fournol of Herpetology, Vol. 20, No. 1, pp. 90-93, 1986
Copyright 1986 Society for the Study of Amphibians and Reptiles
The Distribution of Ampullary
Organs in Gymnophiona
BERND FRITZSCH,
University of Bielefeld, Faculty of
Biology, P.O. Box 8640,4800 Bielefeld, F . R. Germany.
MARVALEE
H. WAKE, Department of Zoology and
Museum of Vertebrate Zoology, University of California, Berkeley, California 94720, USA.
Following their first description in 1887 (Sarasin and Sarasin), the ampullary organs or “Nebenohren” of gymnophiones were neglected for
nearly a century. The attempt by Coggi (1905) to
compare the two subtypes of the lateral-line organs of gymnophiones with the lateral-line system of sharks (the ”Nebenohren” with the ampullae of Lorenzini; the neuromasts with each
other) was not noticed. It was not until Hether-
NOTES
ington and Wake (1979) clearly defined for the
first time the two types of organs of the lateralline system of gymnophiones that the notion of
Coggi was revived. About the same time neuroanatomical, electrophysiological, and behavioral studies showed that many urodeles, like most
non-teleost fish and some teleosts, possess ampullary organs in the lateral-line system which
function as electroreceptors (Fritzsch, 1981; Himstedt et al., 1982; Fritzsch and Wahnschaffe, 1983;
Fritzsch and Wake, 1984; Munz et al., 1984).These
studies suggest that the ampullary organs in gymnophiones may be electroreceptive. In order to
learn more about the distribution of these neglected sense organs, we examined sectioned material of adults and embryos of a number of gymnophiones.
Prepared heads of 16 species representing 14
genera and three families, including larvae or embryo and fetuses of 6 species, were available for
study. Heads were sectioned either frontally or
transversely; sections were 8-12 pm thick, usually
10 pm. Much of the material was field preserved
in formalin many years ago, and it was difficult
to ascertain without doubt the presence or absence of ampullary organs. Such species consequently were omitted from the study.
We used criteria empirically developed from
research on the ampullary organs and neuromasts
of lchthyophis (Hetherington and Wake, 1979) and
of lungfish (Pfeiffer, 1968) for the identification
of the organs. Neuromasts characteristically are
conical, with elongate mantle and supporting cells
and shorter sensory cells interspersed. All three
cell types bear long cytoplasmic extensions to the
apex of the neuromast, with the tips of sensory
cell processes surrounded by elevated support cell
processes (Fig. Id). The ampullary organs are flaskshaped, more deeply sunken into or below the
epidermis. They are connected to the surface by
a canal. The canal widens at its base into a broad
lumen. The canal is delineated by epidermal cells
whereas at least two types of cells are found clustered around the base of the lumen: ovoid cells
at the luminal surface and densely packed, elongated cells at the basal layer. We interpret the
former as sensory cells and the latter as supporting cells. Occasionally extensions of these cells
into the lumen are visible. The nuclei of the sensory cells are rounder than those of supporting
cells and show prominent granules of heterochromatin. The basal membrane of the epidermis
usually surrounds each organ (Fig. la, ampullary
organ of adult Typhlonectes compressicaudus). The
organs occur on the head with the highest density
at the snout.
The ampullary organs are difficult to identify
in embryos. We observed structures that conform
to descriptions of ampullary organs found in larval urodeles (Fritzsch and Wahnschaffe, 1983)and
Ichthyophis (Hetherington and Wake, 1979) only
in embryos of Typhlonectes compressicaudus. These
organs lie within the epidermis and show a characteristic prominent central pit (Fig. lb). Also, the
91
FIG.1. a. Typhlonectes compressicaudus, 321 mm
total length (TL) adult. Sagittal section of skin of
the lower jaw, 8 pm thick. An ampullary receptor
with its luminal sensory cells and the densely
packed basal supporting cells is shown. Note the
ampulla which leads to a short canal and the basal
membrane which surrounds the organ. Bar = 50
pm. b. Typhlonectes compressicaudus, 70 mm TL fetus. Frontal section of the head. An organ presumed to be an ampullary organ is shown. The
organ has a central pit and two layers of cells with
the luminal cells representing the sensory cells.
Bar = 25 pm. c. Hypogeophis rostratus, 230 mm TL
adult. Sagittal section of skin of lower jaw, with
ampullary organ. Bar = 25 pm. d. Geotrypetes grandisonae, 95 mm TL larva. Frontal section of head
skin. Both a free neuromast and an ampullary organ are indicated. Bar = 25 pm. Abbreviations:
ao = ampullary organ; bm = basement membrane; g = skin gland; n = neuromast.
larvae of Ichthyophis kohtaoensis fully conformed
to the description given by Hetherington and
Wake (1979) with respect to organization and distribution of ampullary organs and neuromasts for
three other species of Ichthyophis. In addition, lateral-line organs (not specified as to type) are reported for embryonic Hypogeophis rostratus (Brauer,
92
NOTES
1899) and for Geotrypetes grandisonae larvae (Largen et al., 1972). A closely related species ( G . seraphini) that lacks free living larvae, does not show
any trace of lateral-line organs (Largen et al., 1972).
We find that G . grandisonae larvae have both neuromasts and ampullary organs. The latter are interspersed among the neuromasts in the lateral
lines (Fig. Id) and over the head and snout. They
do not appear to be present in adults of G. grandisonae or of G. seraphini, as determined from our
sectioned material.
Using the criteria listed above, we identified
ampullary organs on the heads of adult Typhlonectes compressicaudus (Fig. la) and Hypogeophis
rostratus (Fig. IC). Structures hardly distinct from
developing skin glands were found in Caecilia occidentaIis.The data for Caecilia occidentalis indicate
that this species as well may possess ampullary
organs, but more data on this species are clearly
needed. No ampullary organs were found in adult
Ichthyophis. None of the adult specimens of any
other species examined showed any signs of neuromasts.
At present the picture of the distribution of lateral-line organs, and in particular of ampullary
organs, is rather patchy and does not fit a phylogenetic scheme. There are, however, some noteworthy trends among gymnophiones:
a) Free-living larvae of diverse genera possess a
lateral-line system which is most probably
composed of two types of organs, the mechanoreceptive neuromasts and the electroreceptive ampullary organs. In this respect, gymnophiones are similar to urodeles (Fritzsch and
Wahnschaffe, 1983) but not to anwans, which
possess only neuromasts in their lateral-line
system (Fritzsch et al., in press). The presence
of two types of organs in gymnophiones and
in urodeles may reflect the primitive or plesiomorphic condition in amphibians and most anamniote vertebrates (Bullock et al., 1983).
b) Adults of Tvahlonectes are aquatic, and retain
ampullary organs (Fig. 1, and Bradford and
McCormick, pers. comm.). It is possible that
there is an association of the presence of ampullary organs with aquatic life, though this is
not an exclusive association.
Some species of gymnophiones may retain at
least the ampullary organs through direct development (metamorphosis before hatching,
precluding a larval phase), as embryos developing within the oviduct, and even as adults.
If confirmed by neuroanatomical, electrophysiological, and behavioral data, this indicates that
gymnophiones are the only vertebrates that
possess only ampullary organs in their lateralline systems.
These data suggest that among amphibians there
are at least three separate lines of modification of
the lateral-line system:
1. anurans, which have lost ampullary organs
completely during their phylogeny and may
or may not lose the neuromast system during
metamorphosis (Fritzsch et al., in press).
2. urodeles, which have both ampullary organs
and neuromasts or do not develop either structure at all (Fritzsch and Wahnschaffe, 1983);
3. gymnophiones, which have both organ types
as larvae and lose them during metamorphosis,
or possess only ampullary organs both as embryos and as adults, or lack both entirely.
Thus, amphibians provide examples of virtually
every possible permutation of the expression of
the two types of lateral-line organs and thereby
may provide a unique example to test phylogenetic hypotheses through examination of adaptation of a sensory system.
Acknowledgments.-We thank R. Lawson for the
specimens of Hypogeophis rostratus, A. G . C. Grandison (British Museum of Natural History) for loan
of Geotrypetes grandisonae, C. Hillery, K. Schwenk,
and K. Thomas for preparing the sections, and
Mark Bradford and Cathy McCormick for stimulating discussions which gave our work impetus.
This work was supported by a DFG travel grant,
Fr 572, to B. Fritzsch and by NSF BSR 83-05771 to
M. H. Wake.
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