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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°N, 58°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, Papéis 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).

[Illustration: FIG. 1. _Allophryne ruthveni_, male (KU 69890);
(_a_) Dorsum. (_b_) Thenar view of right hand. (_c_) Lateral profile of
head. (_d_) Plantar view of right foot. × 3.5.]

     _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.

[Illustration: FIG. 2. Dorsal (_a_) and lateral (_b_) views of
distal phalanges of third finger of _Allophryne_. × 40.]

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, proötics, and
     exoccipitals form a compact central zone. An elongate
     frontoparietal fontanelle is present.

[Illustration: FIG. 3. Dorsal view of skull of _Allophryne_
(AMNH 70110). × 12.]

     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 proötic. 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 propósito de los Leptodactylidae (Amphibia Anura).
           Papéis 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



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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.