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
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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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DOI: https://doi.org/10.1007/BF01633098