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The ontogeny of the filter apparatus of anuran larvae (Amphibia, Anura)

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Summary

The pharynx ofBufo calamita, Rana temporaria andBombina variegata larvae (larval Types IV and III) changes considerably during the latter part of embryonic development. The entodermal regions between the visceral pockets flatten inward to form the anlagen of the filter plates. The ectoderm thrusts forward from the area of the persistent epidermal gills overlying the anlagen of the filter plates. The esophagus pushes dorsolaterally into the pharynx to give rise to the ciliary cushions. Comparison with the development ofXenopus laevis (larval Type I) reveals shared characters: (1) the filter plates are overlapped by the sensory layer of the epiderm and (2) the ciliary grooves are, like the ciliary cushions of larval Types III and IV, anteriorly directed dorsolateral extensions of the esophagus. In all the species studied an ectodermal-esophageal filter apparatus develops. The evolutionary origin of this filter apparatus is discussed. The epidermalization of gills is suggested as a common character with the sister group of Dipnoi, and is therefore a plesiomorphic character in all amphibians. The tendency of filter plate epidermalization is considered to be the end of a process which is also indicated in the epidermalization of the first visceral pouch in lung fish. The ciliary groove is unique in anuran larvae within the Lissamphibia, and is therefore seen as an autapomorphic character within amphibians. On the basis of the different structure of the ciliary cushion inX. laevis and in the other species of this study, two alternative levels of evolutionary ciliary groove origin are discussed. Derivation from the esophagus took place: (1) in a common anuran larval ancestor, or (2) at two independent levels; the first in the Pipidae (-Rhinophrynidae) ancestor and the second in the ancestor of all the other anuran families. Several larval characters and cladistic aspects make the first alternative more probable than the second. Larval Type II anatomy and Larval Type II truncation from the Larval Type IV of Ranoidea do not contradict these considerations. There is disproportionately early commencement of ingestion activity inR. temporaria (G Stage 23),B. calamita (G Stage 23), andB. bufo (G Stage 24) compared toXenopus. Feeding in the former three species precedes the differentiation of the filter plates, their mucus production, and the exhaustion of the yolk supply in the gut tissue. By contrast, the goblet cells and the ciliary cells of the ciliary cushions are already differentiated when feeding starts. This suggests that ingestion in these early stages requires mucus production by the ciliary cushions and transport by their ciliary cells. Presumably in fully formed larvae, the ciliary cushions are the mucus donors, whereas the filter plates are the mucus depositors. By contrast,X. laevis does not begin active food intake by suspension feeding until after the yolk supply has been used up from the entoderm of the buccal cavity to deep in the esophagus.

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Abbreviations

AAC :

anlage of apical cell

AC :

apical cell

ACE :

anlage of cerebrum

ACG :

anlage of ciliary groove

AD :

aorta dorsalis

ADV :

anlage of dorsal velum

AG :

anlage of glottis

AFP :

anlage of filter plates

AFR :

anlage of filter rows

AFPC :

anlage of epidermal fold of peribranchial chamber (anlage of ‘operculum’)

ant. :

anterior

AMF :

anlage of middle fold

AO :

adhesive organ

APEG :

anlage of persistent epidermal gills

APOP :

anlage of postnarial papilla

APSF :

anlage of primary side fold

ASC1 :

anlage of Type 1 secretory cell

ATE :

anlage of tuba Eustachii

ATEG :

anlage of transient epidermal gills

AVV :

anlage of ventral velum

B :

branchial arch

BI-IV :

branchial arches I–IV

BFA :

buccal floor arena

BFT :

branchial food trap

BL :

basal lamina

BRA :

buccal roof arena

C :

cilium, cilia

CA :

cartilage of visceral arch

CC :

ciliary cushion

CE :

cerebrum, brain

CG :

ciliary groove

CH :

choana

CHY :

ceratohyale

CIC :

ciliary cell

CL :

capillary vessel

CN :

centriole, basal body

COC :

cuboidal cells

CT :

connective tissue

CTC :

connective tissue cell

d :

dorsal

DV :

dorsal velum

DVI–III :

dorsal vela I–III

E :

esophagus

e :

early

ED :

edge of filter plate

EN :

endothelium

ENC :

entodermal cell

EP :

epiderm

EPC :

epidermal cell

ER :

endoplasmatic reticulum

ET :

erythrocyte

ETZ :

ectodermal-entodermal transition zone

EV :

ear vesicle

EX :

merocrine extrusion

EY :

eye

EZ :

zone of extrusion

FP :

filter plate

FPII :

filter plate of the 2nd branchial arch

FPIV :

filter plate of the 4th branchial arch

FPC :

epidermal fold of peribranchial chamber (operculum)

FC :

filter cavity

FN :

filter niche

FR :

filter row

GL :

glottis

GS :

gill slit

1. GS :

first gill slit

GZ :

glandular zone

H :

heart

HP :

hypobranchial plate

HY :

hyoid arch

IC :

intercellular space, enlarged by fixation and dehydration

L :

late

LJ :

lower jaw

LT :

larval type

LV :

lipid vacuole

M :

mitochondrion

MA :

mandibular arch

MF :

middle fold

med. :

median

MS :

microvillous stubs

MZ :

zone of microtubes

NAC :

nucleus of apical cell

NCIC :

nucleus of ciliary cell

NCL :

nucleus of capillary vessel

NCOC :

nucleus of cuboidal cells

NCT :

nucleus of connective tissue

NENC :

nucleus of entodermal cell

NEPC :

nucleus of epidermal cell

NO :

external nares

NPEC :

nucleus of periderm cell

NRC :

nucleus of random cell

NSC1 :

nucleus of Type 1 secretory cell

NSC3 :

nucleus of Type 3 secretory cell

NSLC :

nucleus of sensory layer cell

NSPC :

nucleus of supporting cell

NSQC :

nucleus of squamous epithelial cell

OC :

oral cavity

OS :

mouth

P :

papilla

PC :

peribranchial chamber

PCW :

peribranchial chamber wall

PE :

periderm

PEC :

periderm cell

PEG :

persistent epidermal gill

PG :

pigment granule

post. :

posterior

PS :

primary side fold

PH :

pharynx

RC :

random cell

RO :

rootlet

SC1 :

Type 1 secretory cell

SC2 :

Type 2 secretory cell, goblet cell

SC3 :

Type 3 secretory cell

SC4 :

Type 4 secretory cell

SG :

secretory groove

SL :

sensory layer

SLC :

sensory layer cell

SP :

secretory pit

SPC :

supporting cell

SQC :

squamous epithelial cell

SR :

secretory ridge

SRC :

secretory ridge cell

SS :

secondary side fold

ST. :

stage

STD :

stomodeum

SU :

spiculum of hypobranchial plate

T :

tentacle

TA :

anlage of tongue

TEG :

transient epidermal gill

TZ :

transitional zone of branchial food trap and ventral velum

UJ :

upper jaw

v :

ventral

VA :

visceral arch

VC :

vacuole

VPI–IV :

visceral pockets I–IV

VP :

visceral pocket

VV :

ventral velum

YV :

yolk vacuoles

References

  • Adolph EF (1929) The quantitative effect of crowding on the rate of growth of tadpoles. Anat Rec 44:227

    Google Scholar 

  • Adolph EF (1931) The size of the body and the size of the environment in the growth of tadpoles. Biol Bull Mar Biol Lab Woods Hole 61:350–375

    Google Scholar 

  • Alvarado RH, Moody A (1970) Sodium chloride transport in tadpoles of the bullfrogRana catesbeiana. Am J Physiol 218:R1510–1516

    Google Scholar 

  • Ashworth R de, Crozier B (1972) Standard waters: recommendations for the preparation of standard waters used for testing pesticidal and other formulations, and an FAO survey of naturally occuring waters. In: Raw GR (ed) CIPAG Monograph I, Collaborative Pesticides Analytical Council, pp 1–64

  • Ax P (1984) Das phylogenetische System. Gustav Fischer, Stuttgart New York, 349 pp

    Google Scholar 

  • Balinsky BI (1970) An introduction to embryology. WB Saunder, Philadelphia, London Toronto, p 725

    Google Scholar 

  • Beaumont MA (1970) Apparition des cellules insulaires A dans pancreas larvaire d'un amphibien anoure:Discoglossus pictus Otth. C R Seances Acad Sci Paris 271:1104–1106

    Google Scholar 

  • Bendix S, Allen MB (1962) Ultra-violet induced mutants ofChlorella pyrenoidosa. Arch Mikrobiol 41:115–141

    Google Scholar 

  • Bentley PJ, Baldwin GP (1980) Comparison of transcutaneous permeability in skins of larval and adult salamanders (Ambystoma tigrinum). Am J Physiol 239:R505–508

    Google Scholar 

  • Berthold G (1980) Microtubes in the epidermal cells ofCarausius morosus (Br.). Their pattern and relation to pigment migration. J Insect Physiol 26:421–425

    Google Scholar 

  • Burggren WW, Feder ME, Pinder AW (1983) Temperature and the balance between aerial and aquatic respiration in larvae ofRana berlandieri andRana catesbeiana. Physiol Zool 56:263–273

    Google Scholar 

  • Conte FP (1969) Salt secretion. In: Hoar WS, Randall DJ (eds) Fish physiology. Excretion, ionic regulation, and metabolism, vol I. Academic Press, New York, London, pp 241–292

    Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New York St Louis San Francisco, 670 pp

    Google Scholar 

  • Epperlein H-H, Halfter W, Tucker RP (1988) The distribution of fibronectin and tenascin along the migratory pathways of the neural crest. Dev 103:743–756

    Google Scholar 

  • Erickson CA (1985) Morphogenesis of the neural crest. In: Browder LM (ed) Developmental Biology, vol 2. The cellular basis of metamorphosis. Plenum Press, New York London, pp 481–543

    Google Scholar 

  • Evans DH (1982) Salt and water exchange across vertebrate gills. In: Houlihan DF, Rankin JC, Shuttleworth TJ (eds) Gills. Cambridge University Press, New York, pp 148–171

    Google Scholar 

  • Fawcett DW (1973) Atlas zur Elektronenmikroskopie der Zelle. Urban und Schwarzenberg, München Berlin Wien, 458 pp

    Google Scholar 

  • Feder ME, Wassersug RJ (1984) Aerial versus aquatic oxygen consumption in larvae of the clawed frog,Xenopus laevis. J Exp Biol 108:231–245

    Google Scholar 

  • Fiala-Medioni A (1978) A scanning electron microscope study of the branchial sac of benthic filter-feeding invertebrates (ascidians). Acta Zool 59:1–9

    Google Scholar 

  • Fox H (1965) Early development of the head and pharynx ofNeoceratodus with a consideration of its phylogeny. J Zool London 146:470–554

    Google Scholar 

  • Fox H (1981) Cytological and morphological changes during amphibian metamorphosis. In: Gilbert LI, Frieden E (eds) Metamorphosis. A problem in developmental biology. Plenum Press, New York, pp 327–362

    Google Scholar 

  • Fox H (1986) Early development of caecilian skin with special reference to the epidermis. J Herpetol 20:154–167

    Google Scholar 

  • Fox H, Mahoney R, Bailey E (1970) Aspects of the ultrastructure of the alimentary canal and associated glands of theXenopus laevis larva. Arch Biol 81:21–50

    Google Scholar 

  • Fox H, Bailey E, Mahoney R (1972) Aspects of the ultrastructure of the alimentary canal and respiratory ducts inXenopus laevis larvae. J Morphol 138:387–406

    Google Scholar 

  • Gerhardt E (1932) Die Kiemenentwicklung bei Anuren (Pelobates fuscus, Hyla arborea) and Urodelen (Triton vulgaris). Zool Jahrb Anat 55:173–220

    Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:160–183

    Google Scholar 

  • Gosner KL, Black IH (1957) The effect of acidity on the development and hatching of New Jersey frogs. Ecology 38:256–262

    Google Scholar 

  • Gradwell N (1971)Xenopus tadpole: on the water pumping mechanism. Herpetologica 27:107–123

    Google Scholar 

  • Gradwell N (1975) The bearing of filter feeding on the water pumping mechanism ofXenopus tadpoles (Anura: Pipidae) Acta Zool 56:119–128

    Google Scholar 

  • Greven H (1980) Ultrastructural investigations of the epidermis and the gill epithelium in the intrauterine larvae ofSalamandra salamandra (L) (Amphibia, Urodela). Z Mikrosk Anat Forsch 94:196–208

    Google Scholar 

  • Hall BK (1987) Tissue interactions in the development and evolution of the vertebrate head. In: Maderson PFA (ed) Developmental and evolutionary aspects of the neural crest. John Wiley and Sons, New York, Chichester, pp 215–259

    Google Scholar 

  • Hall BK (1988) Patterning of connective tissue in the head: discussion report. Dev (Suppl) 103:171–174

    Google Scholar 

  • Hammersen F (1985) Histologie — Farbatlas der mikroskopischen Anatomie. Urban und Schwarzenberg, München Wien Baltimore, pp 259

    Google Scholar 

  • Heusser H (1972) Intra- und interspezifische Crowding-Effekte bei Kaulquappen einheimischer Anuren Arten. Vierteljahresschr Naturforsch Ges Zürich 117:121–128

    Google Scholar 

  • Hibiya T (1982) An atlas of fish histology. Normal and pathological features. Gustav Fischer Verlag, Stuttgart New York, 147 pp

    Google Scholar 

  • Holtfreter J (1939) Gewebeaffinität, ein Mittel der embryonalen Formbildung. Arch Exp Zellforsch 23:169–209

    Google Scholar 

  • Hourdry J (1974) Etude des branchies ‘internes’ puis de leur regression au moment de la metamorphose, chez la larve deDiscoglossus pictus (Otth), amphibien anoure. J Microsc 20:165–182

    Google Scholar 

  • Inger RF (1967) The development of a phylogeny of frogs. Evolution 21:369–384

    Google Scholar 

  • Kenny JS (1969) Feeding mechanisms in anuran larvae. J Zool Lond 157:225–246

    Google Scholar 

  • Kindred JE (1927) Cell division and ciliogenesis in the ciliated epithelium of the pharynx and esophagus of the tadpoles of the green frog,Rana calamitans. J Morphol 43:267–297

    Google Scholar 

  • Kothari S (1983) Histochemical studies in the buccopharynx and esophagus in different stages ofHeteropneustes fossilis (Bloch). Ind J Zool 11:37–45

    Google Scholar 

  • Kratochwill K (1933) Zur Morphologie und Physiologie der Nahrungsaufnahme der Froschlarven. Z Wiss Zool 144:421–468

    Google Scholar 

  • Kumari JS, Rao KH, Rao KS, Shyamasundari K (1983) Observation on the histology of the pharynx in the teleostMegalops cyprinoides. Ind J Zool 24:51–56

    Google Scholar 

  • Langille RM, Hall BK (1988) Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lampreyPetromyzon marinus L. Development 102:301–310

    Google Scholar 

  • Lannoo MJ, Townsend DS, Wassersug RJ (1987) Larval life in the leaves: arboreal tadpole types, with special attention to the morphology, ecology, and behavior of the oophagousOsteopilus brunneus (Hylidae) larva. Fieldiana Zool New Ser 38:1–31

    Google Scholar 

  • Lewinson D, Rosenberg M, Warburg MR (1987) Ultrastructural and ultracytochemical studies of the gill epithelium in the larvae ofSalamandra salamandra (Amphibia, Urodela) Zoomorphology 107:17–25

    Google Scholar 

  • Lucas EA, Reynolds WA (1967) Temperature selection by amphibian larvae. Phys Zool 40:159–171

    Google Scholar 

  • Maderson PFA (1975) Embryonic tissue interactions as the basis for morphological change in evolution. Am Zool 15:315–327

    Google Scholar 

  • Mallatt J (1979) Surface morphology and functions of pharyngeal structures in the larval lampreyPetromyzon marinus. J Morphol 162:249–274

    Google Scholar 

  • Mallatt J, Ridgway (1984) Ultrastructure of a complex epithelial system: The pharyngeal lining of the larval lampreyPetromyzon marinus. J Morphol 180:271–296

    Google Scholar 

  • Mallatt J, Ridgway RL, Paulsen C (1985) Ultrastructural effects of 3-trifluormethyl-3-nitrophenol on gills of the larval lampreyPetromyzon marinus. Can J Zool 63:155–164

    Google Scholar 

  • Mangold O (1929) Das Determinationsproblem. II. Die paarigen Extremitäten der Wirbeltiere in der Entwicklung. Ergebn Biol 5:290–404

    Google Scholar 

  • Marcus E (1930) Zur Entwicklungsgeschichte des Vorderdarmes der Amphibien. Zool Jahrb Anat 52:405–486

    Google Scholar 

  • McDonald DG, Ozog JL, Simons BP (1984) The influence of low pH environments on ion regulation in the larval stages of the anuran amphibian,Rana calamitans. Can J Zool 62:2171–2177

    Google Scholar 

  • McIndoe R, Smith DG (1984) Functional anatomy of the internal gills of the tadpole ofLitoria ewingii (Anura, Hylidae). Zoomorphology 104:280–291

    Google Scholar 

  • Meister MF, Humbert W, Kirsch R, Vivien-Roels B (1983) Structure and ultrastructure of the esophagus in sea-water and fresh-water. Teleosts (Pisces). Zoomorphology 102:33–51

    Google Scholar 

  • Morris R, Pickering AD (1975) Ultrastructure of presumed ion-transporting cells in the gills of ammocoete lampreys,Lampetra fluviatilis (L.) andLampetra planeri (Bloch). Cell Tissue Res 163:327–341

    Google Scholar 

  • Morris R, Pickering AD (1976) Changes in ultrastructure of the gills of the river lamprey,Lampetra fluviatilis (L.) during the anadromous spawning migration. Cell Tissue Res 173:271–277

    Google Scholar 

  • Nieuwkoop PD, Faber J (1956) Normal table ofXenopus laevis (Daudin)-A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. North-Holland, Amsterdam, p 243

    Google Scholar 

  • Northcutt RG (1986) Lungfish neural characters and their bearing on sarcopterygian phylogeny. J Morphol Suppl 1:277–297

    Google Scholar 

  • Orton GL (1953) The systematics of vertebrate larvae. Syst Zool 2:63–75

    Google Scholar 

  • Polak Hlohowskyj CP, Coburn MM, Cavender TM (1989) Comparison of a pharyngeal filtering apparatus in seven species of the herbivorous cyprinid genus,Hybognathus (Pisces, Cyprinidae). Copeia 1989:172–183

    Google Scholar 

  • Portmann A (1952) Die allgemeine biologische Bedeutung der Cerebralisations-Studien. Bull Schweiz Akad Med Wiss 8:253–262

    Google Scholar 

  • Portmann A (1983) Einführung in die vergleichende Morphologie der Wirbeltiere. Schwabe, Basel Stuttgart, 344 pp

    Google Scholar 

  • Rauthner M (1967) Pharynx and epitheliale Organe der Pharynxwand. 1. Kiemen der Anamnier-Kiemendarmderivate der Cyclostomen und Fische. In: Bolk L, Göppert E, Kallius E, Lubosch W (eds) Handbuch der vergleichenden Anatomie der Wirbeltiere, vol 3. Asher, Amsterdam, pp 211–278

    Google Scholar 

  • Romeis B (1968) Mikroskopische Technik. Oldenburg, München Wien, 757 pp

    Google Scholar 

  • Rose SM (1960) A feedback mechanism of growth control in tadpoles. Ecology 41:188–198

    Google Scholar 

  • Rosen DE, Forey PL, Gardiner BG, Patterson C (1981) Lungfishes, tetrapods, paleontology, and plesiomorphology. Bull Am Mus Nat Hist 167:162–275

    Google Scholar 

  • Rosenbauer KA, Kegel BH (1978) Rasterelektronenmikroskopische Technik. Präparationsverfahren in Medizin und Biologie. Thieme, Stuttgart, 241 pp

    Google Scholar 

  • Savage RM (1952) Ecological, physiological and anatomical observations on some species of anuran tadpoles. Proc Zool Soc London 122:467–514

    Google Scholar 

  • Seale DB, Beckvar N (1980) The comparative ability of anuran Larvae (genera:Hyla, Bufo, andRana) to ingest suspended blue-green algae. Copeia 1980:495–503

    Google Scholar 

  • Seale DB, Wassersug RJ (1979) Suspension feeding dynamics of anuran larvae related to their functional morphology. Oecologia 39:259–272

    Google Scholar 

  • Seale DB, Hoff K, Wassersug RJ (1982)Xenopus laevis larvae (Amphibia, Anura) as model suspension feeders. Hydrobiologia 87:161–169

    Google Scholar 

  • Sinha GM (1975) A histochemical study of the mucus cells in the bucco-pharyngeal region of four Indian freshwater fishes in relation to their origin, development, occurence and probable functions. Acta Histochem 53:217–223

    Google Scholar 

  • Slade NA, Wassersug RJ (1975) On the evolution of complex life cycles. Evolution 29:568–571

    Google Scholar 

  • Sokol OM (1975) The phylogeny of anuran larvae: a new look. Copeia 1975:1–23

    Google Scholar 

  • Sokol OM (1981) The filter apparatus of larvalPelodytes punctatus (Amphibia: Anura). Amphibia-Reptilia 2:195–208

    Google Scholar 

  • Steer MW (1981) Understanding cell structure. Cambridge University Press, Cambridge London New York New Rochelle Melbourne Sidney, 126 pp

    Google Scholar 

  • Thorogood P (1988) The development specification of the vertebrate skull. Dev (Suppl) 103:141–153

    Google Scholar 

  • Tihen JA (1965) Evolutionary trends in frogs. Am Zool 5:309–318

    Google Scholar 

  • Trueb L (1973) “Bones, frogs, and evolution”. In: Vial JL (ed) Evolutionary biology of the anurans: contemporary research on major problems. University of Missouri Press, Columbia, pp 65–132

    Google Scholar 

  • Ueck M (1967) Der Manicotto glandulare (‘Drüsenmagen’) der Anurenlarve in Bau, Funktion und Beziehung zur Gesamtlänge des Darmes. Z Wiss Zool 176:173–270

    Google Scholar 

  • Viertel B (1984) Habit, malanin pigmentation, oral disc, oral cavity and filter apparatus of the larvae ofBaleaphryne muletensis. In: Hemmer H, Alcover JA (eds) Historia biologica del ferreret. Editorial Moll, Ciutat de Mallorca, pp 21–43

    Google Scholar 

  • Viertel B (1985) The filter apparatus ofRana temporaria andBufo bufo larvae (Amphibia, Anura). Zoomorphology 105:345–355

    Google Scholar 

  • Viertel B (1987) The filter apparatus ofXenopus laevis, Bombina variegata, andBufo calamita (Amphibia, Anura): a comparison of different larval types. Zool Jb Anat 115:425–452

    Google Scholar 

  • Viertel B (1989) The filter apparatus of anuran larvae — aspects of the filtering mechanism. In: Splechtna H, Hilgers H (eds) Trends in vertebrate morphology, vol 35. Fischer, Suttgart New York, pp 526–533

    Google Scholar 

  • Viertel B (1990) Suspension feeding of anuran larvae at low concentrations ofChlorella algae (Amphibia, Anura). Oecologia 85:167–177

    Google Scholar 

  • Wassersug RJ (1972) The mechanism of ultraplanktonic entrapment in anuran larvae. J Morphol 137:279–288

    Google Scholar 

  • Wassersug RJ (1980) Internal oral features of larvae from eight anuran families: functional, systematic, evolutionary and ecological considerations. Univ Kansas Miscell Publ 68:1–146

    Google Scholar 

  • Wassersug RJ (1984) ThePseudohemiscus tadpole: a morphological link between microhylid (Orton Type 2) and ranoid (Orton Type 4) larvae. Herpetologica 40:138–149

    Google Scholar 

  • Wassersug RJ, Heyer WR (1988) A survey of internal oral features of leptodactyloid larvae (Amphibia: Anura. Smithson Contrib Zool 457:1–99

    Google Scholar 

  • Wassersug RJ, Hoff K (1979) A comparative study of the buccal pumping mechanism of tadpoles. Biol J Linn Soc 12:221–259

    Google Scholar 

  • Wassersug RJ, Pyburn WF (1987) The biology of the Pe-ret'toad,Otophryne robusta (Microhylidae), with special considerations of its fossorial larva and systematic relationships. Zool J Linn Soc 91:137–169

    Google Scholar 

  • Wassersug RJ, Rosenberg K (1979) Surface anatomy of branchial food traps of tadpoles: a comparative study. J Morphol 159:393–426

    Google Scholar 

  • Weisz PB (1945) The normal stages in the development of the South African clawed toad,Xenopus laevis. Anat Rec 93:161–169

    Google Scholar 

  • Welsch U, Storch V (1976) Elektronenmikroskopische Beobachtungen am Kiemenepithel des amphibischen TeleosteersPeriphthalmus vulgaris. Z Mikrosk Anat Forsch 90:447–457

    Google Scholar 

  • White PN, Bruton MN (1983) Food and feeding mechanisms ofGilchristella aestuaris (Clupeidae). S Afr J Zool 18:31–36

    Google Scholar 

  • Whitear M (1977) A functional comparison between the epidermis of fish and amphibians. In: Spearman RIC (ed) Comparative biology of skin. Symp Zool Soc Lond No 39. Academic Press, London, pp 291–313

    Google Scholar 

  • Yoshie S, Honma Y (1979) Scanning electron microscopy of the arctic lamprey,Lampetra japonica, during its metamorphosis, with special reference to tooth formation. Jpn J Ichty 26:181–191

    Google Scholar 

  • Youson JH, Freeman PA (1976) Morphology of the gills of larval and parasitic adult sea lamprey,Petromyzon marinus L. J Morphol 149:73–104

    Google Scholar 

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  1. Institute of Zoology, Johannes Gutenberg University, Saarstraße 21, W-6500, Mainz, Federal Republic of Germany

    Bruno Viertel

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Viertel, B. The ontogeny of the filter apparatus of anuran larvae (Amphibia, Anura). Zoomorphology 110, 239–266 (1991). https://doi.org/10.1007/BF01633098

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