Internal Oral Features of Larvae from Eight Anuran Families: Functional, Systematic, Evolutionary and Ecological Considerations

Herp, QL 668 MISCELLANEOUS IIVERSITY OF KANSAS .E2 PUBLICATION ISEUM OF NATURAL HISTORY W3 NO. 68

By Richard Wassersug

UNIVERSITY OF KANSAS LAWRENCE 1980 UNIVERSITY OF KANSAS PUBLICATIONS MUSEUM OF NATURAL HISTORY

The University of Kansas Publications, Mu: u Natural History, beginning with volume 1 in 1946, was discontinued with ^olunI'! 2u in 1971. Shorter research papers formerly published in the above series are now published as Occasional Papers, Museum of Natural History. The Miscellaneous Publications, Museum of Natural History, began with number 1 in 1946. Longer research papers are published in that series. Monographs of the Museum of Natural History were initiated in 1970. All manuscripts are subjected to critical review by intra- and extramural

specialists; final acceptance is at the discretion of the Director.

Institutional libraries interested in exchanging publications may obtain the Occa- sional Papers and Miscellaneous Publications by addressing the Exchange Librarian, University of Kansas Library, Lawrence, Kansas 66045. Individuals may purchase separate numbers of all series. Prices for all publications of the Museum may be obtained from the Publications Secretary, Museum of Natural History, University of Kansas, Lawrence, Kansas 66045.

HARVARD UNIVERSITY

Library of the

Museum of

Comparative Zoology (VlUS. COMP. ZOOL_. l...:BRARY

JUL 2 1980

r-i W 1^ I V ES: The University of Kansas Museum of Natural History

Miscellaneous Publication No. 68

June 24, 1980

Internal Oral Features of Larvae from Eight Anuran Families: Functional, Systematic, Evolutionary and Ecological Considerations

Richard Wassersug

Department of Anatomy and Committee on Evolutionary Biology University of Chicago Chicago, Illinois 60637

The University of Kansas Lawrence 1980 7 3 University of Kansas Publications, Museum of Natural History

Editor: E. O. Wiley

Miscellaneous Publication No. 68 pp. 1-146; 37 figures Published June 24, 1980

Museum of Natural History The University of Kansas Lawrence, Kansas 66045 U.S.A.

-^31 mo RSITY

^-f ^ u <^ ^

Printed by University of Kansas Printing Service Lawrence, Kansas CONTENTS

INTRODUCTION 1 Acknowledgements 2 Materials 2 Methods 5 DESCRIPTIONS 7 Ascaphidae 7 Ascaphus truei 7 Discoglossidae 10 Alytes ohstetricans 10 Alytes cisternasii 14 Bombina orientalis 16 Discoglossus pictus 19 Rhinophrynidae 21 Rhinophrynus dorsalis 21 Microhylidae 24 Microhyla berdmorei 24 Microhyla heymonsi 27 Microhyla ornata 30 Pelobatidae 32 Scaphiopus bombifrons 32 Megophrys minor ,. 33 Leptobrachium hasselti 37 Leptobrachium oshanensis 40 Oreolalax pingii 43 Hylidae 46 Anotheoa spinosa 46 Gastrotheca riobambae 48 Hyla femoralis 52 Hyla rufitela 55 Hyla dendroscarta 59 Hyla phlebodes 61 Hyla mixe 63 Hyla ebraccata 67 Hijla sarayacuensis 70 Ptychohyla schmidtorum 72 Ptychohyla leonhardschultzei 76 Acris crepitans 80 Smilisca sordida 82 Agalychnis callidryas 85 Centrolenidae 88 Centrolenella fieischmanni 88 Dendrobatidae 91 Colostethus subpunctatus 91 Colostethus nubicola 94 DISCUSSION 97 Functional Considerations 97 Keratinized structures 97 Infralabial papillae 98 Lingual papillae 99 Buccal floor arena 99 Buccal pockets 100 Prepocket papillae and other features of the buccal floor 101 Ventral velum 102 The filter system 105 Branchial food traps and secretory ridges 109 Glottis and laryngeal disc 110 Esophageal funnel 111 Prenarial arena 111 Internal nares 112 Postnarial arena 113 Lateral ridge papillae 114

Buccal roof arena - - 114 Glandular zone and dorsal secretory pits 115 Dorsal velum 116 Pressure cushions 117 Systematic Considerations 117 Ascaphidae 118 Discoglossidae 118 Rhinophrynidae 118 Microhylidae 118 Pelobatidae 119 Hyhdae 119 Dendrobatidae and Centrolenidae 121 Evolutionary Considerations 121 The Ascaphus and Leiopelma life cycles 121 Evolutionary trends in the Discoglossidae 122 The Pipoidea and their relationships 123 The microhylid problem 124

The origins of the "advanced" anurans ( Type 4 larvae ) 125 Evolution of specific larval types in the genus, Hijla 126

The evolution of ontogenies and its role in larval diversity 127 Ecological Considerations 128 Tadpole feeding ecology 128 Particle sorting: the general mechanism 129 Microhabit implications of morphological patterns 130 SUMMARY AND CONCLUSIONS 133 LITERATURE CITED 139 APPENDIX: GLOSSARY OF TERMS 143 INTRODUCTION

It has been a full century since a characters with systematic import, but biologist first studied tadpole morphol- to discern patterns in oral features that ogy for clues to the evolution and sys- can be correlated with our knowledge of tematics of the Anura (Lataste, 1879). tadpole ecology. Generally recognized as the most signifi- I present here a comparative study cant work from these last hundred years of certain internal oral features of anu- is that of Orton (1953, 1957), who sorted ran larvae that have not been empha- all frog families into four groups based sized by Starrett, Sokol, or other work- on larval characters, specifically external ers. The characters described are all oral features and spiracle position. surface features which lie between the While herpetologists have largely ac- opening of the mouth and the esopha- cepted Orton's four superfamilial groups, gus. I have emphasized those organs there is continual disagreement about which come into direct contact with relationships between and within these water and food in the mouths of tad- groups. Controversies have centered on poles and are thus directly involved with the question of how much weight should the feeding process. be given larval characters when larval I have chosen to examine morpholog- morphologies suggest relationships dif- ical structures involved in feeding in ferent from adult morphologies. Resolu- part because they are convenient to tion of this question has been hampered study. The morphology of tadpoles is by the few larval characters which her- dominated by tissue related to feeding petologists have traditionally considered functions, especially ingestion, and it to have taxonomic value. With considera- seems reasonable to assume that a tad- tion of few characters, the chance of pole's oral morphology will demonstrate convergence is obviously high and con- adaptation to the environment in which fidence in derived systematic relation- a larva lives. If we understand the adap- ships is low. Until recently, most work tive significance of morphological fea- concerning the higher relationships of tures, we should be able to determine anurans has involved only a few tadpole much about the ecology of the tadpole from its external characters. Starrett ( 1968, oral morphology. An ultimate 1973) and Sokol (1975, 1977a, 1977b) goal of this comparative study is to un- have now made much progress toward derstand the morphology of anuran establishing the importance of tadpoles larvae in enough detail to be able to to anuran systematics. Although they accurately predict a tadpole's ecology have identified many new internal larval from its morphology. features of value to systematic discus- Although this study is limited to sur- sions, the larger controversy, unfortu- face features, some reference is made to nately, has not been resolved. Starrett underlying, cartilaginous elements such and Sokol disagree on how to interpret as the ceratohyal, which forms the pis- relationships implied by many larval ton of the tadpole buccal pump, and the features. spicule, which supports part of the oral The present study began as a search surfaces. A comparative study of the for additional diagnostic characters to cartilaginous skeleton of the tadpole help clarify systematic problems in the buccal pump is presented elsewhere Anura (Wassersug, 1976a). It has ex- (Wassersug and Holf, 1979). panded into a more general, comparative Only free-living larvae are consid- study of the functional morphology and ered. An ontogenetic series of one spe- feeding ecology of anuran larvae. An cies, Hyla regilla, was examined in detail effort is made here not only to identify in a previous study so that morpho- MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY logical features modified extensively R. Demmer, W. R. Heyer, R. W. Mc- through development could be elimi- Diarmid and C. Richards. nated from further consideration (Was- For logistical support I thank the Di- sersug, 1976b). It was necessary to do rectors and Department Heads of the this because not all material available Committee on Evolutionary Biology and for study is of the same developmental the Department of Anatomy of the Uni- stage. versity of Chicago; the Center for Grad- uate Studies and the Division of Rep- The core of this paper is descriptions tiles, Field of Natural His- of oral structures in the larvae of se- Museum tory, Chicago, and The Museum of lected anuran species. This is followed Natural History at the University of by a four part Discussion. Kansas. The first part of the Discussion Financial support was provided by a (Functional Considerations) reviews the fellowship from the Center for Graduate diversity of the structures, and an effort Studies, Field Museum of Natural His- is made here to correlate known larval tory; Block Fund and Hinds Fund, Uni- ecology with patterns in oral morphol- versity of Chicago; and the National ogy. Functions for many of the oral Science Foundation (BMS 75-03447 and structures presented in the Descriptions DEB 76-19275). are deduced on the basis of what is I am extremely grateful to Marsha known about larval ecology. The sec- Greaves, who executed drawings for ond part of the Discussion (Systematic this paper. Use Hecht graciously pro- Considerations) examines specific sys- vided translations of several articles in tematic questions. The third part (Evo- foreign languages. Shirley Aumiller and lutionary Considerations) deals with Robert Kott helped with photography, questions of evolutionary history as well portions of the manuscript were typed as the evolutionary mechanisms that by Debra Randall and Karen Rosenberg. could account for diversity among tad- Special thanks are due Nancy Bradney, poles. The last part of the Discussion who helped in many aspects of produc- ( Ecological Considerations ) reverses the tion and editing. Steve Busack, William first part. Here, starting from a basic Duellman, Robert Inger, Dianne Scale, understanding of the morphology, an Otto Sokol, Linda Trueb and David attempt is made to assess the ecology of Wake have read various portions of this tadpoles and correlate ecological pat- manuscript; it has profited greatly from terns with known morphological pat- their constructive criticisms. terns.

ACKNOWLEDGMENTS MATERIALS Oral structures of larvae of 31 species This paper augments work presented from eight families are described. The in a doctoral thesis submitted to the tadpoles came from museum collections University of Chicago in 1973. I want or the author's private collection. An to thank the members of my committee, effort was made to examine specimens James Hopson, Robert Inger, George at or near Gosner ( 1960 ) stage 36. Rabb, David Wake and Rainer Zangerl, A few species (e.g. Acris crepitans) for their encouragement, advice, and were chosen for study because they have most of all, their patience. the commonest type of anuran larvae I am grateful to William Duellman, (i.e., denticle pattern 2/3; inhabitants of Hymen Marx and David Wake for al- small ponds and pools) and serve as lowing me to dissect specimens in their reference forms for comparison with tad- care. Additional specimens were gener- poles of more exotic morphologies and ously provided by E. Crespo, M. Delsol, ecologies. All other species were selected — —

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES either because they came from famiHes loosely grouped by common features whose larvae have been associated with either of external morphology or ecol- interesting taxonomic problems or be- ogy (references for most of these com- cause they present unusual larval ecolo- ments are given in the descriptions). gies. Particular emphasis was placed on the frogs assigned to the superorder Ar- Benthic Larvae with Enlarged chaeobatrachia by Duellman (1975); Suctorial Mouths thus Ascaphus ( Ascaphidae , Alytes, ) ASCAPHIDAE. Bombina, Discoglossus (Discoglossidae), Ascaphus truei: adhere to rocks in streams; well for Rhinophrynus ( known Rhinophrynidae ) , and their large suctorial oral disc several pelobatid larvae are described. and adaptation to torrential habitats. Since the Microhylidae is a family of PELOPATIDAE. particularly problematic relationships, — Leptobrachium hasselti: inhabit quiet, clear regions several Microhyla larvae are also de- of scribed. streams, where they graze on algae growing on rocks. In terms of body Hylidae larvae were selected because shape or tail length, L. hasselti larvae of their great ecological diversity (see are little specialized for stream life, and Duellman, 1970) while one member of are among the more generalized mego- the Centrolenidae and two species of phrynine tadpoles. Leptobrachium osha- Dendrobatidae are described solely be- nensis: more specialized to stream life cause of their unusual larval ecology. than L. hasselti (Liu, 1950:191-201) Certain families are not treated here since larvae have very long, strong tails because species from these families have and are good swimmers in running wa- been described or illustrated elsewhere: ter; they stay on the bottom in shallow for example Pipidae (Sokol, 1975, 1977a water and have an expanded oral disc, and other references cited therein); Ran- with a large denticle-free area.^ Oreo- idae [Rana agilis ( Kratochwill, 1933), lalax pingii: similar to Leptobrachium Rana temporaria (Savage, 1952; De- larvae in general appearance; described Jongh, Rana 1968), catesheiana (Grad- as "bottom feeders" (Liu, 1950). Their well, 1970, 1972a), Rana fuscigula morphology suggests that they are inter- (Gradwell, 1972c)], and the Pseudidae mediate in their tolerance for currents {Pseudis paradoxa larvae illustrated by between L. hasselti and L. oshanensis. W. Parker, 1881). One bufonid, Bufo HYLIDAE. Hyla mixe: among the bufo, has been partially described and most highly specialized larvae for stream illustrated by Savage, 1952. The avail- life; have very large oral disc used for ability of specimens set some constraint adhering to rocks in strong currents. on the families that could be studied; Ptychohyla leonhardschultzei: inhabit several major families with tropical dis- small, quiet, peripheral pools in moun- tributions (e.g., Leptodactylidae and tain streams. Smilisca sordida: inhabit Hyperolidae) are left for future work. streams, but only in regions of very Knowledge of the habitats and feed- gentle current; externally, they show ing ecology of the larvae studied here few of the modifications characteristic of is summarized below. The species are stream tadpoles.

^ Liu (1950:200) questioned the common interpretation (after Smith, 1926) that the mouth serves an adhesive function. He watched an L. oshanensis larva in his laboratory and noticed that when it rested on the bottom, only the tips of the marginal papillae touched the substrate. Water flowed into the mouth through the notch at the front and the back of the disc. Liu then concluded that the oral disc served the function of raising the head off the bottom to allow for respiration. His observations, however, remain inconclusive for the natural situation, because he described the action of the disc only in tadpoles confined to quiet water. The disc may still have an adhesive function in currents, not only for this species, but for all other species with enlarged oral discs. — — —

MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Funnel-mouthed Tadpoles bromeliads; macrophagous (according to Orton, 1944) but lack the large mouth MICROHYLIDAE.—Micro/iy/a heij- of Anotheca spinosa and presumably are monsi: inhabit quiet pools and feed on more dietary generalists, feeding on particles at the air-water interface; have small fragments of animal and plant rapidly vibrating, filamentous tail tip matter that collect in their arboreal remain seemingly motionless at and can pond. the surface film for long periods of time. PELOBATIDAE.—Megop/irt/s mi- Midwater Macrophagous Larvae nor: epitomize the surface film-feeding MICROHYLIDAE.—Micro/i|/Za berd- way of life; have a huge, upwardly di- morei: dispersed throughout the water rected, denticle-free oral disc;- occur in column in quiet pools; lack keratinized slow, flowing water and are, consequent- mouth parts and are obligate feeders on ly, equipped with a long, powerful tail fine, suspended matter. Microhyla or- which allows them to resist displacement downstream. nata: found suspended throughout the water column; presumably similar HYLIDAE. Ptychohyla schmidto- in their feeding habits to M. herdmorei. rum: moderately specialized for stream HYLIDAE. Agalychnis callidryas: existence; found in the quieter reaches by rapidly vibrating the pointed tips of of mountain pools; have expanded oral their tails these larvae can hang sus- discs with a large denticle-free area. pended in midwater in ponds; retain the DENDROBATIDAE. — Colostethus typical hylid 2/3 denticle pattern and nuhicola: In aquaria they swim beneath can facultatively graze on substrates be- the surface film (Savage, 1968). They sides feeding on microscopic particles have a large, anterior-directed oral disc midwater (see pers. comm. by McDiar- with surface papillae which, according mid in Heyer, 1976:22). to Savage, aid in sorting particles from the water. Found under vegetation and Temporary Pool Dwellers, Omnivores rocks in side pools and rivulets of small streams; found in pools sufiiciently small RHINOPHRYNIDAE. — Rhinophry- so as to be occupied rarely by fish. nus dorsalis: larvae lack keratinized mouth parts for biting or scraping, but "F0SSORM.L" Stream Forms are omnivores able to cannibalize smaller individuals and also efficient suspen- CENTROLENIDAE.—Cenfro/ene//a sion feeders of ultraplanktonic particles. fleischmanni: extremely elongated larvae PELOBATIDAE.—Scap/iiopws bom- lack suctorial which the mouth or fun- bifrons: active tadpole found in tempo- nel of other stream forms; found in rary pools and known for rapid develop- cracks and crevices amongst the rocks ment and voracious feeding habits. Al- and vegetation in shallow streams. though carnivorous and cannibalistic, HYLIDAE, Arboreal Larvae. Ano- best considered omnivores; an oral disc theca spinosa: live in the shallow water of moderate size surrounding large and that collects in tree holes; known carni- powerful beak; members of genus are vores with large beaks; specialized for efficient suspension feeders (Richmond, feeding on mosquito larvae, other ar- 1947). thropods, and frogs' eggs. Hyla dendro- Additional Pond Larvae scarta: extremely elongated tadpoles which live burrowed in the leaf axils of DISCOGLOSSIDAE.—A/y^es obste-

^ According to Liu (1950:191) the disc folds shut when the tadpole is below the surface, but opens to form a funnel at the surface film when the tadpoles are feeding. The funnel may function in both feeding and respiration as a surface float; literature on the subject has been reviewed by Noble (1927) and Liu (1950). —

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES tricans: typical for quiet water tadpoles small, rocky ponds; details of feeding in general appearance and behavior; able ecology unknown. to stay in midwater by gulping air inter- mittently, but feed on vegetation at or METHODS near the bottom. Alijtes cisternasii: pre- All tadpoles examined were meas- sumably similar to A. obstetricans. Bom- ured from snout to vent and staged ac- bina orientalis: occur in assorted ponds cording to Gosner, 1960. For each tad- or pools, often adjacent to streams; can pole the floor and the roof of the mouth be found in puddles lacking macroscopic were exposed following a simple dissec- vegetation; can be carnivorous. Perhaps tion procedure described by Wassersug appropriately viewed as omnivores with (1976a). Tadpoles were pinned under generalized external structures, capable water in a small tray of darkly stained of camivory and suspension-feeding on paraffin and examined with a dissecting microscopic particles. Discoglossus pic- microscope. The larvae were lightly tus: generalized pond larvae, presum- stained with either methyl blue or crys- ably similar to Alytes and Bombina. tal violet to accentuate surface features, HYLIDAE. Gastrotheca riobambae: specifically mucous-secreting epithelia. inhabit shallow, high elevation pools and Ventral and dorsal surfaces were pho- exhibit no unusual behavior for anuran tographed on 4" X 5" format through a larvae. Hyla femoralis: midwater forms bellows-view camera using a 32 mm that live amongst vegetation in pools; lens; a few photographs were taken with have exceptionally high tail fin with 16 or 64 mm lenses. Tadpoles were usu- terminal filament, but otherwise "typi- ally pinned to the paraffin at the tail cal" in their external morphology and only; care was taken not to distort or feeding habits. Hyla rufitela: live in stretch oral surfaces. Camera lucida small pools, often overgrown with mac- drawings were also made of many of rophytes; have an unusual 2/4 denticle the specimens, particularly the smaller pattern but not known to have unusual ones. Either camera lucida drawings or feeding ecology. Hyla ebraccata and photographs accompany the descriptions Hyla sarayacuensis: hide among the for most species; some descriptions have aquatic plants of the shallow parts of both for purposes of comparison. One ponds, where the adults of the species species is described without photograph breed; larvae characterized by a reduc- or illustration because it is nearly identi- tion of the oral disc and the loss of den- cal to related forms that are illustrated. ticle rows as compared with typical All illustiations in this descriptive pond hylids; members of species group section present the buccal floor and buc- feed on submerged leaves or other de- cal roof as a single plate with the floor bris (Starrett, 1973). Hyla phlebodes: above and roof below; for drawings, dor- found among vegetation in shallower sal and ventral surfaces are magnified parts of pools; have small mouth without equally and a single scale line ( =1 mm) oral disc and denticle rows; members of is given. For the photographs, a single species group feed on the bottom (Star- scale line is given if both halves of the rett, 1973). Acris crepitans: typical gen- plate are magnified equally; otherwise eralist tadpole of small ponds and pools two separate scale lines are used. throughout much of eastern United Just as there are optical limits on States. Colostethus nubicola: inhabits photographical qualities,^ there are hu-

^An effort was made to obtain scanning electron (SEM) photomicrographs of several small specimens because of the potential resolution and depth of field provided by this technique. SEM, however, had to be abandoned because it required pre-coating the specimens with a uniform, con- ductive metallic layer and the convoluted, intricate structure of the gill filters made such preparation impossible. MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY man limits on how accurately certain here that no consistent pattern of left or ventral, pharyngeal features—specifical- right handedness was found, either in- ly, the gill filters—can be drawn. The traspecifically (for Hyla regilla; Wasser- gill filters in many of the drawings are sug, 1976b) or interspecifically. slightly stylized; minor discrepancies be- Because of the complex, qualitative tween the descriptions and the drawings nature of many of the features described, remain. I chose not to use a telegraphic form for Species descriptions are grouped by the descriptive body of the study. Hyla family. Each description is provided regilla, illustrated and described in de- reference or references that per- with a tail in Wassersug ( 1976b ) , is treated as tain(s) to the species morphology, ecol- the "typical" pond tadpole and consid- ogy, or both. The morphological descrip- ered a reference for comparison with tions follow Wassersug (1976a). Mer- the other forms. istic features are presented for both the Figures 1 and 2 show nearly all right sides of the buccal roof left and structures presented in the species de- floor; discrepancies between one and scriptions. All morphological structures side the other, are noted. These and described are briefly defined in the were originally collected to data, which Glossary. Terminology follows Wasser- determine whether asymmetries in ex- sug (1976a). ternal aspects of the respiratory system Two sources are followed for anuran (i.e., position of the spiracle) were re- systematics. I follow Orton (1957) in flected internally, give some indication of the amount of variation in any species. recognizing four larval types. Type 1 Meristic data from the pharynx are all includes the Pipidae and the Rhinophry- taken from the left side. It can be noted nidae; Type 2 consists of the Micro-

Lower Beak

Lingual Papillae

Infralabial Papilla

Buccal Floor Arena Buccal Floor Arena Prepocket Papillae Papillae

Buccal Pocket

Filter

Cavities r, n, ID

Glottis

Fig. 1.—The floor of the mouth in a Hyla femoralis larva. Most morphological features discussed in the text are labelled in this Figure and Fig. 2. The scale line equals 1 mm. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES

Denticle Rows

Upper Beak

Prenarial Arena l—%g^

Prenarial Papillae Narial Valve Postnarial A Projection

Postnarial Papillae

Lateral Ridge Buccal Roof Papilla Arena Lateral Roof Papillae

Lateral Pressure Cushion

Dorsal Velum Medial Pressure Cushion

Esophagus Esophageal Funnel

Fig. 2.—The roof of the mouth in a Hyla femoralis larva. Most of the morphological features discussed in the text are labelled in this Figure or the previous one. The scale line equals 1 mm. hylidae only; Type 3 includes the As- taxonomy of the Anura and recognize caphidae and Discoglossidae; and Type two broad groups of frogs, the archaic

4 includes all the remaining families, ( Archaaeobatrachia ) and advanced Starrett (1973) has given formal names (Neobatrachia) forms. Which families to these groups. As I am not convinced belong to which group is highly contro- that this series represents a phylogenetic versial (cf. Sokol, 1977b) and I deal sequence, I am reluctant to follow Star- with this question to some extent in the rett's names. Unless otherwise noted I discussion sections on systematics and follow Duellman (1975) for the basic evolution.

DESCRIPTIONS

ASCAPHIDAE based on a typical individual with a Ascaphus truei Stejneger 3/11 denticle pattern, of which two upper and three lower rows were multiple. (Fig. 3) Ventral buccal.—The floor of the oral Material—FUNK 166497 (stage 37, cavity is slightly expanded anterolater- sv. 18.0 mm). Bird Tributary to St. Joe ally; bilateral infralabial papillae are River, Shoshone Co., Idaho, U.S.A.; July absent. Immediately inside the mouth 22, 1965. is a single flap-like fold of skin identi- Reference.—Stehhins, 1951 (p. 192). fiable as a posteriorly-directed, bilobed, External.—Ascaphus truei larvae oral valve, the free edge of which sup- have a large suctorial oral disc, and a ports nine very small evenly spaced pa- medial spiracle. This description is pillae. The tongue, a transversely elon- MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 3.—Photographs of the floor (above) and roof (below) of the mouth in an Ascaphus truei larva. The scale Hne in this Figure and all that follov^' equals 1 mm. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES gate dome, is covered with a dense field few. Neighboring filter rows do not of several dozen, straight, blunt papillae. abut, so filter canals are large, open The majority of these lingual papillae channels, almost as wide as the filter are tall and subequal in size, but the row. The branchial food traps are small anterior ones are smaller and thinner but well demarcated ventrally, where a than the rest. The BFA papillae are sharp rim separates them from the filter organized in a broad, V-shaped row that tissue. Secretory ridges could not be begins anterolaterally as prepocket pa- resolved and must be extremely fine or pillae. The BFA papillae are eight per absent. The glottis is a tiny, unper- side, simple, straight and of modest forated slit under the velar margin. size. They become progressively smaller Glottal lips and a conspicuous laryn- posteromedially. Pustulations and pa- geal disc are absent. The esophageal pillae of any sort are absent from the funnel has a narrow dorsal profile. of the floor. remainder buccal Buccal Dorsal buccal.—The buccal roof is pockets are long and shallow and un- dwarfed in comparison to the huge up- perforated. The free velar surface is per beak, and much narrowed anteriorly. comparatively short. Its posterior mar- The roof is transversely arched and has gin is shaped like a very broad "V" with considerable depth compared to other a curved apex and it lacks posterior species. The oral opening is small and projections or a median notch. The velar positioned so far posterior that the pre- margin forms a rim twice as thick as narial arena is also "preoral." The arena the free velar surface in front of it. The is a slim, blind tunnel above the upper margin is curved upward; directed dor- beak. It is devoid of papillae or pustu- sad rather than caudad. It is stiff, but lations. The internal nares are oblique, no spicule support is evident; its rigid- nearly longitudinally oriented slits and ity results in part from the complete are on the lateral walls rather than on anchoring of the ventral velum to the the roof of the buccal cavity. The an- dorsal margin of the filter plate on cb. 2. terior narial walls make an anterolateral In fact, the velar surface extends pos- loop that bounds small, oval, oblique teriorly in thin, tapered bands for half pits on each side. The walls surround- the length of these filter plates. Well- ing these pits are thick and pustulate. formed secretory pits could not be re- The remainder of the anterior walls are solved, however, the velar margin is shallow and lack papillae. The posterior covered densely with extremely small, narial walls are tall and slightly pustu- fine, irregular pittings. The anterior lim- late, but lack narial valve projections. its of this unusual mucosa could not be All major landmarks of the buccal roof determined. proper, such as the median ridge and Ventral pharynx.—The pharynx in papillae that could outline the post- Ascaphus truei is overall proportionally narial and buccal roof arenas, are ab- as large as in typical pond tadpoles, but sent. There are approximately ten small, the filter plates are rotated outward so simple, blunt papillae scattered about that cb. 2 is more transversely oriented the buccal roof behind the nares; these and filter cavity 3 is reduced in volume show some tendency to be concentrated on each side. Filter plates of cb. 2 are in the posterolateral corners of the buc- straight while those of cb. 3 are strongly cal roof. The buccal roof sinks, then bowed, obscuring much of filter cavity rises again just anterior to the dorsal 3 from dorsal view. Counts for number velum, and forms a major, posteriorly

of filter rows on cb. 1-4 are 9, 11, 10, 6 directed V-shaped depression. The an- respectively. The filter mesh of A. truei terior surface of this depression is lined

is much reduced. Secondary filter folds with a few blunt, well-spaced pustula- are short; tertiary folds are short and tions. The glandular zone begins at the 10 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY lowest point of this depression. The the inner upper and two inner lower multiple. spiracle is medial. zone is of uniform anterior-posterior rows The length except directly in front of the Ventral buccal.—The floor of the oral esophagus, where it is much abbreviated. cavity is relatively wide anteriorly and The zone is made up of irregularly rounded rather than pointed. The buc- spaced, minuscule secretory pits that are cal floor is flat but slopes forward so extremely dense. The dorsal velum is that the frontal plane of the mouth short and thick with a smooth ventral meets the frontal plane of the trunk at margin. It is continuous across the mid- an angle; these planes are more nearly line, but its full extent in that region parallel in most tadpoles. Infralabial cannot be determined because of dam- papillae are tall, narrow and have a fine age in dissection. serrated margin rather than secondary Dorsal pharynx.—The two pairs of papillae. The transversely elongate pressure cushions in A. truei are of typi- tongue anlage lacks lingual papillae but cal size and dimension. They are, how- is covered fully by a dense field of stout, ever, covered with a few faint, scattered blunt pustulations. The buccal floor pustulations along with a dense secre- arena is surrounded by eight BFA pa- tory epithelium. The ciliary groove is pillae on one side and ten on the other. broad and shallow. These BFA papillae are less numerous in front of the buccal pockets, more nu- Diagnostic summary.—The oral cav- merous posteriorly and slightly more ity of Ascaphus truei differs from that attenuate and acutely pointed when of all other tadpoles examined in the compared to those of typical pond tad- following, unique characters: presence poles. A couple of the largest papillae of oral valve instead of paired infra- are laterally compressed and have ter- labial papillae; many papillae covering bifurcations. There are two dis- tongue anlage; prenarial arena reduced minal tinct conical prepocket papillae on each to short, blind tunnel; sensory pits an- extremely tiny, pointed pa- terolaterally on the internal nares; large side. Some to V-shaped depression extending across pillae are clustered directly anterior 2 the buccal floor, and there is a posterior buccal roof. A combination of cb. on single small papilla above the lateral the following features further differen- of the ceratohyal on each side in tiates the oral cavity of Ascaphus larvae arm this specimen. Dozens of tiny, precise from all other tadpoles: ventral velum pustulations cover the buccal floor, with fully attached to dorsal margin of filter their greatest concentration anterolateral plates; secretory tissue without pitted or posteromedial. Each buccal pocket ridged pattern; unperforated glottis; ab- and has a large transverse pouch with a sence of prenarial, postnarial and buc- fold rising off its posterior wall cal roof arenas. heavy obscuring its floor. No open slit could DISCOGLOSSIDAE be found within the pockets. The free velar surface is reduced. Spicular sup- Alytes obstetricans Laurenti port is lacking except for a tiny spur of (Figs. 4, 5) cartilage at the points where the dorsal Material.—U ncatalogued, author's edge of the filter plates on cb. 3 meet collection (stage 36, sv. 18.5 mm). Col- the velum. The velar margin is fully lected at "La barlieu," 30 km SE of fused to the top of the filter plates on Lyon, Rhone, France; no date. cb. 2 and fused almost to its edge above References.—Eibl-Eibesfeldt, 1953; cb. 3. The velum edge is curved up- Magnin, 1959. ward above cb. 2. The velar margin is External.—Alytes obstetricans tad- CDncave posteriorly between filter plates poles have a 2/3 denticle pattern with and when viewed from above appears ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 11

ft/y^"i-JU>uu.u,

Fig. 4.—Drawings of the floor (above) and roof (below) of the mouth in an Alytes obstetricans larva. 12 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY as a series of crescents rather than a flection of the upper labial cartilage and continuous posteriorly convex arc. Pro- beak. The prenarial arena is devoid of jections of the velar margin are dis- any papillae, pustulations, ridges or placed medially and are pointed rather other projections. The internal nares of than curved. The projections associated A. obstetricans are elongate, obliquely with the third filter cavity and the me- oriented slits. Their anterior walls each dial notch are long, finger-like papillae. have a low, tiny, anteriorly-directed flap Secretory pits are restricted to the pos- at their most anteromedial corners. Nor- terior projections of the velar margin. mal prenarial papillae are absent, how- The pits are small and of low density. ever; the anterior narial walls abruptly Ventral pharynx.—The branchial bas- expand into huge flaps that extend back kets of A. obstetricans are round, long, the length of the nares. These flaps curl wide and deep. The first and second posteromedially under the narial openings. filter cavities are disproportionately The tall, anteromedial edges of large compared to the third. The dorsal these flaps are serrated. The coiled, posterior margins of the filter plates of cb. 3 arch margins of the flaps have a few upward and blanket much of the third small, pointed, irregular secondary pa- filter cavity. Although the filter plates pillae on each side. The posterior narial are relatively long in A. obstetricans, walls have valves but lack any narial the number of filter rows and density of valve projections. Eight small, pointed the filter mesh is low. Counts for filter cones of subequal size make up the post- rows are 6, 9, 8, 5, for cb. 1-4. The filter narial papillae series. These papillae are mesh is comparatively reduced because clustered in a rather transverse patch in the rows are narrow, and secondary the middle of the postnarial arena. The and tertiary filter folds, while present, median ridge is an anteriorly directed, are very thin. The filter canals are triangular flap. The anterior surface of large, nearly fully open channels. The the median ridge is smooth but two tiny short, flexible surface of the velum is cusps line the lateral margins of the covered ventrally by small, scattered se- ridge on each side. Separate lateral ridge cretory pits rather than by secretory papillae are absent. The BRA is an ridges. These pits grade into weak elongate oval defined by approximately "ridges" farther forward under the im- six, well-spaced papillae on one side and mobile portion of the velum. The five on the other in this specimen. The "ridges," however, are not well-formed BRA papillae are all small, pointed and have a rather streaked appearance. cones of subequal size. In addition to The area covered by the secretory tissue the main rows of papillae, there are two is rather small and sharply separated single papillae lateral to the arena on from the filter epithelium by a rim each side and an arc of tiny conical around the food traps in each filter cav- papillae at the posterolateral margins ity. The glottis is 90% visible from above. of the buccal roof. Randomly dispersed It is long with large thick lips. The within the BRA are 50-60 tiny pustula- laryngeal disc, however, is not exceptions. Pustulations are absent outside of tionally large. The esophageal funnel is the arena. The glandular zone is nor- large and broad in dorsal profile. mal. The dorsal velum is short and not tightly coiled. It is completely and Dorsal buccal.—The buccal roof is broad anteriorly and has a "V" shaped broadly interrupted medially and its me- posterior pharyngeal margin. The pre- dial edges are papillate on each side. narial arena is as large as that of the Dorsal pharynx.—Although two typical pond hylids examined, but ap- broad, shallow waves of the velar sur- pears shorter in photographs because it face are faintly visible in this specimen, is partially obscured by a posterior re- pressure cushions are essentially absent. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 13

Fig. 5.—Photographs of the floor (above) and roof (below) of the moutli in an Alytes obstetricans larva. HISTORY 14 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL

generally fewer denticles than The ciliary groove is similar to or slight- sleeve and larvae. The specimen de- ly broader than that of a typical pond A. obstetricans denticle larvae. scribed here had a 2/3 pattern with all rows multiple. Diagnostic summary.—Tadpoles of the family Discoglossidae can be dis- Ventral buccal.— (Unless otherwise tinguished from those of all other fami- noted A. cisternasii is identical to A. A. cisternasii has several lies by the presence of large Haps of the obstetricans). anterior narial walls which curl posteri- pustulations inside the oral orifice an- orly under the nares and their V-shaped terior to the infralabial papillae. Among posterior pharyngeal margin. All dis- the pustulations on the tongue anlage, coglossid tadpoles have the posterior, two near the midline are particularly ventral velar margin ankylosed to the enlarged and, as such, resemble in shape dorsal margins of the filter plates and and position the typical paired lingual appear to lack well organized secretory papillae of most anuran larvae. Buccal ridges in the branchial food traps. In- floor arena papillae are taller and more ternally Alijtes tadpoles differ from other numerous in this species. I count nine discoglossid larvae in the presence of major papillae on one side, twelve on four long projections of the ventral vel- the other with an equal number of um near the midline and pustulations minor papillae as well as many small covering the tongue anlage. Compared pointed pustulations in the posterior to A. cisternasii, A. obstetricans tadpoles part of the arena and interspersed among lack paired lingual papillae, but have the papillae forming the margins of the an oval-shaped buccal floor arena, short- arena. There are several small conical er, fewer BFA papillae and slightly papillae in front of the pockets on each denser gill filters. A. cisternasii larvae side. Papillae posterior to the BFA are tend to have more papillate and crenu- lacking. There appears to be less spicu- lated structures than the larvae of A. lar support than in A. obstetricans. Sin- obstetricans; this can be seen in the in- gle secretory pits could not be discerned fralabial papillae, the narial flaps and even at 100 X- the median ridge. A. obstetricans, how- Ventral Pharynx.—The branchial bas- ever, is the only discoglossid examined kets are slightly more triangular in dor- with papillation of the median edge of sal view than those of A. obstetricans the dorsal velum. and perhaps a bit smaller in comparison to the size of the buccal cavity overall. Alijtes cisternasii Bosca Counts for filter rows run 9, 10, 8, and (Fig. 6) 5 for cb. 1-4 respectively, which means Material.—Author's collection (stage that for individuals of comparable size and stage A. cisternasii has slightly more 34; sv. 15.5 mm ) . Collected in a perma- nently swampy area, in the province of filters rows than A. obstetricans. In con- Alto Alentejo, Portugal; no date. trast, filter mesh appears slightly denser Reference.—Boulenger, 1891. than in A. obstetricans but this differ- External.—Alytes cisternasii have ence may be due to preservation. The large robust larvae which in terms of filter canals are necessarily less open in of size, shape and denticle pattern are vir- this specimen than in the specimen tually identical to A. obstetricans. The A. obstetricans described above. No secretory ridges evident in the spiracle is medial. Boulenger (1891) were could detect no characters that distin- branchial food traps. The glottis is less guish the larvae of these two species but than 50% visible from above. The glottal Crespo (pers. comm.) finds that in Por- lips are not as thick as in A. obstetricans. tugal A. cisternasii larvae have a larger Dorsal buccal.—The flaps at the an- spiracle with a shorter, free terminal teromedial corners of internal nares in ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 15

of Alytes cisternasii larva. Fig. 6. Drawings of the floor (above) and roof (below) of the mouth an HISTORY 16 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL

papillae degenerate A. obstetricans are present in this species line. Posteriorly, the but much reduced. The large postero- into a jagged fringe. The free edges of medially directed flaps that arise from the infralabial papillae are lined with papillae, the anterior margin of the narial walls short, attenuate, secondary have a more distinctly papillate margin eight on each side in this specimen. The lingual papilla, situated in this species compared with A. obstet- single, median posteriorly ricans. There are nine pointed cones far anterior, is anteriorly to within the postnarial arena. The median flattened and slightly concave posterad. small, ridge in this species has a more crenu- It has a deep median notch and subpapillate projec- late border than in A. obstetricans. The secondary, terminal tions. Posterolaterally on each side of BRA is defined by approximately seven papillae on one side and five on the the tongue anlage are single, large, coni- other in this specimen. The BRA papil- cal pustulations. The papillae of the lae are more attenuate overall. The me- BFA are much reduced in size and dial edges of the dorsal velum lack aligned in a "V" with the arms of the papillae but are pustulate in this speci- "V" forward. Anteriorly each arm turns men. Most other differences illustrated laterally so the BFA papillae series is in Figs. 4 and 6 reflect differences in discontinuous with the prepocket papillate section. series. I counted six BFA papillae on Dorsal pharynx.—As in A. obstetri- one side and seven on the other, with cans. an additional three papillae on each side Diagnostic summary.—See Alytes ob- in the prepocket papillae position. The prepocket papillae and the largest BFA stetricans (p. 14). papilla on each side have fine secondary, Bombina orientalis Boulenger pointed, terminal papillae. Other papil- (Fig. 7) lae in the BFA row are simple, small, laterally compressed cones that grade Material.—Uncatalogued, author's down to pustulations. There are a few collection (stage 34, sv. 14.1 mm). Lab- tiny pustulations near the prepocket pa- oratory raised population, Amphibian pillae, but the remainder of the buccal Facility, University of Michigan, Ann floor is smooth and free of any additional Arbor, Michigan. Initial stock from Ko- papillae or pustulations. The buccal rea with no additional data. pockets are unperforated and have the Reference. Okada, 1931. — same orientation and length to width External.—Bombina orientalis larvae ratio as in A. obstetricans. They are, have denticle pattern with the in- a 2/3 however, shallower. The short, free velar ner rows double. The spiracle is medial, surface lacks spicular support but is characteristic of discoglossid tadpoles. quite inflexible due, in part, to the fact Ventral buccal. floor of the —The that it is fused almost to its margin at mouth of B. orientalis is proportionally the top of the filter plate of cb. 2. The longer that of A. obstetricans with than velar margin is posteriorly concave be- in the increase solely in the pharynx. As tween filter plates, giving the free velar A. obstetricans, the floor tips anteriorly surfaces the appearance of a series of the frontal of the downward from plane crescents as in A. obstetricans. These trunk. The mouth is anteriorly narrower projections are directly above the filter than in A. obstetricans. A single, strong- plates. The median portion of the velum ly compressed, dorsally projecting in- forms a discreet series of waves and fralabial papilla is situated on each side lacks large median notch. The edge of in the typical position. These are not as a to form a thick- tall as in A. obstetricans. Anteriorly, the the velum is curled up papillae grade into a series of pustula- ened rim continuous from one side to the tions that are continuous across the mid- other similar to, but not as large as, the ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 17

of the mouth of a Bambina orientdis lar\'a. Fig. 7.—Drawings of the floor (above) and roof (below) 18 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY raised velar margin in Ascaphus truei. talis the pharynx is longer and narrow- The rim has the buffed texture charac- er such that the roof of the mouth is typi- teristic of secretory tissue but distinct more diamond-shaped rather than secretory pits could not be resolved. cally triangular in ventral profile. The prenarial arena is like that of A. obstet- Ventral pharynx.—The branchial bas- ricans, except that B. orientalis lacks the kets are slightly taller and longer than dorsal reflection of the beaks. The in- those of A. obstetricans and much taller ternal nares are so similar in A. obstetri- and longer than those of typical pond cans and B. orientalis, that only differ- tadpoles. They are tallest posterolater- ences are presented here. In place of ally, where they extend well above the the anteriorly directed flaps of the an- plane of the floor of the mouth. Com- terior walls are a cluster of minuscule pared with A. obstetricans, the third fil- attenuate papillae on each side in B. ter cavities of B. orientalis show further orientalis. The huge flaps of the anterior reduction in volume at the expense of narial walls are larger in B. orientalis larger second filter cavities. The filter than in A. obstetricans, but are more plates, particularly those of cb. 3, are uniform in width. They extend postero- imbricated to a great extent in B. ori- medially over a greater portion of the entalis. Counts for numbers of filter postnarial arena. Two small, conical pa- rows run 8-9, 11, 10, 6 for cb. 1-4. The pillae with fine apical irregularities are filter mesh is similar to that of A. ob- present in the small postnarial arena in stetricans. Filter rows are unusual in a transverse line just anterior to the being very uniform in thickness and median ridge. The median ridge is iden- little expanded ventrally. The main fold tical to that of A. obstetricans, except is very straight and second folds are that fine secondary cusps are clustered single, short crossbars on the main fold. on its ventral corner rather than along Filter rows do not abut and the filter the lateral margins. Lateral ridge papil- canals are large, open channels. Branch- lae and BRA papillae are absent. Ran- ial food traps are extremely short and domly dispersed about the buccal roof separated from the filter surfaces ven- between the median ridge and the glan- trally by a large, distinct rim. Secretory dular zone are a haff tiny, pointed ridges could not be resolved anywhere dozen papillae and an equal number of faint in the food traps even at 75X- They are presumably absent; nevertheless, the pustulations in this specimen. The glandular is of similar proportions to food traps are covered with a buff-tex- zone that of A. obstetricans but the anterior tured tissue that has the superficial char- margin is V-shaped, paralleling the back acteristics of a glandular mucosa. The of the pharynx. Well-defined secretory glottis of B. orientalis is larger than that pits are visible only at the anterior mar- of typical pond tadpoles, but smaller gin of the zone. dorsal is than that of A. obstetricans. The glottal The velum slightly A. obstetri- lips are thickest in B. orientalis. The longer than that of cans, but still shorter than that of pond laryngeal disc is present, but not very distinctive. Fifty percent of the glottis hylids, at least laterally. The velum is broadly interrupted medially and has is obscured from dorsal view by the margin of the velum. The esophageal funnel smooth medial margins reflected poste- has a narrow profile. The bore of the riorly. esophageal funnel, however, is large in Dorsal pharynx.—The pressure cush- B. orientalis and comparable to that of ions are normal in terms of general size A. obstetricans. and depth, though the medial pressure Dorsal buccal.—B. orientalis shares cushions are slightly narrower. The cil-

with A. obstetricans the V-shaped poste- iary groove is similar to, but even broad- rior margin of the pharynx. In B. orien- er than that of A. obstetricans. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 19

Diagnostic summary.—The following side in a row from the lateral edge of set of oral characters readily distin- the tongue anlage to the medial edge of guishes Bombina orientalis larvae from the buccal pockets. There are no pustu- all other discoglossid tadpoles studied: lations within the BFA and only a few single, medial bifurcated, lingual papil- very tiny pustulations on the buccal lae; buccal roof arena absent; secretory floor anterior to the pockets. Prepocket pits present only at the anterior margin papillae are absent. Buccal pockets are of glandular zone. shallow and unperforated, as in Bom- bina. The free velar surface has a thick Discoglossus pictus Otth glandular edge with a cusp projection (Fig. 8) over each filter cavity. The median Material.—Author's collection (stage notch is very weak. 33; sv. 7.7 mm). Laboratory raised spec- Ventral pharynx.—The branchial bas- imens, initially collected near Lyon, kets have similar shape and proportions France; no date. to those of Alytes. Counts for numbers Reference.—Boulenger, 189L of filter rows run 9, 10, 9, and 5 for cb. External.—Discoglossus pictus larvae 1-4. In all details of the filter rows and have a single, medial spiracle and a rela- filter plates D. pictus is virtually indis- tively ventral mouth with two upper and tinguishable from Alytes and Bombina. three lower denticle rows. Typically all The branchial food traps are covered denticle rows are double but the outer with small but distinct secretory pits, rows may be single. which do not appear to be organized as rows or ridges anywhere in the nharvnx. Ventral buccal.—D. pictus is de- The glottis is not scribed by comparison with Alytes and strongly elevated; its lips are thick, but not as thick as tnose Bombina. The floor of the oral cavity of Bombina. Approximately one-third of is more pointed in D. pictus than in A. the glottis lies under the ventral velum. obstetricans and in general proportions In overall proportions the more closely resembles Bombina than glottis of D. pictus is most similar to that of Alytes Alytes. Infralabial papillae are similar cisternasii among its near relatives. D. to those of Alytes only smaller. A few pictus shares a large esophageal funnel pustulations occur around the base of with other discoglossoid tadpoles. these papillae. The tongue anlage has six papillae with robust bases and Dorsal buccal.—In shape and pro- pointed apices arranged in an arc with portions the roof of the buccal cavity is the most medial papillae most anterior. similar to that of Bombina. The rostrum The medial two papillae are fused at is not strongly turned ventrally and the prenarial their base and resemble the single lin- arena is devoid of any surface gual papilla seen in Bombina. A half irregularities, pustulations or papillae. dozen tiny pustulations occur anterior to The large flaps that arise from the an- the lingual papillae on the tongue anterior wall of the nares in other disco- glossoids are present in D. pictus. lage. The BFA is surrounded by 8 major They papillae on each side, aligned in straight have a jagged, irregular free margin and are rows beginning at the medial margin of not as large as in Alytes or Bombina. the buccal pocket and converging pos- The median ridge is similar to that of teriorly, and an equal number of minor Bombina. There are a few pustulations in the postnarial papillae near their bases. The BFA arena but papillae in papillae are simple, attenuate cones that region, as well as lateral to the me- lacking any major secondary pustula- dian ridge, are absent. Ten simple papillae tions or papillae. The arena is particu- arranged roughly in an arc (with larly well demarcated anteriorly because the crown most posterior) define the of large pustulations that run on each posterior edge of the BRA. A few tiny 20 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 8.—Drawings depicting D. pictus; floor of mouth (above) and roof (below). ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 21 papillae on one side define the lateral Ventral buccal.—The wide oral open- margin of the BRA. Several dozen small ing of this larva gives the front of the pustulations occur within the BRA mouth a gently curved outline in dorsal among the papillae that define it. Lat- view. On the lower lip, near the mid- eral to the BRA the buccal roof is line, are two pairs of tiny, thin papillae smooth with the exception of a small and some extremely small pustulations. longitudinally oriented pustulate ridge Because the lower lip curls backward in the far lateral margin of the buccal inside the mouth, the more ventral pair roof on each side. The glandular zone of papillae are obscured from view with- has a V-shaped anterior margin and is out stretching the lips. Lingual papillae of uniform length. Small tightly packed are absent. BFA papillae are clustered secretory pits are visible everywhere on along a broad arc, all well behind the the glandular zone. The dorsal velum is buccal pockets; they do not circumscribe short, weakly curved and broadly inter- an "arena" per se. These papillae, seven rupted on the midline. per side, are simple, anteriorly curved Dorsal pharynx.—The dorsal pharynx structures, large and of subequal size. is indistinguishable from that of A. ob- The largest papillae are nearest the mid- stetricans. line and displaced anterad. None of Diagnostic summary.—The great sim- the papillae are bffurcated, although two ilarity of all the discoglossid tadpoles on each side show some basal fusion. masks their minor differences. Only triv- Within the arc of the BFA are two, ial features distinguish D. pictus from small, attenuate papillae behind the buc- the Bombina and Alytes larvae exam- cal pockets near the midline. Prepocket ined; e.g., papillation is generally greater papillae are absent. There are no papil- than in Bombina, the arch of papillae on lae anywhere anterior to the buccal the tongue enlage is different than either pockets, but above the massive cerato- Alytes examined, the sculpturing of the hyals are numerous, randomly scattered ventral velar margin is least in this pustulations and subpapillate projec- genus, etc. Many of these differences tions. The buccal pockets are very wide, may be size related. deep and not long. They do not appear perforated. There is a large single fold RHINOPHRYNIDAE of epithelium arising from the floor of Rhinophrynus dorsalis Dumeril & Bibron the pockets. The free velar surface is not large. It is (Fig. 9) unusual in that it is fused medially with the dorsal margins Material.—Uncatalogued, author's of the fourth filter plates rather than collection (stage 36, sv. 15.5 mm). Col- continuous across the midline. The velar lected in shallow pools of flooded drain- margin is also fused to the top of the age ditch along Highway 190 approxi- filter plates on cb. 2 but is free for a mately 1.0 km north of Tehauntepec, short distance along cb. 3. Spicular sup- Oaxaca Province, Mexico; July 17, 1970. port for the velar margin is absent and References. Orton, 1943; Stuart, — the velar surface tends to arch upward 1961; Starrett, 1973; Wassersug, 1972. above each filter cavity. Except for the External.—Rhinophrynus larvae have points of attachment, the velar margin orifice lacks an oral a wide oral that forms a rather smooth arch when viewed disc. Keratinized structures, both denti- from above. Posterior projections of the cles and beaks, are absent. There is a velum above the filter cavities and in single, short barbel that extends forward the median notch are absent. Secretory from the middle of the lower lip in the pits could not be resolved anywhere larvae from this population. Spiracular openings are paired and bilaterally sym- along the posterior velar margin. The metrical in the genus. division of the velum into two parts 22 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 9.—Photographs of the floor (above) and roof (below) of the mouth of a Rhinophrynus dorsalis larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 23 means that the glottis is fully exposed observed in any other species. Smooth above the velum and is within the buc- transversely oriented ridges occur on cal cavity. The glottis has a predomi- each side of the roof formed by an nantly horizontal orientation, but is abrupt rise just posterior to the articu- tipped slightly forward. A slight de- lating surface of the ceratohyal with the pression makes the anterior margin of palatoquadrate bars. These ridges, the glottis stand out from the buccal which do not cross the midline, align floor. The glottal lips and laryngeal disc with buccal pockets below. More pos- are comparable in size and shape to teriorly within the glandular zone are those of typical pond tadpoles. three concavities of the roof on each Ventral pharynx.—The branchial bas- side. These correspond to the upwell- kets have a "typical" length to width ings of the free velar surface over each ratio, but encompass an atypically large filter cavity. The middle concavity on proportion of the total oral volume. The each side is the largest and has a steep, first and second filter cavities are strong- transverse anterior wall. The lateral and ly bowed outward; the third filter cavity medial pairs are more gentle, shallow is round and very open when viewed hollows. The internal nares are tiny and from above. The extreme curvature of far anterolateral; a prenarial arena is

the filter plates make it difiicult to esti- ill-defined. Anterior to the nares are a mate height to length ratios. The rela- half dozen small, scattered pustulations. tively tall filter plates are also thick. The narial openings are small transverse These plates are arched through the ovals, slightly larger medially than lat- transverse plane in such a manner that erally. Their anterior and medial mar- they are more imbricated away from gins are weakly defined and have a faint the midline than toward the midline. texture. Prenarial papillae are absent. Counts for filter rows run 11, 13, 13, 8 The posterior narial walls are thin flaps, for cb. 1-4. The filter ruflBes are very more horizontal than vertical, and about

as wide as tall vide long ) . dense. Secondary and tertiary filter folds ( Narial valve are very long and higher order folds projections are absent. The median ridge are numerous. Full filter rows are very and papillae of the buccal roof that wide, particularly ventrally. The filter demarcate postnarial and buccal roof cavities are tall, nearly completely cano- arenas in other tadpoles are absent. Sev- pied passages. They were packed with eral dozen pustulations are dispersed buccal roof the nares fine silt in this specimen and other indi- over the between viduals from this population. With care- and the glandular zone. There are also pairs of small, blunt papillae in the ful manipulation it is possible to curl two forward the velar margin and expose midportion of the buccal roof halfway lateral margin; some of the secretory ridges of the between the midline and symmetrical projections branchial food traps. The food traps they are the only of the buccal roof. The glandular zone are quite tall and narrow, but their full area cannot be determined without sec- is made up of dense, moderately large conspicuous secretory pits that ex- tioning. The secretory ridges are not and tend back onto the pressure cushions. continuous from one filter cavity to the Although the anterior margin of the next. The ridges are tall, thin, and is quite the zone is of gen- highly regular. The esophageal funnel zone wavy, erally uniform length except directly in is of normal proportions. front of the esophagus where it abruptly Buccal roof.—The roof of the oral decreases to a negligible length. The cavity is far more squarish and less triangular in R. dorsalis than in any beaked average length of the zone is equal to or tadpole. The buccal roof is basically flat, slightly greater than in typical pond but has some depressions and ridges not larvae. The dorsal velum is shorter and 24 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY not particularly coiled. It is rather stiff, External.—Microhyla herdmorei tad- projects directly anterad, and is absent poles are of medium size for the genus. on the midline. As is characteristic of the family, they Dorsal pharynx.—As viewed from lack hard mouth parts and have a me- above, the dorsal pharynx on each side dial spiracle. In M. herdmorei the tail is pointed but lacks a vibrating filamen- is shaped like a right, isosceles triangle tous tip. with sides posterior and lateral, and the hypotenuse facing anteromedial. The Ventral huccal.—The floor of the pharynx is larger than in any beaked mouth is shaped somewhat like a trape- tadpole, with pressure cushions extend- zoid (base posterior) with the length ing back well past the posterior margin and width approximately equal. The of the dorsal velum. There are three buccal floor behind the buccal pockets pairs of very large, distinct pressure is extremely elongate. The ceratohyals cushions. The most lateral pairs are tall, are so short, compared to the length of oblique ridges with sharp ventral edges. the branchial baskets, that only a fifth The middle pair are oriented like the of the mouth is anterior to the buccal lateral pair, but are not as tall and have pockets. The tiny lower lip is directed a posterior knob rather than a continu- dorsally. There are three small, blunt ous sharp edge. The medial pair are infralabial papillae on each side con- large, round swellings. Behind the pres- centrated within the loop of the lower sure cushions is a relatively narrow and lip. The most anterodorsal papilla is shallow ciliary groove. a small, simple knob-like projection. There is an anteroventral papilla slightly Diagnostic summary.—The full attachment of the ventral velum to the more attenuate. The third papilla is posterior. It is thick, tops of all filter plates, including those a transversely oriented flap that has a ventral of cb. 4, immediately separates Rhi- common base the papilla. nophrynus from all other species. The with anteroventral The posterior infralabial papillae from each side following is a partial list of other fea- at the tures which, in combination, diagnose abut midline, obscuring much of Rhinophrynus: lingual papillae absent; the oral orifice. The tongue anlage is an massive prepocket buccal surface; buc- elongate oval devoid of lingual papillae. cal floor arena papillae in broad arch; The BFA papillae are arranged along a glottis exposed on posterior buccal floor; semicircle which is open anteriorly. The absence of velar marginal projections; front edge of the arena is formed by the massive branchial baskets; well-devel- buccal pockets. The arena is substantially oped secretory ridges; absence of all wider than the relatively short in- features that would outline postnarial terpocket distance, but limited to the and buccal roof arenas; presence of lat- anterior half of the portion of the buccal eral depressions of buccal roof above floor behind the pockets. The papillae buccal pockets. are small, attenuate cones, evenly spaced and lacking terminal irregularities. I MICROHYLIDAE counted five on one side and six on the other, with the largest ones most pos- Microhyla herdmorei (Blyth) terior. Arising from the center of the (Fig. 10) buccal floor at the back of the arena is Material—YW^n 187567 (stage 32, the glottis—a remarkable anterad dis- sv. 10.8 mm). Rock pool adjacent to placement from the typical mid-pharyn- flowing stream at Khao Yai, Nakhon geal position of this structure in all tad- Ratchasima, Thailand; January 5, 1969. poles with beaks. The elevated laryn-

References.—Inger, 1966 (p. 150); geal disc is tipped so the glottis is Heyer, 1973. directed anterodorsally. The glottal slit ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 25

of Microhyla berdmorei Fig. 10. Drawings of the floor (above) and roof (below) of the mouth a larva. 26 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY is of moderate size with very weak lips. rows inaccessible without dissection of Directly in front of the glottis is a single, the ventral velum. Counts for filter rows small medial papilla. A single, conical, run 22, 20, 18, 10 for cb. 1-4, exceeding mediodorsally directed prepocket papilla the values for any beaked tadpole. The can be found on each side. There are a filter rows have normal proportions in few faint pustulations within the arena terms of folding pattern, but are not that disperse out over the lateral arms quite as tall as in typical pond larvae. of the ceratohyals. A long trachea is Neighboring filter rows fully abut and visible in the buccal floor, dividing the tertiary folds from neighboring rows in- BFA and the rest of the buccal floor, interdigitate. The filter canals are very cluding the edge of the velum, into right small, fully canopied tubes. The bran- and left halves. The buccal pockets are chial food traps are unlike any seen in very large triangular pouches with their beaked species. They are slender, verti- posterior margins far more obliquely cal crescents of a thick secretory tissue oriented than in any hylid examined. (hence the name crescentic organs; Sav- The pockets are not deep compared to age, 1952), isolated at the anterior end their unusual length, nor are they per- of the filter cavities and inaccessible forated. The velar surface is astonish- without dissection of the velar surface. ingly long—about half the length of the The area covered by the organs is very mouth. The freely movable portion of small compared to the size of the filter the velum is, however, only slightly long- cavities. Secretory ridges are very dense er than in typical pond larvae. Spicular within the food traps and are not easily support is absent from this delicate sur- resolved in this specimen. Bound by the face. The velar margin lacks any pos- narrow crescentic organs are vertical re- terior projections and forms a smooth gions of the filter cavities containing a arc as viewed from above. The margin few, loosely defined clusters of secretory is reflected dorsally along its medial edge cells. Most of the ventral surface of the where it joins the trachea. Secretory pits velum is free of secretory tissue of any scattered along the posterior velar edge sort. The esophageal funnel is both nar- are limited to the absolute margin; these row in profile and small in diameter. pits are few in number and quite small Dorsal buccal.—The roof of the in size. mouth shares with the floor a trape- Ventral pharynx.—The volume of the zoidal, almost rectangular profile. In de- branchial baskets is over half of the tails, the roof differs radically from all total volume of the head and body; i.e. non-microhylids examined. The upper larger than in any beaked tadpole. The lip is nearly horizontal so that the pre- increase is primarily in length, with the narial arena is large and square. Far baskets extending so far forward that back in the arena, in line with the front almost half of the baskets are under the of the internal nares is a single, medial, velum. Viewed from above, the baskets conical papilla, which is anteriorly are basically shaped like elongate tri- curved and of medium size. Other sur- angles and have their long axes oriented face features are absent. The most un- closer to the sagittal plane than in any usual aspect of the roof is the internal beaked tadpole examined. The filter cav- nares. Each naris is a shallow, round ities decrease in size as one goes from cul-de-sac with all but the lateral third the first to the third. The filter plates covered by a textured, presumably sen- are almost vertical, except that a slight sory, tissue patch. Thin, flap-like verti- arch to the top portion of the third plate cal walls surround the medial edges of blankets the top of the third filter cavity. these narial depressions. The antero- The extension of the filter plates under medial portions of the walls are low and the velum makes the more anterior filter coarsely serrate; the posteromedial por- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 27 tions are relatively huge, tongue-like est point is at its posterolateral corner, flaps that project anteriorly under the where it is nearly twice as tall as at nares and touch on the midline. These its midpoint. The medial cushion is projections are in a position correspond- more precisely defined and of more uni- ing to that of the narial valve projections form proportions. Laterally, the ciliary in some beaked tadpoles. While they groove of M. berdmorei is shallow and may be homologues to the narial valve very wide. Medially, the groove be- projections, they are clearly not asso- comes a narrow, deeply entrenched ciated with any functional valves, for canal. the nares are not perforated. These pro- Diagnostic summary. — Microhylid jections are strongly concave anterad. A larvae differ from all other tadpoles in vertical ridge descends down the pos- the attachment pattern for their ventral terolateral surface of each projection and velum to their filter plates, the position clearly stiffens it. The bases of these of the glottis, the shape of the branchial ridges align with a small triangular flap food traps, and structure of the unper- on each side of the buccal pocket just forated internal nares. posterolateral to the nares. The nares Microhyla berdmorei is readily dis- lack any sort of rim or wall along their tinguishable from the other microhylids whole lateral margins. A postnarial are- examined by the combination of: large, na is absent. There are no postnarial pa- medially abutting, posterior infralabial pillae, lateral ridge papillae, or median papillae; a single preglottal papillae; ridge to define this arena. Halfway back high count of filter rows; narrow bran- on the buccal roof are four simple, coni- chial food traps; four buccal roof pa- cal BRA papillae. These papillae are too pillae; dorsal velum vestigial medially. close to each other and to the midline Microhyla heymonsi to define a buccal roof arena. On each Vogt side of the midline, the smaller of the (Fig. 11)

papillae is displaced slightly antero- two Materia/.—FMNH 187923 (stage 37, laterad. Beginning lateral to the BRA sv. 6.8 mm). Small pool above dammed papillae and extending in a straight row stream at Sakearat Experimental Sta- anterolaterally across the buccal roof is tion, Amphoe Pak Thong Chai, Chang- a series of evenly spaced pustulations on wat Nakhon Ratchasima, Thailand; Feb- each side. There are a few, very thin ruary 24, 1969. buccal pustulations scattered over the References.—P^ixker, 1934 (p. 135); roof anterior to the BRA papillae; other- Heyer, 1973. wise, papillae and pustulations of the External.—Besides the beakless mouth buccal roof are absent. The glandular and median spiracle typical of micro- zone is of typical length. Its anterior hylid larvae, the tadpoles of Microhyla margin is nearly transverse. The secre- heymonsi are characterized by an oral tory pits are large and conspicuous, but disc expanded into a large, upwardly dorsal velum of very low density. The directed funnel. Only features which its length is 25% longer than at maximum distinguish these larvae from the two that of hylid larvae. It is common pond previously described species of Micro- across the midline, although continuous hyla are dealt with in the following de- in that re- rather abruptly constricted scription. gion. Buccal ventral.—Anteriorly the floor Dorsal pharynx. The two pressure — of the mouth is broad and gently curved, cushions on each side are quite distinc- when viewed from above. Posteriorly, tive. The lateral one is, on the average, the branchial baskets are truncated. The twice as long and tall, and four times prepocket portion of the buccal floor is as wide, as the medial cushion. Its tall- much elongated compared to other spe- 28 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 11.—Drawings of the floor (above) and roof (below) of the mouth of a Microhyla heymonsi larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 29

cies of Microhyla. The posterior shift of the other two species, the full extent of the buccal pockets reflects the unusual the traps could not be determined be- shape of the underlying ceratohyals. cause of difiiculty in staining and the These are extremely elongate medially small size of these tadpoles. The ridges and have posteriorly directed lateral were absent along most of the unat- arms. The infralabial papillae are as in tached velar surface. The esophageal M. berdmorei. BFA papillae are re- funnel was slightly larger and broader duced in size and number (3 on one than in the two other species. side and 4 on the other), grading into Dorsal buccal.—There is a small, pustulations. The papillae are blunt posteriorly directed V-shaped depression rather than conical. There is a single, in the middle of the prenarial arena. A blunt, medial papilla in front of the single, medial papilla of the prenarial glottis. Prepocket papillae are large and arena arises at the posterior apex of this strongly curved medially. The buccal V-shaped concavity. This papilla is pockets are narrow, nearly longitudinal- small, straight, and blunt. The extent of ly oriented slits. They are deep and the presumed sensory patch in the in- their floors inaccessible without further ternal nares could not be determined. dissection; whether or not they are per- The narial walls are more similar to forate not was determined. The glottis, those of M. ornata than to M. berdmorei. lacks elevated lips, sits which on a huge The anteromedial portions of the narial laryngeal disc. is It directed dorsally walls are reflected backward under the positioned and about two-thirds of the narial openings. The bases of the large, distance back on the buccal floor. The posteromedial projections of the narial trachea is shorter much in this species walls are widest in this species. The than in the other Microhyla. The velar ridges on the backs of these projections margin is gently arched lacks and any are not as tall in M. heymonsi as in M. projections. It is virtually continuous ornata or M. berdmorei. They are, how- over the trachea, but left and right sides ever, more sharply defined and com- are interrupted by a small median notch. pletely continuous with the small flaps Secretory pits could not be resolved on posterolateral to the nares. In M. hey- the velar margin. monsi these flaps have arched rather Ventral pharynx.—The branchial bas- than pointed apices. There are two tiny, kets are shaped like equilateral triangles blunt papillae far posterior on the buc- with more than half of the filters under cal floor and several dozen blunt pustu- the velar margin. The baskets are tiny, lations dispersed over the surface in a being proportionally smaller even than W-shaped pattern. I could resolve secre- those of typical, Orton type 4 pond lar- tory pits, but only on the dorsal velum. vae. The third filter cavity is reduced The glandular zone, as a discreet region in size and nearly inaccessible under the of the buccal roof, may be absent. The velum. All filter cavities contained fine, dorsal velum is shorter than in the other flocculent food matter in this specimen. two species, at least in the neighborhood

Counts for filter rows on each filter plate of the midline; nevertheless, the velum is were well below those for other Micro- still continuous across the midline. hyla (and within a row of the counts Dorsal pharynx.—Only lateral pres- for H. regilla). The filter mesh is not as sure cushions are well-defined and these dense as in the other Microhyla. Fine are small, obliquely oriented ovals, much tertiary and higher order filter folds smaller than the medial pressure cush- are lacking. Well-developed secretory ions in the other species. The ciliary ridges are present anteriorly under the groove is comparable to or slightly ventral velum. Although the branchial deeper than that of M. ornata. food traps seem relatively larger than in Diagnostic summary.—The mouth of —

30 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

M. heymonsi grossly differs from the Tertiary folds on the filter rows do not mouth of the other Microhyla in the interdigitate as tightly as in M. berd- following features: longer prepocket morei, but the difference is slight enough buccal surface; ventral velum virtually to be accountable to minor differences continuous across the midline; branchial in preservation. The branchial food traps baskets highly reduced; very large are wider and form nearly complete tori. esophageal funnel; V-shaped groove in The area bound by the food traps has prenarial arena; dorsal velum and pres- faintly developed secretory ridges and, sure cushions reduced. unlike M. berdmorei, these extend posteriorly onto the ventral surface of the Microhyla ornata Dumeril & Bibron ventral velum but are still absent along Material.—Uncatalogued, author's col- the posterior velar margin. lection (stage 36, sv. 5.9 mm). Collected Dorsal buccal.—Walls of the internal in shallow cement drainage ditch on the nares are not as tall as in M. berdmorei. grounds of Applied Scientific Research The anteromedial portions lack serra- Corporation, 196 Ehahoyothin Rd., tions; the shorter, posteromedial projec- Bangkheng, Bangkok, Thailand; August tions do not meet each other on the mid- 22, 1968. line. The ridges on the back of these Reference.—Lui, 1950 (p. 251-252). projections are very faint. The pre-

Microhyla ornata is so similar to M. sumed, sensory field in the internal nares berdmorei that only the differences are covers a greater portion of the narial presented here. depressions. M. ornata has two rather

External.—Microhyla ornata is a than four BRA papillae. They are rela- small species with small tadpoles. Its tively taller than the BRA papillae of larvae can be distinguished externally M. berdmorei. The rows of pustulations from those of previous species by their extending away from the BRA papillae smaller size, rounder snouts and rela- are less conspicuous. The secretory pits tively longer, filamentous tails. of the glandular zone are even less dense than in M. berdmorei. The zone is frag- Ventral buccal.—The floor of the mented into four approximately equal mouth is anteriorly rounder in M. ornata division the than in M. berdmorei. M. ornata lacks portions with one along anterodorsal infralabial papillae and the midline and two other divisions between mar- posterior infralabial papillae are no more the midline and the lateral buccal than gentle swellings incapable of abut- gin. The glandular zone ends anterior ting on the midline. The medial pre- to the base of the velum. The dorsal velum is more complete across the mid- glottal papilla is relatively taller in M. line. Rather than being just a vestige, ornata, and in this species there is a second smaller, medial preglottal papilla the mid-portion of this flap is equal to a in front of the first one. The prepocket fifth of the maximum length of the papillae are relatively larger and curved velum. medially. The margin of the velum has Dorsal pharynx.—Differences are mi- a single, broad posterior projection on nor and attributable to preservation. each side above the filter plates of cb. 3. Diagnostic summary.—Microhyla or- Numerous tiny secretory pits are present nata is virtually identical to M. berd- in a narrow row along the velar margin differences viz., infra- medial to the apices of the posterior pro- morei. The few jections. The medial edge of the velum labial papillae not abutting, double pre- is not reflected posteriorly at the mar- glottal papillae, less filter rows, 2 buccal gins of the trachea. roof papillae, dorsal velum more com-

Ventral pharynx.—Counts for filter plete across midline—may largely be rows run 14-15, 16, 13-14, 9 for cb. 1-4. ascribable to the differences in size. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 31

Fig. 12.—Photographs of the floor (above) and roof (below) of the mouth of a Scaphiopus bombifrons larva. —

32 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

PELOBATIDAE straight or slightly convex anteriorly. Scaphiopus bombifrons Cope There is a short, but relatively wide, median notch. The velum is supported by (Fig. 12) only two pairs of spicules. One pair 75020 (stage 36, Material—FMNH neighbors the midline and the other is Collected from drainage sv. 15.5 mm). nearby, directly over the filter plate of 4.6 west of Fredrick, Tillman ditch km cb. 4. The spicules are wide and not Co., Oklahoma; 4, 1948. July very stiff. Small but dense and con- 1951 205- References.—Stehhins, (p. spicuous secretory pits form a band 207); Bragg, 1965 (p. 63-91). along the posterior velar margin. The head is broad; the External—The band is widest around the median notch oral disc is spiracle is sinistral. The and thins out laterally so that secretory a large moderately small but surrounds pits are absent along the lateral quarter common and powerful beak. The most of the velar margin. denticle pattern is 4/4 but both the up- Ventral pharynx.—The branchial bas- per and lower rows may range from 2 kets are close to perfect ovals with the to 6 in number (Bresler and Bragg, long axes of the ovals running antero- 1954). laterad to posteromesad. The baskets Ventral buccal—The Hoor of the are moderately shallow. They are of mouth in dorsal view closely approxi- average or slightly larger than average mates an equilateral triangle. There are size. The filter plates of the second and two pairs of moderate sized infralabial third ceratobranchials do not project up- papillae. The first pair is far anterior ward, consequently, each basket is a within the arc of the infralabial carti- single common filter cavity. Counts for lage; these project anteriorly out of the filter rows run 10, 14, 10-11, 9 for cb. mouth. The second pair is positioned 1-4. These are all above the average; more dorsolateral and posterior, and those for cb. 2 and 4 significantly so. projects medially. All four papillae are The filter mesh on each filter row is very subequal in size, slim, shghtly com- fine due to multitudinous tiny, tertiary pressed cylinders and lack marginal pa- filter folds on each secondary fold. The pillae. The lingual papillae are typical filter mesh, however, is not dense in height and orientation, although they rather wide gaps exist between neigh- may have a slightly enlarged basal diam- boring filter rows. ( The distance between eter. The apices of the papillae are rows may have been slightly accentu- covered with fine pustulations. The buc- ated by shrinkage from preservatives.) cal floor arena is a poorly defined, egg- Some of the rows, particularly those of shaped patch bearing between 40 and cb. 2 and 3, are wider than normal. The 50 papillae. Those papillae around the filter canals are very tall and moderately edge and within the patch are rather wide. They are about 80% canopied by homogenous; they are all evenly spaced, the filters. The ventral surface of the medium small, straight and a few have velum is covered by buff textured tissue, fine terminal pustulations. Posteriorly, indicative of a secretory mucosa. At the papillae are replaced by pustula- 75 X magnification no organized ridges tions. Papillae and pustulations are ab- or secretory pits could be resolved. This sent directly in front of or behind the species presumably lacks secretory buccal pockets, which are very narrow, ridges. The glottis, glottal lips and transverse depressions. The pockets are laryngeal disc are typical in size and shallow and unperforated. The free shape. The glottis is fully visible on the velar surface has an average relative pharynx when viewed from directly area but otherwise is quite unusual. The large and the margin of the velum is a wide, smooth above. The esophagus is edged "V," with each side being nearly funnel is broad in dorsal profile. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 33

Dorsal buccal.—S. bombifrons has a Dorsal pharynx.—A single, massive slightly larger prenarial arena and small- pressure cushion covers the dorsal er postnarial arena than seen in a typical pharynx on each side. These cushions type 4 larva such as Hyla regilla. The are deep, elongate ovals with their ma- smaller postnarial arena is the result of jor axes running anterolateral to postero- relative displacement on the median dorsal. The ciliary groove was damaged ridge anteriorly. The most unique fea- in dissection, but appears very broad ture of S. bombifrons is a small, round, medially. keratinized knob in the center of the Diagnostic Summary. — Scaphiopus prenarial arena. Other than this, the pre- bombifrons larvae are unique among the narial arena is devoid of any papillae, species examined in the following fea- pustulations or ridges. The internal tures: pattern and shape of infralabial nares are narrow, oblique slits. The papillae; shape of lingual papillae; shape anterior narial walls have slightly pustu- of ventral velar margin; presence of late anteromedial corners but lack pre- keratinized knob in prenarial arena; size narial papillae. The narial valves have and shape of pressure cushions. slightly arched margins, but lack narial valve projections. A deep groove behind Megophrys minor Stejneger each narial valve sets the valves off from (Fig. 13) the postnarial arena. postnarial The Material—FMNH 49857 (stage 34, is laterally arena bound by two medium sv. 16.5 mm). Collected from pools un- sized, robust papillae aligned directly der cascades of small mountain streams behind the medial edges of the nares. or in side pools of large mountain papillae pustulate These two have streams where current is slow, at ap- crowns and a secondary, short, conical proximately 9100 m elevation, near papilla at their lateral bases. A single, Taosze, Mount Omei, Szechwan, China; posterolat- tiny, pointed papilla occurs June 15, 1946. eral to the two postnarial papillae. The Reference.—Liu, 1950 (p. 188-191). ridge is a moderately tall, tri- median External.—Megophrys minor larvae angular flap with a relatively shorter have a huge, upwardly directed, denticle base. The ridge is thick and stiff. There free oral disc. They are generally is a single, large, pointed, asymmetric, thought to lack keratinized beaks, but marginal projection on the median ridge the fine, hair-like structures at the mar- in this specimen. The anterior surface gin of the oral orifice (noted by Liu, has pustulations, but they are concen- 1950) are undoubtedly vestiges of oral trated in a rim around the edge of the beak serrations. The tadpoles have a flap. There are two small, pointed pus- long, powerful tail; the spiracle is sinis- tulations within the prenarial arena. A tral. buccal roof arena is absent. Scattered Ventral buccal.—The anterodorsad about the buccal roof behind the median direction of the lower beak results from ridge are a few dozen pointed pustula- a general, dorsal curvature of the an- tions. Two or three of the more anterior terior portion of the mouth. Because ones are slightly larger than the others. the prepocket portion of the oral floor The glandular zone is overall very wide, is relatively large and expanded antero- only narrowing slightly near the midline; laterally, when the mouth is pinned flat its anterior margin is a distinct, broad the oral floor is in the shape of an elon- are uniformly "V." The secretory pits gate trapezoid rather than a triangle. large and conspicuous, but not particu- M. minor has four infralabial papillae larly dense. The dorsal velum is very within the loop of infralabia and visible long and broadly interrupted on the mid- in the oral orifice of an undissected tad- line. Each side is anterodorsally coiled. pole. These papillae were illustrated 34 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

of a Megophrys minor Fig. 13.—Photographs of the floor (above) and roof (below) of the mouth larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 35 and described in detail by Liu, 1950 in a narrow, transverse arch behind the (Fig. 382 and p. 190). In addition buccal pockets and in an anterior-pos- there are five other infralabial papillae, terior line bowed outward slightly, above one on the midline, posterior to the visi- the lateral portions of the ceratohyals. ble four, and two others on each side, The buccal pockets are very short and dorsolateral to the loop of the infralabial strongly arched anteriorly. Despite the cartilage. All the infralabial papillae are fact that they are quite shallow, folds thick, fleshy lobes that lack terminal ser- at the bottom o£ each pocket make it rations or papillae. The five most mesial difficult to determine if the pockets are papillae curve slightly anterad. The four perforated. If the pockets are perfo- most lateral papillae are elevated knobs. rated, the openings must be extremely The most anterior and dorsal pair of small. The free velar surface is moder- lateral infralabial papillae are oval (an- ately large and supported by long, thin teromedial to posterolateral major axis), spicules. The posterior margin is un- palp-like projections on the posterior usual in having a U-shaped medial mar- corners of the infralabial cartilage. The gin and a straight, nearly transverse lat- more dorsal pair of lateral infralabial eral margin. There is a sharp inflection papillae are also oval (transverse major point between the straight and curved axis) but are smaller than the pair just portions. Posterior projections are lack- described. The medial papilla is a tri- ing; the median notch is small. The angularly shaped projection that fits in curved portion of the posterior margin tightly between the smaller and more is slightly thickened and his a buffed posterior pair of external visible papillae. texture; however, individual secretory Lingual anlage and lingual papillae were pits could not be resolved, even at 75 X not observed in the normal position. The magnification, anywhere along the velar medial infralabial papilla could be a margin. homologue of the lingual papillae; how- Ventral pharynx.—The branchial bas- ever, the far anterior placement of this kets are similar in size, shape and propor- papilla argues against such a hypothesis. tion to those of other megophrynines, Buccal floor arena papillae are absent. particularly Leptobrachium. As viewed Instead of a BFA M. minor has two from above, the baskets are oval, nearly massive ridges that run the length of round, and cover an area slightly less the prepocket surface of the buccal floor. than they do in H. regilla. They are very Each ridge has a predominantly anterior shallow, and the filter plates of cb. 2

to posterior orientation. They are slight- and 3 are very low so that there is only ly bowed inward and have elevated ter- a single common filter cavity on each

minal knobs. The ridges are quite resil- side. Counts for filter rows run 8, 9, 9, ient, but not supported by cartilage. 7 for cb. 1-4. The first three values are They are set off from the rest of the insignificantly different from those of H.

buccal floor by deep creases both in regilla while the count for cb. 4 is sig- front and in back of them. Immediately nificantly above the H. regilla mean. medial to the ends of the buccal pockets The filter rows are quite wide, but the are small, anteriorly concave flaps that filter nitches are larger than in other

surround the terminal knobs of each megophrynine tadpoles because the fil- ridge. There is one blunt, rather antero- ter folds are very thin. This may be, in medial, prepocket papilla on each side, part, a preservational artifact. On many plus a small series of prepocket pustu- of the filter rows tertiary filter folds are lations. A half-dozen stubby pustula- so long that they abut with the filter tions are scattered over the dorsomedial folds of neighboring rows. Filter rows portion of the buccal floor. A few small from opposing filter plates meet end to pustulations are also on the buccal floor end above each gill slit rather than inter- 36 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY digitating, and thus they obscure the the prenarial papillae and the narial relatively tall, they gill slits. The filter canals are small but valve projections are most are fully canopied. Nevertheless, are still far shorter and less attenuate the general low density of the filter mesh than in other megophrynine larvae ex- makes the canals rather open, diffuse amined. The postnarial arena is a mod- corridors. The ventral surface of the erately small, smooth, triangular recess ventral velum is covered v^ith a fine, buff in the buccal roof. The arena is filled textured tissue, suggesting a secretory by the body of the median ridge, which mucosa. Organized secretory tissue, as is a massive, nipple-shaped, anteriorly either pits or ridges, could not be re- directed projection. This projection ex- solved at even 75 X magnification and tends far forward, anterior to the nares is presumed absent from the branchial and under the posteromedial "knob" in food traps. The glottis is small, with a the prenarial arena. Despite its unusual typical amount of exposure posterior to size and shape, the median ridge in M. the ventral velum. It has elevated lips, minor is similar to the typical flap-like sits on a transversely oriented laryngeal median ridge in most other species, be- disc, and is oriented slightly anteriorly ing joined to the buccal roof along a rather than dorsally. The esophageal narrow, transverse line and free to move funnel has a moderately large bore, but ventrally in the sagittal plane. The post- a generally narrower profile than that narial arena is bound laterally by wide, of other megophrynine larvae. low ridges that extend far posterior and are major features on the buccal roof. Dorsal buccal.—The upper beak is ridges are the presumed homo- nearly straight rather than curved, thus, These logues of the postnarial papillae and pos- the prenarial arena is very wide and the sibly the BRA papillae collectively. The buccal roof more trapezoidal than tri- anterad projections that angular in shape. Individual papillae ridges begin as far as the tips are absent from the buccal roof; instead extend almost as forward ridges rows of papillae are replaced by ridges. of the median ridge. The become internal nares Projecting down from the middle third the medial walls of the and bow outward along most of their of the prenarial arena is a large, V- length. The end of each ridge is re- shaped ridge. The anterior corners of curved. ridges are tallest and thin- the ridge are the thickest and tallest The anteriorly, and lowest and widest portions and are reflected medially. nest posteriorly. They end just behind the There is a deep sulcus within the apex middle of the buccal floor and well be- of the "V." Behind the apex a medium hind the base of the median ridge. The sized, round "knob" descends from the lateral ridge papillae are represented by roof. On each side paralleling the arms large, thick, obliquely oriented flaps, far of the V-shaped ridge, but far lateral, lateral to the middle of the ridges just is a short, thin ridge. Posterior to the described. each side anterolateral to ends of these ridges and directly lateral On these flaps is a similar subsidiary pro- to the apex of the V-shaped ridge are jection. These subsidiary lateral ridge clusters of medium small, blunt pustu- "papillae" are only a third to a half the lations. The nares are of moderate size size of the main ones. Posteromedial and transversely oriented. The inter- to the main lateral ridges are small narial distance is large. The anterior narial walls are slightly pustulate along ridges each with a gently crenulate mar- their more medial halves and possess a gin and a predominantly anterior-pos-

stiff, medium tall, conical papilla along terior orientation. These ridges are in a their more lateral halves. The narial position comparable to the lateral roof valves are tall and each possesses a papillae seen in many tadpoles and are distinct, pointed projection. Although presumed homologues of these struc- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 37 tures. They blend posteriorly into a External. — Leptobrachium. hasselti cluster of pustulations. A buccal roof tadpoles commonly have a 6/6 or 7/6 arena is absent. Pustulations are present denticle pattern but there is both zoo- behind the median ridge and mesial to geographic and ontogenetic variation in the posterior arms of the long ridges the number of denticle rows (see Inger, that bound the postnarial arena. There 1966, Table 3). The spiracle is sinistral. is also a loose cluster of faint, blunt The body is deep and the tail is shorter pustulations in the posteromedial por- than in most megophrynine tadpoles. tion of the buccal roof. The glandular Ventral buccal.—The floor of the zone is narrow and thins out toward the mouth is broad despite the fact that midline; it is absent in front of the anteriorly the oral orifice is compara- esophagus. The secretory pits at the tively small. There is a single, major anterior margin of the glandular zone hand-shaped infralabial papilla on each are elongate in an anterior-posterior side which is typical in size, shape and direction. The remaining secretory pits position but with marginal "fingers" long are relatively heterogenous in size and and attenuate. Between the lateral mar- shape, larger but the and rounder pits gin of the keratinized beak and the in- tend to along the be posterior margin fralabial papilla is a series of three of the zone. It is difficult to separate the papillae or pustulations in a straight dorsal velum from the pressure cushions anterior to posterior row. The largest is for the velum seems very short and di- the most anterior one. Ventral and me- rected ventrally rather than anteriorly dial to the hand-like infralabial papillae anteroventrally. or This may, however, are two moderately tall, attenuate pa- be an artifact from shrinkage. The pillae. These have pustulate surfaces. velum is broadly interrupted medially Lingual papillae are not evident on the and the medial margins on each side are tongue anlage but the two papillae just reflected dorsally into the esophageal mentioned could be possible analogues funnel. — or even homologues of the lingual pa- Dorsal pharynx. M. minor has only pillae. The buccal floor arena is well one large pressure cushion per side. The defined by 10-12 moderately large, at- cushion is tallest and widest far lateral tenuate, conical BFA papillae on each and triangular in shape. The ciliary side and a field of 20 or more smaller, groove was damaged in dissection and but similarly shaped papillae posterior- its proportions could not be determined ly. The lateral BFA papillae are aligned in this specimen. parallel to the sagittal plane. The tall- Diagnostic summary.—Megophrys, as est ones show some slight, marginal represented by Megophrys minor, differs pustulation but none are bifurcate. from all other tadpoles examined in the There is evidence of preservational structure of the infralabial papillae; artifact in papillae; the BFA papil- shape of the ventral velar margin; large, lae are compressed flat against the nipple-shaped median ridge and large buccal floor, with the lateral papillae lateral ridge papillae. pointing away from the midline. Pre- pocket papillae are absent, but there Leptobrachium hasselti Tschudi are well developed pustulations in the (Fig. 14) prepocket position on each side of the buccal floor. Anterior to these, Material—FW^n 14828 (stage 35, above the lateral amis of the cera- sv. 27.8 mm). Swampy area adjacent to tohyal, are a few dozen or so tiny stream at Labang Camp on Sungei Seran, Bintulu District, Fourth Div., papillae and associated pustulations in a Sarawac, Borneo; November 5, 1963. diffuse patch. Tiny conical papillae Reference.—Ingei; 1966 (p. 33-36). and pustulations are also present in 38 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 14.—Photographs of the floor (above) and roof (below) of the mouth of a Leptobrachium hasselti larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 39 abundance on the buccal surface in a them. Branchial food traps are com- triangular area between the BFA, the pletely confined to the horizontal free back of the buccal pockets and the velar velar surface; however these surfaces are surface. The buccal pockets have a nearly covered by large, dense secretory pits transverse orientation: they are wide instead of secretory ridges. These pits and deep. They are clearly perforated, completely cover the food traps and can although the perforations are not visible be found on the ventral surface of the without retracting the large folds on the ventral velum directly in front of the posterior wall of each pocket. The free glottis where they tend to align in trans- velar surface is very long; it is supported verse rows. The glottis is small, with by long, thin spicules that extend back weakly developed lips; a laryngeal disc to the posterior velar margin. The velar is not visible. Ninety per cent or more margin is nearly straight on each side of the glottis is fully visible when viewed of the midline, its medial portion is from above but this large exposure may coarsely serrated. There is a well de- have resulted in part from tissue shrink- veloped median notch bound by two age. The esophageal funnel is anteriorly papillae-like projections on each side. broad but not large. are to The more medial projections two Dorsal buccal.—The buccal roof is three times the size of those immediately broad overall, but the prenarial arena is lateral. The velum possesses a secondary narrow. Six pustulations within the nar- margin between the branchial baskets ial arena show no particular symmetry. ventral to the main edge. This secon- The nares are wide and have a strong dary edge also possesses a pair of pos- transverse orientation. A small pustulate terior projections. Large, conspicuous ridge projects from the anteromedial secretory pits of moderate to low density corner of each naris toward the center can be found along the middle half of of the prenarial arena. In the middle of the velar margin. The pits are concen- the otherwise low anterior narial walls trated on the medial posterior projection. arise single, tall, attenuate prenarial pa- Ventral pharynx.—The branchial bas- pillae on each side, matched by equally kets are oval, elongate in the transverse tall and attenuate narial valve projec- plane, and extremely shallow. All filter tions of the posterior wall. Both the cavities are of nearly equal volume, but prenarial papillae and the narial valve the filter plates are so short that they projections point away from the narial effectively form a single common cavity openings, presumably because of shrink- for each branchial basket. The shorten- age. The median ridge is near the nares ing of the filter plates is reflected in an and the postnarial papillae are in a increase in length to height ratios for transverse line between the median all the filter plates, particularly those of ridge and the laterally displaced lateral the second and third ceratobranchials. ridge papillae; consequently, the post- Counts for filter rows run 5, 8, 9, 6 for narial arena is shaped much like a trans- cb. 1-4. The values for the first two versely elongate oval, two to three times arches are extremely low while the two as wide as long. The postnarial papillae other values are within the typical tad- are more attenuate than those of H. pole range. The filter mesh is not dense regilla but equally numerous. The me- although the filter rows are all very dian ridge, which lacks a secondary wide. The wide rows result from longer ridge, is small and shaped like a half- secondary and tertiary filter folds. Nev- circle with fine, evenly spaced, marginal ertheless, neighboring filter rows do not serrations. Lateral ridge papillae are abut and the filter canals are shallow, twice as tall as the median ridge. They 60% canopied by the filters, and about a are narrow, transversely compressed third as wide as the rows that bound flaps with two attenuate peaks. The 40 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY medial peaks are two to three times as uncommon for there to be one row more tall as the lateral peaks. The buccal roof or less above or below. The spiracle is arena is a well-defined oval bounded by sinistral; the body and tail are elongate. eleven attenuate conical papillae on one Ventral buccal.—The lower beak is side and twelve on the other. Far lateral larger and positioned more dorsally in to the middle of the BRA are clusters of L. oshanensis than in L. hasselti. The two or three smaller, secondary papillae. floor of the mouth is of typical width The buccal roof is evenly covered and not as broad as in L. hasselti. Very with fine pustulations. In addition, large, hand-like infralabial papillae are there are larger, more robust pustula- present; like many other oral papillae, tions scattered within the BRA. Later- they show a tendency to be divided into ally the glandular zone is of typical long, secondary papillae. The infralabial length along the anterior-posterior axis papillae are tall structures with a half- but medially it is reduced to a length dozen or more extremely attenuate, of only two or three secretory pits. The pointed "fingers" that arch anterad. dorsal velum has been badly distorted There are two rather than three papillae from alcohol storage and its full extent on each side anterior to the infralabial cannot be determined. There is a large papillae. The more anterior papillae are gap between the left and right halves the larger. These are flattened into the of the velum and the medial edges—un- transverse plane, bifurcated and are usual in being papillate—are reflected pointing out of the mouth. The papillae dorsomedially. I counted seven papillae between these and the hand-like papil- on each side and roughly an equal num- lae are small, simple projections. The ber of pustulations. two medial papillae, which were noted Dorsal pharynx.—The nature of the as possible anteriorly displaced lingual pressure cushions could not be deter- papillae in L. hasselti, are taller in L. mined because of shrinkage. It seems, oshanensis and also project anteriorly. however, that there is a single cushion Papillae are absent from the tongue an- that fits into the common filter cavity lage. On each side, laterally adjoining rather than multiple pressure cushions the tongue anlage, are small, oval swell- on each side. The ciliary groove is un- ings; on the top of these swellings are usually wide, particularly laterally, but one or two moderate sized attenuate this again may be a preservational arti- papillae. The buccal floor arena differs fact. from that of L. hasselti in being fully Diagnostic summary.—See Oreolalax open posteriorly. The BFA papillae pingii (p. 46). rows converge slightly both anteriorly and posteriorly, giving the arena a typi- Leptobrachium oshanensis (Liu) cal oval design. While BFA papillae (Fig. 15) are as numerous as in L. hasselti, they are taller Material—FUNK 49589 (stage 34, and even more attenuate. sv. 12.2 mm). Collected from side pools Three BFA papillae on one side and and pools beneath cascades of small four on the other have terminal divisions. streams at approximately 1-1.1 km eleva- The papillae in the middle of the series tion, Mt. Omei, Szechwan, China; June are much larger than those in the front 15, 1946. or back of the rows. There are one or two small, conical spikes in the pre- Reference.—Liu, 1950 (p. 199-201). External.—Leptobrachium oshanen- pocket positions. These are at the back sis larvae have an enlarged oral disc of a short row of similarly shaped pa- (like many stream tadpoles) but much pillae that extend in a line anterome- of it is denticle free. The usual pattern dially over the lateral arms of the cera- for denticle rows is 4/3, but it is not tohyals. L. oshanensis lacks the papil- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 41

Fig. 15.—Photographs of the floor (above) and roof (below) of the mouth of a Lcptohrachium oshanensis larva. 42 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY late patches seen in L. hasselti in front tiny anterior papillae on the glottal lips. and behind the buccal pockets. There The laryngeal disc is visible as a very is, however, a relatively dense field of wide, transversely oriented, oval ridge. stiff, conical pustulations within the pos- The esophageal funnel is of comparable terior half of the buccal floor arena not size and proportions in the two species. seen in the other species. These pustu- Dorsal buccal.—The roof of the lations extend farthest forward on the mouth has roughly the same proportions midline to about the level of the buccal as in L. hasselti. The upper beak is re- pockets. Posteriorly, they reach the flected posteriorly in L. oshanensis, ob- velar margin and generally increase in scuring about 40% of the prenarial arena size as one goes backwards over the from ventral view. The number of pus- buccal floor. The buccal pockets are tulations in the prenarial arena is re- longer and not as wide as in L. hasselti. duced. The prenarial papillae and narial The bottoms of the pockets are fully valve projections are not quite as tall obscured by massive folds from the pos- as in L. hasselti, but are still far taller terior walls. I could not find clear nat- than in any hylid. The narial valve pro- ural perforations. The free velar sur- jections are displaced slightly laterally. face differs from that of L. hasselti in The median ridge is farther posterior having weak posterior projections rather and the postnarial arena is larger than than medial crenulations over the filter in L. hasselti but not as large as in a cavities and in having a uniform, nar- typical tadpole. The positions of the row, but thickened band of secretory postnarial papillae are as in H. regilla, pits along its posterior margin. A deep not as in L. hasselti. The median ridge median notch is bound by massive and lateral ridge papillae are similar brushes of extremely attenuate papillae. to those of L. hasselti except for being These arise from a double—dorsal and slightly taller and wider. The papillae ventral—medial edge on the ventral that define the buccal roof arena are velum, as in L. hasselti. The numerous like those of L. hasselti in number and papillae are preserved in an anteriorly position, but more attenuate in L. folded direction in this specimen. oshanensis. The largest papillae are an- Ventral pharynx.—The branchial bas- terior. The papillae in the clusters lat- kets are smaller than in L. hasselti. The eral to the BRA are more numerous in filter plates have even less height. this species. The BRA encloses a field

Counts for filter rows run 7, 10, 8, 5 for of stout conical pustulations, which are cb. 1-4. These values are below the very large, stiff, subpapillate structures mean for H. regilla, but none signifi- of only moderate density at the front of cantly. The values for cb. 1 and 2 are the arena. Posteriorly, the pustulations actually above the values for L. hasselti; become both smaller and more numer- this is possible within the smaller bran- ous. The pustulate field ends in a trans- chial baskets of this species because verse line that laterally abuts with the the filter rows are narrower. Filter ca- glandular zone; the glandular zone is nals are slightly more open in L. osha- broadly interrupted medially. The dor- nensis than in L. hasselti. As with L. sal velum is also interrupted in front of hasselti, the branchial food traps are the esophagus but the gap between the covered with secretory pits rather than left and right portions of the glandular ridges and the pits are continuous across zone is twice the width of the gap be- the ventral surface of the ventral velum tween the left and right halves of the and in front of the glottis. The glottal velum. Secretory pits within the glan- lips are larger in this species than in L. dular zone are similar in both species.

hasselti and the glottis is fully exposed The dorsal velum is generally short; it

within the median notch. There are two is anchored on each side of the roof just )

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 43 behind the medial Hmits of the glandu- est buccal papillae in O. pingii have this lar zone. Although it is a free flap both unusual pustulate surface. The most an- lateral and medial to these points, the terior infralabial papillae are very stout medial portions of the dorsal velum are and are divided into four or more pro- relatively immobile. The medial por- jections. Smaller papillae between the tions of the velum are turned backwards main infralabial papillae and the anterior and are lined with long, attenuate pa- pair are absent. The medial pair of in- pillae, twice as many as in L. hasselti. fralabial papillae, between the main Papillae in this general region are not infralabial papillae, are very tall and restricted to the margin of the velum; have two or more terminal subdivisions. they are also prevalent on the pharyngeal As in Leptohrachium, the lingual anlage surface of the velum and on the buccal lacks papillae. The buccal floor arena roof above the medial edges of the is similar to that of L. oshanensis; the velum. BFA papillae are a bit larger. The Dorsal pharynx.—The lateral and me- largest BFA papillae are fused basally dial pressure cushions are completely with their neighbors. Papillae in the confluent. The ciliary groove is very prepocket position and over the lateral wide and shallow. arms of the ceratohyals are like those of Diagnostic summary.—See Oreolalax L. oshanensis in position and shape. Pa- pingii (p. 46). pillate patches are present directly behind the buccal pockets as in L. hasselti, Oreolalax pingii ( Liu although they are not as numerous as in (Fig. 16) that species. The pustulate field within the BFA is more similar to that of L. Material—FMNH 50988 (stage 36, oshanensis than that of L. hasselti, but sv. 25.8 mm). Collected among stones differs from the former in extending far- in slow-running streams at approximate- ther forward on the midline and being ly 2.7-3.4 km elevation, between Hsuan- of overall smaller, blunter, and shenpa and Lolokou (N. 28°0', W. 102° made up less dense pustulations. The far poste- 30') on the road between Sichang and rior portion of this pustulate field has Chaochiao, Sikang, China; May, 1942. the smallest pustulations and the great- Reference.—Liu, 1950 (p. 149-150). est density. The buccal pockets are in- External.—O. pingii tadpoles have an termediate between those of L. hasselti invariant 5/5 denticle pattern. The spir- and L. oshanensis in all aspects that have acle is sinistral. In general appearance been considered; there is a definite small they are similar to Leptohrachium lar- perforation of the pockets in this species. vae. In terms of tail length O. pingii The free velar margin is supported larvae are intermediate between L. has- by thicker spicules in O. pingii than in selti and L. oshanensis. Internally O. either species of Leptohrachium. There pingii larvae are sufficiently similar to are three distinct small, round, posterior the two species of Leptohrachium de- projections of the velar margin on each scribed above that comparison with side. These are similar in position to those species is emphasized in the fol- those of H. regilla but more distinct. lowing description. The median notch and the two projec- Ventral buccal. The buccal floor is — tions that immediately bound it are a more triangular than in either species of bit larger than in L. hasselti, but other- Leptohrachium and the prepocket por- wise similar. The odd, secondary, ven- tion is relatively longer. The infralabial tral edge to the medial portion of the papillae are most similar to those of L. velar margin characteristic of both spe- oshanensis. They differ in being overall — of Leptohrachium is rudimentary smaller and in being covered by large, cies — pointed pustulations. All but the small- in O. pingii. On the ventral side of the NATURAL HISTORY 44 MISCELLANEOUS PUBLICATION MUSEUM OF

the mouth of an Oreolalax pingii Fig. 16.—Photographs of the floor (above) and roof (below) of larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 45 medial portion of the velar margin are surface, but lacks a secondary ridge. The four small, simple, posteriorly directed postnarial arena is average in size. Post- papillae. The lateral pair are the largest, narial papillae (four per side) are posi- but are still too small to reach the velar tioned in oblique clusters as in H. regilla margin and be seen from above. Secre- and L. oshanensis. These papillae are tory pits on the velar margin are as in larger than in L. oshanensis, the largest L. oshanensis. being the most posterolateral. All have Ventral pharynx.—The branchial bas- serrated anterior margins. The lateral flap-like struc- kets of O. pingii resemble those of L. ridge papillae are huge, tures positioned far lateral as in Lepto- hasselti in shape; they are intermediate between those of the two species of brachium, but much larger than in that three, rather than two, Leptobrachium in relative size. Essen- genus, and with terminal projections. The of O. tially there is only one common filter BRA cavity in O. pingii larvae on each side; pingii is anteriorly narrower, but poste- that of L. oshanensis. for it is only far forward, under the riorly wider, than field of velum, that the filter plates of any cerato- Within the arena proper is a two to sized branchial is as tall as its filter rows. to three dozen small medium terminal Counts for filter rows are identical to papillae, most of which have those of L. oshanensis. No characters of pustulations. A small, triangular cluster laterally the the filter themselves serve to distinguish of papillae extends from di- the filters of O. pingii from those of L. posterior portion of the BRA. The oshanensis. Secretory pits could be found mensions of the glandular zone are most only on the ventral surface of the ventral comparable to those of L. hasselti. The species velum. In that regard, O. pingii is no zone differs, however, from either different from the species of Leptobrach- of Leptobrachium in having extremely ium. In terms of the pattern of the pits large and conspicuous secretory pits in front of the glottis, the glottis itself, along its anterior margin. The dorsal and the esophageal funnel, O. pingii is velum is shorter than that of L. oshanen- indistinguishable from L. hasselti. sis and interrupted medially. The anterior margin of the velum is nearly Dorsal buccal.—The buccal roof is transverse except in the neighborhood more triangular in O. pingii than in of the midline, where it is reflected either species of Leptobatrachium. In posteriorly. Papillae are present along size and proportions the prenarial arena the medial half of the velar margin. is intermediate between that of the two These are as numerous as in L. hasselti species of Leptobrachium. There are and intermediate between those of L. two tall, but simple, cylindrical papillae hasselti and L. oshanensis in size. positioned far laterally within the prenarial arena. These project ventrally be- Dorsal pharynx.—A single, trans- tween the main infralabial papillae and versely elongate pressure cushion is pres- the anterior infralabial pair. The inter- ent on each side. These cushions extend nal nares are most similar to those of from the lateral margin of the pharynx L. hasselti. They differ in the following halfway to the medial margins of the ways: the anterior walls are pustulate dorsal velum. Their shorter, anterior- posterior axes are a quarter or less the ( and there is a second prenarial papillae on one side in this specimen); the narial length of their longer, transverse axes. anterior valve projections are not as tall. The The cushions have indented and give median ridge is more posterior in O. medial margins, which them an pingii than in either species of Lepto- autonomy from the dorsal velum not brachium, but still semicircular in shape. seen in any other tadpoles. The ciliary Marginal serrations are very coarse. The groove is similar to that of Leptobrach- median ridge has a pustulate anterior ium. 46 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Diagnostic summary.—The non- is only one lingual papilla in this speci- Megophrys megophrynines form a tight men. It is terminally bifurcated and cluster of species that share the unique laterally expanded, and looks much like character of having multiple, layered two normal papillae that have fused on papillation of the medial portion of the the midline. The buccal floor arena is ventral velar margin. They also tend to very broad. The lateral row of papillae have extremely tall prenarial and post- outlining the arena converge little to- narial papillae and papillation of the ward the midline at either the front or medial margin of the dorsal velum. Lep- the back of the arena. The BFA papillae tobrachium oshanensis can be distin- are average in number, but shorter and guished from L. hasselti by an assort- blunter than in typical hylids. The ment of minor characters. The most larger papillae, i.e., those in the pos- conspicuous of these includes the size terior half of the arena, are flattened of the infralabial papillae and extent of against the floor of the cavity and di- papillation of the medial margins of the rected out away from the midline rather dorsal and ventral vela. Oreolalax can than medial as in most other tadpoles readily be distinguished from the species examined. This unusual orientation may, of Leptohrachium examined by the un- in part, result from shrinkage following usual pustulation of its buccal papillae. preservation. The two largest BFA papillae on each side have terminal bifur- HYLIDAE cations. Some three dozen small, blunt Anotheca spinosa Steindachner pustulations and tiny papillae are scattered about in the posterior half of the (Figs. 17,18) BFA. A half dozen similar projections Material—K\J 60017 (stage 37, sv. are above the lateral arms of the cerato- 14.5 mm). Collected in tree hole con- hyal outside of the arena. The buccal taining approximately 60 ml of water at pockets are short, slender, and more 1600 m elevation, Vista Hermosa, Oa- obliquely oriented than those of a typi- xaca, Mexico; August 12, 1960. cal hylid; they are not perforated. The

Reference.—DueWmsin, 1970 (p. 149- free velar surface is very much reduced. 150). Supporting spicules are thin and short. External.—Anotheca spinosa has The posterior margin of the velum is transverse very faint stout, muscular larvae with very broad predominantly with crenulations projecting posteriorly over beaks and a 2/2 denticle pattern in early shallow stages. The upper rows of denticles tend the first two filter cavities. The notch is so broad that it covers to disintegrate in later stages. The spir- median no less than half of the velar edge. Se- acle is sinistral. cretory pits could not be found on the Ventral buccal.—The floor of the margin and are likely absent. mouth in the frontal plane is roughly an Ventral pharynx. The branchial bas- equilateral triangle. Two distinct pustu- — kets are greatly reduced. The filter plates lations are aligned directly behind the are reduced in all directions, although keratinized beak on each side. Behind they still retain height. Vestiges of these and about halfway between the some filter rows are present as thin, irregular symphysis and the articulation of the folds of epithelium. These number 3, 3, infralabial cartilage with Meckel's carti- 3, 2 for cb. 1-4. Only the main folds are lage is an infralabial papilla on each present. The filter canals are completely side; the papillae are shaped like slightly compressed cylinders and point antero- open and two to four times as wide as dorsally. Secondary, stubby, terminal the vestiges of the filter rows. Branchial projections on the papillae number five food traps are absent; that is, no orga- on one side and four on the other. There nized secretory ridges could be resolved ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 47

Fig. 17.—Drawings of the floor (above) and roof (below) of the mouth of an Anotheca spinosa larva. .

48 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

anywhere in the pharynx. The glottal pressed in the sagittal plane and col- slit and lips are large and vertically lapsed asymmetrically against the buccal oriented. They are 50% under the velar roof in this specimen. Anterolateral to margin. The glottis sits on a large, the median (ridge) papilla and within gently domed, laryngeal disc. The the postnarial arena are fifteen to twenty esophageal funnel is of enormous width pustulations and a single, simple pa- and extremely broad profile. pilla. Posterolateral to the median Dorsal buccal.—The roof of the (ridge) papilla are two typical lateral mouth shares the equilateral triangular ridge papillae. The buccal roof is devoid shape of the floor of the mouth. The of any papillae that could outline a buc- lateral margins of the roof, however, cal roof arena. A hundred or more blunt curve downward more than in other tad- pustulations, including a few stubby sub- poles examined, giving the roof consid- papillate projections, cover the buccal erable depth. The internal nares and roof proper. I could not resolve a glan- median ridge are far forward on the dular zone. The dorsal velum is completely buccal roof. The prenarial arena is twice absent. as broad as long. Two tall, knobby pro- Dorsal pharynx.—Without a dorsal jections with blunt apices arise from velum the buccal and pharyngeal roofs the middle of the prenarial arena. The are completely confluent. There are no tips of these projections are turned pos- pressure cushions. teriorly. The stout common pedestals Diagnostic summary.—Anotheca lar- for these projections bow forward on the vae are uniquely different from all other midline and extends back on each side tadpoles examined in the following fea- as ridges that become continuous with tures: single medial lingual papillae; the posterior wall of the internal nares. gigantic median notch and ventral velar

The internal nares are shallow slits, margin; filter rows reduced to thin, sin- more elongate and oblique than in a gle folds; dorsal velum and dorsal typical hylid larva. The far anteromedial pharyngeal features absent. corners are pustulate flaps. Anterior Gastrotheca riobambae (Fowler) walls are effectively absent except laterally where there are some blunt pus- (Fig. 19) tulations and a distinct, pustulate, pre- Material.—Author's collection (stage narial papilla on each side. The posterior 37, sv. 20.6 mm). Laboratory raised; narial walls each have a slight to mod- Mus. Nat. Hist. Univ. Kansas. erate narial valve projection, but the References.—Hoogmoed, 1967; Duell- projections are in the middle rather than man, 1974. at the anteromedial end of the posterior External.—G. riobambae larvae are wall. There is a deep groove that sep- large, with dorsolateral to nearly dor- arates the posterolateral portion of the sal eyes, a 2/3 denticle formula, and posterior narial wall from the postnarial sinistral spiracle. Tadpoles of this species arena on each side. It is not clear are often known under the name Gastro- whether the posterior narial walls of A. theca marsupiata (see Duellman and spinosa tadpoles would be eflScient as Fritts, 1972 and Duellman, 1974, for the valves. The postnarial arena contains most recent discussion of the systematics two tall, straight papillae that project of the genus ) anterolaterally under the narial valve Ventral buccal.—The width to length projections. These have pustulate apices ratio for the mouth is typical for a hylid and some sign of terminal bifurcation. tadpole but the floor is noticeably round- The median ridge is reduced to a tall er than in most species examined. There papilla with an expanded base and a are four infralabial papillae in a trans- pustulate anterior margin. It is com- verse line. The medial pair consists of ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 49

Fig. 18.—Photographs of the floor (above) and roof (below) of the mouth of an Anotheca spinosa larva. 50 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 19.—Photographs of the floor (above) and roof (below) of the mouth of a Gastrotheca riobambae larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 51 moderately tall, finger-like projections. forward by a relatively gigantic laryn- The lateral two are shorter and may be geal disc. The projections are covered considered bipartite. On each side dor- with dense, conspicuous secretory pits. sal to the infralabial papillae, in the Ventral pharynx.—The branchial bas- angle between the upper and lower kets are long and deep. The baskets beaks, is a small, but distinct kerati- overall have a more circular, rather than nized spur. These spurs are directed typically oval, dorsal profile. This shape anteriorly and separate from the main seems to reflect modifications of the keratinized beaks. They are just far third filter cavity. The tiny, third filter enough back inside the mouth so that cavity, as viewed from above, is a nearly they cannot contact a smooth substrate closed chamber capped by the imbricat- when the lower jaw is fully depressed. ing, curved dorsal margin of the filter G. riohamhae has four lingual papillae. plate on cb. 3. Filter plates of cb. 1 and The two tallest are near the midline; the cb. 2 are relatively long; plates of cb. 3 other two are slightly shorter and pos- are exceptionally tall. Counts for filter terolateral to the medial pair. The buc- rows are very near the mean for H. cal floor arena is wide. The BFA pa- regilla, but filter rows are wider with pillae series is continuous posteriorly longer secondary folds. Filter canals are across the midline. I counted 17 BFA of typical proportions. Filter rows at papillae on one side, 19 on the other; the bottom of the plates lining filter only nine rather small BFA papillae are cavities 1 and 2 are fused, not only with anterior to the buccal pockets. The neighboring rows on each plate, but with papillae behind the pockets are not in the abutting filter rows of the opposing tight rows but spread out laterally to plate. Thus, the gill slits are completely cover the region of the buccal floor be- obscured from dorsal view and water tween the median ends of the buccal that enters those two filter cavities must pockets and the front of the second filter pass through individual filter niches in cavity. The four largest papillae, viz. order to reach the atrial chamber. The those just medial to the buccal pockets, branchial food traps of G. riohamhae show basal bifurcation; a few of the cover a disproportionately large area in other larger papillae have minor pustu- the anterior portions of the filter cavities. lations along their sides. Posterome- Secretory ridges are of greater absolute

dially within the arena is a pair of small size and height than in a typical hylid papillae. There are also about sixty tiny, tadpole, but whether this difference is faint pustulations randomly dispersed significant could not be determined. within the caudal two-thirds of the While the glottal slit and glottal lip pro- arena. G. riohamhae has typical pre- portions are not unusual, the glottis in pocket papillae. The buccal pockets are G. riohamhae differs from most other wide, with a strongly oblique orienta- tadpoles examined in having a predomi- tion. The pockets are shallow and per- nantly vertical orientation. The glottis forated. The free velar surface is long, sits on a huge, but not very conspicuous supported by spicules; the posterior pro- laryngeal disc. G. riohamhae has esoph- jections of the velar margin are also long. ageal funnel of very broad profile. The projections associated with the third Dorsal huccal.—The roof of the filter cavity are displaced medially. All mouth of G. riohamhae is broad ante- pairs of projections are directed postero- riorly and quite round. The nares and medial. The single pair of projections median ridge are positioned far back on surrounding the median notch are thick- the buccal roof, resulting in relatively er than the rest of the velar surface; they large pre- and postnarial arenas. The are directed dorsad because the mid- caudal haff of the large prenarial arena

portion of the velar margin is forced is filled by a gentle, upside-down, U- 52 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY shaped depression of the rostrum. Pus- dorsal velum is average or a bit larger tulations are absent within this arena. than average for a hylid tadpole; the The internal nares are transversely ori- gap between the left and right sides of ented, quite small, and nearly as wide as the dorsal velum is great. long. The walls, particularly the medial Dorsal pharynx.—G. riobambae has portion of the anterior wall, are very two large and conspicuous pressure thick. Pustulations are few and faint on cushions, obliquely oriented on each the anterior wall; prenarial papillae are side. The lateral cushions are the larger absent. Narial valve projections are very and rounder, and the medial cushions slight. A deep groove separates the poste- are of subequal width to the lateral pair. rior narial wall from the postnarial arena. The ciliary groove is not noticeably dif- Postnarial papillae are typical in posi- ferent from that of any typical hylid tion and number, although with pustu- larva. late anterior margins. The median ridge Diagnostic summary.—Gastrotheca is not unusual in shape or marginal riobambae has: ventral fusion over the sculpturing, but lacks pustulations or a gill slits of the filter rows from neigh- secondary ridge on its anterior surface. boring filter plates; a medially directed Within the postnarial arena are three spur on each side at the front of the or four tiny, blunt papillae. One is lo- mouth and four lingual papillae. Cur- cated medially in the anterior half of the sory examination of larvae from other arena; the remaining ones are aligned Gastrotheca species (G. monticola, KU transversely just in front of the median 142847, N = 1, stage 35; G. marsupiata, ridge. The lateral ridge papillae are KU 139442, N = 4, all stage 36) sug- slightly compressed into the sagittal gest that these features characterize the plane. They are bifurcate, with shorter genus not the species. In G. marsupiata anterior and taller posterior projections, the fusion of the filter rows, however, is and have very tiny pustulations on their incomplete in the posterior portion of anterior surfaces. The BRA is well de- the filter cavity. fined—oval in shape with a truncated Sonnini Latreille anterior margin—by a continuous arc of Hyla femoralis & no less than 16 papillae. These papillae (Fig. 20) are simple and moderate in size. In Material. — Uncatalogued, author's general, BRA papillae are evenly spaced collection (stage 36, sv. 16.0 mm). Col- in single file; however, in the postero- lected from small pond, 1.25 km NE lateral margins of the arena there are Florida Technical Univ., Orange Co. one or two small secondary papillae Florida; August 12, 1975. neighboring the main row. Fifty to one Reference.—Wright, 1932. hundred small, pointed pustulations are External.—This is possibly the most randomly dispersed within the arena. beautiful tadpole in North America. This Three or four small, pointed papillae specimen has a tall tail fin, which is al- may be found clustered along the far most as tall as it is long, and ends in a lateral margins of the buccal roof. The pointed flagellum. The denticle pattern glandular zone of G. riobambae is naris 2/3; the spiracle is sinistral. row and tends to be of a uniform width Ventral buccal.—H. femoralis is so across the buccal roof. Secretory pits similar to H. regilla that only differences are very conspicuous and large, as were are emphasized in this description. The the secretory ridges in the ventral floor of the mouth is slightly broader pharynx; the apparent accentuation of posteriorly in H. femoralis than in H. larval secretory tissue in this species, regilla. The infralabial papillae are however, may not be significant when smaller and narrower. The lingual pa- overall size is taken into account. The pillae are positioned far forward and ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 53

Fig. 20.—Drawings of the floor (above) and roof (below) of the mouth of a Hyla femoralis larva. 54 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY almost touch the infralabial papillae. The indistinguishable in shape from that of buccal floor arena is an oval area well H. regilla, except that the dorsal pharyn- defined by 11 papillae on one side, eight geal region is longer. In the center of on the other. The two to three largest the prenarial arena descends a bulge papillae on each side, those directly me- approximately twice as wide as the mini- dial to the buccal pockets, arise from a mum distance between the internal common ridge-like base. Approximately nares. The bulge has a distinctive an- 20 pustulations occur in the posterior terior arched margin which is lined with half of the BFA. Four to six large pustu- a half-dozen blunt pustulations (similar lations /subpapillate structures are dis- structures are seen in Smilisca sordida). persed on the buccal floor anterior to the The internal nares are identical to those buccal pockets. The buccal pockets are of H. regilla in proportion, shape, orien- shallow. The floor of each pocket is tation and valvular structure. The pre- completely obscured by a large fleshy narial papillae however are smaller than fold from its dorsal wall. Any perfora- those of the average H. regilla. The tion of the floor of the buccal pockets median ridge is small and has a pustu- must be relatively small and very me- late irregular margin. Two large papil- dial. The free velar surface is slightly lae with strongly pustulate edges lie longer than in H. regilla. halfway between the median ridge and Ventral pharynx.—The branchial bas- the internal nares. Smaller papillae arise kets are larger than those of H. regilla. from the base of these large papillae on The posterior margin of the baskets are their anteromedial side. There are two elongated, reflecting elongation of the large pustulations in the anterior portion second and third filter plates. The second of the postnarial arena and a large bi- and particularly the third filter plates are cusped subpapillate projection in the noticeably taller in this species. The middle of the posterior part of the post- third filter plate has an arched dorsal narial arena. There is a large, flap-like, margin which curls medially and nearly laterally compressed, irregularly shaped completely covers the third filter cavity. projection in the typical position of the Filter counts cb. 1-4 were: 11, 11, 14, lateral ridge papillae on each side. The 17; these are all well above the counts buccal roof has three distinct papillae for H. regilla at any stage. Filter rows on each side arranged in an oblique row abut completely; the filter canals are (anterolateral to posteromedial). These

narrow and hidden from view. The fil- define the lateral bounds of the BRA. ters have a fully developed mesh made There is a single tiny papilla located far up of secondary, tertiary and higher laterally on the buccal roof. Approxi- order filter folds. Among the hylids ex- mately fifty pustulations are distributed amined only Agalychnis had a filter mesh between the median ridge and the pos- that was denser. Branchial food traps terior quarter of the BRA. The more are necessarily large, covering the ven- posterior pustulations are smaller and tral surface of the ventral velum and more numerous. Three to four pustula- much of the anterior region of each tions occur on the buccal roof lateral to filter cavity. A pattern of well organized the BRA. The glandular zone is rela- secretory ridges could be observed on tively narrow and slightly longer later- the underside of the ventral velum. The ally than medially. It is made up of glottis is of average size and only a large distinct secretory pits. The dorsal quarter covered by the margin of the velum is of comparable size to that of ventral velum. The lips are slightly H. regilla. It is barely continuous across heavier than those of H. regilla. The the midline. esophageal funnel is narrow. Dorsal pharynx.—The pressure cush- Dorsal buccal.—The buccal roof is ions are large obliquely oriented swell- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 55 ings. The lateral pressure cushion is the terior papilla on each side appears to be larger. The medial pressure cushion has the homologue of the infralabial papilla itself a medial swelling presumably a in species that have only one per side. pressure cushion for the third filter cav- This papilla is a large, transverse, slight- ity. The ciliary groove is a large open ly conical fan. It has a constricted base trough. and strongly papillate margin. The sec- Diagnostic summary.—The oral cav- ondary marginal papillae, numbering ity of H. femoralis is very similar to that four and six per side, are further deco- of H. regilla but can be distinguished rated with yet finer jagged projections. from the latter species by larger bran- The BFA is demarcated by many small chial baskets, taller filter plates and papillae and pointed pustulations. In ad- denser gill filters. Papillation and pustu- dition to having papillae outlining an lation is slightly more extensive in H. ovoid BFA, a transverse row of papillae femoralis than in H. regilla. above the junction of the ceratohyals and hypobranchial plates splits the arena Hyla rufitela Fouquette into anterior and posterior portions. I (Figs. 21, 22) counted thirteen BFA papillae on one Material. — Uncatalogued; author's side and fifteen on the other. Little weight can collection (stage 36, sv. 15.4 mm). Col- be given these counts, how- lected in grassy pools on the edge of the ever, because of great diflBculty in as- town Rincon de Osa, Puntarenas, Costa sessing what is a "miniscule papilla" versus a "subpapillate Rica; March 3, 1970. pustulation" in this particular species. Larger Reference.—DueWman, 1970 (p. 243- projections that are 244). unquestionably of "papilla" proportions tend to be small, com- External.—This tadpole is propor- pressed cylinders; three had terminal bi- tioned like most "generalized" hylid lar- furcations. The largest papillae are in vae. The spiracle is sinistral. These tad- the transverse poles are otherwise unusual in having a row and pointed anteriorly. The concentration of 2/4 denticle pattern. pustulations and papillae elsewhere on the buccal Ventral buccal.—The interior of the floor, including lingual papillae and pre- mouth has a rounded appearance though pocket papillae are typical of hylid lar- the width to length ratio for the oral vae. The buccal pockets are long and floor is average. This species has super- very obliquely oriented, with a predomi- numerary infralabial papillae, eight per nant angle of 30° from the transverse side in the specimen at hand. Of the plane. The pockets are definitely per- eight, three are far anterior, stubby, forated, but the slits are obscured from blunt and with auxiliary pustulations; dorsal view by strong forward projec- these form a transverse row on each tions of the mediodorsal portion of the side. The largest of the three is nearest posterior pocket walls. The extensive to the midline. Immediately behind the free velar surface is supported by long, middle of these is a wide, blunt papillae thin spicules that nearly reach the velar of medium size. Posterior to this are margin, which is a relatively smooth three compressed papillae with jagged broad arch. Marginal projections over margins which form a second transverse the filter cavities are single, faint peaks. row. The middle papilla of this poste- The medial portion of the velar margin rior row is of the same size as the pa- is the smoothest segment, with only the pillae in the front row; the other two tiniest are much smaller. The last infralabial median notch. A very narrow papilla on each side is behind the second band of moderately large and distinctive row, and it is the largest of all eight secretory pits lines the dorsal surface of papillae. Topographically the most pos- the velar margin. The pits are absent 56 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

a Hyla larva. Fig. 21.—Drawings of the floor (above) and roof (below) of the mouth of rufitela ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 57 lateral to the tip of the spicule over cb. pockets the anterior narial wall has one 2 and in the immediate neighborhood of to three tiny, pointed prenarial papillae the median notch. and pustulations. The narial opening is Ventral pharynx.—The branchial bas- a large elongate oval, oriented a bit obliquely than in typical hylid lar- kets in toto, and the filter cavities in more narial tall particular, are large, despite the fact vae. The posterior walls are Narial that the w^idth to length ratio for the with an arched ventral margin. valve projections have pustulate apices branchial baskets is not unusual. The that extend forward part way under the increased size is reflected in counts of unusual prenarial vacuities. There are filter rows, viz. 9, 11, 11, 9 for cb. 1-4. These are higher than for most hylids six to eight postnarial papillae, with examined, the count for cb. 4 significant- additional pustulations; these loosely aligned in a broad, anteriorly directed ly so. Ratios of length to height for the papillae are all rather small, filter plates are not great. Thus, al- "V." The though the plates are longer, they are subequal, blunt cylinders. The larger are the more posterolateral and tend to not taller. The filter mesh is dense; filter terminal pustulations. rows are wide and secondary filter folds have The median are long. There are few partial filter ridge is more rectangular than triangular. Its free is slightly rows. The filter canals are fully cano- margin sculptured pied. The branchial food traps are long with faint serrations; a few pustulations occur on the ventral half of the anterior because the velar surface is large. The surface. Lateral ridge papillae are traps, however, do not cover a great ver- shaped like halves of crescents with their tical area and are presumably limited by the shallowness of the branchial baskets. peaks pointed medially. Their longer, Secretory ridges are visible through the more anterior margins are strongly ser- velum. These are extremely uniform in rated. Two or three tiny, pointed pa- spacing and shape and continuous above pillae are found in the lateral margins of the buccal roof, but they do not de- all the filter cavities on each side. The fine a BRA. Instead, there are 200 or glottis is 80% blanketed by the ventral small pustulations evenly spaced velum. The glottal lips are of uneven more thickness (thickest posteriorly) but of in the middle third of the buccal roof. typical elevation. The esophageal funnel These thin out laterally. The glandular has a slightly narrower dorsal profile zone is made up of large, distinctive secretory pits. zone, overall, is short than in typical hylid larvae. The and of uneven length. The zone is long- Dorsal buccal.—The buccal roof has est laterally and nearly absent on the the same general positioning of major midline. The dorsal velum is of normal features, such as nares and median proportions or of slightly greater lateral ridge, of most hylids; specific regions, length than in other hylids examined. It however, differ grossly. In the middle extends across the midline as a low, but of the prenarial arena is a small trans- movable flap-like ridge. verse pustulate row, or low ridge, no wider than the internarial distance. The Dorsal pharynx.—Pressure cushions are anterior narial wall makes a full loop present as two large, obliquely ori- into the prenarial arena on each side, ented bulges on the posterior surface forming huge vacuities with high, thick, of the dorsal velum on each side. These pustulate walls. Although these pockets are more distinctive than those seen in are attached to the internal nares, they other species of the genus. The lateral are cul de sacs with smooth round bot- cushion is the longer; the medial cushion toms. These structures may be Jacob- is the rounder. Medial to the inner cush- son's organs, but they have not been ion on each side is a small roll in the seen in any other hylids. Lateral to these dorsal velum which may be a vestige of HISTORY 58 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL

of a Hyla rufitela larva. Fig. 22.—Photographs of the floor (above) and roof (below) of the mouth ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 59 a third cushion. Behind the pressure notch over the glottis, but no distinctive cushions are comparatively broad, shal- marginal papillae. low ciliary grooves. Ventral pharynx.—The branchial bas- Diagnostic summary.—Hyla rufitela kets are oval, almost round, in dorsal differs from all other tadpoles examined view with a length to width ratio of by the development of large cul de sac about 1. They are of average depth, vacuities extending anteriorly from the compared to other hylids of similar size. anterior narial walls. The first and second filter cavities are quite open and fully exposed from Hyla dendroscarta Taylor above. The third filter cavity, however, (Fig. 23) is small and largely hidden by the im- brications of the filter plates the third Material.—MVZ uncatalogued ( stage on 26, sv. 12.0 mm). Collected from large ceratobranchial. The dorsal margin is bromeliad by the road at 1400 m eleva- straight on the second filter plate, but tion (Highway 150), approximately 5 km has a distinctive apex on the third filter W Orizada, Vera Cruz, Mexico; Sept. 16, plate. I counted: 10 filter rows on cb. 1972. 1; 10 on cb. 2; 10 on cb. 3; 7 on cb. 4. Reference. — Duellman, 1970 (p. The filter rows are particularly dense 436). and thick at the base of the branchial External.—Hyla dendroscarta larvae baskets. They are packed such that are extremely elongate, with a dorsoven- without subjecting them to extreme ma- trally flattened body and a sinistral spir- nipulation they completely obscure the gill slits Partial filter acle. The denticle pattern is 3/4. in dorsal view. rows are short. The density of the Ventral buccal.—The buccal cavity filters at the base of the filter rows, is an is squarish, rather broad anteriorly. The unusual feature; the filter density overall infralabial papillae are simple pads that is slightly less that of typical pond hy- lack secondary papillae and pustulations. lids, largely due to more open filter They are of moderate size and just touch canals. The ventral surface of the ven- on the midline. There are two, typical, tral velum is covered by secretory tissue, lingual papillae. The BFA is well de- evidenced by its buffed texture and marcated by two nearly straight rows of staining properties. The branchial food papillae that converge posteriorly to traps are relatively short and well or- form a "V." I counted eight on one side ganized secretory ridges were not ob- and nine on the other, with an equal served. The glottis is well developed number of pustulations arranged along particularly for a tadpole of this stage. the same general line as the papillae. The glottis lies more than half way under Some small additional papillae occur the margin of the ventral velum but is lateral to the posterior margin of the still fully visible in dorsal view because arena. All the papillae have sharp of a large notch above it. The pharyn- apices. The central region of the arena geal disc is not particularly elevated. A is bare. The prepocket region is bare. tiny papilla projects up from the front Careful manipulation failed to reveal of the glottal lips where they meet on open buccal pockets at 50 X magnifica- the midline. This is completely hidden tion. The free velar surface is of average in the undistorted specimen by the ven- length for typical pond larva, but has a tral velum. relatively dense glandular margin. Indi- Dorsal buccal. vidual secretory pits could not be re- —The roof of the mouth shares with the floor a generally solved at 125 X- Supporting spicules appear to be relatively short but the mar- squarish shape. The nares and median gin appears quite stiff. There are a few ridge have a typical position in the minor crenulations and a deep median mouth for hylid larvae. There is a small 60 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 23.—Drawings of the floor (above) and roof (below) of the mouth of a Hyla dendroscarta larva. —

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 61 medial swelling in the prenarial arena. readily characterizes this larvae. This In the middle of this swelling are two, feature, however, may simply reflect the short, blunt papillae oriented on a trans- early ontogenetic stage of this specimen verse line and adjacent to each other at (H. dendroscarta larvae are rare in col- the midline. The nares are obliquely lections and this was the largest speci- oriented with a slightly swollen rim sur- men available for study. The specimen rounding them both anteriorly and pos- was 40% longer than a free-living, feed- teriorly. A few minor pustulations arise ing, stage 25 individual also examined). from the lateral portions of the narial Several less questionable, but also less wall, but prenarial papillae proper are obvious features collectively distinguish absent. The narial valves are large free this larvae from others examined. These flaps with a distinctive projection aris- include: simple, blunt infralabial pa- ing between the midpoint and the me- pillae in association with tall, attenuate dial margin of the posterior wall. The BFA, BRA and lingual papillae; absence postnarial arena is triangularly shaped of obvious secretory pits or ridges in and is defined anteriorly by a short row branchial food traps, presence of papilla of papillae, two on one side and three at anterior edge of glottis; thickened rim on the other, plus a relatively small me- around naries. dian ridge posteriorly. The short median Hyla phlebodes Stejneger ridge has three distinctive projections with the single medial one most distinc- (Fig. 24) tive. Lateral to the ridge are median Material—KU 68405 (stage 31, sv. two attenuate lateral ridge papillae, one 7.3 mm). Collected in forest pool at of which has a secondary pustulation 100 m elevation, Puerto Viejo, Heredia, its base. lateral near These ridge pa- Costa Rica; July 15, 1961. pillae are in line with two rows of buc- Reference.—DueWman, 1970 (p. 222). cal roof papillae that extend backward External. — Hyla phlebodes (like in almost parallel lines. Pustulations are other members of the Hyla microceph- lacking in the postnarial arena but are ala species group) is characterized by a quite evident in the BRA. The BRA is tail that terminates in a long pointed a tall trapezoid with the median ridge filament, tiny recessed beaks, and the and the lateral ridge papillae forming absence of denticles and oral disc pa- the wider base. Seven tall papillae, all pillae. The spiracle is sinistral. lacking secondary pustulations, form the Ventral buccal.—The trend toward BRA papillate rows on each side. Pa- reduction of oral structures seen exter- pillae and pustulations are lacking else- nally is continued internally; this reduc- where on the buccal roof. The glandular tion is greater in H. phlebodes than in zone is short with a relatively uniform other Hyla larvae examined. The floor length from the lateral margin of the of the mouth is disproportionately elon- roof of the mouth to the midline. gate anterior to the buccal pockets. Be- Dorsal pharynx. The dorsal velum — cause of the tiny beaks the mouth comes is also short with two, distinctive, round to an acute anterior termination. Single, pressure cushions of subequal size. The relatively huge, infralabial papillae on dorsal velum is absent on the midline. each side overlap one another at the The esophageal funnel has a narrow pro- midline. These are roundish, slightly file. The ciliary groove is barely visible antero-posteriorly compressed structures, laterally but it is a distinct, open trough which lack any secondary projections. as it leads into the esophagus. Each is larger than the oral orifice. Diagnostic summary.—The varying There are no other papillae anywhere density of gill filters—very dense ven- inside the mouth. The only surface trally and much less dense dorsally features arising from the buccal floor 62 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Hyla phlehodes larva. Fig. 24.—Drawings of the floor (above) and roof (below) of the mouth of a ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 63

are five or six tiny pustulations above A discrete anterior margin for the secre- the lateral portion of the cerato- tory zone could not be resolved, al- hyal on each side. The buccal pockets though tiny secretory pits are present are tiny, shallow and unperforated. They posteriorly in the esophageal funnel. extend back from the midline at a great Remnants of a dorsal velum are present angle. The free velar surface is very as two tiny, asymmetric, anteriorly di- short and unsupported by spicules. The rected flaps. These flaps are completely trailing edge is a smooth curve without absent both in front of the large esopha- any posteriorly directed projections al- geal funnel and laterally; in total they though a large, deep, median notch is traverse only a quarter of the mouth. present. Secretory pits could re- not be Dorsal pharynx.—The two small flaps solved on the velar margin and are prob- identified as remnants of the dorsal ably absent. velum are far posterior and a dorsal Ventral pharynx.—The branchial bas- pharynx is essentially absent. Pressure kets are reduced in all planes. Filter cushions are not present and the ciliary plates are practically absent. Knobs on groove is a tiny crease behind the ves- the gill bars, vestiges of filter rows, line tigeal dorsal velum. the gill slits. These "filter rows" num- Diagnostic summary.—Some material ber 4, 5, 5, 3 for ceratobranchials 1-4 of Hyla microcephala has been available respectively. Filter folds are absent. for study; in that no major differences There is little space left for branchial were found between H. microcephala food traps in the shallow pharynx, and and Hyla phlebodes, the following diag- they may be absent. Secretory ridges, if nosis can stand as a diagnosis for the present, restricted to would have to be H. microcephala species group as a the ventral surface of the velum, but whole. These larvae can be distin- could resolved that surface. none be on guished from all other tadpoles exam- large glottal slit fills A the median notch ined by the unique knob-like vestiges of of the velum. The slit sits on well- the filter rows on the diminutive cerato- developed, elevated lips and is fully branchials. In addition, H. phlebodes exposed when viewed from above. There has the most massive, and unusually is a large, unelevated laryngeal disc. shaped, ceratohyals (and associated Behind this extends a broad esophageal musculature) of any Hyla examined. funnel. The following selected features in com- Dorsal buccal.—The buccal roof, like bination further diagnose this species: the buccal floor, is elongate. The nares large, medially, overlapping infralabial are far anterior and the prenarial arena papillae; buccal papillae absent; glottis is proportionally small. Surface struc- large; branchial baskets very small and tures are absent in the prenarial arena. filter row remnants few in number; se- The internal nares are small slits oriented cretory ridges absent; esophageal funnel at an angle 35° from the transverse large. plane. The narial walls are not tall and lack any sculpturing such as prenarial Hyla mixe Duellman papillae or narial valve projections. Not (Fig. 25) quite halfway back on the buccal roof

are two single pustulations, one each Material—KU 104183 (stage 28, sv. aligned directly behind the lateral mar- 11.8 mm). Collected attached to small gins of the nares. With intense staining stones in gravel-bottom pools in cascad- some faint pustulations may be seen on ing small stream on N slope of the Sierra the middle posterior portion of the roof. de Juarez, 4.2 km S of Compamento The buccal roof is otherwise devoid of Vista Hermosa, Oaxaca, Mexico; Feb- any ridges, pustulations, papillae, etc. ruary 16, 1966. 64 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 25. —Drawings of the floor (above) and roof (below) of the mouth of a Hyla mixe larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 65

Reference.—DueUman 1970 (p. 426- larger papillae have bumps or pustula- 427). tions about halfway from their base. The External.—Tadpoles of this genus papillae are virtually all curved; those in have a relatively huge, ventral, oral disc the typical BFA position are curved an- with a 7/10 to 7/11 denticle pattern. teromedially; those in the prepocket The spiracle is sinistral. position arch directly posterior over the buccal pockets. Anterior to the fringe Ventral buccal.—The width to length the buccal floor is void of pustulations ratio of the whole oral cavity reveals a or projections. Behind the fringe are relatively short oral cavity in this spe- secondary transverse rows of very small, cies. These tadpoles have the most ex- anteriorly curved papillae. These treme proliferation of internal oral pa- rows are made up of five papillae pillae seen in any Hijla. Five small on one side and four on the other. posteriorly directed papillae are present They are restricted to the areas at the anterior limit of the infralabial between the base of the region. These are evenly spaced imme- spicules of cb. 2 and cb. 3 on the most posterior part of the non-velar diately behind the keratinized beak. buccal floor. The buccal pockets are slender Two, major, fringed flaps are behind this and transversely elongate. They are row and quite similar in shape and posi- deep and each is occluded by a large, ante- tion to typical hand-like infralabial pa- riorly directed fold arising from the pos- pillae. These later papillae are wide, terior dorsal surface of the and their secondary marginal papillae pocket on each side. The overhanging papillae (four per side) are long and attenuated. from the prepocket portion of Fine tertiary divisions of the marginal the papillae wall on the buccal floor further papillae are present on both sides. Two obscures the entrance pustulations are present adjacent to the to the buccal pockets. It is doubtful that the midline between the major pair of in- pockets are perforated this fralabial papillae. No other symmetrical in species. Although the ratio of length projections neighbor the midline in the the of the mouth to the immediate region behind these pustula- maximum length of the velum is within the range for tions, so they may be the homologues of more typical hylids; the total velar area the lingual papillae despite their rela- may actually be a bit larger. The supporting spicules are tively anterior position and small size. relatively heavy and long. They reach The buccal floor arena is sharply de- the posterior margin of marcated posteriorly and laterally by a the velum, causing protuberances in the velar continuous fringe of 70 small to medium- margin visible from sized, pointed papillae. The fringe be- above. Four undulating peaks on the velar gins far laterally in front of the buccal margin are distinctly leptokurtic; they point pockets, curves mesad around the end posteromedially rather than posteriorly. of the pockets, and continues obliquely Two auxiliary peaks neighbor the median to a point on the midline just anterior notch. A few small secretory to where the free velar surface begins. pits were seen on the dorsal The BFA papillae and prepocket pa- surface of the posterior edge of the velum, but the pillae series are thus connected. This overall density or anterior extent of the secretory pits line of papillae is occasionally two pa- could not be assessed. pillae wide along its length. The papillae in the anterolateral and posteromedial Ventral pharynx.—The branchial bas- portions of the BFA are the shortest. kets are relatively short, and this may The tallest papillae are immediately me- account for the appearance of shorten- dial to the buccal pockets. A very few ing in the whole oral cavity. The most of the larger papillae exhibit bifurca- extensive reduction is in the fourth cera- tions near their bases. Many of the tobranchial. Compared to other mem- 66 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY bers of the genus, the branchial baskets of the cone near its pointed tip. Directly are shaped as if they were pushed out- in front of the internal nares are single, ward along their posteromedial margin. small, thin papillae, one on each side. The third filter cavity is a slim, deep No other structures are present in the pocket concealed by the recumbent dor- prenarial arena. The internal nares are sal margin of the filter plates on cb. 3. 3 1/2 times wider than long (length Because the branchial baskets are short measured along longer axis), significant- while the velum is not, the filter cavities ly longer than in more typical hylid lar- are blanketed more fully by the velum vae. The angle made by the long axis than in most species examined. Less of the internal nares from the transverse than 10% of filter cavity 3 lies behind the plane (45°) is very large. The anterior trailing edge of the ventral velum. In narial walls are characterized by a few terms of relative height of the filter knobby pustulations and a single tiny pa- plates and numbers of filter rows (i.e., pilla on each side very near the antero- cb. 1 = 10, cb. 2 = 10-12, cb. 3 = 9-10, medial corners on each side. The poste- cb. 4 =r 4-5), Hijla mixe is not signifi- rior wall is not very tall and completely cantly different from more typical hylid lacks a narial valve projection. Each larvae. The filter mesh is less dense. side of the postnarial arena is bound by Secondary and finer filter folds are thin a straight row of three attenuate postnar- and the space between neighboring filter ial papillae. These rows are oriented rows is large. Thus, the filter canals nearly parallel to the sagittal plane, but may be slightly more open in H. mixe with their most anterior papillae slightly than in other congeners. The large, stiff closer than their posterior papillae. The spicules made exploration of the ventral three papillae on each side increase in velar surface particularly difficult and size from front to back. The largest one I could not resolve secretory ridges any- is as tall as the conical protuberance in where under the velum. However, in the prenarial arena. The two other pos- this specimen broad bands of light, floc- terior papillae in each row arch slightly culent food matter were adhering to the medially and have secondary pustula- ventral surface of the velum parallel to tions on their anterior margins. In the the posterior velar margin, suggesting position of the median ridge is a single, the presence of some organized secre- tall, extremely attenuate papilla which tory tissue in this region. The glottis is curves slightly anteriorly and has a ru- open and slightly elevated but glottal gose anterior surface. It is subequal to lips are absent and the laryngeal disc the tallest postnarial papillae. There are is not visible; this may in part reflect no pustulations within the postnarial the early developmental stage of this arena. Two projections are evenly spaced specimen. The glottis is more than 80% directly behind the median papilla on hidden from dorsal view by the edge of the midline. The anterior one is a plain, the velum. Behind the glottis is a mod- small papilla; the posterior one is but a erately broad esophageal funnel. pustulation. The lateral ridge papillae Dorsal buccal.—A massive soft, fleshy are developed into relatively huge, lon- cone extends down from the prenarial gitudinally oriented, papillate flaps. The arena into the medial space between the flaps are as tall as long and point me- infralabial papillae. The base of the dially. They are displaced slightly pos- structure is oval in shape, about half as terior in relation to the median (ridge)

long as wide, and is 50% wider than the papilla. Distinct attenuate marginal pa- internarial distance. The height of the pillae, four on one flap and five on the

cone is equal to its width. As the cone other, account for more than half of the

descends it gently curls anteriorly. A maximum height of these projections. half dozen pustulations cover the sides The marginal "papillae" have pustulate ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 67 sides in addition to one or two minor formed. The larva are also distinguished basal bifurcations. The median (ridge) by having: reduced third filter cavities; papilla and the flap-like ridge papillae a massive cone-like projection of the outline the anterior end of a large, nearly prenarial arena; a median ridge reduced rectangular, buccal roof arena. The pos- to a papillae; extremely large lateral terior portion of this BRA is defined by ridge papillae. lateral rows of five simple, thin papillae. Hyla ebraccata Cope The first four in each row are in a continuous line running back from the flap- (Fig. 26) like lateral ridge papillae. The last and Material—KU 104130 (stage 35, sv. smallest papilla in each row is displaced 10.8 mm). Collected amidst emergent medially. The tallest papillae in the weedy, vegetation in shallow pond in BRA series are half the height of the clearing at edge of forest, at 100 meters lateral ridge papillae. Some half dozen elevation, Puerto Viejo, Heredia, Costa faint pustulations are scattered in the Rica; June 21, 1966. anterior end of the BRA. Lateral to the Re/erence.—Duellman, 1970 (p. 230- BRA and two-thirds of the distance back 232). the buccal roof are single, small pa- on External. — Hyla ebraccata larvae pillae, one per side. The only other fea- have a long, pointed filamentous tail. tures on the buccal roof are some pustu- They have a small, anteriorly directed lations directly behind these lateral roof mouth without denticle rows and a papillae. These pustulations contact the highly reduced oral disc. The eyes are anterior edge of the glandular zone. The far lateral; the spiracle is sinistral. glandular zone has a very uniform, buff Ventral buccal.—These larvae are texture. It was virtually impossible to characterized by a series of reductions resolve the individual miniscule secre- in the oral cavity from what may be con- tory pits of the glandular zone even at sidered the typical anuran condition. 75 X- The anterior margin of the secre- Single anterior to posterior compressed tory zone is arched posteriorly, so that infralabial papillae are present on both the zone has a 50% greater length later- sides. These small, flap-like papillae are ally than on the midline. The dorsal approximately twice as wide as tall and velum is strongly coiled, but did not have a slightly rugose dorsal margin. appear to be particularly long in this On the midline are a pair of small pa- specimen ( some of the dorsal velum was pillae which may be homologues of the destroyed in dissection). If the velum lingual papillae. Their far forward posi- is continuous across the midline, it is not tion, on the infralabial cartilage directly exceptionally tall in that region. between the infralabial papillae, speaks Dorsal pharynx. single, —A shallow, against homologizing these projections mediolaterally elongated pressure cush- with the lingual papillae; on the other ion could be resolved on one side but hand, there are no other papillae di- was removed from the specimen along rectly behind them and the anlage of the with portions of the dorsal velum in tongue is absent. Five or six very fine, order to gain access to the filter cavities simple papillae are dispersed laterally during the study of ventral features. about the buccal floor and in front of Details of the ciliary groove could not the buccal pockets. A buccal floor arena be determined. per se is absent. Pustulations present on Diagnostic summary.—Hyla mixe the buccal floor are scattered largely in tadpoles are unique among the tadpoles front of the buccal pockets and are examined in having the papillae of the about as numerous as the buccal floor buccal floor arena so numerous and close papillae. The buccal pockets are shal- to each other that a continuous fringe is low and clearly not perforated. The 68 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 26.—Drawings of the floor (above) and roof (below) of the mouth of a Hyla ehraccata larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES trailing edge of the ventral velum is a moderately wide and not dense. The rather smooth semicircle. The undula- trough between the secretory ridges is tions in the edge normally present above shallow. As viewed from above about each filter cavity in other hylid larvae half of the glottis is under the velum. are reduced greatly in amplitude. The The laryngeal disc is transversely elon- lateral peaks over filter cavity 1 are more gated. The posterior margin of the disc distinct than those over filter cavity 3. is turned up so that the glottal slit is The medial portion of the velar margin oriented more vertically than horizon- has a weak notch but is, otherwise, free tally. Glottal lips are well developed. of any abrupt contouring. Tiny secre- The esophageal funnel is broad and tory pits are on the dorsal velar margin. the lumen of the esophagus extremely These occur quite far forward and cover large. The funnel is tightly juxtaposed much, if not all, of the free dorsal velar to the laryngeal disc and by its mere surface. The pits are densest near the size seems responsible for the distortion midline. The free velar surface is com- in the laryngeal disc. paratively short considering that the Dorsal buccal.—The prenarial arena spicules are quite long. This makes the is short. A single, relatively large bulge, edge rather stiff and immobile medially. which is convex anteriorly, arises in this The free velar surface also tends to be arena and takes up most of its area. thick; secretory ridges cannot be seen There are between one and two dozen without turning the edge over. tiny pustulations in the prenarial arena, Ventral pharynx.—The branchial bas- mostly on the margins of the "bulge." kets are about as long and wide as in The internal nares are small; narial walls typical members of the genus, but not are not tall. Prenarial papillae are ab- nearly as deep. The filter plates are so sent from the anterior walls, although the short, and imbricated to such an extent, walls' margins are slightly rugose. The that filter tissue on cb. 2 and 3 is vir- narial valves are two to three times as tually restricted to the lateral faces. The wide as tall and lack narial valve projec- filter plates of the first three ceratobran- tions. Both postnarial and buccal roof chials are four to five times as long arenas are absent. A short, transverse as high. Those of the fourth cerato- crease halfway back on the buccal roof branchial are about twice as long as may be a remnant of the median ridge. high. The number of full filter rows on It is not particularly wide, nor straight,

the filter plates are: cb. 1 = 8, cb. 2 = and is relatively farther posterior than 8-9, cb. 3 = 11, cb. 4 = 8-9. Except for the median ridge in most Orton type 4

the high number of filter rows on cb. 4, tadpoles. In front of this crease are a these are well within the range for more dozen or so very tiny, pointed pustula- typical hylid larvae. There are no par- tions. These are absent in the back half tial filter rows. The filter mesh is very of the buccal roof. The only papillae on loose and, although secondary filter folds the buccal roof are two, lateral to the are numerous, they are quite thin and median (ridge) crease and displaced tertiary folds are lacking. Neighboring slightly forward. These papillae are filter rows on each filter plate do not small, simple and may be considered abut, consequently, filter canals are open either lateral ridge or buccal roof pa- channels along their whole length. Well pillae, depending on the faith one has defined branchial food traps are asso- in the homology of the "crease" with the ciated only with the third filter cavity; median ridge. The tiny secretory pits, all secretory ridges are concentrated comprising the glandular zone, are suf- laterally and restricted almost complete- ficiently difficult to resolve that the an- ly to the horizontal surface of the velum. terior limits of the zone cannot be Where secretory ridges appear, they are determined. Laterally, the dorsal velum 70 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

sort, as those suggested as possible is short; however, the velum is continu- such ous across the midline. Whereas the lingual papillae in H. ebraccata, are the lateral portions of the dorsal velum absent. The tiny secretory pits on project anteriorly, the velum twists dorsal edge of the ventral velum are just sharply to project directly caudad on as dense in H. ebraccata, but thin out the midline. This middle portion of the anteriorly and may not cover the whole velum is half as long as the velum at its free velar surface. widest lateral point. Ventral pharynx.—H. sarayacuensis Dorsal pharynx.—Both medial and exhibits some slight further reduction in lateral pressure cushions are fused into the pharyngeal region compared with a single, relatively large but shallow, H. ebraccata. Counts for filter rows roundish pad. Consistent with the large on the filter plates run: cb. 1 = 6, esophageal funnel, the ciliary groove is cb. 2 = 6-7, cb. 3 = 8, cb. 4 = 8. wide and not very deeply entrenched. The values for the first three cerato- Diagnostic summary.—See Hyla sa- branchials can be considered low; rayacuensis (p. 72). those for cb. 2 significantly so. Again, the number of filter rows on cb. 4 is Hyla sarayacuensis Shreve significantly above the average for more (Fig. 27) typical larvae of the genus. Only with Material—Yi\5 121413 (stage 34, sv. the greatest diflBculty and repetitive staining could secretory ridges be re- 11.1 mm). Collected in grass marsh at Bran- 1260 meter elevation, Rio Negro, Tungu- solved under the ventral velum. well demarcated. rahua, Ecuador; July 25, 1968. chial food traps are not Reference.—None. The greatest concentration of secretory seems to be lateral and anterior External.—The larvae of Hyla sa- ridges topography is quite rayacuensis have not been described in and even here the faint. detail. It is sufficient to say that H. sarayacuensis tadpoles possess the assort- Dorsal buccal.—As in H. ebraccata, ment of larval features characteristic of in the prenarial arena a faint, anteriorly the Hyla leucophyllata group: a tiny convex bulge is seen, but pustulations inset terminal mouth, absence of a pa- are absent. Small prenarial papillae are pillate labial disc and denticle rows, present, three on one side and one one xiphiceral tail filament with tall equal on the other. These projections arise or subequal dorsal and ventral fins. The from the medial half of the anterior

spiracle is sinistral. Compared to H. narial walls. Other pustulations or ru- ebraccata, H. sarayacuensis tadpoles gosities are absent from the narial walls. have a relatively tall tail. The two lateral roof papillae, seen in H. saraya- Ventral buccal.—The interior of the H. ebraccata, are present in cuensis. are slightly behind the mouth of H. sarayacuensis is so similar They papilla half the distance to H. ebraccata that all features which median and anterior unify the two species and contrast them laterally. In this specimen the be with more typical Hyla larvae are not margins of the secretory zone could is of uniform length repeated. Instead, emphasis is placed resolved. The zone on the few differences between H. sa- and has a smooth semicircular anterior rayacuensis and H. ebraccata. A single margin. The ratio of the length of the anterior to posterior compressed infra- buccal roof to the length of the glandu- that the labial papilla is present on each side in lar zone was 4:1, which means H. sarayacuensis. These have blunt dor- zone is unusually long. The dorsal velum slight- sal margins and are smaller and about is similar to H. ebraccata but has half as wide as the infralabial papillae ly shorter median and lateral lengths. in H. ebraccata. Medial papillae of any Dorsal pharynx.—Details of the dor- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 71

Fig. 27.—Drawings of the floor (above) and roof (below) of the mouth of a Hyla sarayacuensis larva. 72 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

each side are sal pharynx region could not be deter- more posterolateral on mined because of damage during dissec- single, large fleshy infralabial papillae. slightly compressed and bear tion. These are Diagnostic summary.—Hijla ebrac- faint, terminal pustulations and pointed Dorsolateral to these papillae, cata and Hijla saraijacuensis as repre- apices. Meckel's cartilage, are soft palps sentatives of the Hijla leucophyllata spe- over or cushion-like bulges of the buccal cies group are characterized by the oval and obliquely following oral features: medially elon- lining. These are lingual papillae are ex- gate prepocket buccal surface; reduction oriented. The ceptionally long and thin, and arch for- of the oral papillation and projections anlage is narrow and that define arenas; reduced marginal ward. The tongue projections of ventral velum; proportion- extending obliquely back from its base low elevations of the ally large third filter cavity with com- are two wide but paratively high number of filter rows in buccal surface. These curve slightly to- the medial margins of the buccal cb. 4; less dense filter mesh than typical ward fading into the buccal (2/3 denticle patterns) hyhd tadpoles; pockets before arranged reduction of area of secretory ridges in floor. The BFA papillae are the posteromedial portion of the bran- in a "U" which is open anteriorly. The flares laterally such that chial food traps; secretory pits covering top of the "U" extensive areas of dorsal surface of ven- the BFA papillae are in a continuous the prepocket papillae. These tral velum and posterior buccal roof; row with small large esophageal funnel. Both Hyla papillae are all attenuate, of to ebraccata and Hyla sarayacuensis tad- medium size, with curved pointed tips. poles are definable by the combination I counted 18 on one side and 20 on the of characters given above; the differ- other. Two or three of these on each ences between these two species are side can be considered prepocket pa- minor and given in the descriptions. pillae. Only three BFA papillae were bifurcated. The center of the arena is Ptychohyla schmidtorum chamulae devoid of pustulations. The only pustu- Duellman lations present on the buccal floor are (Figs. 28, 29) at the posterior margin of the BFA and anterolateral above the body of the Material—K\J 75409 (stage 35, sv. ceratohyals. Two or three medially di- 12.7 mm). Collected attached to stones rected papillae are among these antero- in pools in montane stream at 1600 me- lateral patches of pustulations. The buc- ters elevation, 17.6 km NW of Pueblo cal pockets are wide in P. schmidtorum; Nuevo Solistahuacan, Chiapas, Mexico; they are also clearly perforated in this June 14, 1963. species. P. schmidtorum has a relatively Reference.—DueWman, 1970 (p. 529- large free velar surface supported by 4 532). pairs of long spicules, the more medial External.—A slightly elongate tad- of which fully reach the velar margin. pole, with a 3/3 denticle pattern. The The posterior edge of the velum has circumference of the oral disc is ex- moderately acute peaks associated with panded into a denticle-free funnel of each filter cavity. The peaks of the third modest size. The spiracle is sinistral. filter cavity are displaced medially and Ventral buccal. The buccal floor is — are the largest. In addition to these un- comparatively short and broad. The dulations the velar margin is shghtly most anterior features in the mouth are arched around the tips of the spicules. eight medium sized, attenuate papillae, middle portion of the velum is four per side. These line the base of The or five the keratinized beak and arch forward, strongly emarglnated, with four pointing out of the oral orifice. A bit papilla-like projections (preserved fold- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 73

Fig. 28.—Drawings of the floor (above) and roof (below) of the mouth of a Ptychohtjla schmid- tortim larva. 74 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

ed up and forward in this specimen). nares have a nearly transverse orienta- Their Individual secretory pits could not be tion and are laterally elongate. they resolved on this surface, although the anterior walls are thin and low; apices of the trailing velar projections lack any pustulations or prenarial pa- are long and tended to have a buffed texture. pillae. Their posterior walls low and narial valve projections are Ventral pharynx.—The branchial bas- faint or not present. P. schmidtorum kets of P. schmidtorum are of average lacks a well defined postnarial arena. In size for a hyHd, but have the appearance the position of the median ridge is a of being displaced laterally along their papilla. Lateral to it posteromedial border. The baskets are single, stiff, tall are obliquely oriented ( anteromedial to relatively shallow, yet the filter plates posterodorsal) ridges on each side. are imbricated to an extreme and, con- These ridges have thick, wide bases and sequently, are still quite tall. Ratios for curved, bumpy ventral margins. They maximum height to maximum length are tallest and thickest anteriorly, show the filter plates of P. schmidtorum abruptly descending from the buccal to be as tall or taller than typical hylid roof at a position where one would ex- tadpoles. Numbers of filter rows on each pect to find the most anterior postnarial plate fall well within the normal hyhd papillae in other species. They continue range; the filter mesh, however, is not back an equal distance behind the me- dense. The filter rows are low, narrow dian (ridge) papilla and appear to be creases with short secondary branches. homologues of the postnarial papillae. Higher degree folds are rare and, when Continuing posteriorly from the end of present, short. They occur predomi- ridges are papillae nately along the ventral margin, where these oblique BRA in two lines that converge slightly to- the filter rows are their widest. The ward the midline; seven and eight to a filter canals are wide, open channels as side. The first and last papillae in the wide or wider than the filter rows. Se- rows are diminutive; others are moder- cretory ridges are visible through the ately large, and the five largest (three dorsal surface of the velum; their size on one side, two on the other) have and proportions are typical for a hylid terminal bifurcations. The most poste- tadpole. The branchial food traps are rior BRA papillae are displaced slightly not unusual. The glottis would not be toward the middle, reinforcing the im- visible in dorsal view, if the mid-portion age of a circumscribed "arena." Within of the velum had been preserved in the of the are approximately normal position. The glottis has a small the middle BRA the ten largest concen- and rather inconspicuous laryngeal disc. 50 pustulations, trated anteriorly near the base of the The esophageal funnel is not large but (ridge) papilla. Directly lateral has a broad profile in dorsal view. median to the end of the oblique ridges are two Dorsal buccal.—Anteriorly the roof moderately large, laterally compressed of the mouth is slightly expanded, other- papillae, one per side. Both of these wise gross dorsal proportions are typical have terminal bifurcations. They also for a hylid. There is a central trough are possible homologues of the lateral that runs the length of the prenarial ridge papillae. Directly behind these, arena. It is surrounded posteriorly by lateral to the BRA and in a line with a narrow V-shaped ridge (open ante- the middle of the arena, are tight clus- riorly) that increases progressively in including one height toward the internal nares. The ters of small pustulations, ridge terminates posteriorly in a single or two simple, small papillae. Still fur- projection. Other papillae and pustu- ther posterior, lateral to the end of the lations in the prenarial arena are absent. BRA, are two small, tranversely oriented

The internarial distance is great. The knolls. The glandular zone is very short ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 75

Fig. 29.—Photographs of the floor (above) and roof (below) of the mouth of a Ptychohyla schmidtorum larva. 76 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY and of uneven thickness. It is nearly a transverse row at the base of the kera- absent on the midhne but wider later- tinized beaks are two pairs of small, ally. Secretory pits are similar in size jagged papillae. The smaller of the pairs and density to many other hylids exam- is more lateral. Several subpapillate pus- ined but are not especially conspicuous, tulations are still more lateral. Behind presumably because of differences in these pustulations on each side is a preservation. The dorsal velum is slight- major infralabial papilla, shaped like a ly shortened; it is completely absent on cupped hand with long, pointed "fingers" the midline. The free velar margin is projecting forward. The fingers, four moderately crenulate, particularly me- and five per side, have scattered, pointed dially. pustulations on their margins. The two Dorsal pharynx.—Pressure cushions lingual papillae are very attenuate, as are absent in P. schmidtorum. The cil- are most other oral papillae. The BRA iary groove is very broad and shallow^. is an elongate oval. The arena is sur- Diagnostic summary.—Tadpoles of rounded by 86 moderately tall, thin, the genus Ptychohyla can be distin- pointed papillae in this specimen. These guished from larvae of the other hylids papillae are strongly curved so as to examined by a combination of the fol- point medially. Clusters of papillae near lowing characters: attenuate lingual pa- the lateral ends of the buccal pockets pillae; buccal floor and roof arenas elon- are fused at their base to form multi- gate; median projections of the posterior papillate structures which look like mini- velar margin elongate; third filter cavity ature deer antlers, one per side. These truncated; filter mesh of low density; have six "points" on one side and eight median ridge attenuate. on the other. Only two other papillae Ptychohyla schmidtorum was the on the buccal floor show any sign of only funnel-mouthed hylid larva I ex- bifurcation. There are three and four amined. In its oral cavity, the larvae small, conical prepocket papillae on op- exhibits the assorted modification asso- posite sides. Between the anterior end ciated with the funnel-mouthed condi- of the BFA papilla series and the pre- tion; principally, the fusion of papillae pocket papillae are twelve to twenty pa- series into ridges and the posteriorly di- pillae of the same shape and size as rected V-shaped depression of the pre- those in the BFA series. These fully narial arena. cover the surfaces above the body of the ceratohyals. Papillae from the BFA se- Ptychohyla leonhardschultzei (Ahl) ries also extend laterally behind the buc- (Figs. 30, 31) cal pockets to cover a small region of the buccal floor anterior to the second Material—KV 139924 (stage 26, sv. filter cavity. There are some 60 or so 14.4 mm ) . Collected on bottom of riffles very tiny pustulations dispersed within in streams at 720 m elevation, 18.1 km N buccal arena. The buccal pockets of San Pedro Mixtepec, Oaxaca, Mexico; the are long, shallow, and perhaps a bit March 20, 1970. more transversely oriented than in typi- Reference. — Duellman, 1970 (p. hylid larvae. are conspicuously 543). cal They perforated. The free velar surface is External. —The body is slightly elon- large. It is supported by stiff spicules; gate. The denticle formula is 4/6. The the more medial pairs reach the velar oral disc is relatively large, but does not have the expanded, denticle-free margin margin. Single, symmetrical, leptokurtic seen in P. schmidtorum. projections of the velar margin are Ventral buccal.—The floor of the aligned over filter cavities 1 and 2; the mouth in P. leonhardschultzei is rela- more medial of these projections point

tively short; it has a squarish shape. In posteromedially. Eight other distinct ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 77

Fig. 30.—Drawings of the floor (above) and roof (below) of the mouth of a Ptychohyla leonhardschultzei larva. 78 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY projections are clumped together on the lack narial valve projections. Postnarial velar margin above the glottis. Secretory papillae are located on narrow, obliquely pits are mostly limited to the surface oriented ( anteromedial to posterolat- of the posterior projections. Pits are eral) ridges of moderate size between nearly absent from the velar surface it- the anterior end of the internal nares self except for a very narrow band near and the median ridge. The tallest post- the midline. narial papillae are in the middle of their ridges, where the ridges Ventral pharynx.—The branchial bas- supporting themselves are tallest. I counted seven kets are of typical width to length ratio papillae per side. The smaller but have the appearance of being dis- postnarial papillae grade into pustulations at the placed laterally along their posterome- end of the ridges; the larger are of mod- dial border. The third filter cavities are est proportion with jagged anterior mar- reduced in size and partially obscured gins. median ridge is a small isos- from dorsal view by the medially imbri- The celes triangle, with a basal width equal cating, curved margins of the third filter to its height, and with sHghtly concave plates. Filter plates of cb. 1 and cb. 2 sides. It has four pustulations scattered are relatively short, while those of cb. 3 over its anterior surface. There are two are comparatively tall. Counts for num- or three tiny, pointed papillae in front ber of filter rows fell within the normal of the ridge in the postnarial range for typical hylid larvae, but those median arena. Laterally, at the posterior end of cb. 1 and cb. 4 were slightly low, of the ridges supporting the postnarial while those of cb. 2 and cb. 3 were papillae, are two relatively giant, multi- slightly high. The filter mesh of P. leon- papillate flaps. These flaps, presumed hardschultzei is quite open, but not as of the lateral ridge papillae, spacious as in Ptychohyla schmidtorum. homologues are compressed into the sagittal plane. P. leonhardschultzei has a typical They have five, attenuate pointed papil- branching pattern for the filter folds, but lae along their lateral margins. Two or all the folds are exceptionally slender, three of these papillae have minor bi- resulting in large filter niches. Branchial furcations. Extending directly back from food traps and their secretory ridges are the base of the flaps on each side is a not unusual. The glottis is 80% under row of tall, thin, pointed papillae that the velum. It is small and has thin, define the lateral limits of the BRA. elevated lips. The laryngeal disc is not These rows converge only slightly until visible. The esophageal funnel is of com- are far the buccal roof, parable size to that of the more typical they back on the hylid larvae examined. where they turn sharply toward midline. The BRA is thus roughly a rec- Dorsal buccal.—The buccal roof ap- tangle, with rounded corners. It is bound pears wide anteriorly. The central por- by a total of 34 BRA papillae in this tion of the prenarial arena is displaced specimen. Three or four of these pa- ventrally along the edge of an anteriorly pillae have a tiny, pointed pustulation convex arch. This arch is slightly wider near their apices but in general, buccal than the internarial distance. The edge roof papillae are little ornamented. A of the arch is lined with a dozen or so hundred or so small blunt pustulations large, blunt pustulations or subpapillar are dispersed within the arena. Ten projections and has its greatest depth to twelve tiny papillae, not quite as tall anteriorly. The internal nares of P. leonhardschultzei are elongate. Prenarial pa- as those in the BRA series, form a sec- pillae are lacking, but about a half ondary line or cluster of papillae lateral dozen pointed pustulations are dispersed to the middle of the arena. Lateral to over the medial half of the anterior the posterior end of the arena are small narial wall; the posterior narial walls pustulate fields also including a couple ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 79

the mouth of a Ptychohyla leon- Fig. 31.—Photographs of the floor (above) and roof (below) of hardschultzei larva. 80 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY of tiny papillae on each side. The glan- there are three lingual papillae. Exami- crepitans, however, dular zone is not wide. Secretory pits nation of other A. are small in P. leonhardschultzei, al- shows that two lingual papillae are typi- though they are not atypically dense. cal and that this individual is abnormal Overall, the dorsal velum is of typical in that feature). The buccal pockets of size and shape, but it is interrupted me- A. crepitans are clearly perforated. The of dially and its free medial edges are secretory pits on the dorsal margin sculptured into a series of small, simple the velum are possibly a bit larger than papillae on each side. those of H. regilla, but the difference is Dorsal pharynx.—The pressure cush- slight and may be accounted for by pres- ions are equal to, or larger than, those ervational differences. of more typical hylid larvae. The me- Ventral pharynx.—The filter rows fall dial pressure cushions are the larger and within the normal range for H. regilla rounder of the pairs. The ciliary groove of comparable stage; filter rows are a bit is deep and narrow. wider in A. crepitans than in H. regilla. Diagnostic summary.—Tadpoles of Overall, the filter mesh appears slightly this species have the greatest number of less dense in A. crepitans. Again this buccal floor and buccal roof arena pa- difference is small enough to be ascrib- pillae of any species examined and, as able to differences in preservation. such, can be distinguished readily from Dorsal buccal.—All major features all other hylid larvae examined. are as in H. regilla; the few distinctions between A. crepitans and H. regilla are Acris crepitans Baird almost all comprehendable as simple (Fig. 32) augmentations associated with overall Material—FMNU 11916 (stage 36, increase in size. There are twice as many sv. 16.8 mm). Collected 6.4 km W of prenarial papillae in A. crepitans as in Fort Worth, Tarrant Co., Texas; March the average H. regilla; the narial valve 29, 1931. projections are more attenuate. I count- Reference.—Stebbins, 1951 (p. 301- ed seven postnarial papillae in oblong 304); Heyer, 1976. (anterolateral to posteromedial) clusters Externa/.—Tadpoles of the genus on each side of the midline in this speci- Acris have a 2/3 denticle pattern and a men; this is significantly more than in of bi- sinistral spiracle. Their body form and H. regilla. At least one these was habits typify the "common" pond tad- furcated. A couple of small papillae pole. and a half dozen or so pustulations were within the postnarial arena. The median Ventral buccal.—Acris crepitans lar- ridge and lateral ridge papillae are simi- vae are indistinguishable from H. regilla lar to those of H. regilla. Additional larvae in the shape of their mouths and papillae, anterolateral to the lateral general oral proportions. The few dif- ridge papillae, are present. There are ferences between the two species large- twice as many BRA papillae in A. crepi- ly correlate with the greater size of A. tans as there are in H. regilla. Ten or crepitans. The position and shape of more papillae with some associated pus- papillae on the buccal floor, including tulations occur lateral to the BRA on the infrarostral, lingual, BFA and the Evenly dispersed within the buccal pocket papillae, are identical to each side. arena are well over a hundred medium H. regilla. The same situation holds for to small pustulations. The glandular pustulations on the buccal floor. The zone is identical to that of H. regilla, BFA papillae may be slightly taller and a bit easier to resolve more numerous than those of H. regilla, although it is specimen on but not significantly so. (In the speci- secretory pits in the one men on which this description is based, hand. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 81

Fig. 32.—Photographs of the floor (above) and roof (below) of the mouth of an Acris crepitans larva. 82 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Dorsal pharynx.—Pressure cushions BFA papillae, those directly medial to can be discerned as two round faint the ends of the buccal pockets, are fused swellings on the posterior surfaces of to their neighbors at their bases. There the dorsal velum on each side. These are single, prepocket papillae on each cushions and the ciliary groove are inside, which are relatively tiny and sharp- distinguishable from those of H. regilla. ly pointed. A dozen or so large pustu- Diagnostic summary.—Tadpoles of lations are in the posterior half of the the genus Acris are so similar externally, BFA. Fine pustulations are also scat- that it is reasonable to consider Acris tered above the lateral arms of the crepitans as representative of the genus. ceratohyals, among the BFA papillae, Acris crepitans tadpoles have a high- and posteriorly behind the arena. This er number of postnarial papillae than last posterior patch extends laterally to any other larvae examined. There are the front of the second filter cavity. significantly more buccal roof arena pa- Single, tiny papillae are among the pus- pillae in Acris crepitans tadpoles than in tulations on the ceratohyal arms in front Hyla regilla tadpoles. Otherwise, the of the second filter cavity. The buccal larvae of these two species are virtually pockets of S. sordida are large, long and identical. more transversely oriented than those of H. regilla. They are conspicuously per- Smilisca sordida (Peters) forated. The free velar surface is large (Fig. 33) and supported by stiff, long spicules that Material. — Uncatalogued, author's come close to reaching the velar margin. collection (stage 37, sv. 11.5 mm). Col- Posterior projections from the velar sur- lected singly in clear shallow, but slow face are long and leptokurtic. The pro- flowing water of the Rio Rincon near jections associated with the third filter ten mile mark on the Pacifica Road from cavities are displaced medially. The pro- Rincon de Osa, Puntarenas, Costa Rica; jections of both the second and third

March 4, 1970. filter cavities are pointed posteromedially. or tall secondary projec- Reference. — Duellman, 1970 (p. One two 617). tions are developed next to the relatively deep median notch. Large, conspicuous External.—These tadpoles have a 2/3 secretory pits form a thin band on the denticle pattern and a sinistral spiracle; posteromedial portion of the velar mar- only a slight ventral shift of the mouth gin. This band is diminished laterally; and elongation of the tail distinguishes distal to the second filter cavity the pits these tadpoles from typical pond polli- are restricted to the marginal projections wogs. Externally they show few of the of the velum. modifications characteristic of stream tadpoles. Ventral pharynx.—The branchial baskets viewed from above are typical in Ventral buccal.—Anteriorly the floor size and shape. They are, however, not of the mouth is slightly expanded lat- particularly deep and individual filter erally. The infralabial papillae are plates are imbricated to a great extent. cupped flaps of skin no different in size The third filter cavity is reduced in and shape than those of typical pond width. In terms of other characters of hylid larvae, but with finely serrated the filters, viz. the length to height ratio margins rather than papillate "fingers." of the filter plates, number of filter plates Lingual papillae are tall. The buccal on the rows, pattern of the filter folding, floor arena is defined by a modest num- of filter etc., S. sordida is ber of papillae, some eight per side. The density mesh, BFA papillae do not converge strongly indistinguishable from more typical hy- toward the midline at the anterior limit lid larvae. Branchial food traps are of the BFA. The three or four largest necessarily shallow because of the shal- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 83

Smilisca sordida larva. Fig. 33.—Drawings of the floor (above) and roof (below) of the mouth of a 84 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

lowness of the branchial baskets, but, bering five per side. There is a gap because of the larger free velar surface, equal to a seventh of the length of the the actual area covered by secretory buccal roof separating the first BRA

ridges is not reduced. The secretory papillae from the posterior edge of the ridges are similar to those of typical lateral flaps. The BRA papillae rows pond larvae. The glottis is typical. The converge only slightly towards the mid- laryngeal disc is not visible. The esoph- line and outline a rather elongate buccal ageal funnel is a bit broader but no roof arena. There are sixty or more pus- larger in S. sordida than in the reference tulations within the arena; their greatest hylid larva. concentration is posterior. Directly lateral to the gap between the lateral flaps Dorsal buccal.—The buccal roof has the anterior papillae are the same length to width ratio as H. and most BRA small clusters of four or five pustulations regilla, but a slightly more square, less one tiny papilla per side. glan- triangular shape. The central portion of and The dular zone is slightly shortened both the prenarial arena bulges ventrally. On medially and laterally compared with the surface of this shallow bulge is an more typical larvae. secretory anteriorly directed pustulate arch. The pond The pits are not unusual in any way. The arch is twice as wide as the internarial dorsal velum is short and has a broad distance. The internal nares of S. sor- gap across the midline. dida are more elongate and obliquely The more me- a pustulate oriented than in a typical pond larva. dial limits of the velum have Prenarial papillae are lacking, but many margin. tiny, pointed pustulations line the whole Dorsal pharynx.—Pressure cushions length of the low, anterior narial walls. are of comparable length to those of H. The posterior narial walls lack narial regilla but are necessarily smaller be- valve projections. Postnarial papillae, cause of the decrease in free velar sur- two on one side, four on the other are face. The ciliary groove is narrow. small, simple, blunt projections. These Diagnostic summary.—Because only are in obliquely oriented ( anteromedial one species of Smilisca was examined in-

to posterolateral) lines that include an ternally, it would be premature to at- equal number of evenly spaced pustu- tempt to diagnose the genus. The Smi- lations. The reduced median ridge is as lisca sordida group of Smilisca includes

tall as it is wide and has a peaked rather stream breeders; it is a reasonable hy- than horizontal ventral margin. This pothesis, however, that the oral cavity ventral margin is lined with many fine of S. sordida larvae will resemble that serrations, and there are single isolated of other stream Smilisca tadpoles more

pustulations on the anterior surface of than it will resemble that of the larvae the median ridge. Extending back from from the non-stream breeding Smilisca of the postnarial papillae row, the ends baudinii group. On the other hand, it posterolateral to the median ridge, are is possible that with such slight differ- large, nearly longitudinally oriented ences between typical pond larvae, such flaps. These are presumed homologues as Hyla regilla, and Smilisca sordida, of the lateral ridge papillae. Each flap other species of Smilisca may not be is tallest posteriorly and deeply notched, distinguishable from S. sordida in larval so that it has at least five sharp peaks are a few along its margin plus a couple of minor, oral anatomy. The following pointed pustulations. Continuing pos- of the oral features in which Smilisca teriorly in line with the long axes of the sordida larvae differ from Hyla regilla lateral flaps are single rows of BRA pa- tadpoles: lingual papillae taller; spic- pillae on each side. These are slender, ules stiffer and longer; velar marginal pointed papillae of modest size, num- projections longer; filter plates more im- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 85 bricated; branchial food traps shallower; into a dense field of numerous tiny pus- pressure cushions smaller. tulations and subpapillae above the body of the large ceratohyal on each side. Agalychnis callidnjas (Cope) Six to nine (X = 7.5) BFA papillae (Fig. 34) make up the row on each side; none are bifurcated. The posterior four to five Material. — Author's collection (3 papillae are equal or subequal in size specimens: stage 35, sv. 19.9 mm; stage are in a perfectly 37, sv. 18.6 mm; stage 39, sv. 19.2 mm). and shape. These Collected in massive swarming schools straight row. The papillae at the begin- in the "Caiman" pond, by Pacifica Road, ning of the series are similar, but smaller 9.7 km south of Rincon de Osa, Punta- and not in such straight lines. Anteriorly small papillae lie inside the arena. renas, Costa Rica; March 4, 1970. two These are next to and parallel the main Reference.—Duellman, 1970 (p. 107- 108). papillae row. Sixty or more tiny pustulations cover the buccal floor. They are External.—Tadpoles of the genus most concentrated posteromedially in Agalychnis all have an elongate, fila- the BFA and laterally above the cerato- mentous tail. Their eyes are far lateral, hyals. There are no isolated prepocket their mouths are directed anteriorly or papillae per se but a few small papillae, anteroventrally; the spiracle is just left not separable from the pustulate lateral of the midline. The denticle pattern is, field at the anterior end of the however, the common 2/3 arrangement. BFA papillae rows, may be homologous to Ventral buccal.—The floor of the the prepocket papillae in other species. mouth is anteriorly broader and poste- The buccal pockets may be perforated riorly more elongate than in typical hy- in the stage 37 specimen, but are lid larvae. A single, tiny, soft spur is not evidently open in either the stage present on the infrarostral cartilage 35 or 39 specimens; a consistent spe- posterior to the edge of the beak but in cies pattern cannot be resolved with line with the keratinized cutting edge the small sample at hand. The anterior on each side. The infralabial papillae to posterior length of the free velar all lie well medial to these spurs. Three margin over the filter cavities is larger, to five infralabial papillae per side are and the supporting spicules longer, than present. The largest papilla on each side in most other hylids. The margin of the is always the most medial. These more ventral velum has four posteriorly di- medial papillae are tall, tapered, and rected acute peaks. The peaks, which round to slightly oval in cross section. are most obviously homologous with the They curve directly anterad. The small- velar crenulations normally above the er, more lateral papillae are round in third filter cavity in other hylids, are section and do not curve anterad. These displaced medially. Several paired auxil- more lateral infrarostral papillae form iary projections in this region effectively an anterior to posterior line or cluster, produce a field of papillae trialing off with the most anterior papilla slightly the edge of the velum above the glottis. larger than the more posterior ones. Single, broad crenulations are present on The largest medial papillae are 1.5 to the velar margin between the peaks 2 times taller than any of the lateral above filter cavities 1 and 2; these are papillae. All papillae are unbifurcated. also posteriorly directed. The pitted The two lingual papillae are so close to glandular zone on the dorsal surface of each other and to the midline that they the ventral has effectively share a common base. The velum a sharply defined buccal floor arena is outlined by two anterior margin. The glandular tissue is posteriorly converging lines of papillae. densest on or near the major peaks and Anteriorly these rows flare out laterally tends to thicken the edge of the velum. 86 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Fig. 34.—Photographs of the floor (above) and roof (below) of the mouth of an Agalychnis callidryas larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 87

Ventral pharynx.—Agalychnis is char- appears fully developed, although not acterized by substantially larger bran- large. The glottal lips are raised on a chial baskets, a greater amount of filter strongly developed anterior to posterior- surface, and a finer filter mesh than any ly directed ridge. The papillate mid- other hylid examined. Filter plates are portion of the ventral velum margin longer and particularly taller than in makes it impossible to estimate, in any H. regilla, although the length to width consistent way, the amount of glottis ratio for the branchial baskets in toto obscured by the velum. The esophageal do not differ; the additional filter surface funnel is of relatively narrow profile. in Agalychnis is taken up in increased Dorsal buccal. — The roof of the curvature and imbrication of the filter mouth is quite wide anteriorly. In the plates. axis The major of the second center of the large prenarial arena is a filter cavity projects back from the mid- single, darkly staining, semicircular line at a very acute angle. The cerato- (concaved posteriorly) low ridge. Even- branchials and the filter plates that they ly spaced on the top of the ridge are support are strongly bowed outward. short, knobby projections, 4 to 7 per Filter plate 1 is so curved that in cross side. Posterolaterally these are mere section it circumscribes half a circle. pustulations, but anteromedially they de- The dorsal margins of the filter plates velop into unusually shaped, low nodu- on cb. 2 and cb. 3 are not straight, but lar papillae. There is a faint medial arch upward to a peak just behind the gap in the ridge. Medially within the edge of the ventral velum. These plates semicircle, are one or two more typical, are strongly imbricated toward the mid- prenarial pustulations. The internal line causing the filter cavities, particu- nares are not unusual in shape, except larly cavity 3, to be almost completely that the openings to the olfactory cap- encircled by filter epithelium. The num- sule are small and far lateral. There are ber of full filter rows on each plate are no distinct prenarial papillae, although fol- exceptionally high; they range as the raised anterior wall of each naris is lows: cb. 1 = 11-13, cb. 2 = 12-15, cb. rugose in texture, particularly medially. 8-9. filter 3 = 12-13, cb. 4 = The mesh The narial valve projection is shorter is far tighter than in other hylids. Sec- than in more typical hylid larvae. Be- ondary filter folds are numerous and tween the nares and the median ridge dense. Filter rows do not simply termi- lie three distinct papillae on each side. nate at the ventral borders of the filter These papillae all arise from a common plates, but interdigitate with the rows on straight ridge oriented anteromedially to the opposite filter plates, completely ob- posterolaterally. On each side the most scuring the gill slits. Partial, tapered anterior of the three papillae lies direct- filter rows project deeply ventrad be- ly behind the narial valve projection. tween normal full rows and fill any This is a very large, conical, acutely spaces full filter Fil- between the rows. pointed papilla. It is taller than the ter canals are virtually complete tubes, narial wall and projects anteriorly under rarely visible without displacement of the narial valve projection in one speci- the filter rows. Narrow and closely men but a bit more medially in the packed secretory ridges are readily visi- other two. The middle papilla in the ble on the ventral surface of the ventral series is the smallest. It is a simple, tiny, velum. The ridges appear discontinuous finger-shaped papilla aligned behind the directly under the spicule of cb. 2. middle of the nares and about halfway Branchial food traps cover a large pro- back in the narial arena. This papilla portion of the anterior surface in the is directed anteriorly. The last papilla filter cavities extending down the medial on the ridge is a simple, stout, cone one- anterior wall of each cavity. The glottis half to one-third the size of the largest 88 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY anterior papilla. This last papilla aligns pillae in these lateral "clusters" are, on itself behind the lateral end of the nares the average, one-fourth the height of and two-thirds of the way back in the the main BRA papillae. The glandular narial arena. It is oriented medially. In zone is well defined and made up of two of the three specimens, postnarial conspicuous secretory pits, which are papillae show some very fine pustula- large, round and abutting. These extend tions along their most anterior margins. well over the dorsal velum and onto the A single, basal bifurcation was found pressure cushions. They are densest on asymmetrically on the third papilla in the edge of the velum. The anterior one of the specimens; elaborate bifurca- margin of the glandular zone is strongly tions of the posterior narial papillae are scalloped. Two lateral swells on each probably rare in this species. The last side match perfectly the anterior limits papilla in the posterior narial papillae of the free edge of the ventral velum row may be homologous to the lateral over filter cavities 2 and 3 below. The ridge papillae; however, they are dis- dorsal veliun is divided on the midline placed a bit forward and because they by a substantial gap. The medial mar- sit on a common ridge with the other gins of the dorsal velum may point to- papillae within the narial arena they are wards each other or the edges may turn considered here part of the postnarial posterior to form a funnel that parallels papillae series. There are no other pa- the esophageal funnel. Laterally, the pillae directly lateral to the median edge of the dorsal velum is thick, glan- ridge. The median ridge is a transverse dular, and not curled. The velum is flap, shaped like an isosceles triangle. relatively and absolutely smaller than

It is positioned slightly anterior to the in more typical hylid larvae. middle of the buccal roof. The ridge has Dorsal pharynx.—The pressure cush- a basal width one to two times its height ions are comparatively huge, obliquely and a single or occasionally bifurcated oriented ovals, extending well down apex. No secondary anterior fringe is into filter cavities 1 and 2. The me- present. Between seven and ten pustu- dial cushions are about three times as lations are scattered within the post- wide as the lateral cushions and twice narial arena. The buccal roof arena as tall. The ciliary groove is relatively covers the flat, medial one-third of the narrow and deeply entrenched. buccal roof. The arena is bound later- Diagnostic summary.—Of the spe- ally by two patches of simple, moder- cies examined in detail, Agalychnis calli- differs all other hylids sensu ately small, finger-like papillae, seven to dryas from ( nine per side. The patches trend antero- lato) in having massive branchial bas- laterally to posteromedially. Posteriorly, kets, dorsally arched filter plates, and an the patches tend to narrow into single extremely dense filter mesh. Cursory rows. The papillae do not vary much in examination of other species in the genus size, but the largest ones are generally of Phyllomedusa suggest that the diag- in the middle portion of the patches. noses will not distinguish A. callidryas None of the papillae are bifurcated. from other middle American phyllome- Within the arena are approximately dusine tadpoles. eighty randomly dispersed, darkly stain- GENTROLENIDAE ing spots, almost too small to be called pustulations. These are absent outside Centrolenella fleischmanni (Boettger) of the arena. A secondary cluster of (Fig. 35) lateral roof papillae appears on each Material. — Uncatalogued, author's side about halfway between the main collection (R. W. McDiarmid Field No. BRA papillae patches and the lateral 6865 "clutch #3") (stage 30, sv. 6.9 edge of the mouth. The one to six pa- mm). Raised from eggs. Monteverde, ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 89

Fig. 35.—Drawings of the floor (above) and roof (below) of the mouth of a C entrolenella fieischmanni larva. 90 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Puntarenas Prov., Costa Rica; collected Ventral pharynx.—Seen from above pharynx is long laterally and July 4, 1971; preserved Aug. 20, 1971. the ventral Reference. — Starrett, I960; Villa, narrows sharply toward the midline. The 1971; Heyer, 1976. result is that the branchial baskets appear relatively triangular in shape. The External.—The tadpole of Centrole- baskets are extremely shallow. The filter nella fieischmanni is extremely elongate, plates are short and only slightly imbri- with a tail more than twice as long as cated. The tallest plate is the second. its body. The denticle pattern is 2/3 The fourth filter plate is strongly arched and a single, sinistral spiracle is located in the transverse plane. Filter rows are 3/ 4th the way back on the body. The well organized along the dorsal margins external nares are tiny pores; the eyes of the filter plate particularly the second are small, deepset and directed dorsally. filter plate; ventrally the filters become Ventral buccal.—Internally the floor less organized and have a puffy, spongy- of the mouth is of the overall triangular like texture. It is possible to discern sec- shape of most tadpoles; however the ondary and occasionally tertiary filter oral orifice itself is narrow and the buc- folds on some of the filter rows but cal surface behind the buccal pockets is others appear relatively disorganized, exceptionally elongate. There are two lacking an obvious branching pattern. pairs of infralabial papillae; a medial Despite the fact that the higher order pair adjacent to the midline and a lateral filter folds are not always visible, there pair placed more typically over Meckel's are no large spaces between filter rows; cartilage. The medial papillae are sim- filter canals appear to be relatively nar- ple, tall, but blunt structures that over- row, shallow slits. Counts for filter rows lap on the midline. The lateral pair are run: cb. 1, 9; cb. 2, 15; cb. 3, 11; cb. 4, small, anteroposteriorly flattened flaps, 10. These should be considered mini- which are slightly concave anteriorly; mum estimates as it was very difficult one has slight marginal pustulations, but to collect these data on such a small they both lack secondary papillae. The specimen. The gill filters are unusual in base of the lingual papillae is a trans- that they show such a broad range of versely oriented ridge and on its apex structural organization. The light grainy is a transverse row of four small lingual texture characteristic of secretory tissue papillae. There is but one BFA papillae is evident on the short surface of the on one side, four on the other; these branchial food traps; however, even at are displaced far laterally and barely 100 X, well organized secretory ridges define an arena. The papillae lack sec- could not be discerned in this region ondary pustulations; they are flattened and may be lacking in the species. The against the buccal floor and have slight- glottis is distinct with heavy lips. An ly knobby crowns. Most of the buccal elevated laryngeal disc is absent at this floor lies behind these papillae and com- stage. The esophageal funnel is of completely lacks topographic relief. Papillae parable shape to that of most other anu- and pustulations are also absent from rans examined. within the BFA or in the region anterior Dorsal buccal. The buccal roof has to the buccal pockets. The prepocket — the basic triangular shape typical of region is small. The buccal pockets are other anurans. The prenarial arena is shallow creases with a strongly oblique narrow, long and nearly vertically ori- orientation. Buccal slits appear (?) pat- ented, a reflection of the ventral position ent. The free velar surface is gently curved, lacking projections. The median of the oral orifice. There is one stiff,

notch is very weak and shallow. A thin enlarged triangular projection which ex-

zone of glandular tissue is evident over tends down from the posterior portion the margin. of the prenarial arena. It has a slightly ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 91 compressed, transversely oriented base. the remainder of the buccal roof. The There are no other papillae or pustula- boundaries and general proportions of tions in the prenarial arena. The inter- the glandular zone could not be dis- nal nares are large, longitudinally ori- cerned in this specimen and a distinct ented, open pits. The long median walls glandular zone may be lacking in this of these vacuities virtually meet on the species. The dorsal velum is short, un- midline. The prenarial papillae are curled, anteriorly directed, and continu- points that extend forward from the ous across the midline. front of the tall narial walls. Narial Dorsal pharynx.—On the posterior valve projections are lacking. The narial surface of the dorsal velum are two walls on each side circumscribe a large extremely slight swellings on each side, shallow narial depression the ( Jacobson's only evidence of pressure cushions. organs?) at the base of which is a small The medial swellings are larger and slit whose margins completely abut. Be- more obvious. The ciliary groove is a cause of the small size of the specimen, shallow broad channel. complete exploration was impossible, but Diagnostic summary. — Many fine these slits appeared to be patent internal features of papillae pattern and shape narial openings. The postnarial arena is are unique in this form compared to the extremely small and contains a single other larvae described. The combina- sharp papilla located on the midline in tion of the following major features, the middle of the arena. It is hidden however, readily serve to distinguish the from ventral view by a simple, triangu- oral cavity of this species from all oth- larly shaped median ridge that is ad- ers: long buccal floor and roof behind pressed against the buccal roof. Al- buccal slits and median ridge respec- though the median ridge is not large, tively, with both areas lacking papillae the narial depressions are so long that and pustulations; shallow branchial bas- the apex of the median ridge projects kets; very large, longitudinally oriented between the posterior portions of the in- internal narial depressions; four lingual ternal nares. Immediately to the sides papillae. and slightly anterior to the median ridge DENDROBATIDAE lie two pointed papillae, presumed homologues of the lateral ridge papillae. Colostethus subpunctatus (Cope) They fit in the space between the median (Fig. 36) ridge and the posterior wall of the in- Material—MYZ 63199 (stage 34, sv. ternal nares. A short distance lateral 11.7 mm). Collected from small rain and slightly posterior to each lateral pool at 2650 m elevation Bogota, Cundi- ridge papilla lies single a obliquely ori- namarca, Colombia; Oct. 15, 1950. ented, posteromedial to anterolateral External.—Colostethus subpunctatus compressed flap on each side. The hom- larvae have flattened venters and dor- ologues of these projections are uncer- sally directed eyes. The spiracle is sinis- tain. Whereas they are too far posterior tral and denticle formula is 2/3. to be associated with the median ridge, Reference.—Stebbins and Hendrick- they are too far anterior to be obvious son, 1959. buccal roof papillae. Each flap has a Ventral buccal. The floor of the terminal, anterolateral, fingerlike projec- — mouth is generally similar to that of tion that points anteriorly, and a more many pond tadpoles. In addition to posteriomedial cusp similarly directed weak spurs, directed anteriorly at the along the same edge. All of the struc- very margins at the oral orifice, there tures so far described lie in the anterior are three major papillae associated with half of the buccal roof. Papillae and the infralabial region. The smallest in- pustulations of any sort are lacking from fralabial papillae are two blunt projec- 92 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

"""••. -J./; ?:".-- ,«'" '.•", r '^VL**'' '

of a Colostethus suhpunc- Fig. 36.—Drawings of the floor (above) and roof (below) of the mouth tatus larva. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 93 tions arising from the posterior floor of tween the left and right branchial bas- the infralabial region. Their bases abut kets is very large. Filter rows count run on the midhne. In the typical position 8, 9, 9, 5—similar to that of typical pond for infralabial papillae in other species, tadpoles. The filter mesh is low in densi- arise transversely compress large bifur- ty. Neighboring filter rows do not abut, cate palps with secondary, small, mar- except at their ventral extremes, and par- ginal pustulations. The tips of these tial filter rows are short; thus leaving the palps touch on the midline. The third filter canals as large open channels. pail' of infralabial papillae arise from Many of the filter rows lack tertiary or the anterolateral edge of the large pair higher order folds, particularly in the just described. These are flaps com- small third filter cavity. The branchial pressed in the transverse plane. They are food traps are relatively shallow. At nearly as wide as the previously de- 50 X magnification a weak pattern of scribed pair, but not as tall. They have transversely oriented ridges can be seen several marginal serrations, but lack secon the ventral surface of the ventral ondary papillae. The two lingual pa- velum. The glottis is completely exposed pillae are tall. The buccal floor arena is in the median notch. It is slightly ele- well defined by nine papillae on one side vated and has distinctive lips; however, and ten on the other. The arena is rela- it is quite small in all dimensions com- tively narrow and the BFA papillar rows pared to the overall size of the buccal have a slightly oblique (anterolateral cavity in this tadpole. The esophageal to posteromedial) orientation. BFA pa- funnel is very large. pillae are similar to those in most pond Dorsal buccal.—In general propor- tadpoles; however, they lack extensive tions the roof of the mouth is similar marginal papillations and are noticeably to that of pond tadpoles. There is large taller and more attenuate. One or two prenarial arena; from the middle of the small papillae lie anterior to the medial arena descends a broad, anteriorly di- margin of the buccal pockets. There is rected, pustulate arch. Halfway between a weak field of pustulations in the pos- this structure and the internal nares lies terior two thirds of the BFA. Buccal a single large pustulation on the mid- pockets are more obliquely oriented than line. The internal nares have a relative- in H. regilla. Large mucosal folds from ly horizontal orientation with a heavy, the posterior walls obscure the base of thick anterior wall, that lacks prenarial each buccal pocket. The pockets are of papillae. The posterior narial valve has average depth and may be perforated on a weak narial valve projection. Aligned one side in this specimen. The free in a row in the postnarial arena, parallel velar margin is of average length, but to the internal nares, run 4 robust pa- relatively thick and inflexible. Tiny, but pillae on each side. The most posterior dense, secretory pits can be resolved at of these lies lateral to the median ridge 50 X lining the free edge of the velum. and may be the homologue to the lateral The free edge is strongly sculptured with ridge papilla. These are transversely posteromedially directed cusps above flattened bifid structures. All of the the second and third filter plates and papillae associated with the postnarial additional posteriorly directed cusps arena including the median ridge have above the fourth filter plates. There is pustulate anterior margins. The smallest a very deep, distinct median notch. postnarial papillae is most anterior. The Ventral pharynx.—The branchial bas- median ridge is a simple, triangular flap kets are of comparable size and shape of average size. The buccal roof arena to those of typical pond tadpoles. The is defined by five, extremely attenuate

filter plates, however, are strongly imbri- papillae on one side and four on the cated medially and the medial gap be- other. A few subpapillate projections 94 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

arise far lateral to the buccal roof. There displaced posteriorly in relation to the are several dozen barely visible pustu- tongue anlage. As a result the lingual lations distributed within the BRA. The papillae lie directly medial, rather than glandular zone has a very distinctive posterior, to the major infralabial pa- "V" shaped anterior margin with large pillae. The more medial infralabial pa- conspicuous secretory pits. Posteriorly pillae are small, robust, blunt projections the secretory pits tend to become much arising from the base of the keratinized smaller, denser, and less distinct, until beak at the anterior limit of the mouth. one reaches the regions of the pressure The larger, infralabial pair, in a more cushions, where they again become large typical position for infralabial papillae, and conspicuous. The free velar edge is are complex bifurcated structures. They short, discontinuous on the midline. The are directed medially but do not come medial limits of the velar margin have into contact or touch the interceding two or three small, simple papillae. lingual papillae. These infralabial pa- Dorsal pharynx.—The dorsal pharynx pillae have a cupped dorsal portion with was damaged in dissection, but enough the hollow of the cup pointing posterior- of the pressure cushions were preserved ly. The lower portion is a single blunt to indicate that these are relatively shal- projection, directed medially. The in- low bulges with the lateral cushion far fralabial papillae are fleshy, stiff struc- more distinct than the medial. Details tures that lack additional surface pustu- of the ciliary groove were not preserved. lations or papillae. The buccal floor Diagnostic summary.—No single fea- arena is exceedingly broad. Two, soft, ture distinguishes these larvae from oth- longitudinally oriented swellings arise ers examined; however, the following from the buccal floor anterior to the buc- characters, in combination easily diag- cal pockets. These run approximately nose the oral cavity of C. subpunctatus from the back of the infralabial region larvae: 3 pairs of infralabial papillae, to the medial corner of the buccal pock- BFA and BRA papillae very tall, bran- ets and define lateral boundaries for the chial baskets widely separated, filter BFA. The posterior half of the BFA is plates strongly imbricated but filter mesh defined by conventional rows of typical weak, glottis small, secretory pits large. papillae; however, these rows continue laterally as small papillae in front of Colostethus nuhicola (Dunn) the buccal pockets. I counted five BFA (Fig. 37) papillae on each side. Assorted pustulations occur in the posterior portion of Material.—Author's collection, uncat- the BFA and on the buccal floor direct- alogued (stage 34.5, sv. 8.3 mm). Col- ly anterior to the buccal pockets. The lected under leaves in small side pools buccal pockets have a large, fleshy pos- off of a tributary to the Rio Aquabiena, terior flap. They are deep and appear behind Tropical Science Center, Rincon, perforated in this specimen. The free Osa Penn., Costa Rica; March 8, 1970. velar surface is long and supported by Reference. — Dunn, 1924; Savage, long, conspicuous spicules. The free 1968; Heyer, 1976. edge is similar to that of Colostethus External.—Colostethus nuhicola lar- subpunctatus; there are small posteriorly vae have an umbelliform, denticle-free, directed peaks on the free velar edge oral disk, directed anteriorly in my speci- medially mens. The anterior surface of the disk over the second filter plate and is pustulate; the nonmuscular portion of directed peaks over the third filter plate.

the tail is slight; the spiracle is lateral. A tiny cusp, pointed posteriorly on each Ventral buccal.—The floor of the side, is aligned over the top of the fourth mouth is broad; the oral orifice wide. filter plate. There is a well-developed The lower beak is directed dorsally and medial notch. Secretory tissue exposed ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 95

Fig. 37.—Drawings of the floor (above) and roof (below) of the mouth of a Colosteihus nubicola larva. 96 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY on the dorsal side is similar to that of bous projection arises from the lateral C. subpunctatus. wall of the buccal roof on each side. Ventral pharynx.—Branchial baskets Each fills the space between the narial valve are similarly shaped to those of C. sub- projection and the lateral margins punctatus; however, the second filter of the nares. The postnarial arena is extremely small and is bounded poste- plate is not as tall while the third is papilla slightly taller and has a curved dorsal riorly by a small, truncated margin which virtually covers the third which on topographic grounds may be ridge. filter cavity. Counts for filter rows are the homologue of the median No other papillae are present in the post- 7, 8, 8, 5 for cb. 1-4; these are slightly fleshy less than those of Hyla regilla at a com- narial region except for a giant parable stage. The filter density and flap behind each narial valve projection a pustulation (homologue of lateral fold pattern is almost indistinguishable and from that of C. subpunctatus and less ridge papilla) immediately lateral to the dense than that of typical pond tadpoles. median ridge on each side. The flaps Tertiary filter folds are less well devel- just described is the largest structures oped in this dendrobatid than in the on the buccal roof. They are transverse- one previously described. Filter canals ly compressed with a rounded, free edge are very open channels. The branchial that covers the medial half of the inter- food traps are shallow, but cover a large nal nares on each side. The next largest area due to the large free surface of the structures associated with the buccal ventral velum. Secretory ridges could roof are simple, soft, oval projections barely be discerned at 50 X magnifica- arising from the far lateral walls of the posterolateral to the tion. The glottis is two thirds covered buccal roof directly by the ventral velum. In size and shape large flaps just described. These more homologues of it is similar to C. subpunctatus. The lateral structures may be in typical anu- esophageal funnel is relatively broad but lateral roof papillae more not as large as in C. subpunctatus. ran larvae. A faint, longitudinal ridge runs the length of the middle third of Dorsal buccal.—The buccal roof is the buccal roof on each side. These elongate. The prenarial arena is flat and structures vaguely define the lateral mar- very conspicuous. A narrow sharp ridge gins of a narrow BRA. There is a field runs from the anteromedial margin of of some twenty to thirty small pustula- the dorsal beak two-thirds of the way region directly behind and back in the prenarial arena. A papilla tions in the descends on each side of the prenarial medial to the ridges, but no papillae of arena about halfway between the upper any sort are present on the buccal roof

( papillae. The beak and the nares. Each is transversely behind the median ridge ) compressed with a gently curved, free, glandular zone is large, but its anterior ventral edge. Medially the ventral edge margin is poorly defined in this speci- for each papilla continues along the men. Individual secretory pits could buccal roof as a posteriorly directed not be discerned. The dorsal velum is ridge that converge on a tiny papilla of comparable size to that of more typi- midway between the internal nares. cal pond tadpoles. It is barely continu- There are no pustulations or additional ous across the midline. structures in the prenarial arena. The internal nares are oriented transversely. Dorsal pharynx.—Pressure cushions Their anterior walls are shallow and are distinct. The lateral cushion is small- lack projections or papillations of any er and more elongate along an anterior-

sort. There is a short, but distinct, narial posterior axis. The medial cushion is a valve projection far medial on the pos- larger, more oval bulge. The ciliary terior edge of the narial valve. A glo- groove was not preserved in dissection. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 97

Diagnostic summary. — Colostethus place of the BFA papillae, were ob- nubicola is very different from C. sub- served in no other species. The great punctatus in its buccal anatomy but it difference between C. nubicola and C. shares many features with other funnel- subpunctatus, plus the fact that only two mouthed larvae from other families. species have been examined, means that However, its particular pattern of infra- it is not possible to provide a single labial papillae, large flaps behind the diagnosis for the family Dendrobatidae nostrils, and parallel, pustulate ridges in at this time.

DISCUSSION

FUNCTIONAL CONSIDERATIONS assist in shredding food that is spit in and out of the mouth. From structural relationships and The second knowledge of the habits of various tad- type of internal keratinized structure is the poles, functions can be hypothesized for median cornified knob in the prenarial arena of many of the structures presented in the Scaphio- pus Descriptions. In the following section bombifrons. This knob has not been described previously, although it was variation in internal oral features is re- mentioned as a feature viewed and possible functions for these that could separate Spea from Scaphiopus structures are discussed. In many cases in Altig's "Key to additional comparative and experimen- U.S. tadpoles" (1970). The knob is ideally positioned to assist in tal work will be necessary to verify func- cutting long, firm plant tions proposed here. material. Elon- gate matter drawn into the mouth would Keratinized Structures be held in position by the medially directed pair of infralabial papillae. The Two types of internal keratinized lower beak would close between the structures have been observed. The first knob and the upper beak, thereby shear- is a medially directed spur located at ing the material. The presence of such the posterodorsal corner of the infrala- a preparative aid to ingestion in S. bom- bial cartilage, just posterior to the lower bifrons is consistent with the beak. These spurs are well developed known voraciousness of these larvae. in Gastrotheca riobambae and show weak development in Agalijchnis calli- Ueck (1967) reports keratinized dryas and Colostethus subpunctatus. structures within the oral tube of a Hy- They are too far back in the junction of menochirus boettgeri larva. Examina- the jaws to be applied to the substrate tion of a photomicrograph (Ueck, 1967, and the fact that they are directed me- Fig. 53), indicates identical morphology dially prevents their occlusion with with my own sectioned material of this either the upper or lower beaks. They species. What Ueck calls "die verhorn- have not been discussed in the litera- ten Zellen" appear to be cornified squa- ture, but have been illustrated in Rana mous cells in a thickened layer identi- is rugulosa by Noble ( 1927, Fig. 10). Their cal to what seen in the mouth of adult occurrence in tadpoles of such diverse Hymenochirus (O. Sokol, pers. comm.). morphology, ecology, and relationship GriflBths (1963) said that the mouth of makes it difficult to infer a function for Pseudhymenochirus is "armed" with these poorly known structures. The minute denticles. Although he cited an spurs simply may be associated with unpublished observation for proof of relatively large size in free-swimming this, I find no evidence for such denti- tadpoles of certain of the more advanced cles in my own sectioned material of

Type 4 families. It is possible that they this genus or any other pipid larvae. .

98 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Infralabial Papillae The infralabial papillae extend into the prenarial arena. The common com- There are normally two major infra- plex, hand-like infralabial papillae are labial papillae in all free-swimming tad- aligned directly in front of the internal poles of Types 3 and 4. These may be nares. In this position the papillae could augmented by as many as six minor very easily serve the function of direct- papillae on each side ( e.g., Hyla rufitela, ing particulate matter medially and Agalychnis callidryas). The two major away from the nares, where large parti- infralabial papillae can be long and sec- cles could cause obstruction. ondarily papillate (e.g., Ptychohyla leon- A possible function for the simple hardschultzei, Leptobrachium oshanen- globose papillae of some species is sis, Oreolalax) or short and globose (e.g., chemoreception; however, the papillae Hyla phlebodes, Hyla dendroscarta) have a poor surface-to-volume ratio for In Ascaphus the individual papillae this purpose. The papillae may be me- are replaced by a large, bilobed oral chanical sensors; in species where they valve (Gradwell 1971a, 1973). This are in medial contact, objects entering structure can be derived easily from two the mouth will collide with them. In infralabial papillae that have fused on Centrolenella, Microhyla and Mego- the midline. This valve allows Ascaphus phrys, the papillae are arranged so that larvae to cling to substrata without con- large particles can be prevented from tinuous pumping. However, such a valve accidentally entering the mouth cavity, does not occur in other suctorial tad- a function proposed by Liu (1950, p. poles (e.g., Hyla mixe; see also Grad- 191). Indeed, in funnel-mouthed forms well, 1975b, for Litoria lesueuri, L. (e.g., Ptychohyla schmidtorum, Mego- booroolongensis, L. glandulosa, L. citro- phrys minor, Microhyla. heymonsi, Colo- pa, and Mixophyes balbus) and is not stethus nubicola) the marginal palps fit essential for suctorial clinging. into the lateral margins of the posterior- Rhinophrynus has four tiny papillae ly directed "V" of the prenarial arena. unlike any seen in other tadpoles. A tight tongue-in-groove configuration is Judging from the drawings by Weisz formed, making it impossible for large (1945), Sterba (1950), Sokol (1962, particles to enter the corners of the 1977a) and Ueck (1967), infralabial pa- mouth. pillae are absent in the Pipidae. Microhyla has two or three knob-like Abundant medium size plant frag- infralabial papillae per side. ments have been observed in the guts of Hyla microcephala, which is similar There are three possible functions for to Hijla phlebodes and a close rela- the infralabial papillae: they may func- tive of it (Wassersug and Rosenberg, tion as respiratory structures, sensory 1979). The globose, medially abutting, structures, or mechanical interactors infralabial papillae of these species may with food or water currents. Respiration serve a function of providing informa- can hardly be a major function of these tion on the position of plant fragments, structures; for even in the species with informing the tadpole when filamentous highly dendritic infralabial papillae, plant matter is far enough back in the their surface area is only a small fraction mouth to be bitten off. of the surface area of the remainder of the buccal floor and pharynx. Accord- The globose infralabial papillae of ing to Gradwell (1972a, for R. cates- Hyla dendroscarta are an enigma. They beiana), "Relative to the pharynx and may simply be embryonic, considering examined. gill cavity the buccal lining is poorly the early stage of the tadpole vascularized and is probably of little Large, elongate infralabial papillae significance for blood oxygenization by are seen in all stream-adapted tadpoles the buccal water currents." that feed on the bottom (e.g., Ptychohyla )

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 99 leonhardschultzei, Oreolalax, Lepto- hylids examined, only Gastrotheca has brachium oshanensls, Hijla mixe) except four lingual papillae. Rana esculenta, Ascaphus. Duellman (1970, p. 412) il- R. pipiens, Pelobates fuscus and Bufo lustrated large, complex infralabial pa- cinerus (:= B. viridis) have two lingual pillae in Hijla smaragdina, a species of papillae (Schultze, 1870; Hammerman, the stream-adapted Hyla sumichrasti 1964), whereas Rana sylvatica, R. cates- group. The papillae point out of the beiana and R. clamitans have four mouth in these stream forms and may (Helff and Melhcker, 1941; Hammer- serve as taste or pressure receptors when man, 1964). Hammerman (1964) the tadpoles contact a hard surface. claimed that R. temporaria has two lin- Support for this hypothesis must await gual papillae, but Savage (1952) illu- experimental or neurohistological stud- strates and Dejongh (1968) reports four

ies. in this species. Kratochwill ( 1933) re- Lingual Papillae ported four lingual papillae in Rana

agilis = R. dalmatina ) . Kenny ( 1969a ( Ascaphus has a dense field of several illustrates two lingual papillae in Phyl- dozen lingual papillae, whereas lingual lomedusa trinitatis. Lingual papillae papillae are absent in microhylids, Rhi- have a chemoreceptive function (Ham- nophrynus, and, by definition, in the merman, 1967, 1969; Helff and Mel- aglossal pipids. Discoglossid larvae have licker, 1941). a variety of patterns for the surface anatomy of the lingual anlage. At one ex- Buccal Floor Arena treme is Alytes obstetricans, with a dense The BFA is nonexistent in certain field of pustulations similar to the field species (e.g., Megophrys minor, Hyla of papillae in Ascaphus; at the other phlebodes, H. ebraccata, H. sarayacuen- extreme is Bombina orientalis with a sis) or ill-defined (e.g., Scaphiopus bom- single medial projection. Ahjtes cister- bifrons, Centrolenella fleischmaiini) be- nasii has two lingual papillae and many cause of the absence of papillae. In all pustulations; Discoglossus pictus has an other species studied papillae of the arch of six enlarged papillae of which buccal floor define some sort of bilateral- the medial ones are fused. These latter ly symmetrical area. The arena is usu- two species demonstrate morphological ally oval or egg-shaped in the hylids, patterns intemiediately between the ex- pelobatids and Alytes. Illustrations in tremes of the family. the literature indicate that the oval pat- A single medial projection occurs in tern also occurs in Rana and Bufo (see Anotheca, but it is grossly dissimilar to Savage, 1952). In Ascaphus, Bombina, that of Bombina. Duellman (1970, p. Discoglossus, Colostethus, Agalychnis 326) illustrated a single medial projec- (and its relative Phyllomedusa trinitatis, tion in Hyla zeteki. If this is a homo- Kenny, 1969a), Hyla dendroscarta, and logue to the lingual papilla, it is a re- the stream-adapted Hyla mixe and markable convergence with Anotheca. Ptychohyla schmidtorum, the papillae ( Both H. zeteki and Anotheca are large- at the front of the arena diverge to form mouthed, carnivorous, arboreal larvae.) a "V" or "U" shaped arena. In Rhino- tadpoles examined The remaining phrynus and the microhylids the papillae normally either zero, two, or four had are limited to a broad arc behind the lingual papillae. The papillae were ab- buccal pockets. Papillae of the buccal sent in H. phlebodes, H. sarayacuensis, floor are evidently absent in the Pipidae H. mixe and the megophrynine pelobat- (Sokol, 1962, 1977a; Ueck, 1967; Sterba, ids. In some of these forms, however, 1950). anterior papillae or pustulations near the infralabial papillae may be homologues The BFA papillae are most often of the lingual papillae. Among the slightly compressed, conical structures, 100 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY which if large enough, curve medially. pass through the BFA and BRA papillae Certain tadpoles have rather specific at the back of the arena, it could be types of papillae unlike those seen in coughed out of the mouth. Such cough- any other species (e.g., the blunt, out- ing motions are well known in tadpoles turned cylindrical papillae of Anotheca; subjected to irritating substances in the the pustulate papillae of Oreolalax). The water. One reason for having a buccal papillae are most numerous and attenu- straining mechanism is that it prevents ate in the stream species, the extremes large particles from entering the pharyn- being Ptychohyla leonhardschultzei (89 geal cavity where they might clog the papillae) and Hyla mixe (70 papillae). filters or the food traps. A similar siev- Gradwell (1972c) independently noted ing function has been proposed by Se- that papillae of the buccal floor are vertzov (1969). "better developed" in the stream-adapted Stream-adapted tadpoles that scrape tadpoles of Rana fiiscigula than in lar- food from rocks have the densest mesh val R. catesheiana. of buccal floor and roof papillae. These Bifurcation of BFA papillae seems to are tadpoles which ingest a rather be associated with the size of individual coarse, self-generated suspension of papillae rather than with an arena of foods, as opposed to the free suspension some specific shape or with the number of microscopic plankton found in ponds of papillae. Terminal bifurcations are or pools. The stream tadpoles have re- commonest on the larger papillae in spe- duced gill filters, and instead of using cies which have tall papillae. pharyngeal structures to strain their food the major Possible functions for the BFA pa- job may be done by the BFA papillae. pillae are similar to those proposed for and BRA the infralabial papillae. Again, respira- The pond-adapted tadpoles of the tion may be ruled out as a primary func- Hyla leucophyllata and H. microcephala tion, although in some of the stream- groups lack buccal arenas, and must use adapted species the surface of the BFA their small orifices as the primary food papillae is substantial. A sensory func- sieve. The reduced BFA of Scaphiopus tion is most commonly proposed (Kra- bombifrons is difficult to interpret. It is tochwill, 1933; Kenny, 1969a and 1969b). possible that with its relatively fine filter filter Gradwell ( 1972a ) wrote that "the shape mesh and single large, cavity on and orientation (of these papillae) sug- each side, Scaphiopus faces little risk gest a role as detectors of particulate of clogging the filters. material in the respiratory system." Megophrys minor and, to a lesser While this is plausible, I suspect that extent, Ptychohyla schmidtorum and the papillae may do more than just Colostethus nubicola, have replaced sense particles; they could be important rows of papillae with ridges. Both of both in sorting and directing particulate these funnel-mouthed forms have two matter in the mouth. In most species ridges that extend posteriorly from the the buccal roof arena and buccal floor tongue anlage and interlock with ridges arena intermesh; thus, the spaces be- on the roof of the mouth. These massive tween the papillae are not large (0.1- structures probably act as baffles, chan- 1.0 mm on the average). When a parti- neling particles backward in the mouth. cle larger than the distance between two buccal floor or roof papillae comes into Buccal Pockets the mouth it should be retained medially. The shape and size of the buccal Because the arenas narrow posteriorly, pockets depend on the shape of the particles would then be funneled poste- posterior margin of the ceratohyals and riorly and into the esophagus. Of course, the anterior margin of the branchial bas- if a particle is so large that it cannot kets. The pockets may be very large in ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 101

all dimensions, as in Leptobrachium, or function for it. Perhaps perforation is so small as to be nearly absent, as in simply an embryonic feature occasionally Hyla phlebodes. The pockets are evi- retained in Type 4 tadpoles. dently perforated only in Centrolenella Prepocket Papillae fleischmanni, Colostethus nubicola, Ptij- and Other Features of the Buccal chohyla, Similisca sordida, Hyla rufitela, Floor Gastrotheca riobambae, Hyla regilla (6 Prepocket papillae, or at least papillae out of 9 individuals), Oreolalax pingii or pustulations over the body of the and Leptobrachium hasselti. Some in- ceratohyals, are present in virtually all dividuals examined were too small to species examined except Scaphiopus determine the state of this character. bombifrons. Typically there are one to Perforation does not seem to be associa- three papillae that project backward ated consistently with any particular over the buccal pockets. These papillae habitat or behavior and is a variable are most numerous in species with a character within genera and species. "U" or "V" shaped buccal ffoor arena, The buccal pockets, as folds of skin, where the BFA papillae series becomes allow some autonomous movement of continuous with the prepocket papillae the buccal pump relative to the bran- series. In species which have few BFA chial baskets. One might expect that papillae, there are few papillae on the species with much rotation in the buc- arms of the ceratohyals. Microhyla, Cal- cal pump (see Wassersug and Hoff, luella, and Glyphoglossus (see Savage, 1979) would have the deepest pockets, 1952, Figs. 21 and 26) and, presumably, but this does not appear to be so. other microhylids have only one very large prepocket papilla. The significance of perforation of the From the literature one can conclude that such papil- pockets is not clear. Gradwell and Pasz- lae are tor (1968) discovered that the buccal absent in the pipids. pockets were open gill slits in Rana The prepocket papillae may prevent catesbeiana and constructed an elaborate particles from entering the buccal pock- hypothesis for the function of "this pha- ets. Together with the papillae of the ryngeal by-pass." They suggested that buccal arenas they could act as sieves. The lateral roof papillae, the open slits may be a common feature in species which escaped the notice of earlier work- where they occur, are aligned over the ers because of concealment by the pos- buccal pockets and may assist the pre- terior walls of the ceratohyals. In a pocket papillae in some protective function. In Rhinophrynus, where prepocket later article Gradwell ( 1972a ) viewed lateral the condition of Rana catesbeiana as ex- and roof papillae are absent, ceptional, differing from "Ascaphus, there are transverse ridges on the buccal Xenopus, Scaphiopus, Phyllomedusa, and roof that insert into the buccal pockets; these many other genera." The Australian lep- may accomplish the same protec- todactylid Mixophyes balbus lacks per- tive task. forated buccal pockets (Gradwell, In many species with numerous buccal floor papillae, 1975b ) . I doubt that the pharyngeal by- a distinctive row or pass is of much significance in terms of patch of papillae and pustulations may passage of water. Even in species with develop behind as well as in front of large buccal pockets the slits are small the buccal pockets. In at least one genus compared to the pharyngeal gill open- (viz., Ftychohyla) these are opposed ings. Epithelial folds from the walls of dorsally by a similar patch. Again, a the pockets clearly act as valves, retard- straining or sieving function may be in- ing passage of fluid. The strange ecolog- ferred for these structures. ical and taxonomic distribution of this In species of Microhyla there are one character makes it difficult to identify a or more papillae aligned directly in front ^

102 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY of the glottis. These could be very im- Rhinophrynus the velum is fully (to its portant in sensing particles entering the posterior margin) attached to the tops mouth and also in directing particles of the filter plates of cb. 2 and 3. In the away from the glottis. Rhinophrynus, microhylids it is attached only partially which, like the microhylids, has its glot- (anteriorly) to the tops of these arches. tis arising from the middle of the buccal In both cases major projections of the floor, also has anteromedial papillae in velar margin are lacking, the margin is front of the glottis on the buccal floor gently curved, and the glottis arises from arena. In Rhinophrynus, however, these the buccal floor anterior to the velar are paired and lateral to, rather than margin. This condition, which I ob- centered on, the midline. served in Microhyla herdmorei and M. Other tadpoles have unique arrange- ornata, was observed by Savage (1952, molossus, ments of buccal floor features for which 1955) in Glyphoglossus Chap- erina fusca, CaUuella guttulata, Kaloula it is not so easy to hypothesize functions. pulchra, harheri Examples are the transverse row of buc- and Hypopachus ( in cal floor papillae seen in Hyla rufitela aquae), and by Gradwell (1974) Phrynonierus annectens. Clearly the pat- and the lateral papillate lobes of the tongue anlage in Leptohrachium osha- tern is typical of the family. nensis. The singular occurrence of these Of the four other configurations for features and our limited knowledge of the velum, one is shared by the Orton the ecology and behavior of these tad- Type 3 tadpoles, Ascaphus, Romhina, poles make functional speculations in- Discoglossus and Ahjtes. This is the con- appropriate at this time. dition in which the velum is continuous across the midline, but anchored to the

Ventral Velum tops of cb. 2 and 3, and the margin is

This is an important valve which either straight or convex anteriorly be- separates the anterior buccal cavity from tween the filter cavities. These four gen- the posterior pharyngeal cavity. Kenny, era are listed here in the order of de- Gradwell, Dejongh and others have pre- creasing thickness of the velar margin. sented evidence to show that the margin The most common configuration is of the ventral velum can press against for the velum to be continuous across the buccal roof and prevent regurgita- the midline, and partially attached to tion of water from the pharynx when the tops of the filter rows. Posterior pro-

the buccal floor is depressed. The ven- jections of the velar margin are usually tral velum also supports the mucosa of present and conspicuous. This is the the branchial food traps. Only the val- condition for the dendrobatids, centro- vular function of the velum is considered lenids, and most hylids examined. Judg- here. Although secretory pits on the ing from the literature, this pattern is dorsoposterior margin of the velum are typical of other advanced Type 4 tad- discussed in this section, comments on poles. Scaphiopus bombifrons and the the ventral secretory tissue are reserved megophrynines seem to be exceptions. for the section on the food traps. In those tadpoles a fifth configuration is Six major configurations of the ven- seen. These species have the velum an- tral velum are noted. Two of these have chored anteriorly but virtually lack any the ventral velum divided into right and attachment of the velum to the tops of left halves and interrupted on the mid- cb. 2 and cb. 3. Schultze (1892) illus- line. Of these two, one is the condition very tall found in Rhinophrynus; the other is the trated Pelobates fuscus with condition in the microhylids (with the filter plates on cb. 2 and 3, so it is possi- technical exception of Microhyla hey- ble the velum in that species is more monsi, see Description and below). In like that in the other Orton Type 4 tad- )

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 103 poles than that in the pelobatids I ex- velum can close passively from back amined. pressure. This is the same mechanism

The last configuration is the absence that closes similarly shaped pocket valves in circulatory of a valvular velum in the pipids ( Sokol, the vertebrate sys- 1962, for Hymenochirus; Menzies, 1967, tem. Because of the long attachment of for Pseudhymenochirus; Weisz, 1945; the velum to the tops of the filter plates Sterba, 1950; and Gradwell, 1971a, for in Ascaphus, discoglossids and Rhino- Xenopus; Sokol, 1977a, for Pipa). Not phrynus, not only the velum but the pos- all pipids are identical. In Xenopus the terior portion of the hypobranchial plate floor of the common pharyngeobranchial must rotate upward in order for the tract is covered by secretory ridges mor- buccal floor to be sealed off from the phologically similar and presumably ho- filter chambers. In all tadpoles except mologous (Kenny, 1969b) to those pipids (Sokol, 1977a) the anterior edges found on the ventral surface of the ven- of the hypobranchial plates are over- tral velum in Type 4 tadpoles. In Hy- lapped by the ceratohyals. As the cera- menochirus and Pseudhymenochirus the tohyals are depressed the hypobranchial surface is devoid of any organized secre- plate rotates on a transverse axis. This tory tissue. mechanism aids in closing the velar valve and is reviewed in Wassersug and In species with a valvular velum Hoff (1979). (As a functional com- there is always positive pressure in the plex, this mechanism provides insight atrial chamber surrounding the gill fila- into why pipids, which lack the hypo- ments and one-way flow out of the spir- branchial/ ceratohyal articulation, also acle. The division of the ventral velum lack a valvular velum. into right and left halves in Rhino- In Ascaphus truei there is posterior- phrynus and the microhylids should not a ly directed "V"-shaped trench on the affect the valvular function of the velum. buccal roof above the ventral velar mar- Even for species with an undivided vel- gin. The thickened velar margin insets um, Kratochwill (1933) and Kenny into the trench the valve is shut. (1969a) argued that the flow of water when Such a structural arrangement is remi- from the buccal cavity into the pharynx niscent of a gasket on a high pressure will be by separate right and left seal. That such a system should appear streams. Gradwell (1970) verified this in this torrent-adapted larva is no sur- and showed experimentally that each prise. Gradwell (1971a) found a mean side of the velum can act independently maximum oral disc suction of - 125 torr in R. catesbeiana. This independence is in five live, stage 32 Ascaphus tadpoles. obligatory in Rhinophrynus and the microhylids. In the pipids, which lack a The discoglossids show a thickened velar similar of valvular velum, one-way flow is achieved margin to that Ascaphus by the opercular flaps acting like valves, but not as extensive. They also lack a opening and closing with each cyclic trench on their buccal roof. depression of the buccal floor. For these Although Rhinophrynus has little mo- species atrial pressures must be lower bility of the velar margin, the roof of than ambient pressures during part of the mouth above the free velar surface the cycle. is contoured to assure sufficiently large For any species the mobility of the contact area to close the valve. velar margin and the strength of the All the stream tadpoles with suctorial valvular seal are determined by the velar mouths except Ascaphus have spicules length and thickness, the extent of at- that are longer, stouter, or both, than the tachment of the velum to the underlying spicules of Hyla regilla or Acris crepi- filter plate, and the stiffness and length tans. These stream forms must produce of the spicules. In most species the relatively great negative buccal pressures 104 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY in order to adhere to rocks with their Agalychnis. When present, projections oral discs. Presumably, the enlarged usually number one each for each filter spicules serve to strengthen the valve cavity, with two or more additional pro- and prevent prolapse. The tadpoles of jections in front of the esophagus. Su- the Hyla leucophyllata species group pernumerary projections are present in have wide spicules and a thickened free Leptobrachium and Oreolalax. In these, velar surface. One can hypothesize that general projections may arise from the these tadpoles produce relatively great ventral medial surface of the velum as suction during inspiration. This may be well as from the posterior medial edge. important for drawing rather large frag- The most extreme development of super- ments into the mouth. Hyla phlebodes numerary projections is seen in Lepto- has a very short ventral velum unsup- brachium oshanensis, which has a multi- ported by spicules. The shortness of the layered papillate fringe on the medial velum insures some protection from col- edge of its ventral velum. When the lapse when the valve is elevated. Micro- branchial baskets are an unusual shape, hyla heymonsi, which appears to feed on such as with the reduction of filter cav- large particles, has the thickest and pre- ity 3 in certain stream tadpoles, there is sumably the strongest ventral velum in a concomitant shift in the position of the in the example of the genus. Microhyla berdmorei and M. projections (medial tadpoles; see ornata, in contrast, have very delicate the stream below). ventral vela and it is clear that they There is no literature concerning the could not endure a high pressure differ- possible function of the velar projections, ential between the buccal and pharyn- although they must affect the valvular geal cavities without a collapse of the workings of the velum. With long and valve. numerous projections such as are pres- it im- Two arboreal species, Hyla dendro- ent in stream tadpoles, becomes or scarta and Anotheca spinosa, have re- possible for the velar seal to open close abruptly. The projections may play duced ventral vela with little or no spic- flow and ular support. The velum may be a func- a role in regulating laminar directing currents over the edge of the tional valve in H. dendroscarta, but is so velum when the buccal floor is elevated reduced in A. spinosa that it is hard to and water is pushed over the velar edge imagine how it could function. In Ano- into the pharynx. theca the pharyngeal cavity itself is also extremely reduced, so that it may not The medial portion of the ventral matter whether the velum is valvular or velum is displaced dorsally and anterior- not. The most unusual vela were seen ly in Anotheca and Gastrotheca due to in Megophrys minor and Scaphiopus a large laryngeal disc. The same portion bombifrons. At the present, the func- of the velum is turned upward and for- tional implications of their velar shapes ward in Ptychohyla schmidtorum and are obscure. Leptobrachium oshanensis, but neither has a large, early devel- Two general patterns are evident for of these species glottis. Although the configura- sculpturing of the velar margins as seen oping tion in these two species may be a pres- in dorsal view. This edge is most likely ervational artifact, it is strange that it to appear as a smooth, gentle arc in tad- larvae similar poles associated with standing water. In should occur in of such tadpoles associated with moving water overall ecology. marginal projections are distinct and In a general way, the extent of de- numerous along the velar margin. There velopment of the median notch reflects are, however, some outstanding excep- the size and development of the glottis. tions. Marginal projections are lacking At one extreme is Anotheca spinosa with in Ascaphus and quite distinctive in a median notch half the width of the ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 105 ventral velum and a large, functional has been proposed for the mucous strand glottis, which develops early, exposed generated by the secretory ridges under within. At the other extreme is Ascaphus the velum (Wassersug, 1972). truei, which lacks a median notch and functional lungs as a larva. The Filter System The secretory pits on the velar mar- Different species vary enormously in gin have been discussed previously by the extent of the development of the fil-

) for ters. This variation is most evident in Kenny ( 1969b one species ( Pseudis paradoxa) and more recently and exten- the size and shape of the branchial bas- sively for a large variety of species kets. Massive branchial baskets charac- by Wassersug and Rosenberg (1979). terize Agalychnis calUdryas, Phyllome- No particular pattern of density or size dusa trinitatis (Kenny, 1969a), the mi- is evident other than that the pits are crohylids excluding Microhyla heymonsi most common on the posterior projec- ( see Savage, 1952, 1955, for genera other tions of the velar margin and conse- than Microhyla ) , Xenopus ( Sterba, 1950; quently most numerous in species with Ueck, 1967) and free-swimming Pipa well developed posterior velar projec- (Sokol, 1977a). Among the species ex- tions. In Ascaphus and Bombina a fine- amined, Bombina orientaUs, Scaphiopus grained secretory tissue is seen under bombifrons, Hyla femoralis, Hyla rufi- the dissecting microscope instead of well tela, and Gastrotheca riobambae have organized secretory pits. In Alytes a few baskets slightly larger than "typical" tiny pits can be seen on the margin, pond larvae, such as Hyla regilla and while in Rhinophrynus secretory pits per Acris crepitans, but not nearly as large se are absent from this region. In spe- as in the species just mentioned. In cies with a reduced velum (e.g., Hyla those species with an enlarged pharynx phlebodes) secretory tissue along the the greatest increase in size is in the ventral velar margin cannot be resolved length of the filter plate. Also common- with light or scanning electron micro- ly exhibited is an increase in height. scope (Wassersug and Rosenberg, The ceratobranchials tend to have a 1979). more longitudinal, less oblique, orientation in The pits of the ventral velum oppose these forms. Scaphiopus is some- the secretory tissue of the glandular zone what an exception in that its branchial baskets are and presumably function in concert with bowl-shaped and, although larger overall than that tissue. As noted by Kratochwill those of H. regilla, the filter plates of 2 (1933), the edge of the free velar sur- cb. and 3 are much face matches the shape of the glandular reduced in height. zone. Gradwell (1970) suggested that Large branchial baskets are asso- friction of the velar edge meeting the ciated with specialization for suspension- buccal roof may be reduced by mucous feeding, particularly in species which secretion. This mucus could be extruded lack keratinized mouth parts (Savage, from the margin of the ventral velum as 1952). However, one must be cautious well as the glandular zone and, as dis- of this generalization (see Kenny, cussed by Wassersug and Rosenberg, 1969a ) ; pharyngeal size alone cannot be could act both to lubricate and seal the the determining factor for the size range valve. Kenny (1969b) and Wassersug or volume of particles removed from the and Rosenberg (1979) have suggest- water by a tadpole. The density of the ed that the secretory pits may be in- filter mesh, and other oral features such volved in the food trapping process. as buccal floor and roof papillae, bran- Mucous strands excreted by the secre- chial food traps (Wassersug and Rosen- tory pits of the roof and floor could berg, 1979), volume of the buccal catch and aggregate plankton much as pump (Wassersug and Hoff, 1979) and )

106 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY size of the orifice will have a pro- mentous tails and reduced denticle rows found effect on the quality and quantity, may be convergent with truly special- including size range, of food ingested. ized suspension-feeders such as Xenop- At the other extreme, the filter bas- us, but this now appears to be an over- kets are much reduced in Hijla phle- generalization, at least for H. phlehodes. bodes and Anotheca spinosa, and slightly In an earlier part of this discussion, it reduced in Hyla saraijacuensis, Colo- was suggested that H. phlehodes tad- stethus nubicola, Microhyla heijmonsi poles may ingest vegetative strands that and Megophrys minor. Filter surfaces they cut into fragments of moderate are totally lacking in Hymenochirus ( So- size. The reduction of the branchial kol, 1962; Ueck, 1967) and in Pseud- baskets is consistent with the view that hymenochirus (pers. obs.). Reduction larger fragments and not the smaller important food for this is exhibited in both the height and plankton are the length of the filter plates. species. Larvae of the ranid genus Ooeidozyga have mouths which are sim- Reduction of the branchial baskets ilar in gross features to the hylids of the occurs in three types of tadpoles. The H. leucophyllata and H. microcephala first includes known carnivores such as Hymenochirus and Anotheca. These species groups. Serial sections of the pharynx and digestive tract of an Ooei- tadpoles lack any ability to extract fine larva reveal reduced bran- plankton from suspension and instead dozyga laevis chial baskets as well as coarse plant select relatively large individual prey matter in the intestines (Wassersug, un- items. From stomach contents (Parker, published). While this further demon- 1931; Cei, 1968) it would seem that the strates convergence with certain hylid aberrant leptodactylid Lepidohatrachus larvae, the observation does not support fits into this class; indeed, serial sections the view that Ooeidozyga larvae are of Lepidohatrachus llanensis larvae re- carnivorous (Alcala, 1962). Heyer con- veal extreme reduction of the branchial cluded from his study of larval gut con- baskets (Wassersug, unpublished). tents that Ooeidozyga tadpoles are omni- The second type includes tadpoles vores, or if carnivorous, only facultative- which feed at the surface using upturned ly so. funnel mouths. Examples are Colo- Stream-adapted tadpoles do not show stethus nubicola, Microhyla heymonsi toward either expand- and Megophrys minor. This reduction any strong trend branchial baskets. How- suggests that funnel-mouthed tadpoles ed or reduced ever, a common feature of bottom-dwell- are not as dependent on microscopic ing forms with suctorial mouths is an particles for food as is implied by some anterolateral displacement of the pos- of the older literature. Pope ( 1931 teromedial edge of the branchial bas- commented on the sparsity of micro- kets. This gives the third filter cavity a scopic organisms in the clear mountain truncated appearance. Also, there is a pools inhabited by funnel-mouthed lar- tendency (except in the stream mego- vae. Heyer (1973) found small arthro- phrynines) toward extensive imbrication pods in the guts of larval M. heymonsi, the filter plates. These modifications, and Smith (1917) showed surprise at of amounting to a broadening and dorsal- the relatively large particles that Micro- of the pharynx, are hyla achatina could ingest. ventral shortening consistent with the low, broad, profile The last type of tadpole with reduced orga- branchial baskets includes pond species characteristic of stream-adapted which lack denticle rows, exemplified by nisms (Hora, 1930). Centrolenella lar- Hyla phlehodes and, to a lesser extent, vae, in contrast, exhibit elongation of the by Hyla sarayacuensis. Wassersug (1973) filter cavity. Their branchial profile ap- suggested that hylid larvae with fila- pears to reflect the general elongation of ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 107

the tadpole and can be understood as an 1962 ) , whereas Pipa carvalhoi has counts adaptation to burrowing (Gans, 1975). of approximately 14, 19, 25 and 16 (So-

Although relative size only is dis- kol, pers. comm.), all significantly above cussed above (i.e. size of the pharynx the range for H. regilla. From Sterba's compared to size of the buccal cavity), ( 1950 ) illustration it is clear that Xeno- it should be noted that there seems to pus laevis has significantly more filter be a natural upper limit on the absolute rows on all arches than does H. regilla. size of the branchial baskets. Despite The number of filter rows seems like a their giantism, larvae of Pseudis para- rough, but good, indicator of the amount doxa have branchial baskets no larger of effort any species puts into micropha- than those of bullfrog tadpoles one third gous suspension feeding. to one half their total length (Parker, Substantial variations in the filter 1881). mesh between species provide a clear Directly correlated with the overall indication of a species' ability to extract size and shape of the branchial baskets small particles from suspension. Filter is the number of filter rows on each filter porosity, however, may not be the abso- plate. The number of filter rows, how- lute determinant of the lower size limit ever, is somewhat affected by the abso- of the particles a filter feeder can extract lute size of the pharynx, so comparison (Kenny, 1969a; Wassersug, 1972; see of species with very large larvae with LaBarbera, 1978). Of the species ex- species with very small larvae may give amined, Rhinophrynus dorsalis, Agalych- slightly different counts even though the w.s callidryas, Microhyla berdmorei, and tadpoles have the same shape and pro- M. ornata have a particularly tight filter portions. mesh, whereas Anotheca and Hyla phlebodes have no filter mesh. Species with Of the species examined, the highest a filter mesh sHghtly denser than that of counts for filter rows were in Microhyla Hyla regilla include Hyla femoralis, berdmorei, M. ornata, Rhinophrynus dor- Hyla rufitela and Gastrotheca riobam- salis and AgaJychnis callidryas, whereas bae. Species with a slightly less dense the lowest counts were in Anotheca spi- mesh are Ascaphus truei, the discoglos- nosa and Hyla phlebodes. In the above sids, megophrynine pelobatids, dendro- species, counts were significantly (p < batids, Microhyla heymonsi, and the re- .05) different from Hyla regilla for all maining hylids with the exception of four filter plates (cf. Table 1; Wasser- Acris crepitans and Smilisca sordida. sug, 1976b). In certain other species, Scaphiopus bombifrons has a denser fil- one or two, rather than all four, filter ter mesh than H. regilla on the rows plates had significantly fewer or more proper but greater spaces between the filter rows than H. regilla. Thus, Hyla rows. sarayacuensis shows a tendency toward A tight filter is reducing the number of filter rows as mesh most commonly achieved longer does Leptohrachium hasselti, whereas by tertiary branches on Scaphiopus bombifrons and Hyla femo- the filter folds and by an increase in the number of higher folds. ralis show a tendency toward increasing order It is possible the number of rows. to achieve a tighter mesh without changes in the branching pattern by Kratochwill (1933) gave counts for widening the individual side folds (e.g., filter rows in Rana dalmatina that were Agalychnis) or by widening the rows in within the range for Hyla regilla, except toto (e.g. Gastrotheca). The continua- for cb. 4, which had a higher count. tion of filter rows from one filter plate to Such a difference may reflect differences in the shape of the branchial baskets or the next over the gill slits at the bottom in counting procedure. There are no filter of the filter cavities is a unique feature rows to count in Hymenochirus (Sokol, of Gastrotheca. This assures that large — .

108 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY particulate matter in the filter cavities have filter shelves. The acuteness of the cannot accidently escape through the gill ridge tips will vary with preservation. slits into the atrial chamber. Sokol Gradwell preserved his specimens in (1977a) reports a somewhat similar sit- Bouin's Reagent, which tends to shrink uation in free-swimming Pipa larvae. In tadpoles more than preservatives used these tadpoles, however, filter ruffles are by Kenny. Shrinkage would accentuate fused with the ruffles on neighboring the ridge tips, narrow the filter shelves, rows of each filter plate rather than ver- and open the filter niches in such a way tically over the gill slit. In Pipa, filter that individual filter crevices may not be canals are present but overlaid with a obvious. continuous filter mesh that must be cut Gradwell (1972a) has discussed the in order to expose the canals. I have filters as respiratory structures. They are verified this unusual anatomy in my own well vascularized, but their actual im- material of Pipa parva. portance to gas exchange has not been

Reduction of filter mesh is most com- measured and must vary greatly between monly achieved by deletion of higher species. In tadpoles such as Xenopus order folds and shortening of secondary which lack gill filaments, the gill filters folds. Slight reduction can be accom- are obviously important respiratory plished without a change in the branch- structures ( Millard, 1943 ) ing pattern by a simple thinning of all In many of the specimens examined, the folds. Wispy ribbons of tissue re- flocculent matter covers the filter sur- main as the vestiges of filter rows in faces or packs the anterior ends of the Anotheca spinosa. In the extreme reduc- filter cavities. There can be little question of the filter rows of Hijla phlebodes tion that the main function of the filters the main fold is retained as a raised knob is to retain in the pharyngeal cavity par- on the gill bar. ticulate material which enters the mouth A few species have filter rows that with the respiratory current. The cur- are distinctive for other reasons than the rent discussion is limited to a considera- tightness of their filter mesh. Ascaphus tion of the role of the filters in feeding. truei and Bomhina orientalis share un- Kenny ( 1969a ) set the lower limit usually straight main filter folds with for the dimensions of the filter niches at short, robust, side branches. 5 /xm for PhyUomedusa trinitatis. Be- Kenny (1969a) labelled the tops of cause P. trinitatis has large, dense filters, the filter folds as filter ridges in Phyllo- this may be near the lower limit of the medusa trinitatis and called the edges pore size for anurans in general. This of the filter ridges "filter shelves." How- measurement of 5 /xm, however, was ever, Gradwell (1972a) states that he made on fixed material and, as noted by found no filter shelves or filter crevices Kratochwill (1933), under positive pha- in Rana catesbeiana, whereas he does ryngeal pressure the filters should identify "pointed cells" at the crests of flatten and expand to form a tighter the ridges. I suspect that the discrep- mesh. The strange, truncated shape of ancy observed here is more the result of the filters and their resilience may relate semantics and preservational artifacts to this ability to vary surface area and than true differences between species. porosity with pressure. Under actual Both Kenny's and Gradwell's Fig. 9 feeding conditions the filter niches may

their independent illustrations of the fil- be smaller than 5 /xm in some of the ter rows—are somewhat ambiguous. I species specialized for suspension-feed- interpret the "tops of the filter ridges" of ing. Nevertheless, when very fine par- Kenny to be the same as the "pointed ticulate matter is found on filter surfaces, cells" of Gradwell. Under this designa- the particles are invaribly clumped in tion, Rana catesbeiana must necessarily mucus; yet the filters themselves are not ,

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 109

secretory. Thus, despite fluctuating filter cies examined, the largest collecting sur- niche porosity, ultraplanktonic entrap- faces were observed in Gastrotheca rio- ment must be initiated elsewhere in the hamhae and Agalychnis callidryas. The mouth than on the filter surfaces. smallest were seen in Hyla phlebodes. Questions remain as to how food Branchial food traps are absent in Ano- matter is removed from the filter, and theca and we may conclude from the why mucus does not adhere more tena- literature that they are absent in Hymen- ciously to these surfaces. Kenny (1969a) chirus and Pseudhymenochirus (Sokol,

has suggested that there is some back- 1977a). wash through the filters during part of The shape of the area covered by every pumping cycle. In Rana cates- secretory tissue is largely determined by beiana, however, the pharyngeal pres- the shape of the ventral velum. Where sure is only briefly and very slightly the velum is completely anchored to the negative during the pumping cycle top of the filter plate (in Ascaphidae,

(Gradwell, 1972b), so that backwashing Discoglossidae, and Rhinophrynidae ) is unlikely. Reorientation of the filter each filter cavity has a separate collect- plates may actually dislodge food parti- ing area. In Ascaphus and the discoglos- cles from the filter plates during each sids the branchial food traps are further pumping stroke. Because of rotation distinguished by a large, elevated rim in the hypobranchial plate the filter that separates them ventrally from the plates should be stretched every time filter surfaces on the filter plates. Lepto- the buccal floor is depressed. In most brachium has an expansion of the area species, the pressure cushions are shaped covered by secretory tissue onto the dor- to fit the filter cavities closely. The se- sally facing surface between the fourth cretory pits found on the cushions might ceratobranchials anterior to the glottis. help lift material from the filters. The The microhyids and Rhinophrynus answer to why mucus does not clog the have collecting surfaces which are simi- filters lie could conceivably in some lar in their gross shape. The surface is aspect of the histochemistry of the mu- more (e.g., Microhyla berdmorei or less cus and the cells that make up the filter (e.g., Microhyla heymonsi), restricted epithelium. Kenny (1969b) noted that to a dense, narrow, vertical crescent at the cells which line the filter niches can the anterior end of the filter cavity. In be distinguished from other cells in the Microhyla berdmorei much of the velar filters because they stain unusually heav- surface is devoid of secretory tissue. ily with Orange G. Perhaps the most unusual collecting Branchial Food Traps and surfaces occur in Xenopus. Here the secretory ridges Secretory Ridges are transposed to the ventral surface of the common bucco- In most species the entire free velar pharyngeal cavity along the top of the surface is covered ventrally secretory by filter plates. The gross shape of this ridges. Thus, rele- the parameter most secretory surface has been described and vant to the size of the branchial food illustrated by Weisz (1945), Sterba traps is the size of the free velar surface. (1950), Gradwell (1971a, 1975a) and The height of the branchial baskets may Sokol (1977a). Pipa and Hymenochirus size of the collecting sur- also affect the lack these collecting surfaces (Sokol, face because the secretory ridges com- 1975). monly cover a portion of the anterior The histology of the secretory tissue

and lateral surfaces of the , filter plate. has received extensive discussion by branchial baskets are very When the Kenny ( 1969b ) and Wassersug and Ro- shallow, the ventral extent of the secre- senberg (1979). Kenny reported se- tory area must be limited. Of the spe- cretory pits in Pseudis paradoxa along .

110 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY the margin of the ventral velum and Although I have concurred with this thought them unique to P. paradoxa. view (Wassersug, 1972), the question of Secretory pits are in fact common on the the functional meaning of the textural most posterior edge of the velum in patterns of secretory tissue remains un- many species, particularly those with answered. long velar projections. Organized secre- Glottis and Laryngeal Disc tory ridges (Wassersug, 1972) are absent in the Ascaphidae, Discoglossidae There seems to be considerable range and Pelobatidae. In these forms the in the size of the glottis and laryngeal collecting surfaces have a fine-grained discs, although most species do not vary texture under light microscopy, indicat- much from the proportions observed in ing the presence of secretory cells but Hyla regilla. The extremes were seen in without the ridge organization. Rhino- the discoglossids, Anotheca and Hyla phrynus shows some development of phlebodes at the upper limit and As- ridges on part of the branchial food trap caphus truei at the lower. To some ex- surface. Secretory ridges degenerate in tent an enlarged glottis seems to char- Hyla regilla near metamorphic climax. acterize large individuals. A large glot- Kenny (1969b) found no evidence tis is clearly associated with early func- that secretory cells were arranged either tioning of the lungs for respiration or in pits or rows in the tadpoles of the hydrostasis. The small glottis seen in hylid Amphodus auratus. Amphodus larval Ascaphus truei is consistent with larvae are arboreal, and Kenny associated the fact that these tadpoles live in well- the absence of a ridged pattern with oxygenated water where stability in a the unusual larval habitat of this species. current could be jeopardized by air- I could not perceive secretory tissue un- filled lungs. Although Ascaphus truei is der the velum in either Anotheca spinosa the extreme, other stream-bottom forms or Hyla phlebodes, nor could I find any also show some reduction in the size of ridges in Hyla dendroscarta. In members the glottis compared with typical pond of the Hyla leucophyllata group, secre- larvae. Bufo larvae which have a small tory ridges appear concentrated in the nonfunctional glottis develop their lungs more anterolateral region of the pharynx just before metamorphosis ( Savage, 1950 near the ciliary groove. Whereas the and 1961; Starrett, 1973) and it is no above tadpoles are a rather heterogen- surprise that they are relatively restrict- eous assemblage, they do offer some sup- ed to a bottom habitat in water of low port for the idea that absence of secre- turbidity (Wassersug, 1973; see also tory tissue in tadpoles of advanced frogs Wassersug and Seibert, 1975). is associated with abandonment of mi- The position of the glottis in relation crophagous suspension-feeding as the to the velar margin again reflects larval sole source of nourishment. lung utilization. Rhinophrynus, micro- The amplitude and frequency of se- hylid, and pipid larvae all have the glot- cretory ridges may be important in de- tis fully exposed on the buccal floor. termining the potential of the secretory These are tadpoles which have the abil- surface to trap particles of a particular ity to stay in the water column con- size or density. The pattern of the ridges tinuously, and their lungs must have a the re- seen in Xenopus (Kenny, 1969b) is hydrostatic function. Although unique for that genus. The ridged pat- maining tadpoles have the glottis behind

tern in the microhylids is also unique for the ventral velum, many have it fully or that family. In a general way, Kenny nearly fully exposed when viewed from associates the features of the ridges in above. These include the larvae of Xenopus and the microhylids with a spe- Scaphiopus bombifrons, Leptobrachium cialized, suspension-feeding way of life. oshanensis, Hyla phlebodes, Hyla den- ,

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 111 droscarta, and Colostethus subpunctatus. lumen characterizes the non funnel- On the other hand, the nonfunctional mouthed microhylids and Agalychnis glottis of Ascaphus tadpoles is fully callidryas. The narrow esophageal fun- blanketed by the ventral velar margin. nel in the larvae of these species is Evidently, accessibility to the glottis ascribable to the relatively elongate may be associated with early function of branchial baskets that bound the esoph- the lungs for respiratory as well as hy- agus. drostatic regulation. Prenarial Arena

Esophageal Funnel For any tadpole, the size and shape of the prenarial arena is determined by The lumen of the esophageal funnel the position of the internal nares, the will limit the size of the largest food breadth of the upper beak, and the item that can enter the alimentary canal. curvature of the rostrum. The nares are In this regard the data in the descrip- far forward in Rhinophrynus tadpoles tions, although subjective and only com- and larvae of the Hyla microcephala and parative, are valuable as one index of Hyla leucophyllata species groups; con- feeding potential. Ueck (1967) noted a sequently, these species have small pre- great discrepancy between the sizes of narial arenas. Another larva with a the esophagus in Xenopus and Hymeno- greatly reduced prenarial arena is As- chirus. Xenopus has a strictly micropha- caphus truei; this is also the species with gous diet and consequently a slender the strongest posteroventral curvature of esophagus. Hymenochirus is strictly a the rostrum. Wide prenarial arenas char- carnivore on large prey; it has a com- acterize the amphignathodontine hylids, paratively huge esophagus. microhylids, and funnel-mouthed tad- Among the tadpoles examined, the poles in general, although a compara- largest esophageal bore is seen in Ano- tively narrow prenarial region is found theca larvae. The discoglossids, Hyla in the megophrynine pelobatids, exclud- phlebodes, H. ehraccata, H. sarayacuen- ing Megophrys. sis, and the funnel-mouthed microhylids, Many species have specific structures all have relatively large esophagi, within the prenarial arena. The func- suggesting an ability to ingest compara- tional significance of only a few of these tively large particles. The non funnel- are comprehensible given the sample at mouthed microhylid larvae have esoph- hand. A distinct, posteriorly directed agi with the smallest diameter. This "V" shaped ridge occurs in Ftychohyla observation is consistent with the view schmidtorum, Megophrys minor, Colo- that these tadpoles are specialized for stethus nubicola and Microhyla hey- microphagy. monsi, but in no other species examined. The profile of the esophageal funnel The ridges interlock with a palp-like reflects the shape of the posterior margin infralabial papillae in these funnel- of the branchial baskets. Because of the mouthed forms and, as has been sug- lateral displacement of the third filter gested earlier, could prevent large par- cavity in tadpoles associated with the ticles from entering the corners of the stream habitat (with the exception of mouth. We may expect to find this Ascaphus truei), these forms tend to structural arrangement in other funnel- have broad esophageal funnels. Dis- mouthed species. tinctly esophageal funnels can also broad The huge, fleshy, pustulate cone de- be seen in the discoglossids, certain den- scending from the prenarial arena in drobatids Colostethus subpunctatus ( ) Hyla mixe is of sufficient size to occlude amphignathodontine hylids, and the the oral opening. In the absence of an Hyla microcephala and H. leucophyllata oral valve derived from the infralabial species groups. A conspicuously narrow papillae (cf. Ascaphus), this dorsal 112 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY structure may serve a valvular function. forate until late in development in the A pustulate or papillate, anteriorly microhylids may relate to the efficiency curved crest is present in the prenarial of their buccal pump. Presumably, the arena of Htjla femoralis, Colostethus sub- risk of leakage at a valve is reduced with punctatus, Ptychohyla leonhardschultzei, fewer orifices that open and close with Agalychnis calUdnjas, Anotheca spinosa, each pumping cycle. and Smilisca sordida. This is a group In nonmicrohylid larvae the anterior of larvae of such ecological and taxo- narial walls are commonly thickened nomic diversity that a single function and pustulate, with one or two small, may be unlikely for this crest. Centro- prenarial papillae. While it is possible lenella fleischmanni has a short trans- that such prenarial projections are sen- verse ridge in the prenarial area; several sory, their position directly in front of other tadpoles have single, knob-like or under the narial openings suggests structures in this region (e.g. Hyla ru- that at least the larger papillae serve a fitela ) . Comparing pictures of the dorsal protective function. They could keep and ventral surfaces of the various tad- larger particles from moving up into the poles shows that all these structures lie nares, where they might disrupt valvu- immediately above and behind the lower lar action or might detrimentally coat beak when the mouth is closed. They olfactory surfaces. In species where gen- may have a mechanical function related eral oral papillation is reduced, pustu- to maintaining beak occlusion or posi- lations or papillae of the narial walls tioning and anchoring macroscopic food are invariably absent. On the other items during mastication. Alternatively, hand, proliferation of floor and roof pa- future histological work may reveal that pillae does not necessarily mean an in- this prenarial feature serves a sensory crease in the number or size of prenarial role. Orton Type 1, 2 and 3 larvae lack papillae. these structures. Megophrynine pelobatids tend to The keratinized knob in the prenarial have a short ridge projecting forward arena of Scaphiopus bombifrons has from the anteromedial edge of the narial been discussed already under the head- wall into the prenarial arena. In approx- ing Keratinized Structures. imately the same region anterior to the nares, Hyla rufitela and Centrolenella Internal Nares fleischmanni develop a large cul de sac The nares are perforated in all but not of the same shape but presumably microhylid tadpoles. They may be large having the same chemoreceptive func- open vacuities, as in Centrolenella and tion. Ascaphus truei has somewhat simi- the discoglossids, or diminutive struc- lar, but smaller and more lateral, pits tures, as in Hyla phlebodes and Rhi- adjoining the anterolateral wall on each nophrynus. When the nares are larger side. The "ciliated epithelial bands" re- than in typical pond larvae, such as ported in this region by Van Eeden

Hyla regilla, they also tend to be more ( 1951 ) may be important in cleansing elongate and more obliquely oriented. these organs. Leptobrachium and Oreo- A few species have internal nares more lalax have the most attenuate prenarial transversely oriented than H. regilla; papillae of any of the tadpoles examined; these include the megophrynine pelo- however, the most extreme modification batids, Rhinophrynus, the dendrobatids, of anteronarial walls are the flaps found and Ptychohyla schmidtorum. In the in the discoglossids. These flaps are elongate Centrolenella fleischmanni tad- most likely protective. The fact that poles the nares are, understandably, they should develop in the discoglossids longitudinally oriented. and no other taxa may be related to the The fact that the nares do not per- plane of the buccal floor and roof in ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 113 discoglossids compared to other families. the narial valves are abbreviated trans- Discoglossids have a buccal floor that versely but expanded forward and down- tips gently downward anterior to the ward as large, cup-shaped projections. pharynx and they lack a strong rostral Judging from the diagram of Savage curvature. Most other species examined (1952, 1961), and Gradwell (1974), this have a comparatively horizontal buccal is typical of the family. These projec- cavity and abrupt curvature in the ros- tions are stiffened by a ridge that runs tral region. With this latter orientation down their posterior margin. Noble feeding currents impinge on the pre- (1927) illustrates these projections in narial arena before being deflected back- Microhyla pulchra, noting that they ward. In the discoglossids, however, would effectively isolate the olfactory feeding currents must flow into the chambers from the buccal cavity on each mouth along a more posteriorly directed side. He also speculates that these flaps course toward the internal nares. If not could control and even direct water into for the flaps on the anterior narial walls, the higher portions of the olfactory olfactory tissues could be abraded by chambers. Gradwell offered the same coarse particles in the feeding currents. hypothesis for the function of these The posterior walls of the nares are structures in Phrynomerus; it seems like sufiiciently flexible and properly posi- a very reasonable hypothesis. tioned to act as valves in all the tadpoles POSTNARIAL ArENA examined except the microhylids and possibly the arboreal hylids. The di- Superposed photographic prints and mensions of the valves strictly reflect drawings of the floor and the roof of the dimensions of the nares. The narial the mouth reveal that the tongue anlage valve projections, however, vary sub- makes a near-perfect fit into the post- stantially in size. In approximately half narial arena. Species which have a poorly outlined postnarial arena (e.g., micro- the species examined ( megophrynine pelobatids, microhylids, Hyla rufitela, hylids, Rhinophrynus, Hyla phlebodes, H. femoralis, H. dendroscarta, Anotheca H. ebraccata, and H. sarayacuensis) also spinosa, Gastrotheca riobambae, Aga- tend to show little development of the lychnis callidryas, and Acris crepitans) tongue during the stages that I exam- have narial valve projections equal to or ined. Similarly, it is reasonable that larger than those of H. regilla. Dendro- postnarial arena structures are absent in batids have smaller valve projections. the aglossal pipids. Other than to form Of the remaining forms many, such as a receptacle for the growing tongue, the roles of the postnarial papillae and me- all Orton Type 1 and 3 larvae, Centrole- dian ridge are not evident. Although nella, Hyla phlebodes, H. ebraccata, and H. sarayacuensis tadpoles, lack the pro- they have been variously illustrated Schulze, jections. The narial valve projections of (Goette, 1874; 1889; Kenny, Anotheca spinosa are in the middle of 1969a and 1969b), and Dejongh (1968) the posterior walls on each side rather offered a fairly complete description for temporaria, has dis- than at the medial corners. The most Rana no author attenuate narial valve projections occur cussed these or any of the other buccal in Leptobrachium and Oreolalax larvae. roof structures in a systematic fashion. Although narial valve projections may Except for Kenny (1969a and 1969b), labelled these projections along be sensory structures, it is equally likely who that, in conjunction with prenarial pa- with the lateral ridge papillae as "sen- pillae and pustulations, they block large sory," no function has ever been sug- particles from entering the internal gested for them. nares. When a postnarial arena is present, In the microhylids that I examined it is bound laterally by an average of 2 114 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY or 3 postnarial papillae and assorted pus- ridge papillae invariably are reduced or tulations. The greatest number of post- absent. Increases in the number and narial papillae that I counted in any size of arena papillae vary directly with specimen was 7 per side (Acris crepi- increases in the size of the lateral ridge tans). In funnel-mouthed larvae, these papillae. However, the papillae are ab- papillae are consolidated into a massive sent in all Orton Types 1, 2, and 3 lar- ridge on each side. A smaller ridge is vae that I examined. developed in Ptychohyla leonhardschult- The papillae may be simple and cy- zei and to a still lesser extent in Centro- lindrical with minor terminal and an- lenella fleischmanni and Agalychnis cal- terior pustulations or secondary papillae lidryas. (e.g., Hyla regilla, H. dendroscarta, Acris The median ridge defines the back crepitans, and Anotheca spinosa); or of the postnarial arena. The ridge has a they may be rather huge flaps with long, curved, pointed, or straight margin in finger-like, marginal papillae (e.g., Hyla most tadpoles examined and in ones il- mixe, Ptychohyla leonhardschultzei, lustrated by other authors; although the Oreolalax). There are all grades be- pattern is rather species-specific, from tween these extremes. In funnel-mouthed looking across the samples it is clear larvae the lateral ridge papillae are that there is a continuous spectrum of thick, stout projections lacking secon- possible shapes for this structure. In dary papillation. Hyla mixe, Centrolenella fleischmanni, Kenny (1969b) illustrated the lateral Anotheca spinosa, and Ptychohyla ridge papillae of Hyla geographica as schmidtorum the median ridge is re- being rather small flaps with jagged mar- duced to a tall papilla. In Megophrys gins. Savage's (1952) illustration of minor, the ridge is replaced by a large, these structures shows them to be of the nipple-shaped, projection; a similar but rather huge "hand-like" variety in Bufo much smaller projection occurs in Colo- bufo. In general, large lateral ridge pa- stethus nubicola. pillae seem to be associated with the Serrations or fine papillae often oc- stream habitat. cur on the free ventral margin of the These papillae could have any or all median ridge in tadpoles with a wide of the functions suggested for oral pa- ridge. When the median ridge is rela- pillae elsewhere in the mouth—sensory, tively large it is often covered with pus- respiratory, or mechanical (as intercep- tulations or a secondary serrated ridge tors of feeding currents). Their position on its anterior surface. in front of the buccal pockets and their Because of the medial position of the relatively large size in tadpoles that in- postnarial arena, this collection of pro- gest coarse material (e.g., stream forms; jections, together with the tongue an- see Ecological Considerations) offer lage, may be important in dividing up some support to a mechanical intercep- the respiratory current into right and tor hypothesis. This does not rule out

left streams. This is not to say that the other functions. papillae are without additional possible Buccal Roof Arena functions such as the sensory role implied by Kenny. The buccal roof arena has already received attention under the heading of Lateral Ridge Papillae Buccal Floor Arena and only a few are here. The structures which I have called comments added the lateral ridge papillae are develop- Anterior BRA papillae are positioned mentally associated with the postnarial medially to the anterior BFA papillae; and buccal roof arenas. When these thus, buccal roof arenas tend to be more arenas are reduced or absent, the lateral elongate and rectangular than buccal .

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 115 floor arenas. The number of BRA pa- H. ebraccata, and Centrolenella that its pillae correlates directly with the num- length could not be determined. The ber of BFA papilla although there are posterior extension of secretory pits onto never as many roof as floor papillae the dorsal velum and pressure pads is (maximum number observed was 34 in highly variable.

Ptychohyla leonhardschultzei) . When Kenny (1969b) illustrates the glan- the BFA is reduced, the BRA generally dular zone of Hyla geographica as di- diminishes. In Colostethus nubicola the vided medially. In Xenopus laevis and BRA papillae are reduced in height and Pipa (Sokol, 1977a), the glandular zone coalesced into ridges. is largely restricted to the individual BRA papillae are, typically, simple pressure pads (Wassersug, unpublished cones. They are rarely bifurcated or dec- scanning electron micrographs ) but may orated with terminal pustulations. extend far anterior to the pressure pads

Although all the authors mentioned in Xenopus tropicalis (Sokol, pers. above as providing illustrations of post- comm ) narial structures included some or all of Whereas the shape and size of the the buccal roof proper in their drawings, total glandular zone fails to reveal pat- their illustrations appear incomplete in terns that can be easily associated with regard to post-median ridge features. function, phylogeny, or ecology, the se- As to size, shape, number, and position cretory pits themselves do reveal such of the accuracy of the representations of patterns. Ascapthus truei has irregular- buccal roof arena papillae cannot be de- ly shaped, poorly defined pits that are termined, because independent descrip- much smaller than those of Hyla regilla. tions of these structures are not pro- Bombina is similar to Ascaphus, but has vided. well defined pits, at least along the an- The possible functions for the BRA terior margin of the glandular zone. papillae are treated above with those of Other tadpoles with smaller pits than the BFA papillae. those of Hyla regilla include Centrole- nella fleischmanni, Hyla phlebodes, H. Glandular Zone and Dorsal mixe, H. ebraccata, and Ptychohyla leon-

Secretory Pits hardschultzei. None of these species is Few generalizations can be made believed to be particularly micropha- about the size and shape of the glandu- gous. On the other hand, a list of tadpoles lar zone. Some tadpoles which clearly with secretory pits much larger than those of regilla are not specialized for microphagy (e.g., Hyla include Hyla Microhyla heymonsi, Anotheca) com- rufitela, Agalychnis callidryas, Gastro- theca pletely lack a visible glandular zone in riobambae, Rhinophrynus dorsalis, Microhyla berdmorei, the stages that I examined. In other Scaphiopus bombifrons, and Xenopus laevis. tadpoles the zone is interrupted medially These are all tadpoles that, (e.g., Rhinophrynus, Microhyla ornata, based on the totality Leptobrachium oshanensis) or extreme- of characters examined and their known behavior ecology, ly reduced in that region (e.g., Mego- and should be as eflB- phrys minor, Oreolalax, Leptobrachium cient as, if not more eflBcient than, Hyla regilla in hasselti, Hyla rufitela). The glandular microphagous suspension-feed- zone was, on the average, proportion- ing. Thus there seems to be a weak ately wider in Hyla mixe, Hyla saraya- inverse relationship between the size of cuensis, and the megophrynine pelo- the secretory pits and the typical size of batids than in Hyla regilla. It was the particles upon which a larva feeds. narrower in Ptychohyla, Smilisca, and There also seems to be a loose inverse Gastrotheca. The anterior margin of the correlation between the size of secretory zone was so indistinct in Hijla phlebodes. pits and their density; the density of the )

116 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY secretory pits is reduced in forms with Dorsal Velum as good microphagous abilities such Of the species I examined, the only Rhinophrynus, Microhyla berdmorei, M. one which completely lacks a dorsal bombifrons, ornata, and Scaphiopus velum is Anotheca spinosa. In a few compared to more typical pond larvae. others, the dorsal velum appears vesti- Feeding currents are directed against gial (e.g., Hyla phlebodes with its two, the glandular zone by the ventral velum, tiny, lateral flaps). In pipids, which lack particularly when the velum is in a par- a valvular ventral velum, the dorsal tially elevated position. Kenny (1969a) velum is also absent. called this region the "dorsal food traps" In most species the dorsal velum is and considered the glandular zone a pri- distinct and is divided into right and mary site for mucous entrapment of food left halves. The few species in which particles. In the earlier discussion of the velum is continuous across the mid- secretory pits on the ventral velar pro- line include Ascaphus truei, the micro- jections, I hypothesized a possible mech- hylids, Centrolenella, Hyla rufitela, H. anism for the generation of mucous femoralis and tadpoles of the Hyla leu- strands from the glandular zone. Kenny cophyllata species group. In species has suggested that the ventral velum where the velum is broadly interrupted may actually push particles onto the medially, the free medial edges are often zone during valvular closure. There can reflected posteriorly, leading into the be little question that food is in one way esophagus. along the or another trapped in mucus In Orton Type 3 tadpoles, the velum zone, for in some specimens flocculent is shorter than in Hyla regilla. The vel- matter can be found adhering directly um is also distinctly shorter than that of to this surface. H. regilla in Rhinophrynus, Centrole- Whether the glandular zone is a pri- nella, Agalychnis, Hyla ebraccata, Hyla mary region for food entrapment is sarayacuensis, Ptychohyla schmidtorum, another question. In specimens where Smilisca sordida, and the megophrynine particles were adhering to the glandular pelobatids (with the possible exception zone, they were also adhering to the of Leptobrachium hasselti). The only branchial food traps and were in far species in which the velum is unques- greater abundance on the latter surfaces. tionably longer than that of H. regilla Massive accumulations of particulate are Microhyla berdmorei, Microhyla or- matter on the glandular zone would pre- nata, and Scaphiopus bombifrons. vent normal valvular closure. For the Papillae occur along the free medial valve to be operational when there is margin of the dorsal velum in Ptycho- substantial mucous entrapment on the hyla and the megophrynine pelobatids. glandular zone, mucus and food aggre- Although they were not seen in Hyla gates must be swept off the surface with mixe, these papillae may be common in efficiency and regularity. suctorial, stream larvae of Orton Type 4. Alytes shows some papillation in this Hypothetically, there are other pos- region of the velum. These papillae have sible functions for the mucous secretion not been discussed or illustrated previ- of the glandular zone besides food en- ously; presumably, they serve a sensory be important for trapment. Mucus may or mechanical straining function, but ventral proper valvular function of the these are mere speculations.

( Gradwell, 1970 velum. Both lubricant At present it is not possible to asso- and sealant ( Kratochwill, 1933) roles ciate the size of the dorsal velum with have been proposed for this secretion in other aspects of the biology of any group relation to the valvular operation of the of tadpoles. ventral velum. There are two schools of thought ;

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 117 concerning the primary function of the when the branchial baskets are elongate, dorsal velum. These schools are identi- the pressure cushions are elongate (e.g., fiable with the two names given this microhylids, Agalijchnis, Rhinophrynus) structure, viz., "dorsal velum" and "pos- when the filter plates of the second and terior filter valve." Among the latter third ceratobranchials are reduced so school, Kratochwill (1933) holds that that there is a single filter cavity on each the dorsal velum, in conjunction with the side, there is also a single pressure cush- pressure cushions, functions as the pos- ion on each side (pelobatids). terior half of the valve system that seals When the filter cavities are extremely off the filter chambers from the buccal large, as in Rhinophrynus, Xenopus cavities. Kenny ( 1969a ) has essentially (Sterba, 1950), and Pipa (Sokol, 1977a), the same view, although he does not be- there are three rather than two distinct lieve that closure is complete. Since cushions on each side. Sokol (1977a) microhylids have a ventral velum par- reports another oddity in Pipa parva; tially anchored to tops of the filter plates this is the occurrence of papillae at the (fully anchored at the top of cb. 4), anteroventral corners of the huge pres- Gradwell (1974) has argued that a val- sure cushions of this genus. vular function is essential for the dorsal The function of the pressure cushions velum in these larvae. Savage (1961), is not clear. Kratochwill (1933) as- as a proponent of the "velum" school, sumed that they could abut tightly to proposes that the major function of this the filter surfaces and actually push fold is to deflect currents down into the water through the filters on the expira- filter cavities in such a way that vortices tion half of each pumping cycle. This form in the branchial baskets between seems doubtful, considering the delicate the individual filter plates. Dejongh nature of these pads, although I concede

( 1968 ) , who also used the term "velum" that in living tadpoles fluid pressure may sees this structure as having a protective make these structures stiffer than they function. In his view that when the appear in preserved larvae. A stronger ventral velum is in its down position, objection is that a single cushion rarely the dorsal velum is pulled taut and pre- fills a whole filter cavity. vents water from flowing directly along The pressure cushions have also been the ciliary groove where it could displace thought to serve as a protective rim for mucous strands. Although it is obvious the ciliary groove. Although the poste- (and was recognized by Kratochwill) rior margin of the cushions makes up that the dorsal velum could act both as the anterior margin of the ciliary groove, a valve and a velum, topographically at far more tissue is involved in the cush- least, a velar function is obligatory for ions than is necessary to demarcate the this structure. In accepting a velar func- groove. Thus, I doubt that this is the tion, I am not accepting all the details sole function of the cushions.

of Savage's centrifugal feeding mechan- Although I cannot offer a completely ism. Indeed, the objections that Kenny satisfying hypothesis for the function of (1969a) raised to Savage's centrifugal the cushions, I suspect from the com- feeding theory seem completely valid. mon occurrence of scattered secretory pits on these surfaces that they are in- Pressure Cushions volved in direct contact with food mat- Pressure cushions were regularly ter. A possible role in lifting food from the filters damaged in dissection and will not be was mentioned above. discussed in detail. Overall, the cushions SYSTEMATIC CONSIDERATIONS show a very strong correlation in size and shape with the size and shape of "Tadpole morphology represents per- the branchial baskets. For example. haps one of the most useful and most ) )

118 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY misused of the available character com- the three genera have very similar lar- plexes to be used in frog classification." val oral structures. (Lynch, 1971:200). Certain of their shared features, such as expanded internal narial flaps and An effort is made here to discern the pharyngeal shape, warrant including shared, derived characters among inter- these genera in the same family on nal oral features that either substantiate strictly phenetic grounds. I consider it or refute traditional taxonomic schemes. unlikely that these similarities are due No formal effort is made to reassign any to convergence. The features in ques- taxa, since such activities cannot be tion may be primitive ones for anurans justified solely on the basis of larval and of little use in discerning sister characters. Species are discussed by groups. If much weight, however, is family in the same order in which they given immunological data, we may find are presented in the Descriptions. grounds for splitting the Archaeoba- Results from this study generally sup- trachia as currently recognized into sev- port traditional systematic assignments eral additional families. at the familial and lower taxonomic level. Suprafamilial relationships are Rhinophrynidae discussed separately in the section titled Although Rhinophrynus dorsalis lar- Phylogenetic Considerations. vae share certain features of other fami- ASCAPHIDAE lies, such as an exposed glottis on the floor of the mouth (a la Microhylidae Ascaphus larvae have many features and the full attachment of the ventral which distinguish them from all other velum to the dorsal margins of the sec- tadpoles, including the direct-develop- ond and third filter plates (a la Disco- ing Leiopelma embryos. Although I glossidae), they are overall unlike any have not personally examined Leiopelma other tadpoles examined and completely ontogenetic series from the genus have justify the monotypic assignment of this been described by Stephenson ( 1950a, species. 1950b, 1955). In comparing Stephen- son's figures and description with my Microhylidae I figures and description of Ascaphus At the familial level it is clear that can find no common, clearly derived fea- the microhylids are tightly united and, tures in these genera. In the absence of at the same time, separate from all other shared, derived characters it may be con- frog families by the uniqueness of their cluded that early developmental stages larvae (Orton, 1957). Although Savage do not provide any evidence for group- (1952, 1955), Nelson and Cuellar ing Ascaphus and Leiopelma in the (1968), and Gradwell (1974) have all same family. I support Savage (1973) described larval oral features in a variety recogniz- and Coin et al. (1978) in of microhyhd genera, their descriptions ing two families, the Ascaphidae and are neither detailed enough nor com- the Leiopelmatidae {contra Duellman, parative enough to help determine 1975). whether internal oral features can be DiSCOGLOSSIDAE useful in discerning relationships within this family. Of the three species of Lanza, Cei and Crespo ( 1975, 1976 Microhyla I examined, M. ornata and have argued on the basis of immunolog- M. berdmorei are extremely similar. Con- Discoglossi- ical data for partitioning the sidering the large number of superficially dae into the Bombinatidae (with Bom,- similar species in the genus (Parker,

hina) and the Discoglossidae (with Dis- 1934) it is doubtful that the minor oral coglossus and Alytes). Except in some features used to distinguish these two fine points of lingual papillae pattern. species would separate either of them ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 119 from all other species in the genus. The define the family. Whether there are funnel-mouthed form, M. heymonsi, any larval features unique to the Hyli- however, is immediately separable from dae cannot be determined until more the rest of the genus (with the possible tadpoles of other advanced families are exception of the other known funnel- studied. At present it seems that all mouthed species, M. achatina) in both hylids have a basically similar pattern external and internal features. It is of attachment for the ventral velum. doubtful that any other free-swimming Moreover, all have perforated, slit-like microhylid larvae are much like M. hey- or oval internal naries. But comparison monsi in oral features; M. achatina and with descriptions in the literature for M. heymonsi may be justifiably removed other families, such as the Ranidae and from the genus Microhyla, if any weight Bufonidae, and my own preliminary ob- is given to their larval characters. servation of leptodactylid larvae, suggest that these are not unique features; Pelobatidae alone they will not distinguish the hylids The shallow filter plates of cb. 2 and from most other neobatrachian families. cb. 3 and the bowl shape of the bran- Recently there has been much work chial baskets are unique features shared on the subfamilial systematics of the by all pelobatid larvae examined and Hylidae. Duelhnan (1970) associated the family is easily justified on these the genera Anotheca and Gastrotheca features. Three major subfamilial groups in the subfamily Amphignathodontinae, can be seen in the material at hand, and while Maxson (1977) has argued from the European pelobatids may form a immunological data that Anotheca more fourth division. Megophrys stands apart appropriately belongs in the hylinine from the other pelobatids because of subfamily. Both Anotheca spinosa and adaptations associated with the funnel- Gastrotheca riohamhae share a generally mouth. It forms the first division. The robust habitus and have the medial por- second division consists of the nonfun- tion of the ventral velum deflected by a nel-mouthed megophrynines represented large laryngeal disc. The large laryngeal here by Leptobrachium and Oreolalax. disc in both species probably results Tadpoles of these genera are sufficiently from independent convergence on early similar in larval morphology to justify lung use. The larva of Anotheca spinosa their separation from Megophrys (In- is otherwise so bizarre that oral struc- ger, 1966). The third division consists tures are of little use in establishing its of Scaphiopus, which is grossly different subfamilial status. from the other pelobatids. Many of Maxson (1976) has also used immu- these differences may relate to the fact nological data to argue for elevation of that these are temporary pond dwellers the Phyllomedusinae to familial status. rather than inhabitants of streams. The one phyllomedusine larva that I examined, Agalychnis Hylidae callidryas, differs from all the other hylids in many fea- Although the hylid larvae examined tures (e.g., the shape of the prepocket were few compared to the number of buccal surface, buccal floor arena, velar species in this family, the sample was margin, filter and apparatus ) , but is vir- originally selected because of its ecologi- tually identical to Phyllomedusa trini- cal diversity, and consequently demon- tatis as illustrated by Kenny (1969a). strated much correlated morphological Considering the extreme similarity diversity (see Functional Considerations among phyllomedusine tadpoles in gross and Ecolog'.cal Considerations). Given external morphology (for Central Amer- this great morphological diversity, few ican species, see Duellman, 1970), be- unique features emerge which might havior, and ecology (Starrett, 1973; 120 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Wassersug, 1973), we may safely con- ever, for elevating the rank of some of clude that internal oral features of A. these groups (see below). callidryas are typical for the subfamily. H. rufitela is the northernmost mem- Phyllomedusine tadpoles as a group ber of the Hyla alhomarginata species seem to be more speciaHzed for suspen- group, and has a larva externally like

1969a ) than typical pond Hyla such as H. regilla H. sion feeding ( contra Kenny, ( other hylid larvae. Whether this war- eximia species group) except for its 2/4 rants their separation from the Hylidae denticle pattern. But internally, certain at the family level cannot be determined features such as the narial vacuities and at this time. the transverse row of papillae on the At least three species of Phyllome- buccal floor, justify supraspecific sepa- dusa, P. guttata, P. cochranae and P. ration of this Hyla from the other Hyla jandaia are funnel-mouthed forms (Bo- in this study. Unfortunately, not enough kermann and Sazima, 1978) with a par- is known about other members of the ticular external morphology regularly alhomarginata species group to say associated with a complex internal mor- whether these features are diagnostic of phology unlike that seen in P. trinitatis the group in general. Hyla dendroscarta or A. callidryas. If further examination (PI. bromeliacia group) has a variety of of funnel-mouthed phyllomedusines re- oral features which again would sepa- veals the typical internal specializations rate it from more typical pond Hyla lar- of other funnel-mouthed larvae, this may vae. Likewise, the similarity between warrant placing them in their own genus. Hyla ehraccata and Hyla sarayacuensis

If, however, they show the specializa- justifies their separation from the other tions for microphagy characteristic of forms. H. ehraccata and H. sarayacuen- other phyllomedusine larvae, then, col- sis form a closely united group readily lectively, the uniformity and uniqueness distinguishable in their oral anatomy of the phyllomedusine larvae may sup- from all other tadpoles examined; simi- port the elevation of the subfamily to larities in their larval morphologies com- family status. pletely justify their association in the Distinguishing features of the larvae Hyla leucophyllata species group. Equal- of the four genera of Hylinae frogs, ly divergent from the basic pond hyli- are H. mixe H. mixomaculata Ptychohyla, Hyla, Smilisca, and Acris, nine type ( are all of a quantitative rather than qual- group) and H. phlehodes (Hyla micro-

itative nature. There is as much differ- cephala species group ) . In the shape of ence between species within the genera its branchial baskets and gill filter den- Ptychohyla and Hyla as there is between sity, Hyla femoralis likewise stands apart members of all four genera. Hijla re- from the other Hyla examined, including gilla, Acris crepitans, and Smilisca sor- the Holarctic H. regilla. Maxson and dida are all very similar and show the Wilson (1975, Table 4) reach the same generalized "pond" tadpole pattern for opinion based on albumin similarities. internal oral structures. If one general conclusion can be Ptychohyla schmidtorum and P. leon- reached from the diversity of larval oral hardschultzei differ from one another at structures in Hyla, it is that the genus least as much internally as externally, is an artificial group that warrants frag- completely supporting the separation of mentation into several genera. There is these forms into the two species groups, no question that, if adult frogs showed P. schmidtorum and P. euthysanota, re- as much diversity in oral structures as spectively (Duellman, 1970). these tadpoles do, herpetologists would All species groups within Hyla rec- have partitioned them into separate gen- ognized by Duellman (1970) appear era decades ago. valid according to the features I have On the other hand, there are no examined. A case can be made, how- unique features of Smilisca or Acris tad- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 121 poles that would help to define these that elongation is a general character- genera as distinct from Hijla. Maxson istic of centrolenid larvae, these internal and Wilson (1975) considered Acris as features probably characterize the fam- very different from Hyla at the organis- ily and serve to distinguish these larvae mal level (based on karyotypic and from tadpoles of other families. adult osteological characters; cf. Duell- man, 1970 and Gaudin, 1974 ) but wrote, EVOLUTIONARY "A protein-based classification would in- CONSIDERATIONS clude [Acris] in the same taxonomic The Ascaphus and Leiopelma category as the North American Hyla Life Cycles species but exclude many South Ameri- can species currently placed in the genus Despite their extreme specialization Hyla." In this conflict of organismal for life in torrential streams, Ascaphus versus molecular evolution the tadpoles larvae have all the essential, anatomical appear to support the systematic ar- features for suspension-feeding (Was- rangement derived from protein struc- sersug, 1975). They have, for example, ture rather than the one based on adult well developed gill filters. Although the characters. According to Maxson and filter mesh in Ascaphus is not nearly as

Wilson's data for two Holarctic Hyla dense as in typical pond forms, the fil- that I examined, Hyla regilla is more ters are more fully developed than in similar to Acris than it is to Hyla femo- certain other stream forms that clearly ralis. Again, this similarity is borne out had pond-inhabiting ancestors (e.g., by tadpole oral characters. In terms of Ptychohyla). Ascaphus larvae have ex- both molecular structure and larval anat- panded ceratohyals that can serve as a omy, Acris is more similar to certain spe- buccal pump and a ventral velum that cies of Hyla than are many species of can act as a valve to maintain one-way Hyla to each other. The oral morphol- flow to the branchial food traps. Al- ogy of hylinine tadpoles provides the though they lack secretory ridges in the first anatomical support for systematic pharynx they have otherwise well-devel- patterns formulated from molecular oped branchial food traps (Wassersug data. For this reason tadpole structures and Rosenberg, 1979 ) . These larvae have deserve consideration in future work on functional narial valves. The filters, buc- anuran taxonomy. cal pump and valves are all essential features of the tadpole suspension-feed- Dendrobatidae and Centrolenidae ing mechanism (Wassersug, 1975). Of the two families remaining, there Experimental work has shown that are no internal oral features that readily Ascaphus tadpoles can extract food par- distinguish the dendrobatid larvae from ticles from suspension (Altig and Bro- other advanced families. The differences die, 1972), although their eflBciency (in between Colostethus subpunctatus and terms of the particle sizes they capture) Colostethus nubicola are massive and, is below that of more typical pond again, if internal oral features of the forms (Wassersug, 1972). As noted by larvae are taken into consideration, the Gradwell (1973) and Starrett (1973), funnel-mouthed form could justifiably there is no support for the popularly ac- be separated into a different genus. cepted (cf. Morton, 1967:42) suggestion Features that are unique to Centro- by Noble (1927) that these larvae take lenella fleischmanni are virtually all as- in most of their food through their sociated with the extreme elongation of naries. the tadpole (e.g., elongated internal Some authors (Eaton, 1959; Schmal- naries, elongation of the second and hausen, 1968) have considered the

third ceratobranchials ) . Considering stream tadpoles of Ascaphus to repre- 122 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY sent the generalized anuran larva. This vertical position. The midportion of the view is based on an effort to explain the ceratohyal is expanded in the frontal hard mouth parts of tadpoles as a gen- plane as it is in all aquatic larvae with eralized feature initially evolved as an a buccal pump. Long ceratohyals asso- aid for hanging onto rocks in streams. ciated with the filter plates of suspen- Such a view is founded on the belief sion-feeding forms line the otherwise that the most generalized extant frog nonfunctional gill slits. In fact, what must have the most primitive tadpole. Stephenson identified as a branchial

Hard mouth parts in most other tad- pouch in his serial sections ( 1950a, Plate poles are primarily used to generate a 1 ) , may be a vestige of the ciliary groove suspension of food particles, and it is used to transport particles trapped in equally plausible that they did not ini- mucus to the esophagus in suspension- tially evolve as a response to life in feeding tadpoles. In contrast, Eleuthero- streams. As with other organisms, an dactylus, a direct-developing frog that anuran may be a mosaic of primitive no one doubts evolved from an aquatic and derived characters; there is no real ancestor, shows far fewer features asso- reason why a frog and its larva must be ciated with feeding in its jaw suspension at the same grade of specialization. It and branchial skeleton than Leiopelma seems most likely that Ascaphus tad- (See Lynn, 1942). Evidently, Leiopelma poles are secondarily specialized for arrived at terrestrial development from stream life. an ancestor with an aquatic, suspension- Developmental series of Leiopelma feeding, larva. have not been available for study. Evolutionary Trends in the Stephenson 1950a, 1950b , who has ex- ( ) DiSCOGLOSSIDAE amined ontogenetic material of this genus, believed that the direct-develop- A case can be made for grouping ing embryo of Leiopelma represented a Ascaphus closely with the discoglossids. link between the salamander and frog These forms are similar not only in the type larva. Stephenson (1955) wrote way the ventral velum attaches to the that, "no evidence exists of terrestrial filter plates, but also in the gross shape specializations as shown by certain anu- of the buccal floor arenas, the position rans which have secondarily acquired a of the glottis, and the absence of a well- terrestrial mode of development follow- developed ridge pattern for the secre- ing abandonment of a specialized tory tissue of the branchial food traps aquatic tadpole's stage." In direct con- (Wassersug and Rosenberg, 1979).

trast to that statement, it is generally The multiple pustulations on the accepted by most workers that Leio- tongue anlage in Alytes are similar to pelma secondarily acquired direct de- the multiple papillation of the tongue velopment from a free-swimming tad- anlage in Ascaphus. In features of the

pole stage. pharynx, it is Bombina among the disco- From my analysis of Stephenson's glossids which is most similar to As- caphus. Typical advanced tadpoles have ( 1950a ) reconstruction of the embryonic chondrocranium and visceral arches of well organized ridges running trans-

Leiopelma larvae, it is fair to say that versely across the branchial food traps, this genus shows a substantial number and pits along the posterior margin. of vestigial features, ones specifically as- Ascaphus and Bombina lack both the sociated with an aquatic, suspension- secretory pits and ridges that character- feeding existence. The jaw suspension ize the branchial food traps of most

in developing Leiopelma is directed an- "advanced" anuran families (e.g., hylid, teroventrally and only secondarily ro- bufonid, ranid). Alytes and Discoglos- tates at metamorphosis into a more sus, in contrast, have secretory cells clus- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 123 tered to form ill-defined pits. The micro- similar to the discoglossids; most con- anatomy of the food traps suggests a spicuous is the full attachment of the morphological sequence going from As- ventral velum to filter plates cb. 2 and caphus to Bomhina to Alijtes and Disco- 3. Rhinophrynus, however, has ad- glossus and then to more advanced vanced upon the discoglossid grade in anuran larvae. Phylogenetically, the se- having developed secretory ridges in the cretory pits evidently appeared before branchial food traps (Wassersug and secretory ridges (Wassersug and Rosen- Rosenberg, 1979). In several super- berg, 1979). ficial features, Rhinophrynus closely re- These ideas neither support nor con- sembles the microhylids. These include: flict with the proposal of Lanza, Cei and buccal floor exposure for the glottis; Crespo (1975, 1976) to partition the absence of posterior projections from the Discaglossidae [sensu lato) into two velar margin; branchial food traps restricted to the anterior portion of families. Sokol ( 1977b ) recognizes the the suborder Discoglossoidei, to encompass filter cavities (crescentic organs); larger branchial baskets with a denser filter the two families Leiopelmatidae ( ^ As- caphus and Leiopelma) and Discoglossi- mesh; and the absence of postnarial and dae; the similarity of Ascaphus tadpoles buccal roof papillae. Except for the to discoglossid larvae makes this an emi- buccal floor exposure of the glottis, the nently reasonable association. restricted size of the branchial food traps and the density of the filter mesh, this

The Pipoidea and Their Relationships combination of character states is not unique to Rhinophrynus the Since Orton (1957) first proposed and micro- that Rhinophrynus and the Pipidae were hylids; it occurs, for instance, in certain hylids. glottis closely related, virtually all herpetolo- Although the is exposed in Rhinophrynus gists (except for Griffiths and de Car- and microhylids, its position is farther vallo, 1965) have formally or informally much forward in the microhylids than in recognized the superfamily Pipoidea. It Rhinophrynus. In other features, such as the overall is thus surprising how little resemblance shape of the visceral skeleton, exists between oral structures in Rhi- the resemblance breaks nophrynus tadpoles and pipid larvae. down. Presumably, similarities between Rhinophrynus The shape of the prepocket buccal sur- and microhylids are due to convergence face, the presence of a valvular ventral on a largely suspension-feeding, velum, the shape of the branchial food nectonic way of life. traps, the shape of the dorsal velum If we accept Rhinophrynus as a and pressure cushions, all distinguish pipoid, then it follows that Rhinophrynus Rhinophrynus larvae from any pipid has, overall, the most generalized Orton genus. This does not necessarily mean Type 1 larva. This view is based on the that Rhinophrynus is not closely related belief that the absence of a valvular to the pipids at the superfamilial level velum in the Pipidae is best compre- or that Orton's Type 1 larva is invalid. hended as a derived character. There is Starrett (1968, 1973) and Sokol (1975, little support for the opposite hypothesis 1977a) have both reaffirmed the validity offered by Gradwell (1975a), which of the Rhinophrynus-pipid association. would derive virtually all anurans from Hymenochirus, Xenopus and Pipa larvae the genus Xenopus. The unusual posi- all differ so much from each other that, tion and microanatomy of the secretory provided they are validly grouped at ridges in Xenopus (Wassersug and Ro- the familial level, Rhinophrynus could senberg, 1979), the papillate pressure still be reasonably united with them at cushions and fused filter rows in Pipa, the next higher level. and the complete loss of filter-feeding

Certain features of Rhinophrynus are structures in Hymenochirus, must all be ,

124 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

in the region between the optic cup highly derived characters. Sokol ( 1977a, case 1977b) has reached a basically similar and the otic capsule. We may hypothe- conclusion with an independent analysis size that evolution has "squeezed" the of these and other characters. ganglia of the fifth and seventh nerves together incidental to the forward dis- Within the Pipidae, the genera palatoquadrate and ex- Xenopus and Pipa bear the strongest placement of the pansion of the ceratohyal. The palato- resemblance in larval oral surface struc- quadrate of the pipids is unlike that of tures (Sokol, 1977a). On the basis of the other anuran larvae, but it neverthe- other characters, however, Sokol places less has a relatively anterior position Hymenochirus closer to Xenopus. Ac- compared to discoglossoid larvae. Con- cording to Sokol the filter apparatuses of sidering the differences in the form of Xenopus and Pipa are extremely differ- the palatoquadrate in pipoid frogs and ent, although one must concede that non-pipoid, non-discoglossoid larvae, it they are more similar to each other than seems possible that an efficient cerato- either is to Hymenochirus. Sokol views hyal pump has evolved along two paths Pipa as evolving away from the extreme above the discoglossoid grade. One path microphagous condition, as exemplified would have been through the Pipoidea by Xenopus. Pipa appears to be a die- and the other through all remaining tary specialist adapted for feeding on anurans. It seems plausible that the medium-sized planktonic organisms. Hy- trigeminal and facial nerves could have menochirus, of course, is a carnivore, been independently "squeezed" together specialized for feeding on large plank- on both evolutionary courses. tonic organisms. In conclusion, the Pipoidea are an Except for discoglossoid frogs, all extremely specialized and diverse super- anurans including the Pipoidea have a familial group. Internal oral features fused trigeminal and facial ganglia. So- corroborate Sokol's conclusion that the kol views this as a uniquely derived Pipoidea are too specialized to be either character and Lynch (as pers. comm. in an ancestral anuran group, or near the Sokol, 1977b) has gone so far as to sug- ancestral line (contra Starrett, 1973). gest that the Pipoidea are derived from However, in identifying the pipoid lar- pelobatoid frogs. vae as highly specialized and derived, I It is my suspicion that the fusion of consider it premature to propose that the fifth and seventh ganglia is an in- they evolved from any extant family or direct result of the orientation of the superfamilial group. palatoquadrate bar in non-discoglossoid larvae and is associated with perfection The Microhylid Problem of a suspension-feeding larva with a Perhaps the greatest controversy in large, efficient buccal pump. Investiga- the higher taxonomy of the Anura cen- tors as far back as Luther (1914; see ters on the position of the frogs with the Edgeworth, 1930; Wassersug, 1975) Orton Type 2 larvae, the Microhylidae. have explained the unusual chondrocra- Many authors have commented on this nium of tadpoles as an adaptation asso- problem, most recently Starrett ( 1973 ciated with their feeding mechanism. ) Savage (1973), Sokol (1975), Duellman Elongation -nd anterior extension of the Lynch (1973), and Blommers- palatoquadrate has allowed for expan- (1975), Based on the char- sion of the ceratohyal in the horizontal Schlosser (1975). plane to form the piston of the buccal acters used by Orton and Starrett, the pump (Severtzov, 1969). The anterior microhylids bear the closest resemblance displacement of the palatoquadrate, to the pipids and Rhinophrynus. Based however, limits the area for the emer- on characters of the adults and addi- gence of cranial nerves from the brain tional larval features discussed by Sokol, .

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 125 the microhylids are presumed to be The Origins of the "Advanced" ranoid-derived frogs. Anurans ( Type 4 Larvae ) In the structure of their branchial Although it is generally recognized food traps and visceral skeleton, micro- that pelobatoid frogs (families Pelobati- hylid larvae are neither clearly pipoid dae and Pelodytidae ) represent the least nor obviously ranoid. The buccal Hoor specialized families with Orton Type 4 exposure of the glottis in the microhylids larva (Lynch, 1973), the relationship of is most like that of the pipids, but the these frogs to more advanced families is attachment of the ventral velum is more not fully understood. Duellman (1975) similar to that of advanced Type 4 lar- placed the pelobatoid frogs in his sub- vae. My study suggests that the micro- order Archaeobatrachia, suggesting that hylid larvae are profoundly different they are closer to the "ancestral" frogs from both Orton Type 1 and Orton Type than to the "advanced" anurans of the 4 larvae. order Neobatrachia. Pelobatids lack se- Of the microhylids examined (see cretory ridges in the branchial food traps also Savage, 1952), Microhyla heymonsi and in that feature are most similar to looks the most like an Orton Type 4 the archeobatrachian Ascaphus and dis- larva in internal oral features. Specifi- coglossids (Wassersug and Rosenberg, cally, it has a relatively long buccal floor 1979). anterior to the buccal pockets, small The most detailed discussion to date branchial baskets (compared to other on the origin of Type 4 larvae is in microhylids), and a ventral velum vir- Heyer (1975:40-43). Savage, as a pers. tually continuous across the midline. comm. in that paper, suggests that lep- There is little question that these re- todactylids arose directly from a leio- semblances are due to secondary con- pelmatid ancestor. Heyer (who evident- vergence as the ancestor of M. heymonsi ly accepts the Starrett-Savage tenet that abandoned total reliance on microscopic the pipoid larvae represent the ancestral food. The presence, however, of a con- larval form) correctly points out that tinuous or at least nearly continuous one implication of Savage's suggestion is ventral velum in this species raises the that the Type 4 larva must have evolved possibility that microhylids could have twice from a beakless ancestor. Extant evolved from forms with a continuous archeobatrachian species with their re- ventral velum. This excludes the Pipidae lict distributions and exotic larvae pro- (but not Rhinophrynus) vide little information that can help The ancestor of the Microhylidae evaluate Savage's suggestion. To quote need not be from an extant family. If Heyer (1975:42), "The crux of the argu- microhylid larvae evolved from tadpoles ment hinges, then, on whether the pelo- with keratinized beaks, the presence of batid acosmanuran tadpole is really the secretory ridges in the branchial food same as a leptodactyloid (bufonid and traps points to an origin above the dis- ranoid) acosmanuran tadpole." Heyer coglossoid/pelobatoid grade. Blommers- argues that given a limited number of Schlosser (1975) recently described lar- ways that a tadpole can be efficient at vae of Pseudohemisus granulosus, a scraping, one would not expect great scaphiophrynine frog from Malagasy; differences in morphology between pelo- these tadpoles exhibit a mosaic of micro- batid tadpoles and leptodactyloid larvae, hylid/ ranid features in their external even if they are diphyletic. anatomy. As more exotic microhylid lar- I am not so convinced that the Pi- vae are described, I suspect that they will support a microhylid-ranoid rela- poidea are the stem anuran group (see tionship, and resemblances between mi- above), and, if they are not, this alters crohylid larvae and pipoid forms will the problem. Nevertheless, assuming prove to be convergences. that the pelobatids and leptodactyloids 126 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY arose from families with beaked larvae, lata species group, Hyla ebraccata and the question of the phylogenetic rela- Hyla sarayacuensis, exhibit larval spe- tionship of the leptodactyloids to archeo- cializations away from ultra-planktonic batrachian frogs remains. suspension feeding and toward macroph- Lynch (1973) has made a case for agy. They have reduced or lost the pa- the evolution of primitive leptodactylids pillae of the buccal floor and roof. They directly from megophrynine pelobatids.^ have a low filter mesh density and ab- traps. H. sara- I have not examined internal features breviated branchial food of filter of any leptodactylid tadpoles in detail yacuensis has a lower number but these tadpoles seem superficially rows and more reduction of the secretory similar to other neobatrachian, Type 4 ridges in the branchial food traps than larvae. The bow-shaped branchial bas- H. ebraccata and appears to be the more kets and abbreviated attachment of the macrophagous of the two forms. ventral velum to the filter plates of the Of all the hylinine tadpoles studied, phlebodes Hyla microcephala spe- second and third ceratobranchials ap- Hyla ( pear to be uniquely derived character- cies group) larvae have the most ex- istics of the pelobatids and may pre- treme reduction in structures associated clude deriving the pattern of velum with the ingestion of fine, suspended attachment in other Type 4 larvae from matter. this family. I feel that it is most plausi- If one looks at the general pattern of ble that the pelobatid velar structure reduction, a morphological sequence can evolved from the common Type 4 pat- be drawn from Hijla regilla as a typical tern. If Australian myobatrachine larvae Hyla larva to the leucophyllata group have pharyngeal morphology like the and then to the Hyla microcephala group megophrynine pelobatids I would con- as represented by Hyla phlebodes. This sider this strong evidence for the phylog- morphological sequence represents a eny proposed by Lynch. Until more is trend toward a particular type of ma- known about primitive leptodactyloid crophagy dealing with coarse plant mat- (sensu lato) larvae, it is best to view ter and detritus rather than large, live the pelobatids as a sister group rather prey such as eaten by carnivorous tad- than the ancestors of more advanced poles. It is through a similar morpho- frogs. logical series that the ancestors of the Hyla microcephala group might have Evolution of Specific Larval Types evolved, although I do not mean to im- IN THE Genus Hyla ply that the Hyla microcephala group evolved directly from the Hyla leuco- Because of the large and morphologi- phyllata group. cally diverse sample of Hyla larvae exam-

ined it is both possible and appropriate 2) Arboreal Hyla Tadpoles.—The to comment on the adaptive radiation of internal anatomy of Hyla dendroscarta larval types in this genus. The evolution larvae sheds some light on the question of two types are singled out for discus- of how arboreal forms of the Hyla sion, the macrophagous herbivorous bromeliacia group may have evolved. larva and the arboreal larva. These types Duellman (1970:681) stated that the help demonstrate how knowledge of lar- "group containing bromeliacia in north- val morphology can give some insight ern Central America and dendroscarta into evolutionary history below the fa- in southeastern Mexico, apparently di- milial level. verged from the lowland pond-breeding 1) Macrophagous, Herbivorous Hyla picta-stock by adapting to arboreal larvae.—Members of the Hyla leucophyl- breeding habits in a successful attempt

'Lynch (as cited in Sokol, 1977a) suggested that the pipoids could also be derived from the pelobatoids, but I consider this unlikely for the reasons stated above. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 127 to invade the foothills in low mountains above water, that dropped into the wa- where ponds are scarce." Members of ter after hatching, then later developing the H. picta group, however, are quite tadpoles that could survive on the vege- different in larval biology from H. den- tation. This is a more believable evolu- droscarta and H. hromeliacia. H. picta tionary sequence than the quantum jump larvae have a tall tail fin, moderately from pond to tree that is required if the short pointed tail, and occur in grassy Hyla hromeliacia group evolved from a pools. Tadpoles of the H. hromeliacia Hyla pic^a-like stock. group have the long tails of stream Arboreal larvae in other genera and adapted larvae. Internally, H. dendro- families, particularly those with elongate scarta larvae have a mosaic of features larvae, could have followed a similar that are associated with either pond or evolutionary history. Centrolenid larvae stream existence. The lobe-like infra- presumably represent an intermediate labial papillae and absence of velar mar- stage in this evolutionary scenario. ginal projections are characteristic of The present geographic range of H. certain pond tadpoles. On the other miotympanum, H. arhorescandens, and hand, the many tall buccal floor and H. thorectes does not exclude the possi- buccal roof papillae and the truncation bility that their immediate, common an- of the third filter cavity are features that cestor could also have served as the appear in stream larvae. In overall in- ancestor of the H. hromeliacia group. ternal and external proportions, H. den- Based on external and internal morphol- droscarta tadpoles are more like stream ogy of the larvae and the breeding be- than pond larvae. havior of the adult, it is highly probable Duelhnan (1970:429) noted that that the ancestor of H. hromeliacia spe- members of the H. hromeliacia group cies group separated from the nuclear have cranial characters similar to H. central American hylid stock at the level miotympanum but considers any alliance of a common branch leading to H. mio- between these two species tenuous. In tympanum, H. arhorescandens, and H. fact, members of the H. miotympanum thorectes. group have stream larvae that look very much like tadpoles of the H. hromeliacia The Evolution of Ontogenies and Its group. Hyla arhorescandens, the sister Role in Larval Diversity species of H. miotympanum, even has While this study demonstrated a larvae with the unusual 2/4 denticle pat- great deal of morphological diversity in tern that characterizes the middle Amer- the feeding structures of anuran larvae, ican arboreal Hyla larvae. species of A it is worth noting that few truly unique Hyla closely related to the H. miotym- structures were seen in any of the tad- panum group has a breeding behavior poles. that could represent a link between the Most difterences between species are stream breeding of H. miotympanum gradational differences in the relative and the arboreal breeding of H. dendro- size, shape, or number of particularly scarta and H. hromeliacia. This is Hyla common features. thorectes, which, according to Duellman Three specific processes can account (1970, p. 391), has stream larvae but "is for most of the structural diversity: pro- unique among members of the genus in liferation, fusion, and reduction. These northern middle America by depositing are not only processes in the phylogeny its eggs on vegetation above the of anuran larvae, but are common proc- plausible that streams." It seems most esses in their ontogeny as well. Recent- the ancestor of the present bromeliad ly, much attention has been given the breeding Hyla went through just such an role of ontogenetic shifts in phylogenetic evolutionary stage, first leaving eggs evolution (Gould, 1977); the tadpole 128 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY oral structures helped to illustrate how ridges, a common pattern in funnel- important this heterochrony may be in mouthed forms, suggests a relative sup- generating evolutionary diversity. pression of the tendency for the papillae The opportunity for heterochrony in to elongate, without a reduction in the anuran evolution is accentuated by the tendency for papillae bases to grow and fact that developmental programs can be develop. modified not once, as in most vertebrates' Some of the most unusual morpho- development, but twice. They can be logical patterns described in this paper modified first when the embryo develops can be comprehended in the framework into a tadpole, then again when the tad- of heterochrony. A choice example is pole metamorphoses into the frog. the uninterrupted gill filter rows that In comparing different forms, it is bridge the gill slits in Gastrotheca. Al- sometimes possible to tell which part of though it is possible that this pattern is the developmental process has been dis- due to a truly novel fusion of filter rows, torted through evolution. Consider, for there is an ontogenetically simpler hy- example, the different patterns for the pothesis. I suspect that when the gill gill filters seen in hylid larvae with re- pouches develop in the embryo they duced branchial baskets. Both Hyla perforate only at the bottom of the filter phlebocles and Anotheca spinosa have canal and these perforations fail to coa- small branchial baskets with highly re- lesce into continuous slits. Arrested deduced gill filters. In the case of Ano- velopment of the larval gill slits in free- theca the filters are thin, wispy struc- living Gastrotheca may be precursory to tures, whereas in H. phlebodes they are direct development in Gastrotheca lar- blunt, knoblike projections. In the nor- vae that have abandoned the free-living mal ontogeny of a Hyla regilla both tadpole stage. This hypothesis, one of morphologies are seen (Wassersug, arrested development, could be verified 1976b and pers. obser.). In the early or refuted with a growth series of Gas- ontogeny, as the embryo develops into a trotheca embryos. larva, Hyla regilla gill filters appear rela- Major advances in our general under- tively knobby without having a compli- standing of anuran larval diversity will cated, folded pattern. At metamorpho- require attention to subtle differences in

sis, however, as the filters degenerate, ontogenetic processes. they shrink and develop a wispy appearance, much like those of Anotheca. We ECOLOGICAL CONSIDERATIONS can suggest that the reduction of the Tadpole Feeding Ecology gill filters in Hyla phlebodes results from abnormally early and prolonged meta- The autecology of anuran larvae is morphosis of the gill filters relative to poorly known. Much of what is dis- other oral structures. It then follows cussed here constitutes hypotheses pre- that the pattern seen in Anotheca is due sented in relatively broad tenns. For in- to an arrested embryonic development stance, the sizes of food particles are of these same organs. referred to simply as "small," "medium," Other examples can be seen in the or "large." This vague, comparative papillae of the buccal floor and roof. rather than quantitive, terminology is The proliferation, attenuation and bi- necessitated by our ignorance. There is furcation of buccal papillae commonly little hard information on the actual seen in stream bottom larvae with suc- particle size distribution either in the torial mouths suggests differential environments in which tadpoles occur growth of these structures either by or in their alimentary tracts. early, accelerated growth or by prolon- The typical pond larvae is often de- gation of the period over which they scribed as a filter feeder (Griffith, 1961; develop. The fusion of papillae into cf. Savage, 1973); but elsewhere I (Was- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 129 sersug, 1975) have argued that the Particle Sorting: The General broader term "suspension-feeder" is more Mechanism appropriate. As demonstrated by Ru- The complexity of internal oral struc- benstein and Koehl (1977) filter feed- tures in anuran larvae suggests that com- ing, that is, sieving, is only one mechan- plex sorting processes take place be- ism by which aquatic organisms can tween the oral orifice and the esophagus. extract particles suspended in water. The variety of palps, flaps, papillae and Aerosol engineers have identified at least other projections in the tadpole mouth five mechanisms by which particles can are interpreted here as forming a multi- be removed from a fluid. Depending on tiered sorting system used to capture the physical properties of the suspended particles of a variety of sizes with great particles and the entrapping structures eflBciency. (e.g., particle diameter; mass; pore size The sorting starts at the oral orifice. of filters; electrostatic charge, etc.), cer- Particles too large to enter the mouth tain mechanisms will be more effective cannot be ingested unless they are re- than others. duced to smaller particles by the beaks Tadpoles can clearly ingest particles and denticles. Particles small enough to smaller than the pore size of their gill enter the mouth may be too large to pass filters (see Dodd, 1950; Jenssen, 1967; between the infralabial papillae and can Kenny, 1969a; Hendrick, 1973; Wasser- be ejected immediately. sug, 1972 , so they must use other mech- ) Particles small enough to pass the anisms besides simple sieving. Kenny infralabial papillae enter the space be- (1969b), Wassersug (1972), Wassersug tween the buccal floor and buccal roof and Rosenberg (1979), have all dis- arena. From this region there are three cussed mucous entrapment in tadpoles. possible courses a particle can take. If This process may involve inertial impac- the particle is too large to pass between tion or electrochemical attraction (elec- any of the papillae of the buccal floor, trostatic entrapment; cf. Rubenstein and it can be coughed out of the mouth. Koehl, 1977; LaBarbera, 1978). Follow- Presumably, all particles rejected would ing Rubenstein and Koehl, it is likely be too large to pass down the esophagus. that tadpoles capture particles by at least If a particle is too large to go between three methods: direct interception, in- the papillae on the right and left side of ertial impaction, and electrostatic en- the arena, but small enough to pass be- trapment. tween the papillae at the back of the Although many herpetologists have arena, the general funnel-like shape of made a distinction between the feeding the buccal floor arena will shunt it di- ecologies of tadpoles with and without rectly posterior and into the esophagus. keratinized mouth parts, there may be Any particle small enough to pass be- little or no difference between the way tween the papillae laterally can go to in which these animals feed. It is fair either the left or right side and over the to say that all free-living tadpoles, ex- ventral velum into the pharynx. cept for some extremely specialized mac- Once in the pharynx, a particle may rophagous forms, can suspension-feed. be trapped by direct interception and Tadpoles with hard mouth parts may inertial impaction on the gill filters. Par- also graze on periphyton, macrophytes, ticles so small as to pass through the large detrital material, but their and gill filters can still be aggregated in grazing activity primarily serves to pro- mucus on the branchial food traps. The duce a suspension. This suspension is larger aggregates formed there can then then handled internally by basically the be retained by the gill filters (Wasser- same mechanisms that tadpoles lacking sug, 1972). hard mouth parts use. How particles trapped in the filter 130 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY cavities are transported posterolaterally theca and Hymenochirus larvae. Not to the ciliary groove and ultimately to only obligate carnivores, but several the esophagus is poorly understood. A herbivore/ detritivore larvae have aban- reasonable, but admittedly vague, hy- doned indiscriminate suspension-feeding pothesis is that particulate matter com- in favor of macrophagy. Htjla micro- pressed between the pressure cushions cephala and Ooeidozyga larvae are ex- and the gill filters is shunted later- amples. ally by a rhythmic pulsing action of the Another common pattern is the pro- pharynx. It should be possible to test liferation of buccal sieving structures in this hypothesis by giving tadpoles dyed larvae which also have reduced filter food and sacrificing them individually at density (high filter porosity). This successively longer intervals after feed- places emphasis on the gross sieving ing. Dissection of these larvae should structures rather than finer entrapping reveal the path of food through the surfaces and appears to be an adaptation pharynx and clarify the transport mech- for feeding on a relatively coarse sus- anism. In any case it is evident that tad- pension of particles. Benthic, thigmo- poles have alternative methods of trap- tactic tadpoles commonly show this pat- ping particles that depend on particle tern. size. The ingestive system appears ar- Fusion of buccal floor and roof pa- ranged so that gross structures which pillae into ridges, which is characteristic can trap large particles protect smaller, of funnel-mouthed tadpoles, enables the more delicate surfaces which are de- buccal cavity to serve as a particle guid- signed for handling the finer particles. ing system, rather than a particle sieving Specifically, buccal structures protect the system. This morphological arrangement branchial baskets from clogging by chan- appears ideal for handling a relatively neling larger particles, that have already narrow size range of moderately coarse passed through the infralabial papillae, particles. directly to the esophagus. Enlargement of the branchial baskets It follows from the above general and a very high density of the gill filters outline that interspecific differences in is most often associated with relatively the size, shape, and spacing of the vari- few, widely spaced buccal papillae. Tad- ous trapping structures will reflect differ- poles with this pattern appear well ences in the particle sizes upon which adapted for feeding on a suspension of different larvae feed most eSiciently. uniformly small particles. Indeed, larvae with this morphology are the obligate microhabitat implications of microphagous suspension-feeders; Mi- Morphological Patterns crohyla ornata and Xenopus laevis are Several common morphological pat- two examples. terns in the overall proportions of the Each of these patterns correlates well various sorting and sieving structures of with the distribution of particle size in tadpoles provide clues to the feeding the environments where the larvae ex- of ecologies of these organisms. Many hibiting them live. For example, micro- these patterns were alluded to in the planktonic algae are likely to be rare in section on Functional Considerations the aphotic environment of Anotheca and are summarized here. spinosa. Food source in this habitat will Several anurans have larvae which be those large organisms near the top of show a loss or reduction in all of the the food chain, on which Anotheca is particle sorting and trapping structures. clearly specialized to feed. This morphological pattern is consistent- Benthic, thigmotactic tadpoles are ly associated with extreme macrophagy, best represented by stream larvae. as illustrated by the carnivorous Ano- Stream environments are relatively oli- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 131 gotrophic; with a rapid exchange of wa- microphagous suspension-feeders often ter, and constant nutrient washout, there metamorphose at a relatively small size is httle chance for a phytoplanktonic and quite soon after hatching. They are bloom in a stream. Most primary pro- specialized for ingesting the earliest, pri- ductivity in this habitat is in the form of mary productivity which develops in periphyton, which can be gleaned only temporary ponds, namely small phyto- by grazing upon the substrate. The plankton. The absence of keratinized grazing activity of tadpoles with beaks mouth parts in most of these forms can and denticles produces a relatively be construed as an energy-conserving coarse suspension of particles. adaptation. While hard mouth parts Tadpoles adapted for feeding on would allow these larvae to graze on these self-generated suspensions are not macrophytes, periphyton, and other de- likely to encounter large particles or ex- tritus, such material is often absent in ceptionally small particles with any fre- their ephemeral environment and these quency. Although it may appear advan- morphological structures are energeti- tageous for stream tadpoles to have large cally expensive to develop and main- and dense gill filters that could com- tain. pletely retain all of the smallest particles A few tadpoles are unusual in ap- ever encountered, extremely small food pearing to be specialized for handling particles are too rare in a stream habitat food of two different size classes. Sca- to warrant the energetic cost of develop- phiopus and Rhinophnjnus typify this ing and maintaining the tissues neces- bimodal size selection potential. They sary for capturing all such particles. At are both temporary pond breeders in the other extreme, thigmotactic stream seasonally dry areas. In these environ- larvae are not likely to run into very ments much of the potential food is large particles such as those regularly either unicellular algae or the larger ingested by macrophagous carnivores herbivores, such as conspecifics, that and herbivores. The large gap at the graze on this algae. On the one hand, back of the buccal floor and buccal roof these larvae are efiicient, ultraplanktonic arena, which allows many tadpoles to suspension-feeders able to handle the shunt the largest particles they ingest initial phytoplanktonic blooms in the directly from the buccal cavity into the small bodies of water where they breed. esophagus, is absent in these forms. On the other hand, the ephemeral nature The funnel-mouth adaptation appears of their ponds requires that they be able even more specialized for selecting rela- to grow to a large size extremely fast tively large particles in a relatively nar- and this means they must be able to row size range. Lacking the multi-tiered ingest all other possible food items in sieving system, funnel-mouthed tadpoles their ponds. In having few, widely have abandoned the ability to feed in- spaced, buccal floor papillae and dense discriminately over a broad range of gill filters, these larvae are adapted for particle sizes in favor of the capacity to handling both the largest and the small- handle large particles which might float est particles in their environment; they in the backwashes of quiet streams or are not likely, however, to feed efficiently adhere loosely to surfaces. on the medium sized particles that most tadpoles generate while grazing. Tadpoles specialized for extreme microphagy seem to occur most commonly In contrast to the extreme forms just in midwater in small, stagnant pools or described, the majority of pond larvae ponds which have high insolation, a high appear adapted for handling a relatively nutrient load, and an abundance of uni- broad spectrum of food sizes and types. cellular phytoplankton (see Heyer, In the "average" temporary pond (e.g., 1973, 1974; Wassersug, 1973). These a temporate zone, vernal pond) the size ).

132 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY distribution of potential food can fluc- to be exposed to a very broad range of tuate so drastically that most larvae particle sizes. They may have few po- would never reach metamorphosis if tential competitors for food resources they ate food in a narrow size range and are understandably dietary general- only. Because of extreme fluctuation in ists. In contrast, in wet, lowland, tropi- the resource base it is not surprising that cal ponds developmental time can be there has been little documentation of rapid but the anuran fauna is very large, direct (exploitation) competition among and competition for breeding sites severe tadpoles for food. Competition among ( Crump, 1974, and others cited therein ) most anurans has resulted in spatial and This is a situation where many anuran temporal separation of larvae rather than species use the same breeding pond at overt dietary partitioning (Heyer, 1974, the same time and the larvae may not be 1976). Only recently has exploitation able to avoid competition; here one is competition been demonstrated for typi- most likely to find pond tadpoles which cal pond larvae in either the laboratory are dietary specialists.

( Steinwascher, 1978; Scale and Beckvar, Consider Hyla phlebodes; the ex- in press) or the field (Scale, 1973). tremely specialized oral morphology in One can use slight variations in the this larvae and its obligatory, narrow morphological patterns delineated above dietary range suggest that it occurs in to hypothesize about the feeding ecolo- ponds with larvae of many other species gies of specific anuran larvae. Hyla ru- that use other parts of the resource base. fitela and Hyla femoralis, for instance, Contrast this with Gastrotheca riobam- which have denser gill filters than either hae—based on its generalized morphol- Hyla regilla or Acris crepitans, are prob- ogy this large larvae would appear to ably more efficient at ultraplanktonic en- have a very broad diet and to feed effi- trapment than these latter forms. As ciently on a variety of food types. One another example, the Bufo larva illus- can predict that it would occur with trated by Savage (1952) has many tall larvae of relatively few other species. buccal floor papillae, a feature associated Although I have personally collected with benthic, thigmotactic grazing. It is neither species, Duellman (pers. comm. not surprising, then, that Bufo tadpoles has indeed confirmed that H. phlebodes are often found feeding on the bottom, larvae are always found inhabiting ponds grazing on detritus. They appear spe- with tadpoles of several other species, cialized for handling medium to small while G. riobambae (which occurs at fragments of material and may not be high elevation) is found alone. particularly efficient at feeding on either The feeding currents of a tadpole are extremely large or extremely small parti- also its respiratory currents, so it is ap- cles. propriate to add here some comments From all that has been said so far, on ecological patterns in the respiratory we can conclude that tadpole oral fea- systems of anuran larvae. Tadpoles that tures reflect the breadth of the larval are specialized for feeding on large par- diet, at least in terms of particle size, ticles often have a large, exposed glottis and, as indicators of niche breadth, oral on the floor of the mouth and evidently structures can provide some insight into depend extensively on aerial respiration. species packing problems for tadpoles. It is a reasonable hypothesis that, in the To illustrate this latter point we can absence of buccal papillae to act as compare two distinct larval ecotypes. coarse sieves, these larvae should reduce Larvae of moderately large size from their aquatic respiratory pumping activ- cool-temperate climates (e.g., many ran- ity in order to prevent accidental clog- ids) require a relatively long develop- ging of the filter cavities or glottis by mental time, over which they are likely particles that would otherwise be too ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 133 small to be ingested. Macrophagous lar- expansion is well exemplified by the vae, such as Anotheca, probably do not differences between the funnel-mouthed exhibit regular aquatic pumping. It is Microhyla and other Microhyla. Most known that Hymenochirus larvae do not Microhyla have a small buccal displace- exhibit regular respiratory pumping and ment compared to the large volume of only open their mouths to take in either their branchial baskets. These non-fun- air or prey (Sokol, 1962). Many of the nel-mouthed forms cannot completely macrophagous, herbivorous Hyla larvae clear the oral cavity with a single stroke (H. microcephala and H. leucophyllata of the buccal pump, but can maintain a species group) are small and may rely continuous, gentle flow past the gills extensively on cutaneous respiration. throughout a buccal cycle. Thus, they Obligate midwater, microphagous are equipped to clear constantly a sus- anuran larvae often occur in extremely pension of rather fine matter, as well as eutrophic and, potentially hypoxic, habi- to irrigate continuously their respiratory tats; they also exhibit large glotta and surfaces. In contrast, M. heymonsi, with may depend heavily on aerial respira- its comparatively large buccal pump and tion. small branchial baskets, can suck in a large volume of water with each stroke In contrast, stream larvae, which live of the buccal pump. H. heymonsi has in well aerated habitats, can depend on the ability to use gape-and-suck feeding gill and cutaneous respiration to meet to selectively take in rather large their metabolic needs. In these forms, particles but not to maintain a gentle con- aerial respiration could lead to positive buoyancy, which may be maladaptive tinuous respiratory flow while it is feeding. Its relatively large buccal pump (Wilder et al., 1920; Wake, 1966; Was- displacement is well adapted for spo- sersug and Seibert, 1975). radic feeding, but could cause the ani- Differences in both feeding and res- mal to lurch conspicuously forward and piration are often reflected in the rela- backward in the water column if the tive size of the buccal floor since buccal tadpole pumped maximally during nor- floor area is one parameter affecting the mal respiratory activities. volume displaced by the buccal pump More work on the feeding and respi- (Wassersug and Hoff, 1979). This, ratory ecology of anuran larvae will be in turn is intimately related to both necessary before we will completely un- feeding and respiratory patterns. derstand the ecological and evolutionary All macrophagous larvae exhibit a implications of larval morphology. It is, general expansion of the buccal floor in however, already clear that knowledge the prepocket region relative to the rest of tadpole oral morphology can provide of the floor and pharynx that allows major insight into the way of Iffe of them to suck in large particles. This these organisms. SUMMARY AND CONCLUSIONS

This study has been limited to gross In the following pages the morpho- surface features in the mouths of tad- logical variation seen in the oral struc- poles—surfaces where particles are ex- tures of the larvae examined is first sum- tracted from water currents and gas marized, and moi-phological patterns exchange takes place. Internal oral sur- reviewed. Then major conclusions con- faces are described for larvae of eight cerning anuran systematics and tadpole anuran families. When combined with evolution and ecology are enumerated. descriptions elsewhere in the literature, Morphological Variation the anatomy of this region is now known for representatives of a dozen families. An effort was made to interpret the :

134 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

function of all major morphological ( 5 ) Ventral velum.—The ventral vel- structures um is an important valve which regu- (1) Keratinized spurs and projec- lates one-way How from the buccal to tions.—Two keratinized structures are the pharyngeal cavity in all anuran lar- seen inside the mouths of certain tad- vae except the Pipidae. There are six poles. The first, which occurs in many major configurations of the ventral species and may be used in shredding velum which can be associated with spe- food is a bilateral, medially directed cific families or superfamilial groups. keratinized spur at the edge of the oral (6) Gill filters. —Interspecific varia- orifice between the upper and lower tion, in overall size and in relative den- beaks. The second, a medial cornified sity of the gill filters reflects differences projection from the prenarial arena in in tadpole feeding ecology. Tadpoles the macrophagous Scaphiopus bombi- generally recognized as extremely spe- frons, is presumably used in holding and cialized for microphagy have very large shearing prey. branchial baskets and large filter plates

) papillae. In thigmo- with very dense gill filters; these serve ( 2 Infralabial — tactic, benthic larvae these are typically to extract oxygen and food from the large, elongated and dendritic, whereas, water. Obligate macrophagous larvae in larvae adapted for macrophagy, they have reduced branchial baskets and gill may be short and globose or lacking filters; in the extreme macrophagous altogether. These structures have a me- forms, such as Hymenochirus, gill filters chanical and possible chemoreceptive are completely absent. Funnel-mouthed function; they appear particularly im- larvae typically show some reduction in portant in the positioning of food as it the gill filters compared to close rela- comes into the mouth. tives with more typical oral features. (3) Lingual papillae.—Most species Two unusual patterns involving fu- examined have two premetamorphic pa- sion of filter rows are documented. In pillae, but some have one or four. As- Pipa, neighboring filter rows on each caphus and the discoglossids have multi- filter plate are fused so that the filter ple lingual papillae. The pipids, lacking canal between the rows is canopied. In a tongue, also lack lingual papillae. Fol- Gastrotheca, the filter rows are fused lowing Hammerman (1969), I have as- ventrally with opposing filter plates over sumed these structures serve a chemo- the ventral gill slits, which means that receptive function. they have fenestrated gill pouches rather (4) Buccal floor arena (BFA) and than continuous gill slits.

) are Buccal roof arena (BRA) papillae.—Pa- ( 7 Branchial food traps.—There pillae of the buccal roof and floor are two basic patterns for these organs; usually arranged to form a V- or U- one characterizes the Archaeobatrachia shaped area. Species may have no buc- {sensu Duellman, 1975), and the other cal papillae (e.g., Pipidae, macrophagous the Neobatrachia. Overall size and Hylidae) or as many as eighty or more shape of the branchial food traps does papillae on the buccal floor alone. Pa- not seem to correlate strongly with any pillae seem to be important in the pri- aspect of tadpoles' diets. The texture of mary sorting and sieving of particles the secretory surface itself, however, from the water; they may actually be shows some correlation with larval feed- the major food sorting structures in the ing ecology. Forms specialized for mi- mouth of stream-adapted species. crophagy tend to have distinct, widely In funnel-mouthed larvae, papillae spaced ridges, while extreme macropha- often are either absent or fused into gous larvae tend to lose the secretory interlocking dorsal and ventral ridges. tissues in general, and the secretory I interpret these structures as chutes for ridges specifically. Exceptions to the 2 separating out larger food particles. basic forms are the unique secretory . )

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 135 ridge patterns seen in Rhinophrynus, dent in the unperforated nares of the Xenopus, and the Microhylidae. As- Microhylidae. Tadpoles of this family caphus and the discoglossids have an have a stiff flap that extends down from extensive field of secretory epithiha in the posterior margin of the internal nares the branchial food traps but lack secre- and may help direct currents toward tory ridges (see Wassersug and Rosen- these sensory regions. berg, 1979, for details of the micro- ( 12 Postnarial arena. — Tadpoles anatomy of these surfaces ) typically have a symmetrical arrange- (8) Glottis.—The size of the glottis ment of papillae or ridges that are tight- and the extent of its exposure on the ly grouped posterior to the internal floor of the mouth appears to correlate nares. Projections are large and numer- both with aerial respiration and the tad- ous in this region in forms which have pole's buoyancy. Bottom larvae tend to many large and numerous buccal papil- have a small glottis, while obligate mid- lae elsewhere in the mouth. Postnarial water larvae, and those that depend structures, however, are reduced in heavily on aerial respiration (e.g. Ano- forms which typically lack papillae or theca), invariably have a large glottis. show reduction in papillae elsewhere on (9) Esophageal funnel.—The size the buccal roof or floor. Blunt, shallow and shape of the anterior portion of the papillae typically replace rows of post- esophagus reflect the size of the parti- narial papillae in the postnarial arena of cles upon which tadpoles commonly funnel-mouthed larvae. feed; macrophagous larvae tend to have Postnarial papillae are aligned to a large esophagus, whereas obligate mi- form a cap over the lingual anlage when crophagous forms have a small, narrow the mouth is closed. Postnarial struc- esophagus. tures may serve chemoreceptive, me- (10) Prenarial arena.—Diverse spe- chanical-receptive, and particle-sorting cies-specific patterns in ridges, pustula- roles. They may be important in direct- tions, projections, etc. are found in the ing water currents to regions of sensory prenarial arena of anuran larvae. Their epithelia and particulate matter to other

exact function is not well understood regions of the buccal cavity for sorting. but it is hypothesized that they assist the (13) Glandular zone.—The ventral lower beak in holding and positioning velum of tadpoles meets the buccal roof

food as it enters the mouth. during closure along a region of secre- The most distinctive pattern for these tory epithelia, the glandular zone, which structures is seen in funnel-mouthed has been implicated in particle capture. forms, regardless of family; here there The secretory tissue of the zone may

is invariably a distinct, posteriorly di- assist the branchial food traps in aggre- rected, V-shaped ridge in the prenarial gating particulate matter in mucus. arena. There appears to be a slight inverse (11) Internal nares.—The internal correlation between the size of the secre- nares are perforated structures in all but tory pits in the glandular zone and the microhylid larvae. Their orientation particle size that a tadpole typically seems to vary, in part, with the shape of feeds upon. It is proposed here that the the tadpole head. The nares are always glandular zone may also assist the velum associated with valves. In the Dis- in its valvular function. The zone varies coglossidae, large flaps extend under extensively in shape, but in part reflects the nares and presumably protect them the shape of the ventral velum beneath from particles flowing into the mouth. it. Secretory tissue of the glandular zone Several species have pockets of pre- often continues posteriorly onto the sumed sensory epithelia (Jacobson's or- pressure cushions of the dorsal pharynx. gans) arising from the margins of the Macrophagous larvae often lack a glan- internal nares. Sensory epithelium is evi- dular zone. .

136 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

(14) Dorsal velum.—A continuation natural family or superfamily. Bran- of the ventral velum onto the roof of chial food trap anatomy suggests a close the mouth is characteristic of all non- relationship between Ascaphus and the pipid tadpoles but is reduced in extreme Discoglossidae. Among the Discoglossi- macrophagous fonns. The dorsal velum dae, Bombina appears to have the most is invariably positioned slightly posterior generalized larva. to the ventral velum in such a way that (3) Rhinophrynus larvae are exter- it must deflect water from the buccal nally similar to Xenopus and Pipa, but cavity into the anterior part of each internally they are as different from filter cavity when the buccal floor is ele- pipid larvae as they are from the larvae vated. It is proposed here that, in de- of any other family. While the super- flecting water currents ventrally and an- familial association of the Rhinophryni- teriorly, the dorsal velum helps prevent dae and the Pipidae may be valid, Rhi- the resuspension of particulate matter nophrynus must be accepted as the most aggregated and precipitated in the pos- generalized of the Pipoidea. terior parts of the pharynx. Pipoid frogs are so specialized that

( 15) Dorsal pharynx.—The dorsal re- the superfamily could not serve as the gion of the pharynx is small in all tad- immediate ancestors of any extant anu- poles, and the only gross structures of ran families. The recent suggestion that this region are pressure cushions. These the Pipoidea is more closely related to are folds of epithelium that extend ven- the Neobatrachia than to the Archaeo- trally and complement the shape of the batrachia (cf. Sokol, 1976b) finds no filter cavities below. The larger and support in my observations. filter cavities are, the larger deeper the (4) Many features of the ventral and deeper are the pressure cushions. velum, branchial food traps, internal The secretory tissue on these structures nares, and glottal position distinguish role in suggests that they have a food the Microhylidae from all other families. processing. They may help collect food Internally, microhylid larvae do not look in the filter cavities or in some way like pipid tadpoles, although their bran- assist in the lateral movement of food chial food traps are grossly similar to from the filter epithelium to the ciliary those of Rhinophrynus. Ranoid rather groove. than pipoid associations of the Mirco- hylidae are suggested by larval features Systematic Conclusions (specifically, the shape of the ventral Major points from the discussion on velum in Microhyla heymonsi). Systematic Considerations are summar- (5) The Pelobatidae have larvae framework of the ized below in the which are unique in the shape of their Archaeobati-achia-Neobatrachia distinc- branchial baskets and the attachment of Patterns in oral structures gener- tion. their ventral vela. The absence of se- ally support but in some cases refute, cretory ridges in this family is consistent prevailing ideas on the taxonomic rela- with an Archaeobatrachian assignment tionships within and among anuran fam- (cf. Duellman, 1975). I interpret the ilies. shape of the branchial baskets in the (1) Internal oral features of As- Pelobatidae as a unique, derived char- caphus larvae and Leiopelma embryos acter state, which makes it unlikely that provide no evidence for the inclusion of other anuran families evolved directly these genera in the same family. from this family. Primitive leptodacty-

(2) When considering the structure loid (e.g. myobatrachian ) larvae, how- of their internal nares and the shapes of ever, have not been examined and if their pharynxes, the current members their branchial baskets are of the pelo- of the Discoglossidae appear to form a batid form, this will support the idea ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 137 that leptodactyloid frogs have their ori- considerations just reviewed, some gen-

( eral evolutionary conclusions also gin in Asiatic megophrynine ) pelo- may batids. be drawn from this work.

(6) Interspecific variation in oral ( 1 ) The unusual chondrocranium of structures in the HyHdae is enormous. tadpoles is associated with the develop- Most patterns can be interpreted along ment of an expanded ceratohyal and an ecological lines. Externally similar lar- eflficient buccal pump. The development vae from different genera are often very of an enlarged buccal pump, the pres- similar internally, suggesting convergen- ence of an elongated ceratohyal, and the cies or parallelism. On the other hand, presence of a buccal valve in anuran tadpoles of the same genus which differ larvae are all features interpreted as only slightly in external morphology, associated with a generalized suspension- may differ greatly in internal morphol- feeding way of life. This is considered ogy. The following are systematic con- the primitive and generalized way of life clusions at the subfamilial level: for anuran larvae. (a) Anotheca and Gastrotheca are (2) A unique way of life for anuran extremely different in internal larval larvae, not specifically discussed by her- morphology, supporting Maxson's (1977) petologists in the past, is macrophagous removal of Anotheca from the Amphi- herbivory. Extreme reduction in the gnathodontinae. However, Anotheca branchial food traps, loss of buccal papil- larvae are so bizarre, they provide little lation, development of large, pad-like evidence for inclusion of this genus in infralabial papillae, and the presence of the Hylinae. a massive buccal floor area characterize (b) Tadpole oral structures support these tadpoles. This morphology, best the idea that Phyllomedusa and Agahjch- exemplified in Hyla phlebodes, is in- nis are closely related but do not settle terpreted as an adaptation for feeding the issue of the status of the family on coarse plant matter and detritus. Phyllomedusidae. Larvae of the Hyla leucophyllata species (c) Hylinine larvae with similar group show moderate development of ecologies are internally very similar, re- this type of larva. Ooeidozyga in the gardless of genus or species. Ranidae has independently converged (d) Internal oral features support on this morphology. certain phylogenetic relationships pre- (3) The arboreal larvae of the Hyla viously suggested by biochemical data hromeliacia group evolved from an an- only, and which otherwise conflict with cestor with a stream-adapted larva. It traditional taxonomy based on adult os- is suggested that the elongated arboreal teology. An example is the similarity larvae, in general, had stream-adapted between Acris crepitans and Hyla regilla ancestors, and that the Hyla hromeliacia larvae compared to certain other Hyla group specifically evolved from a lineage tadpoles. The basis for this "tadpole: that was ancestral to Hyla miotympan- biochemical" taxonomic congruence is um, H. arborescandens, and H. thorectes. not well understood, and more tadpoles (4) Much of the anatomical differ- will have to be studied to know whether ence between larvae of different species

it is a general pattern. can be explained by heterochronic (e) The genus Hyla is artificial and changes in the early (embryonic) and should be partitioned into several genera. late (metamorphic) ontogeny of the Certain taxa such as the Hyla mixomac- tadpoles. Certain morphological pat- ulata and Hyla microcephala species terns can be identified as due to evolu- groups, probably form valid genera. tionary modifications of specific early or late ontogenetic events when compared Evolutionary Conclusions with more generalized larval develop- In addition to the specific taxonomic mental patterns. Further understanding 138 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY o£ the evolution of anuran larvae diver- larvae can generate a coarse suspension sity will require greater knowledge of with their keratinized mouth parts; they differences in larval ontogenies than is have closely spaced, supernumerary buc- presently available. cal papillae for straining coarse particles, but highly porous gill filters not well Ecological Conclusions adapted for ultraplanktonic entrapment. The majority of internal oral features Funnel-mouthed tadpoles feed selective- in tadpoles are interpreted as part of a ly on large particles floating on the water multi-tiered particle entrapping system surface; they have buccal ridges in place which sorts ingested particles by size. of papillae that seem well adapted for Direct interception and inertial impac- sorting moderately coarse particles from tion are used to different extents on dif- a relatively narrow size range. ferent surfaces. The mucous surfaces of Most pond larvae are adapted for the branchial food traps and the gill handling the broad spectrum of food filters of the pharynx together can effi- types and sizes that may occur in un- ciently trap the smallest particles in- predictable environments. Pond larvae gested by a typical pond larva. Buccal specialized for ingesting a narrow size papillae strain larger particles from the range of particles (e.g., Hyla phlebodes) water and funnel them directly to the are most likely to occur in species rich esophagus, bypassing most of the environments where competition may pharynx. Delicate pharyngeal surfaces have been intense during their evolu- that could be clogged or damaged by tion. large particles are, thus, protected by Respiratory structures vary with the this size-sorting mechanism. availability of dissolved oxygen. Since The size of the particle upon which the amount of phytoplankton in any a species feeds most efficiently may be aquatic body affects the amount of dis- inferred from the size, shape, number solved oxygen, there appears to be a and spacing of buccal and pharyngeal relationship between a tadpole's diet structures. Interspecific differences in and its respiratory structures. Oligo- these features may reflect differences in trophic streams are likely to be well- the size distribution of particles in the aerated, and the benthic tadpoles from microhabitats in which the tadpoles live. these environments tend to have few of In comparison with generalized tad- the morphological features associated poles, extreme macrophagous larvae with aerial respiration. On the other show reduction in all pharyngeal struc- hand, obligate midwater microphagous tures associated with planktonic entrap- larvae may live in extremely eutrophic ment. On the other hand, extreme ponds, and typically have a large glottis, microphagous larvae, live in mid- which a feature associated with a strong de- water, have large branchial baskets and pendence on aerial respiration. dense gill filters well designed for cap- Internal oral structures of anuran turing small phytoplankton that many larvae can used to make reasonably abound in their habitat. Benthic, thig- be motactic larvae typically inhabit streams sound predictions about the feeding and which are probably devoid of phyto- respiratory ecology of anuran larvae plankton but rich in periphyton. These when field data are not available. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 139 LITERATURE CITED

Alcala, a. C. Andean marsupial frogs (Hylidae: 1962. Breeding behavior and early develop- Gastrotheca) . Occas. Papers Mus. ment of frogs of Negros, Philippine Nat. Hist., Univ. Kansas, 9:1-37. Islands. Copeia, 1962:679-726. Dunn, E. R. Altig, R., and E. D. Brodie, Jr. 1924. Some Panamanian frogs. Occas. Pa- 1972. Laboratory behavior of Ascaphus truei pers Mus. Zool., Univ. Michigan, 151: tadpoles. Jour. Herp., 6:21-24. 1-17. Blommers-Schlosser, R. Eaton, T. H., Jr. 1975. Observations on the larval develop- 1959. The ancestry of modem Amphibia: a ment of some Malagasy frogs, with review of the evidence. Univ. Kansas notes on their ecology and biology Publ. Mus. Nat. Hist., 12(2): 155-180.

( Anura : Dyscophinae, Scaphiophry- EdgeWORTH, F. H.

ninae and Cophylinae ) . Beaufortia, 24 1930. On the masticatory and hyoid muscles (309): 7-26. of larvae of Xenopus laevis. Jour.

BoiCERMANN, W. C. A., and I. Sazima Anat, 64:184-188. 1978. Anfibios da Serra do Cipo, Minas ElBL-ElBESFELDT, I. Gerais, Brasil. 4: Descrigao de Phyl- 1953. Die Bestimmung von Kaulquappen lomedusa jandaia sp. n. (Anura, Hy- nach ihrem Verhalten. Deutsch. lidae). Rev. Brasil. Biol., 38:927-930. Aquar. Terr., 6:16-18. BOULENGER, GeORGE A. Cans, Carl 1975. 1891. A synopsis of the tadpoles of the Tetrapod limblessness : evolution and European Batrachians. Proc. Zool. functional corollaries. Amer. Zool., Soc. London, 1891:593-627. 15:455-467. Gaudin, a. Bragg, A. N. J. 1974. An osteological analysis of holarctic 1965. Gnomes of the night, the spadefoot tree frogs, family Hylidae. toads. Univ. Pennsylvania Press, Jour. Herp., 8:141-152. Philadelphia, 127 pp. GOETTE, A. Bresler, and A. N. Bragg J., 1874. Atlas zur Entwicklungsgeschicte der 1954. Variation in the rows of labial teeth Unke. Verlag von Leopold Voss, in tadpoles. Copeia, 1954:255-257. Leipzig. Cei, J. M. Coin, C. J., O. B. Coin, and G. R. Zug 1968. Notes on the tadpoles and breeding 1978. Introduction to Herpetology, 3rd ed. ecology of Lepidobatrachus (Am- W. H. Freeman and Co., San Fran-

phibia: Ceratophryidae ) . Herpeto- cisco, 378 pp. logica, 24:141-146. Gosner, K. L. Crump, L. M. 1960. A simplified table for staging anuran 1^ 1974. Reproductive strategies in a tropical embryos and larvae with notes on anuran community. Univ. Kansas identification. Herpetologica, 16:183- Mus. Nat. Hist. Misc. Publ. 61:1-68. 190. DeJongh, H. S. Gould, S. J. 1968. Functional morphology of the jaw 1977. Ontogeny and Phylogeny. Belknap f^ apparatus of larval and metamorphos- Press of Harvard Univ. Press, Cam- ing Rana temporaria L. Neth. Jour. bridge, Mass., 501 pp. Zool., 18(1):1-103. Gradwell, N., and V. M. Pasztor DODD, J.M. 1968. Hydrostatic pressures during normal 1950. Ciliary feeding mechanism in anuran ventilation in the bullfrog tadpole. larvae. Nature, London, 165:283. Can. Jour. Zool., 46:1169-1174. DUELLMAN, W. E. Gradvi^ll, N. 1970. The hylid frogs of Middle America. 1970. The function of the ventral velum Monog. Mus. Nat. Hist., Univ. Kan- during irrigation in Rana catesbeiana. sas, 1:1-753. Can. Jour. Zool., 48:1179-1186. 1974. A systematic review of the marsupial 1971a. Ascaphus tadpole: experiments on the frogs (Hylidae: Gastroiheca) of the suction and gill irrigation mechanisms. Andes of Ecuador. Occas. Papers Can. Jour. Zool., 49:307-332. Mus. Nat. Hist., Univ. Kansas, 9:1-37. 1971b. Xenopus tadpole: on the water pump- 1975. On the classification of frogs. Occas. ing mechanism. Herpetologica, 27: Papers Mus. Nat. Hist., Univ. Kansas, 107-123. 42:1-14. 1972a. Gill irrigation in Rana catesbeiana. DuELLMAN, W. E., and T. H. Fritts Part I. On the anatomical basis. Can. 1972. A taxonomic review of the Southern Jour. Zool., 50:481-499. 140 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

1972b. Gill irrigation in Rana catesbeiana. form a seasonal tropical location in Part II. On the musculoskeletal mech- Thailand. Ecology, 55:651-656. anism. Can. Jour. ZooL, 50:501-521. 1975. A preliminary analysis of the inter- 1972c. Comments on gill irrigation in Rana generic relationships of the frog fam- fuscigula. Herpetologica, 28:122-125. ily Leptodactylidae. Smithsonian Con- 1973. On the functional morphology of suc- trib. Zool., 199:1-55. tion and gill irrigation in the tadpole 1976. Studies in larval amphibian habitat of Ascaphus, and notes on hibernation. partitioning. Smithsonian Contrib. Herpetologica, 29:84-93. Zool., 242:1-27. 1974. Description of the tadpole of Phry- HOOGMOED, M. S. nomerus annectans, and comments on 1967. Mating and early development of its gill irrigation mechanism. Herpe- Gastrotheca marsupiata (Dumeril and

tologica, 30:53-62. Bibron ) in captivity ( Hylidae, Anura, 1975a. The bearing of filter feeding on the Amphibia). Brit. Jour. Herpetology, water pumping mechanisms of Xeno- 4:1-7.

pus tadpoles (Anura: Pipidae). Acta. HORA, S. L. Zool., 56:119-128. 1930. Ecology, bionomics and evolution of 1975b. Experiments on oral suction and gill the torrential fauna, with special ref- breathing in five species of Australian erence to tlie origins of attachment. tadpole (Anura: Hylidae and Lepto- Phil. Trans. Roy. Soc, London, Series dactylidae). Jour. Zool. Lond., 177: B., 218:171-288. 81-98. Inger, R. F.

Griffiths, I. 1966. The systematics and zoogeography of 1961. The fonn and function of the fore-gut the Amphibia of Borneo. Fieldiana, in anuran larvae (Amphibia, Salien- Zool., 52:1-402. tia) with particular reference to the Jenssen, T. a. manicotto glandulare. Proc. Zool. Soc. 1967. Food habits of the green frog, Rana London, 137:249-283. clamitans, before and during meta- 1963. The phylogeny of the Salientia. Biol. morphosis. Copeia, 1967:214-218. Rev., 38:241-292. Kenny, J. S. Griffiths, I., and A. L. de Carvalho 1969a. Feeding mechanisms in anuran lar- 1965. On the validity of employing larval vae. Jour. Zool., London, 157:225- characters as major phyletic indices 246. in Amphibia, Salientia. Rev. Brasil 1969b. Pharyngeal mucous secreting epithe- Biol, 25:113-121. lia of anuran larvae. Acta Zool., 50: Hammerman, D. L. 143-153. 1964. Occurrence of premetamorphic papil- Kratochwill, K. lae in ranid tadpoles. Amer. Zool., 1933. Zur Morphologic und Physiologic der 4:319. Nahrungsaufnahme der Froschlarven. 1967. Lingual premetamorphic papillae as Zeit. wiss. Zool., 144:421-468. larval taste structures in frogs. Na- LaBarbera, M. C. ture, London, 215:98-99. 1978. Particle capture by a Pacific brittle

1969. The frog tongue: I. General develop- star: an experimental test of the ment and histogenesis of filiform pa- aerosol suspension feeding model. pillae and mucous glands in Rana Science, 201:1147-1149.

catesbeiana. Acta. Zool., 50:11-23. Lanza, B., J. M. Cei, and E. G. Crespo Helff, O. M., and M. C. Mellicker 1975. Immunological evidence for the spe- 1941. Studies on amphibian metamorphosis. cific status of Discoglossus pictus, XIX. Development of the tongue in Otth 1837 and D. sardus, Tschudi Rana sylvatica, including histogenesis 1837, with notes on the families Dis- of "premetamorphic" and filiform pa- coglossidae, Giinther 1858 and Bom- pillae and the mucous glands. Amer. binidae, Fitzinger 1826 (Amphibia Jour. Anat., 68:339-366. Salientia). Monitore Zool. Ital., Hendricks, F. S. (N.S.), 9:153-162. 1973. Intestinal contents of Rana pipiens, 1976. Further immunological evidence for

Schreber ( Ranidae ) larvae. Soutli- the validity of the family Bombinidae west. Nat., 18:93-114. (Amphibia Salientia). Monitore Zool. Heyer, R. W. Ital., (N.S.), 10:311-314. 1973. Ecological interactions of frog larvae Lataste, F. at a seasonal tropical location in Thai- 1879. Etuda sur la discoglosse. Actes Soc. land. Jour. Herp., 7:337-361. Linn. Bordeaux., 33:275-341. 1974. Niche measurements of frog larvae Liu, C. C. ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 141

1950. Amphibians of western China. Fieldi- Noble, G. K. ana Zool. Memoirs, 2:1-400. 1927. The value of life history data in the Luther, A. study of the evolution of the Am- 1914. Uber die vom N. trigeminus versorgte phibia. Ann. New York Acad. Sci., Muskulatur der Amphibien, mit einem 30:31-128. vergleichenden Ausblick iiber den Ad- Okada, Y. ductor mandibulae der Gnathostomen, 1931. Tailless Batrachians of Japanese Em- und einem Beitrag zum Verstandnis pire. Imp Agric. Exp. Stan., pp. 1- der Organisation der Anurenlarven. 215. Acta Soc. Sci. Fennicae., 44(7):1-151. Orton, G. L.

Lynch, J. D. 1943. The tadpole of Bhinophrynus dorsalis. 1971. Evolutionary relationships, osteology, Occas. Papers Mus. Zool., Univ. Mich- and zoogeography of Leptodactyloid igan, 472:1-7. frogs. Univ. Kansas Publ. Mus. Nat. 1944. Studies on the systematic and phylo- Hist., 53:1-238. genetic significance of certain larval 1973. The transition from archaic to ad- characters in the Amphibia Salientia. vanced frogs, pp. 133-182. In: Evo- Unpublished Ph.D. thesis. Univ. lutionary Biology of the Anurans. Michigan, Ann Arbor, Michigan, 254

J. L. Vial, ed., Univ. Missouri Press, pp. Columbia, 470 pp. 1953. The systematics of vertebrate larvae. Lynn, W. G. Syst. Zool., 2:63-75. 1942. The embryology of Eleutherodactylus 1957. The bearing of larval evolution on niibicola, an anuran which has no some problems in frog classification. tadpole stage. Contributions to Em- Syst. Zool, 6:79-86. bryology, 30 (190): 29-62. Parker, H. W. 1961. Types of amphibian metamorphosis. 1931. Reports on an expedition to Brazil Amer. Zool., 1:151-161. and Paraguay in 1926-7, supported by Magnin, E. the trustees of the Percy Sladen Me- 1959. Anatomic du tetard d' Alt/tes obste- morial Fund and the executive com- tricans. Actes Soc. Linn. Bordeaux, mittee of the Carnegie Trust for Scot- 98:1-60. land—Amphibia and Reptiles. Jour. Maxson, L. R. Linn. Soc, London, Zool., 37:285- 1976. The phylogenetic status of phyllome- 289. dusine frogs (Hylidae) as evidenced 1934. A monograph of the frogs of the fam- from immunological studies of their ily Microhylidae. British Mus., Lon- serum albumins. Experientia, 32: don, 208 pp. 1149-1150. Parker, W. K. 1977. Immunological detection of conver- 1881. The structure and development of the gent evolution in the frog Anotheca skull in the Batrachia. Phil. Trans. spinosa. Syst. Zool., 26:72-76. Roy. Soc, 172:1-266. Maxson, L. R., and A. C. Wilson Pope, C. H. 1975. Albumin evolution and organisimal 1931. Notes on amphibians from Fukien, evolution in tree frogs (Hylidae). Hainan and other parts of China. Syst. Zool., 24:1-15. Bull. Amer. Mus. Nat. Hist., 61(8): 397-611. Menzies, J. I. 1967. An ecological note on the frog Pseud- Richmond, N. D. hijmenochirus merlini Chabanaud in 1947. Life history of Scaphiopus holbrookii Sierra Leone. Jour. West Afr. Sci. holbrookii (Harlan). Part I: Larval Associarion, 12:23-28. development and behavior. Ecology, Millard, N. 28:53-67. 1943. The development of the arterial sys- RuBENSTEiN, D. I., and M. A. R. Koehl tem of Xenopiis laevis, including ex- 1977. The mechanism of filter feeding: some periments on the destruction of the theoretical considerations. Amer. Nat- larval aortic arches. Trans. R. Soc. uralist, 111:981-994. S. Air., 30:217-239. Savage, R. M.

Morton, J. 1952. Ecological, physiological and ana- 1967. Guts. Studies in Biology no. 7. St. tomical observations on some species Martin's Press, New York, 59 pp. of anuran tadpoles. Proc Zool. Soc, Nelson, C. E., and H. S. Cuellar London, 122:467-514. 1968. Anatomical comparison of tadpoles of 1955. The ingestive, digestive and respira- the genera Hypovachus and Gastro- tory systems of the microhylid tad-

phryne ( Microhylidae ) . Copeia, 1968: pole, Hypopachus aguae. Copeia, 423-424. 1955:120-127. 142 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

1961. The ecology and life history of the 1975. The phylogeny of Anura larvae: a common frog. Sir Isaac Pitman & new look. Copeia, 1975:1-23. Sons, Ltd., London, 228 pp. 1977a. The free swimming Pipa larvae, with a review of pipid larvae and Savage, J. M. pipid 1968. The dendrobatid frogs of Central phylogeny (Anura: Pipidae). Jour. America. Copeia, 1968:745-776. Morph., 154:357-426. 1973. The geographic distributions of frogs: 1977b. A subordinal classification of frogs patterns and predictions, pp. 325-445. (Amphibia: Anura). Jour. Zool., 182: In: Evolutionary Biology of the Anu- 505-508. Starrett, p. rans. J. L. Vial, ed., Univ. Missouri H. Press, Columbia. 470 pp. 1960. Descriptions of tadpoles of Middle American frogs. SCHMALHAUSEN, I. I. Misc. Publ. Mus. 1968. The origin of terrestrial vertebrates Zool. Univ. Michigan, 110:1-38. (Translated from Russian). Academic 1968. The phylogenetic significance of the musculature in Press, New York, 314 pp. jaw anuran amphibians. Ph.D. dissertation, SCHULZE, F. E. Univ. Michi- gan. 1870. Die Geschmocksorgane der Frosch- 1973. Evolutionary patterns in larval mor- larven. Arch. mikr. Anat., 6:407-419. phology, pp. 251-271. In: Evolution- 1892. t)ber die inneren Kiemen der Ba- ary Biology of the Anurans. J. L. Vial, trachierlarven. II. Mittheilung. Ske- ed., Univ. Missouri Press, Columbia. let, Musculatur, Blutgefasse, Filterap- 470 pp. parat, respiratorische Anhange und Stebbins, R. C. Athmungsbewegungen erwachsener 1951. Amphibians of western North Amer- larven von Pelobates fuscus. Abhdl. ica. Univ. California Press, Los An- der Konigl. Preuss., Akad. Wiss., Ber- geles, 539 pp. lin 1892(3) :l-66. Stebbins, R. C, and J. R. Hendrickson 1889. Uber die inveren Kiemen der Ba- 1959. Field studies of amphibians in Co- trachier larven. I. Mittheilung. Uber lombia, South America. Univ. Cali- das epithel der Lippen, der Mund-, fornia, Pub. Zool., 5:497-540. Rachen, und Kiemenhohle erwach- Steinwascher, K. sener Larven von Pelobates fuscus. 1978. Interference and exploitation compe- Abhdl. der Konigl. Preuss., Akad. tition among tadpoles of Rana utric- Wiss., Berlin, 1889(3):715-768. ularia. Ecology, 59:1039-1046. Seale, D. B. Stephenson, N. G. 1973. Impact of amphibian larval popula- 1950a. On the development of the chondro- tions aquatic on an community. Un- cranium and visceral arches of Leio- Ph.D. thesis. published Washington pelma archeyi. Trans. Zool. Soc, Lon- Univ., St. Louis, Mo., 167 pp. don, 27:203-253. -^ Seale, D. B., and N. Beckvar 1950b. Observations on the development of 1980. The comparative ability of anuran the amphicoelous frogs, Leiopelma larvae (Genera: Hyla, Bufo and and Ascaphus. Jour. Linn. Soc. Zool., Rana) to ingest suspended blue- green 42:18-28. algae. Copeia (in press). 1955. On the development of the frog Leio- "^ Seale, D., and R. Wassersug pelnia hochstetteri Fitzinger. Proc. 1979. Suspension feeding dynamics of anu- Zool. Soc, London, 124:785-801. ran larvae related to their functional Sterba, G. morphology. Oecologia, 39:259-272. 1950. Uber die Morphologischen und Histo- Severtzov, a. S. genetischen Thymusprobleme bei 1969. Food seizing mechanism of Anura Xenopus laevis Daudin nebst einigen larvae. Dokl. Akad. Nauk. SSSR, 187: Bermerkungen iiber die Morphologic 211-214 (Trans.). der Kaulquappen. Abh. Sachsischen Smith, M. A. Akad. Wiss. Leipzig Math.-naturwiss. 1916. Description of five tadpoles from Klasse, 44(l):l-54. Siam. Jour. Nat. His. Soc. Siam, 2: Stuart, L. C. 37-43. 1961. Some observations on the natural his- 1926. The function of the "funnel" mouth tory of tadpoles of Rhinophrynus dor- of the tadpoles of Megalophrys, with salis Dumeril and Bibron. Herpeto- a note on M. aceras Boulenger. Proc. logica, 17:73-79. Zool. Soc., London, 96:983-988. Ueck, M. SOKOL, O. M. 1967. Der Manicotto glandulare ("Driisen- 1962. The tadpole of Hymenochirus boett- magen") der Anurenlarve in Bau, geri. Copeia, 1962:272-284. Funktion und Beziehung zur Gesam- ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 143

tranges des Darmes. Eine mikroskop- Wilder, I., L. WmppLE and E. R. Dunn isch-anatomische, histochemische und 1920. The correlation of lunglessness in sal- elektronenoptische Studie an der om- amanders with a mountain brook hab- nivoren und mikrophagen Larve von itat. Copeia, 1920:63-68. Xenopus laevis und der camivoren Wright, A. H. und makrophagen Larve von Hymen- 1932. Life-histories of the frogs of Okefi- ochirus boettgeri (Anura, Pipidae). nokee swamp, Georgia. Macmillian Zeit. wiss. Zool., 176:173-270. Co., New York, 497 pp.

Van Eeden, J. A. 1951. The development of the chondro- Appendix: Glossary of Terms cranium of Ascaphus truei Stejneger Most terms used in this monograph with special reference to the relations are explained briefly here; fuller descrip- of the palatoquadrate to the neuro- cranium. Acta Zool., 32:41-176. tions and definitions are provided for the

Villa, J. majority of terms in Wassersug (1976a). 1971. Anfibios de Nicaragua. Instituto Geo- Morphological variation for internal oral grafico Nacional and Banco Central features listed here is reviewed under de Nicaragua, Managua, 217 pp. "Functional Considerations" in the Dis- Wake, D. B. 1966. Comparative osteology and evolution cussion section of this paper. of the lungless salamanders, family Advanced tadpoles Orton's Type 4 Plethedontidae. Mem. S. Cal. Acad. — Sci. 4:1-111. larvae.

Wassersug, R. J. Anterior filter valve—see ventral 1972. The mechanism of ultraplanktonic en- velum. trapment in anuran larvae. Jour. Anterior narial papillae papillae Morph., 137:279-288. — arising from the anteromedial corner of 1973. Aspects of social behavior in anuran the internal naries and projecting pos- larvae, pp. 272-297. In: J. L. Vial, ed. Evolutionary Biology of the Anu- teroventrally over the narial passage. rans. Univ. Missouri Press, Columbia. Arboreal tadpoles—any larvae that 470 pp. live in small pools of water which form 1975. The adaptive significance of the tad- in leaves of vegetation pole stage with comments on the above ground. maintenance of complex life cycles in Atrial chamber—the chamber sur- anurans. Amer. Zool., 15:405-417. rounding the gill filaments between the 1976a. Oral morphology of anuran larvae: gill slits and the spiracle. terminology and general description. Beaks—the keratinized structures Occ. Papers Mus. Nat. Hist. Univ. Kansas, 48:1-23. sheathing the supralabial and infralabial 1976b. Internal oral features in Hyla regilla cartilage in most tadpoles, except Orton (Anura: Hylidae) larvae: an onto- Type 1 and 2. genetic study. Occ. Papers Mus. Nat. BFA—see buccal floor arena. Hist. Univ. Kansas, 49:1-24. BRA—see buccal roof arena. Wassersug, R. J., and K. Hoff Branchial food traps regions of se- 1979. A comparative study of the buccal — pumping mechanism of tadpoles. Sub- cretory mucosa covering the roof and mitted to Biol. Jour. Linn. Soc, 12: the anterior wall of the filter cavities in 225-259. most tadpoles. The traps usually cover

Wassersug, R. J., and K. Rosenberg the whole ventral surface of the ventral 1979. Surface anatomy of branchial food velum.

traps of tadpoles : a comparative Buccal cavity the internal study. Jour. Morph., 159:393-426. — portion of the mouth above the ceratohyal and Wassersug, R. J., and E. Seibert 1975. Behavioral responses of amphibian the hypobranchial plate, anterior to the larvae to variation in dissolved oxy- dorsal and ventral vela. 1975:86-103. gen. Copeia, Buccal pockets—deep depressions in Weisz, p. B. the buccal floor between the posterior 1945. The development and morphology of margin of the ceratohyal and the anterior the larva of the South African clawed margin of first toad, Xenopus laevis. Jour. Morph., the ceratobranchial { = 77:163-217. first gill cleft). .

144 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Buccal slits—perforations of the buc- Esophageal funnel—the region where cal pocket (first gill cleft) which con- the pharynx narrows into the esophagus. nect the buccal cavity to the atrial cham- Filter canals—partially or fully cov- ber. ered passages between neighboring filter Buccal floor arena (BFA) —a large, folds on the filter plates. circumscribed area in the center of the Filter chambers—sections of the buccal floor. branchial baskets bounded laterally and

Buccal floor arena papillae ( BFA pa- medially by the filter plates, superiorly pillae) —rows of papillae that define the by the ventral velum, and ventrally by BFA. the gill slits. There are three filter cavi- Buccal roof arena (BRA) —defined ties on each side. area on the buccal roof directly above Filter crevices—small passageways the buccal floor arena. between two neighboring side folds on Buccal roof arena papillae (BRA a single filter row. papillae) —papillae that circumscribe Filter folds—narrow rows of gill fil- and thus define the buccal roof arena. ters that run from dorsal to ventral down cb.—see ceratobranchials. the filter plates. Ceratobranchials (cb. ) —the cartila- Filter niches — open, multi-sided ginous, skeletal elements of the branchial spaces between secondary and tertiary baskets; the gill bars. filter folds on filter canals. Ceratohyal—the major cartilaginous Filter plates — vertically oriented skeletal elements of the buccal floor in plates of connective tissue that arise tadpoles. from the ceratobranchials, which sup- Choanae—see internal naries. port the gill filter folds. Ciliary groove—a horizontal groove Filter rows—see filter folds. that runs in the posterior and lateral Filter ruffles—see filter folds. margin of the pharynx from the anterior, Funnel-mouth tadpoles—any larva lateral corner of the ventral velum to the with an exceptionally large expanded esophagus. It is covered with cilia that oral disc that is directed anterior or transport mucus and food particles to anterodorsally. The oral disc in these the esophagus. fornis is usually free of denticles. Collecting organs—see crescentic or- Gill filters—ruffled, epithelial organs gans. associated with the posterior surfaces of Crescentic organs—small, isolated cb. 1, the anterior surfaces of cb. 4, and branchial food traps of crescentic shape both the anterior and posterior surfaces that lie at the anterior limit of the filter of cb. 2 and 3. cavities in microhylid and rhinophrynid Glandular zone—a transverse band larvae. of secretory membrane that covers the Denticle formulae—numerical expres- posterior portion of the buccal roof to sion of the number of rows of denticles the dorsal velum. above and below the oral orifice (e.g., Glottis—longitudinal slit-like open- two rows above, three rows below ^ a ing to the bronchi that lies on the mid- 2/3 denticle formula). line between the anterior portions of the Denticles—keratinized structures ar- 4th ceratobranchials. ranged in transverse rows that surround Hypobranchial plate—the cartilagi- the beaks of most tadpoles. nous skeletal element between the cera- Dorsal velum—a transverse flap tobranchials and the ceratohyal. It sup- across the posterior part of the mouth ports the posterior portion of the buccal that separates the roof of the buccal floor. cavity from the roof of the pharynx; the Infralabial papillae—the most ante- dorsal continuation of the ventral velum rior projections in the buccal cavity,

= posterior filter valve ) which lie over the infralabial cartilage ( . .

ORAL FEATURES OF LARVAE FROM EIGHT ANURAN FAMILIES 145 and its articulation with Meckel's carti- spiracle (Ascaphidae and Discoglossi- lage. dae). Internal naries—slit-like openings of Orton Type 4 Larvae—tadpoles hav- the anterior buccal roof. ing keratinized mouth parts and a single, Laryngeal disc—the circular, tra- sinistral spiracle (all families except cheal outline surrounding the glottis. those listed under Orton Types 1-3). Lateral ridge papillae—subsidiary Pharyngeal by-pass—see buccal slits. projections that lie lateral to the median Pharyngeal cavity—the region of the ridge on the buccal roof. oral cavity that lies between the dorsal Lateral roof papillae—any small pro- and ventral vela anteriorly and the jections that lie in the midportion of the esophagus posteriorly. It is bounded buccal roof lateral to the BRA papillae. ventrally by the pharyngeal gill slits. Lingual papillae — premetamorphic Pond larvae, typical—tadpoles such projections that occur on the tongue an- as Hyla regilla and Acris crepitans which lage. have a 2/3 denticle formula, live in small Main filter fold—the large, central or medium-size ponds, and feed on sus- ruflfle of each filter row. pended particles in the water column Median notch—a notch in the mid- and graze on the substrate. dle of the ventral velum. Posterior filter valve—see dorsal vel- Median ridge—a transversely orient- um. ed ridge or epithelial flap that lies in Postnarial arena—the region of the the midline of the buccal roof, approxi- buccal roof between the nares anteriorly mately halfway between the upper beak and the transverse median ridge poste- and the dorsal velum. riorly. Narial valve extensive, free flaps of — Postnarial papillae papillae between the posterior walls of the internal naries. — the internal naries and the median ridge. Narial valve projection—single, tall These are usually in distinct, obliquely projections of the narial valve. oriented rows from anteromedial to pos- Opercular chamber—see atrial cham- terolateral behind the narial valve. ber. Postnarial ridges—epithelial folds in Operculum—flap of skin arising from the postnarial arena. the hyoidean arch which covers the gill Prenarial arena the region of the filaments. — buccal roof between the supralabial car- Oral cavity—the region of the ali- tilages anteriorly and the internal naries mentary and respiratory system between posteriorly. the oral orifice anteriorly, the gill slits Prenarial papillae see anterior na- ventrally, and the esophagus posteriorly. — rial papillae. Oral disc—an expanded flap of skin Prepocket surrounding the oral orifice. Denticle papillae—papillae of the rows occur on the oral disc in most buccal floor that lie over the body of Orton Type 3 and 4 larvae. the ceratohyal anterior to the buccal Oral orifice—the entrance into the pocket. mouth or oral cavity. Pressure cushions—loose folds of epi- Orton Type 1 Larvae—tadpoles that thelium descending from the roof of the have paired spiracles, and lack kerati- pharynx posterior to the dorsal velum. nized mouth parts (Pipidae and Rhi- There are usually two pressure cushions

nophrynidae ) on each side of the pharynx. Orton Type 2 Larvae—tadpoles lack- Secretory pits—clusters of secretory ing keratinized mouth parts and having cells that open in distinct pits along the

a single, medial spiracle ( Microhylidae ) posterior margin of the ventral velum Orton Type 3 Larvae—tadpoles with and the glandular zone of the buccal keratinized mouth parts and a medial roof. 146 MISCELLANEOUS PUBLICATION MUSEUM OF NATURAL HISTORY

Secretory ridges — mucus-secreting Spiracle—the opening in the opercu- ridges that cover the branchial food trap lum where water is expelled from the surfaces on the ventral side of the ven- atrial chamber. tral velum in most tadpoles ( see Wasser- Suctorial tadpoles—larvae with an sug and Rosenberg, 1979). enlarged, oral disc used to adhere to Secretory zone—the exposed regions substrate often in lotic environments. of mucus cell apices in the bottom of Tongue anlage — the embryonic secretory pits and at the top of secretory tongue pad that develops in the an- ridges. terior portion of the buccal floor. Side folds—secondary and tertiary Ventral velum—a distinctive, mova- branching patterns of the gill filters of ble (but nonmuscular) flap arising from each filter row. the floor of the buccal cavity; it is at- Spicules—cartilaginous supports for tached anteriorly to the branchial bas- the free, posterior surface of the ventral kets and to the superior margins of the velum. filter plates (= anterior filter valve).

ERNST MAYR LIBRARY

3 2044 110 326 212

Date Due

pjt^rm ICCJL^ CIS O^ RECENT MISCELLANEOUS PUBLICATIONS UNIVERSITY OF KANSAS MUSEUM OF NATURAL HISTORY'

52. Reproductive cycles in lizards and snakes. By Henry S. Fitch. Pp. 1-247, 16 figures in text. June 19, 1970. Paper bound, $5.00.

53. Evolutionary relationships, osteology, and zoogeography of leptodactyloid frogs. By John D. Lynch. Pp. 1-238, 131 figures in text. June 30, 1971. Paper bound, $7.00.

54. The dentition of glossophagine bats: development, morphological characteristics, variation, pathology, and evolution. By Carleton J. Phillips. Pp. 1-138, 49 figures in text. September 24, 1971. Paper bound, $5.00.

55. Middle American lizards of the genus Ameiva (Teiidae) with emphasis on geographic variation. By Arthur C. Echternacht. Pp. 1-86, 28 figures in text. De- cember 14, 1971. Paper bound, $3.00.

56. Systematics of the chiropteran family Mormoopidae. By James Dale Smith. Pp. 1-132, 40 figures in text. March 10, 1972. Paper bound, $5.00.

57. A systematic review of the Teiid lizards, genus Bachia, with remarks on Heter- odactylus and Anotosaura. By James R. Dixon. Pp. 1-47, 15 figures in text. February 2, 1973. Paper bound, $1.50.

58. Systematics of three species of woodrats ( genus Neot07na ) in central North Amer- ica. By Elmer C. Birney. Pp. 1-173, 44 figures in text. April 13, 1973. Paper bound, $7.50.

59. Systematics and evolution of the Andean lizard genus Pholidobolus (Sauria: Teiidae). By Richard R. Montanucci. Pp. 1-52, 8 figures in text. May 14, 1973. Paper bound, $1.75.

60. Mammals of the Black Hills of South Dakota and Wyoming. By Ronald W. Turner. Pp. 1-178, 14 figures in text. April 3, 1974. Paper bound, $7.50.

61. Reproductive strategies in a tropical anuran community. By Martha L. Crump. Pp. 1-68, 13 figures in text. November 15, 1974. Paper bound, $4.50.

62. A demographic study of the ringneck snake (Diadophis punctatus) in Kansas. By Henry S. Fitch. Pp. 1-53, 19 figures in text. April 3, 1975. Paper bound, $3.00.

63. Morphology of the bony stapes (columella) in the Passeriformes and related groups: evolutionary implications. By Alan Feduccia. Pp. 1-34, 16 plates, 7 figures in text. May 30, 1975. Paper bound, $3.00.

64. The phylogency and biogeography of fossil and Recent gars (Actinopterygii:

Lepisosteidae) . By E. O. Wiley, Pp. 1-112, 72 figures in text. November 12, 1976. Paper bound, $2.75.

65. The biology of an equatorial herpetofauna in Amazonian Ecuador. By William E. Duellman. Pp. 1-352, 198 figures in text. August 30, 1978. Paper bound, $15.00.

66. Leptodactylid Frogs of the genus Eleutherodactylus from the Andes of southern Ecuador. By John D. Lynch. Pp. 1-62, 23 figures in text. February 28, 1979. Paper bound, $2.75.

* Postage and handling 5% of total order or a minimum of $0.50. Publications of this and other series are available from the Publications Secretary. '<* ai«ilME"v^M