Osteological notes on Hylorina Sylvatica (Anura: Leptodactylidae)

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Boll. Mus. reg. Sci. nat. Torino

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Vol. 10 - N. I

pp. 209-216

2-6-1992 L _-

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Osteological notes o n Hylorina sylvatica (Anura: Leptodactylidae)

ABSTRACT The review of osteological characters of Hylorina sylvarica show some character states that differ from, or were previously overlooked in, the available descriptions. The most noticeable are the presence ofquadrato-jugal, the separation ofmedial rami ofpterygoid and parasphenoid alae, a cotylar arrangement type 11, the structure of frontoparietals, the joint scapula-suprascapula, the structure ofhyoid apparatus, etc. The scope ofTelmatobiinae needs to be re-interpreted, because available data doesn't support its monophyly.

The monotypic genus Hylorina, one ofthe less known of those inhabiting the austral forest of Chile and Argentina, has received some attention from the osteological point of view (e.g. Jimenez de la Espada, 1875; Boulenger, 1882; Lynch, 1971; 1978 and Heyer, 1975). The available information show some shortcomings, due both to the incompleteness ofthe analyzed structures and to failures in the observation of certain characters, that led to misinterpret the phylogenetic relationships of the genus. The review ofthe osteological characters of Hylorina sylvatica tends to correct some "classical" mistakes, to give information about some previously overlooked characters and to re-diagnose the genus, as a foregoing step to establish its phylogenetic relationships among the Telmatobiinae. Instituto de Herpetología, CONICET - Fundación Miguel Lillo, San Miguel de Tucumán, Argentina.

mlorina sylvatica is a rather scarce species both in nature and in herpetological collections, so that the availability of specimens for osteological preparations is restricted. The study is based on two males, one from Chaitén, Palena Province, Chile, and the other from Termas de Pichicolo, near Hornopirén, X Region, Chile, and are housed at Fundación Miguel Lillo collection under the numbers FML 039 10 and FML 03918 respectively. The material was cleared and stained following Wassersug's (1976) method, and the osteological analysis followed Lynch (1971), Trueb (1973). Heyer (1975) and Fabrezi (1990).

A - S k u l l (figs. la - lb):

Skull longer than width; cephalic index 1.09- 1.15. Frontoparietals bifurcated, fused in the posterior half of parietal region. Frontoparietal fenestra widely open. Frontoparietals widely separated from nasals, covering the sphenetmoid for 25.8-34.4% of its length. Lateral margins don't reach the epiotic eminences and are partly fused with otoccipital. Nasals thin, with irregular margins, and placed at the leve1 of palatines; they can be or 11ot superposed to sphenethmoid and are separated from each other and from maxillar. Ratio maximum widthlmaximum length of nasals: 0.34-0.35. Sphenethmoid as a complete ring, with the anterior margin projecting and the ventral face longer than dorsal (ratio ventral lengthldorsal length of sphenetmoid: 1.61-1.74). Prevomers with 10-13 teeth disorderly grouped, widely separated from one ai~otherand slightly overlapped by sphenethmoid. Maxillary arch complete. Quadrato-jugal completely ossified and not reaching the maxillar. Quadratum ossified. Maxillar with 42-47 teeth that run from the anterior end to a point behind the contact area with pterygoid. Pars facialis high; pterygoid process absent. Premaxillar overlaps the maxillar and bears 12-16 teeth; alary process expanded medially and ii~clinedbackwards. Palatines relatively stout, superposed to pars palatina of maxillar; anterior tip blunt and wide; inner tip acute. Cultriform process of parasphenoid long and thin (ratio parasphenoid lengthlparasphenoid alae: 0.96), overlapping the sphenethmoid on 70-72% of its length. Parasphenoid not fused with otoccipital, and not reaching the palati n es. Anterior rami of pterygoid exceeds 112 of the orbit but doesri't reach the

Fig. 1 - Hylorina sylvatica. l a Dorsal view of skull. - 1 b Detail of the posterior corner oSrn:ixillary arch. - Ic Hyoid. - Id Pectoral girdle. - Dotted areas: cartilage. Scale equals 5 m m .

palatines. Posterior rami shorter than media1 (ratio posteriorlrnedial ramus: 0.74-0.93), separated from the quadratum by a thin sheet of cartilage. Squamosal forms an angle of 45-50' with the horizontal plane of skull. Zygomatic and otic ramus subequal in size; the second with a well developed otic plate. Prootic and exoccipital fused in a completely ossified otoccipital. Occipital canal open. Epiotic eminentes well defined. Operculum not mineralized. Occipital condyles semilunar, protuberant and separated by a distance about 112 of the condylar length. Columella stout, with a small extra-stapes. Tympanic ring U-shaped; anterior end attached to squamosal at midway between otic and zygomatic ramus, and posterior end synchondrotically attached to crista parotica. Angular with noticeable coronoid process and cartilaginous articular region. B - H y o i d (fig. lc): Hyoid plate not mineralized, wider than long (ratio lengthl width: 0.700.90) and with parallel margins. Hyoglossal sinus strong.

Anterior process small; alary process distally expanded and placed in front of the sinus. Posterolateral horns almost parallel to axial axis, their base in front of the posterior margin of the plate. Their length is variable (either shorter or longer than alary process). Thyroh ya1 separated from each ot her, wi th rounded anterior margins; terminal cartilage not mineralized and not fused to cricoid. Cricoid as a not mineralized ring; esophagic process not differentiated; bronchial process noticeably thin. Arytenoid with mineralized areas. C - Vertebral Column: Presacral vertebrae not imbricated, but neural spines of vertebrae 1 and 11 are in contact. Cotylar arrangement of atlas resembles Type 11 of Lynch (1971). Sacra1diapophysis expanded; dista1 end 1.7 times wider than the proximal. Relative length of transverse processes variable: SACRA > 111 > IV = VI11 > 11 > VI1 > V = VI or SACRA > 111 > 11 = IV > V > VI = VI1 > VI1 Urostyle as long as the rest of vertebral column (urostyle lengthlvertebral length: 1.0 1- 1.03), with normally developed spine and cartilaginous tip. Anterior end perpendicular to axial axis, placed behind the cotyles.

D

P e c t o r a l G i r d l e (fig. Id): Omosternum cartilaginous, distally expanded; mesosternum completely ossified; xiphisternum cartilaginous and expanded. Cartilaginous areas of sternum not mineralized. Procoracoid bridge absent; epicoracoid horns reduced. Epicoracoids with mineralized areas; in ventral view, the left one overlaps the right. Clavicule and coracoid without peculiar characters. Scapula 1.8-2.0 times longer than clavicula, and 1.5-1.6times the coracoid. Pars acromialis better developed and reaching a more media1 position than pars glenoidalis. Glenoid cavity surrounded by cartilage, better developed between coracoid and scapula. Suprascapula with mineralized areas and synchondrotically united to scapula (there is a groove in the scapular edge that receives the suprascapula). -

E - Pelvic G i r d l e : Ilium with well cieveloped ilial crest and vestigial dorsal protuberance. Articulation with sacra1 diapophysis of type IIB of Emerson (1979); sesamoid over the articulation cartilaginous. Pubis cartilaginous only in acetabular region.

Fig. 2

- Hylorina

sylvatica. 2a Carpus. - 2b Tarsus. - Scale equals 5 mm.

Ischium fused to pubis in the ventral area of pelvic plate. Posterior and ventral edges of pelvic plate rounded; union between iliums smooth, with a U-shaped sinus; anterior processus absent; preacetabular region not expanded. F - F o r e l i r r i b s (fig. 2a): Humerus with well developed ventral (deltoid) crest; media1 and lateral crests smaller. Radio-ulna without peculiar characters. Carpus Type C of Fabrezi (1990), formed by ossified radiale, ulnare, element Y and carpale distal 2; carpals 3-4-5 fused in one element. Prepollex with three elements, being the distal one cartilaginous. Phalangeal formula typical; terminal phalanges knobbed.

G - H i n d l i m b s (fig. 2b): Al1 the elements noticeable elongated. Tibia-fibula longer than femur (tibia length / femur length: 1.12-1.16). Tarsus consisting of .three ossified elements: tarsale distal 1, 2 and 3; element Y fused with the base of prehallux. Prehallux with ossified base and three segments of mineralized cartilage. Phalangeal formula typical; terminal phalanges knobbed. Proportional length of hindlimb elements, referred to skull length, as follows: femur 1.31-1.35; tibia: 1.52-1.53; tibiale-fibulare: 0.84-0.89; metatarsal IV: 0.56-0.62; proximal phalange, digit IV: 0.38-0.39; second phalange, digit IV: 0.30-0.31; third phalange, digit IV: 0.24; distal phalange digit IV: 0.14-0.15.

Modern studies on Hvlorina sylvatica skeleton were based on stereo-radiographs (Lynch, 1971), or were re-interpretations of the data presented therein (Heyer, 1975). Probably due to this method, some character states were misinterpreted in Lyncll's paper. The most noticeable of these latter are: alary processes of premaxillae directed dorsally, wide at base; quadrato-jugal absent, replaced by a ligamentous sheath; otic rami of squamosal shorter than zygomatic and parasphenoid alae broadly overlapped laterally by the median rami of pterygoid. Our specimens show alary process of premaxillae inclined backwards and medially expanded, quadrato-jugal present as an evident, ossified element that doesn't contact the maxillae, the length of otic and zygomatic ramus of squamosal variable (ratio otic/zygomatic ramus length: 0.94-1.17) and the median rami of pterygoid separated from parasp henoid alae. Some other character states erroneously considered in the 1971 paper (related to pterygoid processes of premaxillae, the extension of the anterior rami of pterygoid and the structure of sternum) were subsequently corrected by Lynch (1978). Heyer (1975) presented some other characters not confirmed in our study, such as frontoparietals separated medially, prevomers in median contact, prootic not fused with frontoparietals and transverse processes of presacral VI11 and sacral ones of subequal width. In the analyzed material frontoparietals are fused together in the posterior half of the parietal region and have areas of fusion with otoccipital, the prevomers are separated and the diapophyses of presacral VI11 are narrower than sacral ones (ratio presacral/sacral diapophysis width: 0.60-0.68). Other peculiar characters in Hylorina sylvatica skeleton, not previously discussed, are: a) A noticeable high number of teeth in prevomer. Although comparative data are relatively scarce, it is possible to point out: Hylorina sylvatica: 10-13; Batrachophrynus and Lynchophrys are edentate; Atelognathus patagonicus: 0-2; Alsodes up to 7; Insuetophrynus: 6-7; Telmatobius ssp. up to 7 and Telmatobufo up to 8. b) The suprascapula is synchondrotically attached to the scapula, character state previously reported for leiopelmatids (Trueb, 1973). c) The scapula is proportionally long (ratio scapula/clavicula length: 1.82.0). The lack of comparative data among lower Telmatobiinae is absolute; measurements taken in one specimen oflnsuetophrynus acarpicus show a ratio of 1.1, and in few species of argentinian Telmatobius, up to 1.4. d) The elongation of posterior limbs of Hylorina svlvatica is a known character, but it seems that not al1 segments contribute in the same way. Here

Table 1 - Proportional length of hindlimb elements, referred to skull length. F = femur; T F = tibia-fibula; tf = tibiale-tibulare; mIV = metatiirsal IC'; ph 1-ph4 = phalanges 1 to 4, digit IV. F

TF

tf

mIV

phl

ph2

ph3

ph4

Insuetophynus acarpicirs

0.96

1.00

0.56

0.42

0.22

0.15

0.12

0.06

Leptorlac!ylus occllarus

1.29

1.38

0.69

0.59

0.37

0.28

0.19

0.13

P/iysalaemus albonorarus

1.23

1.50

0.67

0.55

0.35

0.21

0.14

0.10

Pleurodema tucumana

1.09

1.15

0.57

0.55

0.26

0.16

0.12

0.08

Telrnatobius laticeps

0.93

1.22

0.66

0.59

0.32

0.23

0.16

0.16

Hvlorina sylvatica

again the absence of comparative data is evident. In Table 1 is presented the relative length of different elements of posterior limb (femur, tibia-fibula, tibiale-fibulare, metatarsal 1 and phalanges 1-1V of digit IV), referred to the skull length of some leptodactylids. Although the data are only indicative, it is apparent that the greatest elongation is presented by tibiale and fibulare, while metatarsal IV and dista1 phalange of digit IV have similar proportions than the other species. e) A well defined, ossified sternum seems to be an exclusive character state for Hylorina sylvatica. The presence of ossified sternum was reported for Alsodes, Batrachophrynus, Caudiverbera and some Telmatobius, but in t hose genera it is not possible to recognize mesosternum and xiphisternum. Based on osteological evidences, the genus Hylorina can be diagnosed on the following combination of character states: 1 2 3 4 5

- A great number of prevomerine teeth (10-13). - Mesosternum well defined and ossified. - Suprascapula synchondrotically attached to scapula. - Lateral margins of hyal plate straight and almost parallel. - Posterior limbs greatly elongated.

The polarity of those character states will be establislied after a revision of the genera included in the subfamily. Phylogenetic relationships among lower Telmatobiinae (or Telmatobiinae serzsu stricto, according Heyer, 1975 and Laurent, 1986) as presented by Lynch (1978) need to be reviewed. The presence of quadrato-jugal, the separa-

tion of media1 rami pterygoid and parasphenoid alae and the presence of a cotylar arrangement of atlas Type 11, among others will alter the relationships of Hylorina among the subfamily. Furthermore, it will be necessary to re-interpret the scope of "Telmatobiinae", because available data do not support its monophyly.

La revisione dei caratteri osteologici di Hylorina ~ ~ I v a t i ha c a messo in evidenza che alcuni "character states" erano stati trascurati dai precedenti studi o se ne differenziano. 1 piu notevoli riguardano la presenza di un quadrato-iugale, la separazione dei rami mediali dello pterigoide e delle ali del parasfenoide, una disposizione cotilare di tipo 11, la struttura dei frontoparietali, I'unione fra scapola e soprascapola, la struttura dell'apparato ioideo, etc. Il significato del taxon Telmatobiinae dovra essere reinterpretato in quanto i dati a nostra disposizione non sostengono la sua monofilia. E.O. LA\IL.L.I Instituto de Herpetologia, Fundación Miguel Lillo, Miguel Lillo 251, 4000 Tucurnán, Argentina

LITERATURE CITED BOULENGER G. A., 1882. Catalogue of the Batrachia Salientia s. Ecaudata in the collection of the British Museum. 2nd Ed., London. British Museum. EMERSON S. B., 1979.The ilio-sacral articulation in frogs. Form and function. Biol. J. Linnean Soc., ii: 153-158. FARREZI M., 1990. Estructura y desarrollo del carpo en anuros. Tesis Doctoral (unpublished). Fac. Cs. Nat. Univ. Nac. Tucumán, Argentina: 1-100. HEYER W. R., 1975. A preliminary analysis ofthe intergeneric relationships of the frog family Leptodactylidae. Smithsonian Contrib. Zool. 199: 1-55. JIMENEZ DE LA ESPADA M., 1875. Vertebrados del viaje al Pacífico verificado ... Imp. Miguel Giusta, Madrid: 1-208 + 7 pl. LAURENT R. F., 1986. Des Lissamphibiens (Lissamphibia). Systematique. In P. P. Grassé and M. Delsol (eds.), Traité de Zoologie, XIV (IB): 594-797. LYNCH J. D., 1971. Evolutionary relationships, osteology and zoogeography of Leptodactyloid frogs. Misc. Publ. Mus. Nat. Hist. Univ. Kansas, 53: 1-238. LYNCII J. D., 1978. A re-assessment of the telmatobiine leptodactylid frogs of Patagonia. Occ. Pap. Mus. Nat. Hist. Univ. Kansas, 72: 1-57. TKIIEH L., 1973. Bones, frogs and evolution. In J. L. Vial (ed.), Evolutionary Biology of Anurans: Contemporary research on major problems. Univ. Missouri Press: 65-132. WASSERSUG R. J., 1976. A procedure for differential staining of cartilage and bone in whole formalin fixed vertebrates. Stain. Tech. 51: 131-134.