: 195-206. Lebedev. Zool J Linn Soc Lond 114: 307-348. Romer AS. 1956. Osteology of the reptiles. University Long JA, Barwick RE and Campbell KSW. 1997. Os- of Chicago Press. 772p. teology and functional morphology of the osteolepi- Romer AS. 1972. A Carboniferous labyrinthodont am- form ﬁsh Gogonasus andrewsae Long 1985, from the phibian with complete dermal armor. Kirtlandia 16: Upper Devonian Gogo Formation, WesternAustralia. 1-8. Rec West Aust Mus Suppl 53: 1-89. Van Hoepen ECN. 1915. Stegocephalia of Senekal. Ann Milner AR and Sequeira SEK. 1994. The temnos- Trans Mus 5: 124-149. pondyl amphibians from the Visean of East Kirkton, Zylberberg L, Castanet J and De Ricqles A. 1980. West Lothian, Scotland. Trans R Soc Edinburgh: Structure of the dermal scales in Gymnophiona (Am- Earth Sci 84: 331-361. phibia). J Morph 165: 41-54.

An Acad Bras Cienc (2002) 74 (3)