Chapter I

UNIVERSITY OF KANSAS PUBLICATIONS MUSEUM OF NATURAL HISTORY

Volume 17, No. 10, pp. 493-502, 3 Figs. October 27, 1966

Systematic Status of a South American Frog, Allophryne ruthveni Gaige

BY

JOHN D. LYNCH AND HOWARD L. FREEMAN

UNIVERSITY OF KANSAS LAWRENCE 1966

UNIVERSITY OF KANSAS PUBLICATIONS, MUSEUM OF NATURAL HISTORY

Editors: E. Raymond Hall, Chairman, Henry S. Fitch, Frank B. Cross

Volume 17, No. 10, pp. 493-502, 3 Figs. Published October 27, 1966

UNIVERSITY OF KANSAS Lawrence, Kansas

PRINTED BY ROBERT R. (BOB) SANDERS, STATE PRINTER TOPEKA, KANSAS 1966

31-5378

Systematic Status of a South American Frog, Allophryne ruthveni Gaige

BY

JOHN D. LYNCH AND HOWARD L. FREEMAN

Gaige (1926) described _Allophryne ruthveni_ as a new genus and species of diminutive bufonid from British Guiana. Noble (1931) considered _A. ruthveni_ to be a toothless relative of _Centrolenella_ and placed the genus in the Hylidae. Gallardo (1965) suggested that _Allophryne_ is a leptodactylid of uncertain affinities. Other references to the monotypic genus have consisted only of a listing of the name or of its inclusion in a key. To date the holotype and one paratype (both females) have been reported (Gaige, 1926), and the family position of the genus remains unsettled.

A male of _Allophryne ruthveni_ is among the amphibians and reptiles collected in southern British Guiana by William A. Bentley in January, 1962, and deposited in the Museum of Natural History at The University of Kansas (KU). Four additional specimens (females) are in the American Museum of Natural History; only one of the latter has definite locality data.

_Acknowledgments._--We are grateful to Dr. Ernest E.
Williams, Museum of Comparative Zoology (MCZ) and Dr.
Richard G. Zweifel, American Museum of Natural History
(AMNH) for the loan of specimens. We are further indebted to
Dr. Zweifel for permission to clear and stain one specimen.
Dr. William E. Duellman and Linda Trueb offered many
constructive criticisms. Miss Trueb executed the drawings of
the skull and finger bones. Mr. Martin Wiley provided x-ray
photographs of _Allophryne_.

METHODS AND MATERIALS

Six of the seven known specimens were available for study.
Measurements were taken in the manner described by Duellman
(1956). One specimen was cleared and stained, using the
technique of Davis and Gore (1936), in order to study the
skeleton. X-ray photographs were made of another specimen
for comparison.

_Specimens examined._--Six, as follows: BRITISH GUIANA,
_Dist. Demarara_: Marudi Creek, AMNH 44749; _Dist. Equibo_:
Tumatumari, MCZ 11790 (paratype); _Dist. Rupununi_
(_Berbice_): Wai Wai Country, N of Acarahy Mountains, west
of New River (2 deg.N, 58 deg.W), KU 69890. Also, 3 specimens from
"probably British Guiana," AMNH 70108-10 (70110 cleared and
stained).

SYSTEMATIC ACCOUNT

The availability of additional material and the new information pertaining to osteology permit an amplification of Gaige's (1926) description.

Genus ~Allophryne~ Gaige

_Allophryne_ Gaige, Occas. Papers Mus. Zool., Univ.
Michigan, 176:1, Oct. 14, 1926. Crawford, Annals Carnegie
Mus., 21(1):29, 32, Nov. 14, 1931. Noble, The biology of the
amphibia. McGraw-Hill, p. 510, 1931. Ruthven, Herpetologica,
1:3, July 11, 1936. Gallardo, Papeis Avulsos, 17:79, Jan. 1,
1965.

_Type species._--_Allophryne ruthveni_ Gaige.

_Diagnosis and definition._--A genus of diminutive frogs;
vomers, maxillae, and premaxillae edentate; skin of head
strongly anchored to connective tissue on cranium;
prepollical spine absent in males; disk of third finger
larger than tympanum, smaller than eye; no humeral hook in
either sex; ilia extending anteriorly beyond sacral
expansions; adults attaining snout-vent length of 31 mm.;
male having darkened external subgular vocal sac; skin of
dorsum pustulate.

~Allophryne ruthveni~ Gaige

_Allophryne ruthveni_ Gaige, Occas. Papers Mus. Zool., Univ.
Michigan, 176:1-3, pl. I, Oct. 14, 1926. Crawford, Annals
Carnegie Mus., 21(1):32, Nov. 14, 1931. Ruthven,
Herpetologica, 1:3, July 11, 1936. Barbour and Loveridge,
Bull. Mus. Comp. Zool., 96(2):64, Feb., 1946. Peters, Occas.
Papers Mus. Zool., Univ. Michigan, 539:10, Sept. 19, 1952.

_Holotype._--University of Michigan Museum of Zoology 63419,
adult female, from Tukeit Hill, below Kaiteur Falls, Equibo
District, British Guiana; obtained in May, 1924, by E. N.
Clarke.

_Diagnosis._--Fingers free; toes two-thirds webbed; no
supernumerary tubercles on soles or palms; no tarsal fold;
elongate anal sheath, anal opening on lower surface of
thighs; head broad, interorbital space 2.5 times width of
upper eyelid; snout subacuminate in dorsal profile, strongly
sloping in lateral profile; tympanum visible in males,
concealed in females; venter areolate.

_External Morphology._--(Fig. 1) _Additional features not
mentioned in diagnoses_: Head wider than long, about as wide
as body; supratympanic fold present; canthus rostralis
rounded, loreal region slightly concave, nearly vertical;
nostril at tip of snout; pupil horizontal; no teeth on
maxillary, premaxillary, or vomer; tongue small, round,
thick, not notched behind, free posteriorly for one-sixth of
length; choanae large, only partly visible from directly
below; males having darkened subgular vocal sac; vocal slits
present in male.

Axillary membrane lacking or but slightly developed; no
tubercles or ridge under forearm; two palmar tubercles;
subarticular tubercles small, simple, round, flattened; tips
of fingers slightly expanded, T-shaped, with prominent
transverse groove; first finger shorter than second (stated
as longer than second in diagnosis by Gaige, 1926:2); folds
extending laterally from anus for a short distance, then
downward to venter of thighs; no appendage on heel, no inner
or outer tarsal folds or tubercles; inner metatarsal
tubercle oval, about twice as long as wide; outer metatarsal
tubercle nearly absent; no supernumerary tubercle on sole;
subarticular tubercles on foot small, round, simple, and
diffuse; toes T-shaped, slightly wider than digit; toes
about two-thirds webbed (Fig. 1d).

Skin of venter coarsely areolate; skin of flanks, throat,
chest, undersurfaces of arms, tibia, tarsi, dorsal surfaces
of thighs, tarsi, hands, and feet smooth; skin of dorsal
surfaces of tibia, forearm, back, and top and sides of head
having large horny pustules (sharply spinous in male).

_Color._--Dorsum gray with irregular network of black lines
and elongate blotches; flanks and labial region black with
large white ocelli; dorsal surfaces of limbs gray, marked as
follows: two large, elongate white spots on each thigh,
concealed white spot on base of upper arm, black-edged gray
transverse bars on forearms and shanks, white spot on each
knee and elbow; ventral surfaces pale gray; black-edged
white spot on ventral surface of thigh on each side of anal
opening; chin and throat dark gray with white spots; vocal
sac in male black (Fig. 1a and c).

Gaige (1926) briefly described the color, which conforms to
the above in all particulars. The paratype (MCZ 11790) has
lost the gray color after 40 years in preservation; now
(1966) the ground-color is cream-brown, and the dorsal
spotting, noted by Gaige as being black, is now brown.

The spots on the feet, tarsi, knees, thighs, flanks and
upper arm are white in preservative, but in life possibly
were red or yellow. These colors usually fade to white in
preservative. Red or yellow spots are common aposematic
colors in frogs.

_Variation._--Eight measurements were taken on each specimen
and four ratios were computed; these are summarized in Table
1. Gaige's illustration of the holotype shows that it has a
greatly reduced pattern, whereas the paratype and three of
the other five known specimens have relatively large and
numerous spots. The male (KU 69890) and one female (AMNH
70108) have a reduced pattern intermediate between that of
the holotype and the four other specimens.

TABLE I.--Variation in Measurements and Proportions of Allophryne ruthveni. (Ranges in parentheses below means.)

--------------------------+----------+-----------------
Character | Male (1) | Females (5)
--------------------------+----------+-----------------
Snout-vent (in mm.) | 20.6 | 23.6
| | (18.4-31.0)[A]
| |
Tibia/snout-vent | 0.43 | 0.43
| | (0.41-0.47)
| |
Tympanum/head width | 0.12 | 0.15
| | (0.14-0.16)
| |
Eyelid/interorbital space | 0.55 | 0.53
| | (0.49-0.56)
| |
Tympanum/eye length | 0.40 | 0.46
| | (0.42-0.50)
--------------------------+----------+-----------------

[Footnote A: Holotype is reported to be 31 mm. snout-vent length (Gaige, 1926). The largest measured by us was 26.2 mm. snout-vent.]

The dorsal spinules are most pronounced and extensive on the
male (Fig. 1) and less so in all other specimens examined.
The illustration of the holotype suggests that it has
equally prominent, but fewer, spinules (Gaige, 1926).

The holotype, a gravid female, is the largest known specimen
(31 mm., snout-vent length). Another gravid female (AMNH
70108) has a snout-vent length of 26.2 mm.

_Distribution._--All known specimens have been found in the
foothills of the northeastern face of the Guiana Massif in
British Guiana.

FAMILY POSITION

The following characters of _Allophryne_ are those generally
held to be useful in determining family relationships:

1. Presacral vertebrae procoelus, eight in number.

2. Parahyoid absent.

3. Free ribs lacking.

4. Bidder's organ absent.

5. Intercalary cartilages present in digits; phalangeal
formulae 3-3-4-4 and 3-3-4-5-4.

6. Coccyx articulating with sacrum by two condyles.

7. Tarsal bones not fused.

8. Pectoral girdle arciferal.

9. Epicoracoidal horns present, free.

10. Terminal phalanges T-shaped.

11. Sacrum procoelus and diapophyses expanded.

12. Maxillae, premaxillae, and prevomers edentate.

13. Cranial roofing bones well ossified.

Griffiths (1959) accorded considerable taxonomic weight to the presence or absence of epicoracoidal horns in showing relationships among the genera placed in the Brachycephalidae [= Atelopodidae; Dendrobatidae; and Leptodactylidae (in part)] by Noble (1931). _Allophryne_ possesses well-developed, free epicoracoidal horns, such as those found in the Hylidae, Centrolenidae, Leptodactylidae and Bufonidae.

The presence of intercalary elements in the digits is characteristic of the Centrolenidae, Hylidae, Phrynomeridae, Pseudidae, and the rhacophorine ranids (including the Hyperoliidae). This element is bony in the pseudids and cartilaginous in the other families. Phrynomerids and rhacophorine ranids lack epicoracoidal horns and have firmisternal pectoral girdles. Centrolenids are small, delicate, arboreal frogs having poorly ossified skulls and fused tarsal bones, but agree with _Allophryne_ in having T-shaped terminal phalanges.

Only the presence of intercalary cartilages (Fig. 2) suggests relationship of _Allophryne_ to the Hylidae. The T-shaped terminal phalanges suggest affinities with centrolenids, elutherodactyline leptodactylids, or certain "brachycephalid" frogs. Griffiths (1959) clearly showed that Noble's Brachycephalidae was a polyphyletic assemblage. No hylid genus is edentate, and none has either T-shaped terminal phalanges or the unusual dorsal spinules. Perhaps the presence of intercalary cartilages is not indicative of relationship but instead is a parallelism (or convergence) in _Allophryne_ and genera of the Centrolenidae.

CRANIAL OSTEOLOGY

The skull of _Allophryne_ (Fig. 3) is distinctive among
anurans; it does not closely resemble the skulls of either
hylids or centrolenids, both of which have generally more
delicate (except for casque-headed hylids, such as
_Corythomantis_, _Diaglena_, _Osteocephalus_, _Triprion_)
and generalized skulls. _Allophryne_ on the other hand has a
strongly ossified central region (cranial roofing bones and
sphenethmoid complex) and a weak peripheral zone. The
peripheral elements are reduced (maxilla, pterygoid, and
squamosal) or absent (quadratojugal), whereas the
frontoparietals, nasals, sphenethmoid, prooetics, and
exoccipitals form a compact central zone. An elongate
frontoparietal fontanelle is present.

Dorsally (Fig. 3), the premaxillae are not visible. The
proportionally gigantic septomaxillae are visible anterior
to the nasals. The moderate-sized nasals are separated
medially and in broad contact with the ethmoid posteriorly.
The palatine process of the nasal does not meet the frontal
process of the maxilla. A large frontoparietal fontanelle is
evident between the frontoparietals. The tegmen tympani are
much reduced and maintain only cartilaginous contact with
the posterior arms of the squamosals. The foramen magnum,
occipital condyles, and exoccipitals show no unusual
features. The _pars facialis_ and frontal process of the
maxilla are greatly reduced. The maxilla and premaxilla are
articulated. The high, narrow alary processes of the
premaxillae extend dorsally about two-thirds of the height
of the snout. A cartilaginous internasal septum is
illustrated (Fig. 3), but sectioning is necessary to
determine the true nature and extent of this element.

Ventrally, the skull lacks palatines. The maxillae,
premaxillae, and prevomers are edentate. The parasphenoid is
large with relatively short, stout alary (lateral)
processes. The sphenethmoid is extensive in ventral aspect
and forms the major supporting structure in the anterior
part of the skull. The pterygoid has a broad articulation
with the maxilla, a tenuous contact with the squamosal, but
is not attached to the prooetic. The anterior (zygomatic)
process of the squamosal is greatly reduced (only about
one-third the length of the posterior process).

DISCUSSION

The skull of _Allophryne_ is definitely non-hylid. Most of the post-cranial features do not help to clarify relationships. _Allophryne_ shares several osteological features with the Dendrobatidae: T-shaped terminal phalanges, general cranial morphology and procoelus vertebrae. But, the dendrobatids possess firmisternal pectoral girdles and lack epicoracoidal horns. Also, no dendrobatid has intercalary elements in the digits. We are, therefore, left with a taxonomic enigma. In one or more characters generally regarded as important, _Allophryne_ differs from all presently defined families of frogs. The Hylidae and Dendrobatidae are the only currently recognized families in which the genus might be placed.

The function and taxonomic importance of the large septomaxillae are unknown and are probably associated with the modification of the sphenethmoid-prevomer area. A more detailed study of the cranial osteology of _Allophryne_, especially the structural relationships of the sphenethmoid-prevomer area may elucidate the relationships of _Allophryne_.

The relationships of _Allophryne_ cannot be understood without a re-analysis of some of the features used as major criteria in frog classification (the nature of an intercalated cartilage; the nature of the sternal complex; the relative value of cranial osteology; the vertebral structure; and the thigh musculature). Some of these features have been investigated by other workers, most notably Griffiths, but others have not and need re-examination. A re-analysis of some of the major criteria used in frog classification is in progress (Callison, Lynch, and Trueb) and upon completion of that study we think the relationships of _Allophryne_ will become apparent.

A more comprehensive study of the cranial anatomy of certain hylids, leptodactylids, dendrobatids, and atelopodids along with that of _Allophryne_ is needed to clarify the relationships of _Allophryne_, and might indicate that the recognition of a fifth family is necessary.

CONCLUSION

Among currently recognized families of frogs, _Allophryne_ is least different from the Hylidae although it is our opinion that inclusion of this genus in the Hylidae probably represents an unnatural classification. However, the present evidence suggesting that _Allophryne_ should be in another family is less convincing than evidence suggesting it should be in the Hylidae. We tentatively place _Allophryne_ in the Hylidae.

LITERATURE CITED

DAVIS, D. D. and GORE, U. R.

1936. Clearing and staining skeletons of small vertebrates.
Fieldiana: Technique, 4:1-16.

DUELLMAN, W. E.
1956. The frogs of the hylid genus _Phrynohyas_ Fitzinger,
1843. Misc. Publs. Mus. Zool., Univ. Michigan, 96:1-47,
February 21.

GAIGE, H. T.
1926. A new frog from British Guiana. Occas. Papers Mus.
Zool., Univ. Michigan, 176:1-3, October 14.

GALLARDO, J. M.
1965. A proposito de los Leptodactylidae (Amphibia Anura).
Papeis Avulsos, 17:77-87, January 1.

GRIFFITHS, I.
1959. The phylogeny of _Sminthillus limbatus_ and the status
of the Brachycephalidae (Amphibia: Salientia). Proc.
Zool. Soc. London, 132:457-87, May.

NOBLE, G. K.
1931. The biology of the amphibia. McGraw-Hill, New York,
vii + 577 pp.

_Transmitted August 2, 1966._

31-5378

* * * * *

Transcriber's Notes

Italicized text is shown within _underscores_.

Bold text is shown within ~tildes~.

Table 1 and Figs. 2 and 3 have been moved slightly to avoid breaking up the paragraphs of text.